EyeLink Non-Human Primate Eye-Tracking Publications
All EyeLink non-human primate research publications are listed below in alphabetical order based on the first author. You can search the publications using key words such as Temporal Cortex, Macaque, Antisaccade, etc. You can also search for individual author names. If we missed any EyeLink non-human primate article, please email us!
Becket R Ebitz; Michael L Platt Neuronal activity in primate dorsal anterior cingulate cortex signals Task conflict and predicts adjustments in pupil-linked arousal Journal Article Neuron, 85 (3), pp. 628–640, 2015. @article{Ebitz2015, title = {Neuronal activity in primate dorsal anterior cingulate cortex signals Task conflict and predicts adjustments in pupil-linked arousal}, author = {Becket R Ebitz and Michael L Platt}, doi = {10.1016/j.neuron.2014.12.053}, year = {2015}, date = {2015-01-01}, journal = {Neuron}, volume = {85}, number = {3}, pages = {628--640}, publisher = {Elsevier Inc.}, abstract = {Whether driving a car, shopping for food, or paying attention in a classroom of boisterous teenagers, it's often hard to maintain focus on goals in theface of distraction. Brain imaging studies in humans implicate the dorsal anterior cingulate cortex (dACC) in regulating the conflict between goals and distractors. Here we show that single dACC neurons signal conflict between task goals and distractors in the rhesus macaque, particularly for biologically relevant social stimuli. For some neurons, task conflict signals predicted subsequent changes in pupil size-a peripheral index of arousal linked to noradrenergic tone-associated with reduced distractor interference. dACC neurons also responded to errors, and these signals predicted adjustments in pupil size. These findings provide the first neurophysiological endorsement of the hypothesis that dACC regulates conflict, in part, via modulation of pupil-linked processes such as arousal.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Whether driving a car, shopping for food, or paying attention in a classroom of boisterous teenagers, it's often hard to maintain focus on goals in theface of distraction. Brain imaging studies in humans implicate the dorsal anterior cingulate cortex (dACC) in regulating the conflict between goals and distractors. Here we show that single dACC neurons signal conflict between task goals and distractors in the rhesus macaque, particularly for biologically relevant social stimuli. For some neurons, task conflict signals predicted subsequent changes in pupil size-a peripheral index of arousal linked to noradrenergic tone-associated with reduced distractor interference. dACC neurons also responded to errors, and these signals predicted adjustments in pupil size. These findings provide the first neurophysiological endorsement of the hypothesis that dACC regulates conflict, in part, via modulation of pupil-linked processes such as arousal. |
Becket R Ebitz; Tirin Moore Selective modulation of the pupil light reflex by microstimulation of prefrontal cortex Journal Article Journal of Neuroscience, 37 (19), pp. 5008–5018, 2017. @article{Ebitz2017, title = {Selective modulation of the pupil light reflex by microstimulation of prefrontal cortex}, author = {Becket R Ebitz and Tirin Moore}, doi = {10.1523/JNEUROSCI.2433-16.2017}, year = {2017}, date = {2017-01-01}, journal = {Journal of Neuroscience}, volume = {37}, number = {19}, pages = {5008--5018}, abstract = {The prefrontal cortex (PFC) is thought to flexibly regulate sensorimotor responses, perhaps through modulating activity in other circuits. However, the scope of that control remains unknown: it remains unclear whether the PFC can modulate basic reflexes. One canonical example of a central reflex is the pupil light reflex (PLR): the automatic constriction of the pupil in response to luminance increments. Unlike pupil size, which depends on the interaction of multiple physiological and neuromodulatory influences, the PLR reflects the action of a simple brainstem circuit. However, emerging behavioral evidence suggests that the PLR may be modulated by cognitive processes. Although the neural basis of these modulations remains unknown, one possible source is the PFC, particularly the frontal eye field (FEF), an area of the PFC implicated in the control of attention. We show that microstimulation of the rhesus macaque FEF alters the magnitude of the PLR in a spatially specific manner. FEF microstimulation enhanced the PLR to probes presented within the stimulated visual field, but suppressed the PLR to probes at nonoverlapping locations. The spatial specificity of this effect parallels the effect of FEF stimulation on attention and suggests that FEF is capable of modulating visuomotor transformations performed at a lower level than was previously known. These results provide evidence of the selective regulation of a basic brainstem reflex by the PFC.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The prefrontal cortex (PFC) is thought to flexibly regulate sensorimotor responses, perhaps through modulating activity in other circuits. However, the scope of that control remains unknown: it remains unclear whether the PFC can modulate basic reflexes. One canonical example of a central reflex is the pupil light reflex (PLR): the automatic constriction of the pupil in response to luminance increments. Unlike pupil size, which depends on the interaction of multiple physiological and neuromodulatory influences, the PLR reflects the action of a simple brainstem circuit. However, emerging behavioral evidence suggests that the PLR may be modulated by cognitive processes. Although the neural basis of these modulations remains unknown, one possible source is the PFC, particularly the frontal eye field (FEF), an area of the PFC implicated in the control of attention. We show that microstimulation of the rhesus macaque FEF alters the magnitude of the PLR in a spatially specific manner. FEF microstimulation enhanced the PLR to probes presented within the stimulated visual field, but suppressed the PLR to probes at nonoverlapping locations. The spatial specificity of this effect parallels the effect of FEF stimulation on attention and suggests that FEF is capable of modulating visuomotor transformations performed at a lower level than was previously known. These results provide evidence of the selective regulation of a basic brainstem reflex by the PFC. |
Becket R Ebitz; Eddy Albarran; Tirin Moore Exploration disrupts choice-predictive signals and alters dynamics in prefrontal cortex Journal Article Neuron, 97 (2), pp. 450–461, 2018. @article{Ebitz2018, title = {Exploration disrupts choice-predictive signals and alters dynamics in prefrontal cortex}, author = {Becket R Ebitz and Eddy Albarran and Tirin Moore}, doi = {10.1016/j.neuron.2017.12.007}, year = {2018}, date = {2018-01-01}, journal = {Neuron}, volume = {97}, number = {2}, pages = {450--461}, publisher = {Elsevier Inc.}, abstract = {In uncertain environments, decision-makers must balance two goals: they must “exploit” rewarding options but also “explore” in order to discover rewarding alternatives. Exploring and exploiting necessarily change how the brain responds to identical stimuli, but little is known about how these states, and transitions between them, change how the brain transforms sensory information into action. To address this question, we recorded neural activity in a prefrontal sensorimotor area while monkeys naturally switched between exploring and exploiting rewarding options. We found that exploration profoundly reduced spatially selective, choice-predictive activity in single neurons and delayed choice-predictive population dynamics. At the same time, reward learning was increased in brain and behavior. These results indicate that exploration is related to sudden disruptions in prefrontal sensorimotor control and rapid, reward-dependent reorganization of control dynamics. This may facilitate discovery through trial and error. Exploratory choices permit the discovery of new rewarding options. Ebitz et al. report that spatially selective, choice-predictive neurons in the prefrontal cortex do not predict choice before exploratory decisions. Reduced prefrontal control may underlie flexible decision-making and trial-and-error discovery.}, keywords = {}, pubstate = {published}, tppubtype = {article} } In uncertain environments, decision-makers must balance two goals: they must “exploit” rewarding options but also “explore” in order to discover rewarding alternatives. Exploring and exploiting necessarily change how the brain responds to identical stimuli, but little is known about how these states, and transitions between them, change how the brain transforms sensory information into action. To address this question, we recorded neural activity in a prefrontal sensorimotor area while monkeys naturally switched between exploring and exploiting rewarding options. We found that exploration profoundly reduced spatially selective, choice-predictive activity in single neurons and delayed choice-predictive population dynamics. At the same time, reward learning was increased in brain and behavior. These results indicate that exploration is related to sudden disruptions in prefrontal sensorimotor control and rapid, reward-dependent reorganization of control dynamics. This may facilitate discovery through trial and error. Exploratory choices permit the discovery of new rewarding options. Ebitz et al. report that spatially selective, choice-predictive neurons in the prefrontal cortex do not predict choice before exploratory decisions. Reduced prefrontal control may underlie flexible decision-making and trial-and-error discovery. |
Yasmine El-Shamayleh; Anitha Pasupathy Contour curvature as an invariant code for objects in visual area V4 Journal Article Journal of Neuroscience, 36 (20), pp. 5532–5543, 2016. @article{El-Shamayleh2016, title = {Contour curvature as an invariant code for objects in visual area V4}, author = {Yasmine El-Shamayleh and Anitha Pasupathy}, doi = {10.1523/JNEUROSCI.4139-15.2016}, year = {2016}, date = {2016-01-01}, journal = {Journal of Neuroscience}, volume = {36}, number = {20}, pages = {5532--5543}, abstract = {Size-invariant object recognition-the ability to recognize objects across transformations of scale-is a fundamental feature of biological and artificial vision. To investigate its basis in the primate cerebral cortex, we measured single neuron responses to stimuli of varying size in visual area V4, a cornerstone of the object-processing pathway, in rhesus monkeys (Macaca mulatta). Leveraging two competing models for how neuronal selectivity for the bounding contours of objects may depend on stimulus size, we show that most V4 neurons (∼70%) encode objects in a size-invariant manner, consistent with selectivity for a size-independent parameter of boundary form: for these neurons, "normalized" curvature, rather than "absolute" curvature, provided a better account of responses. Our results demonstrate the suitability of contour curvature as a basis for size-invariant object representation in the visual cortex, and posit V4 as a foundation for behaviorally relevant object codes.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Size-invariant object recognition-the ability to recognize objects across transformations of scale-is a fundamental feature of biological and artificial vision. To investigate its basis in the primate cerebral cortex, we measured single neuron responses to stimuli of varying size in visual area V4, a cornerstone of the object-processing pathway, in rhesus monkeys (Macaca mulatta). Leveraging two competing models for how neuronal selectivity for the bounding contours of objects may depend on stimulus size, we show that most V4 neurons (∼70%) encode objects in a size-invariant manner, consistent with selectivity for a size-independent parameter of boundary form: for these neurons, "normalized" curvature, rather than "absolute" curvature, provided a better account of responses. Our results demonstrate the suitability of contour curvature as a basis for size-invariant object representation in the visual cortex, and posit V4 as a foundation for behaviorally relevant object codes. |
Sarah J Fairhall; Carol A Dickson; Leah Scott; Peter C Pearce A non-invasive method for studying an index of pupil diameter and visual performance in the rhesus monkey Journal Article Journal of Medical Primatology, 35 (2), pp. 67–77, 2006. @article{Fairhall2006, title = {A non-invasive method for studying an index of pupil diameter and visual performance in the rhesus monkey}, author = {Sarah J Fairhall and Carol A Dickson and Leah Scott and Peter C Pearce}, doi = {10.1111/j.1600-0684.2005.00135.x}, year = {2006}, date = {2006-01-01}, journal = {Journal of Medical Primatology}, volume = {35}, number = {2}, pages = {67--77}, abstract = {BACKGROUND: A non-invasive model has been developed to estimate gaze direction and relative pupil diameter, in minimally restrained rhesus monkeys, to investigate the effects of low doses of ocularly administered cholinergic compounds on visual performance. METHODS: Animals were trained to co-operate with a novel device, which enabled eye movements to be recorded using modified human eye-tracking equipment, and to perform a task which determined visual threshold contrast. Responses were made by gaze transfer under twilight conditions. 4% w/v pilocarpine nitrate was studied to demonstrate the suitability of the model. RESULTS: Pilocarpine induced marked miosis for textgreater3 h which was accompanied by a decrement in task performance. CONCLUSIONS: The method obviates the need for invasive surgery and, as the position of point of gaze can be approximately defined, the approach may have utility in other areas of research involving non-human primates.}, keywords = {}, pubstate = {published}, tppubtype = {article} } BACKGROUND: A non-invasive model has been developed to estimate gaze direction and relative pupil diameter, in minimally restrained rhesus monkeys, to investigate the effects of low doses of ocularly administered cholinergic compounds on visual performance. METHODS: Animals were trained to co-operate with a novel device, which enabled eye movements to be recorded using modified human eye-tracking equipment, and to perform a task which determined visual threshold contrast. Responses were made by gaze transfer under twilight conditions. 4% w/v pilocarpine nitrate was studied to demonstrate the suitability of the model. RESULTS: Pilocarpine induced marked miosis for textgreater3 h which was accompanied by a decrement in task performance. CONCLUSIONS: The method obviates the need for invasive surgery and, as the position of point of gaze can be approximately defined, the approach may have utility in other areas of research involving non-human primates. |
Hongwei Fan; Xiaochuan Pan; Rubin Wang; Masamichi Sakagami Differences in reward processing between putative cell types in primate prefrontal cortex Journal Article PLoS ONE, 12 (12), pp. 1–27, 2017. @article{Fan2017a, title = {Differences in reward processing between putative cell types in primate prefrontal cortex}, author = {Hongwei Fan and Xiaochuan Pan and Rubin Wang and Masamichi Sakagami}, doi = {10.1371/journal.pone.0189771}, year = {2017}, date = {2017-01-01}, journal = {PLoS ONE}, volume = {12}, number = {12}, pages = {1--27}, abstract = {Single-unit studies in monkeys have demonstrated that neurons in the prefrontal cortex predict the reward type, reward amount or reward availability associated with a stimulus. To examine contributions of pyramidal cells and interneurons in reward processing, single-unit activity was extracellularly recorded in prefrontal cortices of four monkeys performing a reward prediction task. Based on their shapes of spike waveforms, prefrontal neurons were classified into broad-spike and narrow-spike units that represented putative pyramidal cells and interneurons, respectively. We mainly observed that narrow-spike neurons showed higher firing rates but less bursty discharges than did broad-spike neurons. Both narrow-spike and broad-spike cells selectively responded to the stimulus, reward and their interaction, and the proportions of each type of selective neurons were similar between the two cell classes. Moreover, the two types of cells displayed equal reliability of reward or stimulus discrimination. Furthermore, we found that broad-spike and narrow-spike cells showed distinct mechanisms for encoding reward or stimulus information. Broad-spike neurons raised their firing rate relative to the baseline rate to represent the preferred reward or stimulus information, whereas narrow-spike neurons inhibited their firing rate lower than the baseline rate to encode the non-preferred reward or stimulus information. Our results suggest that narrow-spike and broad-spike cells were equally involved in reward and stimulus processing in the prefrontal cortex. They utilized a binary strategy to complementarily represent reward or stimulus information, which was consistent with the task structure in which the monkeys were required to remember two reward conditions and two visual stimuli.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Single-unit studies in monkeys have demonstrated that neurons in the prefrontal cortex predict the reward type, reward amount or reward availability associated with a stimulus. To examine contributions of pyramidal cells and interneurons in reward processing, single-unit activity was extracellularly recorded in prefrontal cortices of four monkeys performing a reward prediction task. Based on their shapes of spike waveforms, prefrontal neurons were classified into broad-spike and narrow-spike units that represented putative pyramidal cells and interneurons, respectively. We mainly observed that narrow-spike neurons showed higher firing rates but less bursty discharges than did broad-spike neurons. Both narrow-spike and broad-spike cells selectively responded to the stimulus, reward and their interaction, and the proportions of each type of selective neurons were similar between the two cell classes. Moreover, the two types of cells displayed equal reliability of reward or stimulus discrimination. Furthermore, we found that broad-spike and narrow-spike cells showed distinct mechanisms for encoding reward or stimulus information. Broad-spike neurons raised their firing rate relative to the baseline rate to represent the preferred reward or stimulus information, whereas narrow-spike neurons inhibited their firing rate lower than the baseline rate to encode the non-preferred reward or stimulus information. Our results suggest that narrow-spike and broad-spike cells were equally involved in reward and stimulus processing in the prefrontal cortex. They utilized a binary strategy to complementarily represent reward or stimulus information, which was consistent with the task structure in which the monkeys were required to remember two reward conditions and two visual stimuli. |
Shiva Farashahi; Habiba Azab; Benjamin Hayden; Alireza Soltani On the flexibility of basic risk attitudes in monkeys Journal Article Journal of Neuroscience, 38 (18), pp. 4383–4398, 2018. @article{Farashahi2018, title = {On the flexibility of basic risk attitudes in monkeys}, author = {Shiva Farashahi and Habiba Azab and Benjamin Hayden and Alireza Soltani}, doi = {10.1523/jneurosci.2260-17.2018}, year = {2018}, date = {2018-01-01}, journal = {Journal of Neuroscience}, volume = {38}, number = {18}, pages = {4383--4398}, abstract = {Monkeys and other animals appear to share with humans two risk attitudes predicted by prospect theory: an inverse-S-shaped probability weighting function and a steeper utility curve for losses than for gains. These findings suggest that such preferences are stable traits with common neural substrates. We hypothesized instead that animals tailor their preferences to subtle changes in task contexts, making risk attitudes flexible. Previous studies used a limited number of outcomes, trial types, and contexts. To gain a broader perspective, we examined two large datasets of male macaques' risky choices: one from a task with real (juice) gains and another from a token task with gains and losses. In contrast to previous findings, monkeys were risk-seeking for both gains and losses (i.e. lacked a reflection effect) and showed steeper gain than loss curves (loss-seeking). Utility curves for gains were substantially different in the two tasks. Monkeys showed nearly linear probability weightings in one task and S-shaped ones in the other; neither task produced a consistent inverse-S-shaped curve. To account for these observations, we developed and tested various computational models of the processes involved in the construction of reward value. We found that adaptive differential weighting of prospective gamble outcomes could partially account for the observed differences in the utility functions across the two experiments and thus, provide a plausible mechanism underlying flexible risk attitudes. Together, our results support the idea that risky choices are constructed flexibly at the time of elicitation and place important constraints on neural models of economic choice.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Monkeys and other animals appear to share with humans two risk attitudes predicted by prospect theory: an inverse-S-shaped probability weighting function and a steeper utility curve for losses than for gains. These findings suggest that such preferences are stable traits with common neural substrates. We hypothesized instead that animals tailor their preferences to subtle changes in task contexts, making risk attitudes flexible. Previous studies used a limited number of outcomes, trial types, and contexts. To gain a broader perspective, we examined two large datasets of male macaques' risky choices: one from a task with real (juice) gains and another from a token task with gains and losses. In contrast to previous findings, monkeys were risk-seeking for both gains and losses (i.e. lacked a reflection effect) and showed steeper gain than loss curves (loss-seeking). Utility curves for gains were substantially different in the two tasks. Monkeys showed nearly linear probability weightings in one task and S-shaped ones in the other; neither task produced a consistent inverse-S-shaped curve. To account for these observations, we developed and tested various computational models of the processes involved in the construction of reward value. We found that adaptive differential weighting of prospective gamble outcomes could partially account for the observed differences in the utility functions across the two experiments and thus, provide a plausible mechanism underlying flexible risk attitudes. Together, our results support the idea that risky choices are constructed flexibly at the time of elicitation and place important constraints on neural models of economic choice. |
Jose A Fernandez-Leon; Bryan J Hansen; Valentin Dragoi Representation of rapid image sequences in V4 Networks Journal Article Cerebral Cortex, 28 (8), pp. 2675–2684, 2018. @article{Fernandez-Leon2018, title = {Representation of rapid image sequences in V4 Networks}, author = {Jose A Fernandez-Leon and Bryan J Hansen and Valentin Dragoi}, doi = {10.1093/cercor/bhx146}, year = {2018}, date = {2018-01-01}, journal = {Cerebral Cortex}, volume = {28}, number = {8}, pages = {2675--2684}, abstract = {Natural viewing often consists of sequences of brief fixations to image patches of different structure. Whether and how briefly presented sequential stimuli are encoded in a temporal-position manner is poorly understood. Here, we performed multiple-electrode recordings in the visual cortex (area V4) of nonhuman primates (Macaca mulatta) viewing a sequence of 7 briefly flashed natural images, and measured correlations between the cue-triggered population response in the presence and absence of the stimulus. Surprisingly, we found significant correlations for images occurring at the beginning and the end of a sequence, but not for those in the middle. The correlation strength increased with stimulus exposure and favored the image position in the sequence rather than image identity. These results challenge the commonly held view that images are represented in visual cortex exclusively based on their informational content, and indicate that, in the absence of sensory information, neuronal populations exhibit reactivation of stimulus-evoked responses in a way that reflects temporal position within a stimulus sequence.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Natural viewing often consists of sequences of brief fixations to image patches of different structure. Whether and how briefly presented sequential stimuli are encoded in a temporal-position manner is poorly understood. Here, we performed multiple-electrode recordings in the visual cortex (area V4) of nonhuman primates (Macaca mulatta) viewing a sequence of 7 briefly flashed natural images, and measured correlations between the cue-triggered population response in the presence and absence of the stimulus. Surprisingly, we found significant correlations for images occurring at the beginning and the end of a sequence, but not for those in the middle. The correlation strength increased with stimulus exposure and favored the image position in the sequence rather than image identity. These results challenge the commonly held view that images are represented in visual cortex exclusively based on their informational content, and indicate that, in the absence of sensory information, neuronal populations exhibit reactivation of stimulus-evoked responses in a way that reflects temporal position within a stimulus sequence. |
Ian C Fiebelkorn; Mark A Pinsk; Sabine Kastner A dynamic interplay within the frontoparietal network underlies rhythmic spatial attention Journal Article Neuron, 99 (4), pp. 842–853, 2018. @article{Fiebelkorn2018, title = {A dynamic interplay within the frontoparietal network underlies rhythmic spatial attention}, author = {Ian C Fiebelkorn and Mark A Pinsk and Sabine Kastner}, doi = {10.1016/j.neuron.2018.07.038}, year = {2018}, date = {2018-01-01}, journal = {Neuron}, volume = {99}, number = {4}, pages = {842--853}, publisher = {Elsevier Inc.}, abstract = {Classic studies of spatial attention assumed that its neural and behavioral effects were continuous over time. Recent behavioral studies have instead re- vealed that spatial attention leads to alternating pe- riods of heightened or diminished perceptual sensi- tivity. Yet, the neural basis of these rhythmic fluctuations has remained largely unknown. We show that a dynamic interplay within the macaque frontoparietal network accounts for the rhythmic properties of spatial attention. Neural oscillations characterize functional interactions between the frontal eye fields (FEF) and the lateral intraparietal area (LIP), with theta phase (3–8 Hz) coordinating two rhythmically alternating states. The first is defined by FEF-dominated beta-band activity, asso- ciated with suppressed attentional shifts, and LIP- dominated gamma-band activity, associated with enhanced visual processing and better behavioral performance. The second is defined by LIP-specific alpha-band activity, associated with attenuated vi- sual processing and worse behavioral performance. Our findings reveal how network-level interactions organize environmental sampling into rhythmic cycles.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Classic studies of spatial attention assumed that its neural and behavioral effects were continuous over time. Recent behavioral studies have instead re- vealed that spatial attention leads to alternating pe- riods of heightened or diminished perceptual sensi- tivity. Yet, the neural basis of these rhythmic fluctuations has remained largely unknown. We show that a dynamic interplay within the macaque frontoparietal network accounts for the rhythmic properties of spatial attention. Neural oscillations characterize functional interactions between the frontal eye fields (FEF) and the lateral intraparietal area (LIP), with theta phase (3–8 Hz) coordinating two rhythmically alternating states. The first is defined by FEF-dominated beta-band activity, asso- ciated with suppressed attentional shifts, and LIP- dominated gamma-band activity, associated with enhanced visual processing and better behavioral performance. The second is defined by LIP-specific alpha-band activity, associated with attenuated vi- sual processing and worse behavioral performance. Our findings reveal how network-level interactions organize environmental sampling into rhythmic cycles. |
C D Fiorillo Transient activation of midbrain dopamine neurons by reward risk Journal Article Neuroscience, 197 , pp. 162–171, 2011. @article{Fiorillo2011, title = {Transient activation of midbrain dopamine neurons by reward risk}, author = {C D Fiorillo}, doi = {10.1016/j.neuroscience.2011.09.037}, year = {2011}, date = {2011-01-01}, journal = {Neuroscience}, volume = {197}, pages = {162--171}, publisher = {Elsevier Inc.}, abstract = {Dopamine neurons of the ventral midbrain are activated transiently following stimuli that predict future reward. This response has been shown to signal the expected value of future reward, and there is strong evidence that it drives positive reinforcement of stimuli and actions associated with reward in accord with reinforcement learning models. Behavior is also influenced by reward uncertainty, or risk, but it is not known whether the transient response of dopamine neurons is sensitive to reward risk. To investigate this, monkeys were trained to associate distinct visual stimuli with certain or uncertain volumes of juice of nearly the same expected value. In a choice task, monkeys preferred the stimulus predicting an uncertain (risky) reward outcome. In a Pavlovian task, in which the neuronal responses to each stimulus could be measured in isolation, it was found that dopamine neurons were more strongly activated by the stimulus associated with reward risk. Given extensive evidence that dopamine drives reinforcement, these results strongly suggest that dopamine neurons can reinforce risk-seeking behavior (gambling), at least under certain conditions. Risk-seeking behavior has the virtue of promoting exploration and learning, and these results support the hypothesis that dopamine neurons represent the value of exploration.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Dopamine neurons of the ventral midbrain are activated transiently following stimuli that predict future reward. This response has been shown to signal the expected value of future reward, and there is strong evidence that it drives positive reinforcement of stimuli and actions associated with reward in accord with reinforcement learning models. Behavior is also influenced by reward uncertainty, or risk, but it is not known whether the transient response of dopamine neurons is sensitive to reward risk. To investigate this, monkeys were trained to associate distinct visual stimuli with certain or uncertain volumes of juice of nearly the same expected value. In a choice task, monkeys preferred the stimulus predicting an uncertain (risky) reward outcome. In a Pavlovian task, in which the neuronal responses to each stimulus could be measured in isolation, it was found that dopamine neurons were more strongly activated by the stimulus associated with reward risk. Given extensive evidence that dopamine drives reinforcement, these results strongly suggest that dopamine neurons can reinforce risk-seeking behavior (gambling), at least under certain conditions. Risk-seeking behavior has the virtue of promoting exploration and learning, and these results support the hypothesis that dopamine neurons represent the value of exploration. |
Christopher D Fiorillo; Minryung R Song; Sora R Yun Multiphasic temporal dynamics in responses of midbrain dopamine neurons to appetitive and aversive stimuli Journal Article Journal of Neuroscience, 33 (11), pp. 4710–4725, 2013. @article{Fiorillo2013, title = {Multiphasic temporal dynamics in responses of midbrain dopamine neurons to appetitive and aversive stimuli}, author = {Christopher D Fiorillo and Minryung R Song and Sora R Yun}, doi = {10.1523/JNEUROSCI.3883-12.2013}, year = {2013}, date = {2013-01-01}, journal = {Journal of Neuroscience}, volume = {33}, number = {11}, pages = {4710--4725}, abstract = {The transient response of dopamine neurons has been described as reward prediction error (RPE), with activation or suppression by events that are better or worse than expected, respectively. However, at least a minority of neurons are activated by aversive or high-intensity stimuli, casting doubt on the generality of RPE in describing the dopamine signal. To overcome limitations of previous studies, we studied neuronal responses to a wider variety of high-intensity and aversive stimuli, and we quantified and controlled aversiveness through a choice task in which macaques sacrificed juice to avoid aversive stimuli. Whereas most previous work has portrayed the RPE as a single impulse or "phase," here we demonstrate its multiphasic temporal dynamics. Aversive or high-intensity stimuli evoked a triphasic sequence of activation-suppression-activation extending over a period of 40-700 ms. The initial activation at short latencies (40-120 ms) reflected sensory intensity. The influence of motivational value became dominant between 150 and 250 ms, with activation in the case of appetitive stimuli, and suppression in the case of aversive and neutral stimuli. The previously unreported late activation appeared to be a modest "rebound" after strong suppression. Similarly, strong activation by reward was often followed by suppression. We suggest that these "rebounds" may result from overcompensation by homeostatic mechanisms in some cells. Our results are consistent with a realistic RPE, which evolves over time through a dynamic balance of excitation and inhibition.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The transient response of dopamine neurons has been described as reward prediction error (RPE), with activation or suppression by events that are better or worse than expected, respectively. However, at least a minority of neurons are activated by aversive or high-intensity stimuli, casting doubt on the generality of RPE in describing the dopamine signal. To overcome limitations of previous studies, we studied neuronal responses to a wider variety of high-intensity and aversive stimuli, and we quantified and controlled aversiveness through a choice task in which macaques sacrificed juice to avoid aversive stimuli. Whereas most previous work has portrayed the RPE as a single impulse or "phase," here we demonstrate its multiphasic temporal dynamics. Aversive or high-intensity stimuli evoked a triphasic sequence of activation-suppression-activation extending over a period of 40-700 ms. The initial activation at short latencies (40-120 ms) reflected sensory intensity. The influence of motivational value became dominant between 150 and 250 ms, with activation in the case of appetitive stimuli, and suppression in the case of aversive and neutral stimuli. The previously unreported late activation appeared to be a modest "rebound" after strong suppression. Similarly, strong activation by reward was often followed by suppression. We suggest that these "rebounds" may result from overcompensation by homeostatic mechanisms in some cells. Our results are consistent with a realistic RPE, which evolves over time through a dynamic balance of excitation and inhibition. |
Christopher D Fiorillo; Sora R Yun; Minryung R Song Diversity and homogeneity in responses of midbrain dopamine neurons Journal Article Journal of Neuroscience, 33 (11), pp. 4693–4709, 2013. @article{Fiorillo2013a, title = {Diversity and homogeneity in responses of midbrain dopamine neurons}, author = {Christopher D Fiorillo and Sora R Yun and Minryung R Song}, doi = {10.1523/JNEUROSCI.3886-12.2013}, year = {2013}, date = {2013-01-01}, journal = {Journal of Neuroscience}, volume = {33}, number = {11}, pages = {4693--4709}, abstract = {Dopamine neurons of the ventral midbrain have been found to signal a reward prediction error that can mediate positive reinforcement. Despite the demonstration of modest diversity at the cellular and molecular levels, there has been little analysis of response diversity in behaving animals. Here we examine response diversity in rhesus macaques to appetitive, aversive, and neutral stimuli having relative motivational values that were measured and controlled through a choice task. First, consistent with previous studies, we observed a continuum of response variability and an apparent absence of distinct clusters in scatter plots, suggesting a lack of statistically discrete subpopulations of neurons. Second, we found that a group of " sensitive " neurons tend to be more strongly suppressed by a variety of stimuli and to be more strongly activated by juice. Third, neurons in the " ventral tier " of substantia nigra were found to have greater suppression, and a subset of these had higher baseline firing rates and late " rebound " activation after suppression. These neurons could belong to a previously identified subgroup of dopamine neurons that express high levels of H-type cation channels but lack calbindin. Fourth, neurons further rostral exhibited greater suppression. Fifth, although we observed weak activation of some neurons by aversive stimuli, this was not associated with their aversiveness. In conclusion, we find a diversity of response properties, distributed along a continuum, within what may be a single functional population of neurons signaling reward prediction error.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Dopamine neurons of the ventral midbrain have been found to signal a reward prediction error that can mediate positive reinforcement. Despite the demonstration of modest diversity at the cellular and molecular levels, there has been little analysis of response diversity in behaving animals. Here we examine response diversity in rhesus macaques to appetitive, aversive, and neutral stimuli having relative motivational values that were measured and controlled through a choice task. First, consistent with previous studies, we observed a continuum of response variability and an apparent absence of distinct clusters in scatter plots, suggesting a lack of statistically discrete subpopulations of neurons. Second, we found that a group of " sensitive " neurons tend to be more strongly suppressed by a variety of stimuli and to be more strongly activated by juice. Third, neurons in the " ventral tier " of substantia nigra were found to have greater suppression, and a subset of these had higher baseline firing rates and late " rebound " activation after suppression. These neurons could belong to a previously identified subgroup of dopamine neurons that express high levels of H-type cation channels but lack calbindin. Fourth, neurons further rostral exhibited greater suppression. Fifth, although we observed weak activation of some neurons by aversive stimuli, this was not associated with their aversiveness. In conclusion, we find a diversity of response properties, distributed along a continuum, within what may be a single functional population of neurons signaling reward prediction error. |
K A Ford; S Everling Neural activity in primate caudate nucleus associated with pro- and antisaccades Journal Article Journal of Neurophysiology, 102 (4), pp. 2334–2341, 2009. @article{Ford2009, title = {Neural activity in primate caudate nucleus associated with pro- and antisaccades}, author = {K A Ford and S Everling}, doi = {10.1152/jn.00125.2009}, year = {2009}, date = {2009-01-01}, journal = {Journal of Neurophysiology}, volume = {102}, number = {4}, pages = {2334--2341}, abstract = {The basal ganglia (BG) play a central role in movement and it has been demonstrated that the discharge rate of neurons in these structures are modulated by the behavioral context of a given task. Here we used the antisaccade task, in which a saccade toward a flashed visual stimulus must be inhibited in favor of a saccade to the opposite location, to investigate the role of the caudate nucleus, a major input structure of the BG, in flexible behavior. In this study, we recorded extracellular neuronal activity while monkeys performed pro- and antisaccade trials. We identified two populations of neurons: those that preferred contralateral saccades (CSNs) and those that preferred ipsilateral saccades (ISNs). CSNs increased their firing rates for prosaccades, but not for antisaccades, and ISNs increased their firing rates for antisaccades, but not for prosaccades. We propose a model in which CSNs project to the direct BG pathway, facilitating saccades, and ISNs project to the indirect pathway, suppressing saccades. This model suggests one possible mechanism by which these neuronal populations could be modulating activity in the superior colliculus.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The basal ganglia (BG) play a central role in movement and it has been demonstrated that the discharge rate of neurons in these structures are modulated by the behavioral context of a given task. Here we used the antisaccade task, in which a saccade toward a flashed visual stimulus must be inhibited in favor of a saccade to the opposite location, to investigate the role of the caudate nucleus, a major input structure of the BG, in flexible behavior. In this study, we recorded extracellular neuronal activity while monkeys performed pro- and antisaccade trials. We identified two populations of neurons: those that preferred contralateral saccades (CSNs) and those that preferred ipsilateral saccades (ISNs). CSNs increased their firing rates for prosaccades, but not for antisaccades, and ISNs increased their firing rates for antisaccades, but not for prosaccades. We propose a model in which CSNs project to the direct BG pathway, facilitating saccades, and ISNs project to the indirect pathway, suppressing saccades. This model suggests one possible mechanism by which these neuronal populations could be modulating activity in the superior colliculus. |
Amber M Fyall; Yasmine El-Shamayleh; Hannah Choi; Eric Shea-Brown; Anitha Pasupathy Dynamic representation of partially occluded objects in primate prefrontal and visual cortex Journal Article eLife, 6 , pp. 1–25, 2017. @article{Fyall2017, title = {Dynamic representation of partially occluded objects in primate prefrontal and visual cortex}, author = {Amber M Fyall and Yasmine El-Shamayleh and Hannah Choi and Eric Shea-Brown and Anitha Pasupathy}, doi = {10.7554/eLife.25784}, year = {2017}, date = {2017-01-01}, journal = {eLife}, volume = {6}, pages = {1--25}, abstract = {Successful recognition of partially occluded objects is presumed to involve dynamic interactions between brain areas responsible for vision and cognition, but neurophysiological evidence for the involvement of feedback signals is lacking. Here, we demonstrate that neurons in the ventrolateral prefrontal cortex (vlPFC) of monkeys performing a shape discrimination task respond more strongly to occluded than unoccluded stimuli. In contrast, neurons in visual area V4 respond more strongly to unoccluded stimuli. Analyses of V4 response dynamics reveal that many neurons exhibit two transient response peaks, the second of which emerges after vlPFC response onset and displays stronger selectivity for occluded shapes. We replicate these findings using a model of V4/vlPFC interactions in which occlusion-sensitive vlPFC neurons feed back to shape- selective V4 neurons, thereby enhancing V4 responses and selectivity to occluded shapes. These results reveal how signals from frontal and visual cortex could interact to facilitate object recognition under occlusion.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Successful recognition of partially occluded objects is presumed to involve dynamic interactions between brain areas responsible for vision and cognition, but neurophysiological evidence for the involvement of feedback signals is lacking. Here, we demonstrate that neurons in the ventrolateral prefrontal cortex (vlPFC) of monkeys performing a shape discrimination task respond more strongly to occluded than unoccluded stimuli. In contrast, neurons in visual area V4 respond more strongly to unoccluded stimuli. Analyses of V4 response dynamics reveal that many neurons exhibit two transient response peaks, the second of which emerges after vlPFC response onset and displays stronger selectivity for occluded shapes. We replicate these findings using a model of V4/vlPFC interactions in which occlusion-sensitive vlPFC neurons feed back to shape- selective V4 neurons, thereby enhancing V4 responses and selectivity to occluded shapes. These results reveal how signals from frontal and visual cortex could interact to facilitate object recognition under occlusion. |
Ali Ghazizadeh; Whitney Griggs; Okihide Hikosaka Ecological origins of object salience: Reward, uncertainty, aversiveness, and novelty Journal Article Frontiers in Neuroscience, 10 , pp. 1–16, 2016. @article{Ghazizadeh2016, title = {Ecological origins of object salience: Reward, uncertainty, aversiveness, and novelty}, author = {Ali Ghazizadeh and Whitney Griggs and Okihide Hikosaka}, doi = {10.3389/fnins.2016.00378}, year = {2016}, date = {2016-01-01}, journal = {Frontiers in Neuroscience}, volume = {10}, pages = {1--16}, abstract = {Among many objects around us, some of them are more salient than others (i.e., attract our attention automatically). Some objects may be inherently salient (e.g., brighter), but others may become salient by virtue of their ecological relevance through experience. However, the importance of ecological experience in guiding attention has not been studied systematically. To address this question, we let subjects (macaque monkeys) view a large number of complex objects (textgreater300), each experienced repeatedly (textgreater5 days) with rewarding, aversive or no outcome association (mere-perceptual exposure). Test of salience was done on separate days using free viewing with no outcome. We found that gaze was biased among the objects from the outset, affecting saccades to objects or fixations within objects. When the outcome was rewarding, gaze preference was stronger (i.e. positive) for objects with larger or equal but uncertain rewards. The effects of aversive outcomes were variable. Gaze preference was positive for some outcome associations (e.g. airpuff), but negative for others (e.g. time-out), possibly due to differences in threat levels. Finally, novel objects attracted gaze, but mere perceptual exposure of objects reduced their salience (learned negative salience). Our results show that, in primates, object salience is strongly influenced by previous ecological experience and is supported by a large memory capacity. Owing to such learned salience, the capacity to rapidly choose important objects can grow during the entire life to promote biological fitness.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Among many objects around us, some of them are more salient than others (i.e., attract our attention automatically). Some objects may be inherently salient (e.g., brighter), but others may become salient by virtue of their ecological relevance through experience. However, the importance of ecological experience in guiding attention has not been studied systematically. To address this question, we let subjects (macaque monkeys) view a large number of complex objects (textgreater300), each experienced repeatedly (textgreater5 days) with rewarding, aversive or no outcome association (mere-perceptual exposure). Test of salience was done on separate days using free viewing with no outcome. We found that gaze was biased among the objects from the outset, affecting saccades to objects or fixations within objects. When the outcome was rewarding, gaze preference was stronger (i.e. positive) for objects with larger or equal but uncertain rewards. The effects of aversive outcomes were variable. Gaze preference was positive for some outcome associations (e.g. airpuff), but negative for others (e.g. time-out), possibly due to differences in threat levels. Finally, novel objects attracted gaze, but mere perceptual exposure of objects reduced their salience (learned negative salience). Our results show that, in primates, object salience is strongly influenced by previous ecological experience and is supported by a large memory capacity. Owing to such learned salience, the capacity to rapidly choose important objects can grow during the entire life to promote biological fitness. |
D M Glasser; James M G Tsui; Christopher C Pack; D Tadin Perceptual and neural consequences of rapid motion adaptation Journal Article Proceedings of the National Academy of Sciences, 108 (45), pp. E1080–E1088, 2011. @article{Glasser2011, title = {Perceptual and neural consequences of rapid motion adaptation}, author = {D M Glasser and James M G Tsui and Christopher C Pack and D Tadin}, doi = {10.1073/pnas.1101141108}, year = {2011}, date = {2011-01-01}, journal = {Proceedings of the National Academy of Sciences}, volume = {108}, number = {45}, pages = {E1080--E1088}, abstract = {Nervous systems adapt to the prevailing sensory environment, and the consequences of this adaptation can be observed in the responses of single neurons and in perception. Given the variety of timescales underlying events in the natural world, determining the temporal characteristics of adaptation is important to understanding how perception adjusts to its sensory environment. Previous work has shown that neural adaptation can occur on a timescale of milliseconds, but perceptual adaptation has generally been studied over relatively long timescales, typically on the order of seconds. This disparity raises important questions. Can perceptual adaptation be observed at brief, functionally relevant timescales? And if so, how do its properties relate to the rapid adaptation seen in cortical neurons? We address these questions in the context of visual motion processing, a perceptual modality characterized by rapid temporal dynamics. We demonstrate objectively that 25 ms of motion adaptation is sufficient to generate a motion aftereffect, an illusory sensation of movement experienced when a moving stimulus is replaced by a stationary pattern. This rapid adaptation occurs regardless of whether the adapting motion is perceived. In neurophysiological recordings from the middle temporal area of primate visual cortex, we find that brief motion adaptation evokes direction-selective responses to subsequently presented stationary stimuli. A simple model shows that these neural responses can explain the consequences of rapid perceptual adaptation. Overall, we show that the motion aftereffect is not merely an intriguing perceptual illusion, but rather a reflection of rapid neural and perceptual processes that can occur essentially every time we experience motion.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Nervous systems adapt to the prevailing sensory environment, and the consequences of this adaptation can be observed in the responses of single neurons and in perception. Given the variety of timescales underlying events in the natural world, determining the temporal characteristics of adaptation is important to understanding how perception adjusts to its sensory environment. Previous work has shown that neural adaptation can occur on a timescale of milliseconds, but perceptual adaptation has generally been studied over relatively long timescales, typically on the order of seconds. This disparity raises important questions. Can perceptual adaptation be observed at brief, functionally relevant timescales? And if so, how do its properties relate to the rapid adaptation seen in cortical neurons? We address these questions in the context of visual motion processing, a perceptual modality characterized by rapid temporal dynamics. We demonstrate objectively that 25 ms of motion adaptation is sufficient to generate a motion aftereffect, an illusory sensation of movement experienced when a moving stimulus is replaced by a stationary pattern. This rapid adaptation occurs regardless of whether the adapting motion is perceived. In neurophysiological recordings from the middle temporal area of primate visual cortex, we find that brief motion adaptation evokes direction-selective responses to subsequently presented stationary stimuli. A simple model shows that these neural responses can explain the consequences of rapid perceptual adaptation. Overall, we show that the motion aftereffect is not merely an intriguing perceptual illusion, but rather a reflection of rapid neural and perceptual processes that can occur essentially every time we experience motion. |
David C Godlove; Alexander Maier; Geoffrey F Woodman; Jeffrey D Schall Microcircuitry of agranular frontal cortex: Testing the generality of the canonical cortical microcircuit Journal Article Journal of Neuroscience, 34 (15), pp. 5355–5369, 2014. @article{Godlove2014, title = {Microcircuitry of agranular frontal cortex: Testing the generality of the canonical cortical microcircuit}, author = {David C Godlove and Alexander Maier and Geoffrey F Woodman and Jeffrey D Schall}, doi = {10.1523/JNEUROSCI.5127-13.2014}, year = {2014}, date = {2014-01-01}, journal = {Journal of Neuroscience}, volume = {34}, number = {15}, pages = {5355--5369}, abstract = {We investigated whether a frontal area that lacks granular layer IV, supplementary eye field, exhibits features of laminar circuitry similar to those observed in primary sensory areas. We report, for the first time, visually evoked local field potentials (LFPs) and spiking activity recorded simultaneously across all layers of agranular frontal cortex using linear electrode arrays. We calculated current source density from the LFPs and compared the laminar organization of evolving sinks to those reported in sensory areas. Simultaneous, transient synaptic current sinks appeared first in layers III and V followed by more prolonged current sinks in layers I/II and VI. We also found no variation of single- or multi-unit visual response latency across layers, and putative pyramidal neurons and interneurons displayed similar response latencies. Many units exhibited pronounced discharge suppression that was strongest in superficial relative to deep layers. Maximum discharge suppression also occurred later in superficial than in deep layers. These results are discussed in the context of the canonical cortical microcircuit model originally formulated to describe early sensory cortex. The data indicate that agranular cortex resembles sensory areas in certain respects, but the cortical microcircuit is modified in nontrivial ways.}, keywords = {}, pubstate = {published}, tppubtype = {article} } We investigated whether a frontal area that lacks granular layer IV, supplementary eye field, exhibits features of laminar circuitry similar to those observed in primary sensory areas. We report, for the first time, visually evoked local field potentials (LFPs) and spiking activity recorded simultaneously across all layers of agranular frontal cortex using linear electrode arrays. We calculated current source density from the LFPs and compared the laminar organization of evolving sinks to those reported in sensory areas. Simultaneous, transient synaptic current sinks appeared first in layers III and V followed by more prolonged current sinks in layers I/II and VI. We also found no variation of single- or multi-unit visual response latency across layers, and putative pyramidal neurons and interneurons displayed similar response latencies. Many units exhibited pronounced discharge suppression that was strongest in superficial relative to deep layers. Maximum discharge suppression also occurred later in superficial than in deep layers. These results are discussed in the context of the canonical cortical microcircuit model originally formulated to describe early sensory cortex. The data indicate that agranular cortex resembles sensory areas in certain respects, but the cortical microcircuit is modified in nontrivial ways. |
David C Godlove; Jeffrey D Schall Microsaccade production during saccade cancelation in a stop-signal task Journal Article Vision Research, 118 , pp. 5–16, 2016. @article{Godlove2016, title = {Microsaccade production during saccade cancelation in a stop-signal task}, author = {David C Godlove and Jeffrey D Schall}, doi = {10.1016/j.visres.2014.10.025}, year = {2016}, date = {2016-01-01}, journal = {Vision Research}, volume = {118}, pages = {5--16}, publisher = {Elsevier Ltd}, abstract = {We obtained behavioral data to evaluate two alternative hypotheses about the neural mechanisms of gaze control. The "fixation" hypothesis states that neurons in rostral superior colliculus (SC) enforce fixation of gaze. The "microsaccade" hypothesis states that neurons in rostral SC encode microsaccades rather than fixation per se. Previously reported neuronal activity in monkey SC during the saccade stop-signal task leads to specific, dissociable behavioral predictions of these two hypotheses. When subjects are required to cancel partially-prepared saccades, imbalanced activity spreads across rostral and caudal SC with a reliable temporal profile. The microsaccade hypothesis predicts that this imbalance will lead to elevated microsaccade production biased toward the target location, while the fixation hypothesis predicts reduced microsaccade production. We tested these predictions by analyzing the microsaccades produced by 4 monkeys while they voluntarily canceled partially prepared eye movements in response to explicit stop signals. Consistent with the fixation hypothesis and contradicting the microsaccade hypothesis, we found that each subject produced significantly fewer microsaccades when normal saccades were successfully canceled. The few microsaccades escaping this inhibition tended to be directed toward the target location. We additionally investigated interactions between initiating microsaccades and inhibiting normal saccades. Reaction times were longer when microsaccades immediately preceded target presentation. However, pre-target microsaccade production did not affect stop-signal reaction time or alter the probability of canceling saccades following stop signals. These findings demonstrate that imbalanced activity within SC does not necessarily produce microsaccades and add to evidence that saccade preparation and cancelation are separate processes.}, keywords = {}, pubstate = {published}, tppubtype = {article} } We obtained behavioral data to evaluate two alternative hypotheses about the neural mechanisms of gaze control. The "fixation" hypothesis states that neurons in rostral superior colliculus (SC) enforce fixation of gaze. The "microsaccade" hypothesis states that neurons in rostral SC encode microsaccades rather than fixation per se. Previously reported neuronal activity in monkey SC during the saccade stop-signal task leads to specific, dissociable behavioral predictions of these two hypotheses. When subjects are required to cancel partially-prepared saccades, imbalanced activity spreads across rostral and caudal SC with a reliable temporal profile. The microsaccade hypothesis predicts that this imbalance will lead to elevated microsaccade production biased toward the target location, while the fixation hypothesis predicts reduced microsaccade production. We tested these predictions by analyzing the microsaccades produced by 4 monkeys while they voluntarily canceled partially prepared eye movements in response to explicit stop signals. Consistent with the fixation hypothesis and contradicting the microsaccade hypothesis, we found that each subject produced significantly fewer microsaccades when normal saccades were successfully canceled. The few microsaccades escaping this inhibition tended to be directed toward the target location. We additionally investigated interactions between initiating microsaccades and inhibiting normal saccades. Reaction times were longer when microsaccades immediately preceded target presentation. However, pre-target microsaccade production did not affect stop-signal reaction time or alter the probability of canceling saccades following stop signals. These findings demonstrate that imbalanced activity within SC does not necessarily produce microsaccades and add to evidence that saccade preparation and cancelation are separate processes. |
Samanthi C Goonetilleke; Leor Katz; Daniel K Wood; Chao Gu; Alexander C Huk; Brian D Corneil Journal of Neurophysiology, 114 (2), pp. 902–913, 2015. @article{Goonetilleke2015, title = {Cross-species comparison of anticipatory and stimulus-driven neck muscle activity well before saccadic gaze shifts in humans and nonhuman primates}, author = {Samanthi C Goonetilleke and Leor Katz and Daniel K Wood and Chao Gu and Alexander C Huk and Brian D Corneil}, doi = {10.1152/jn.00230.2015}, year = {2015}, date = {2015-01-01}, journal = {Journal of Neurophysiology}, volume = {114}, number = {2}, pages = {902--913}, abstract = {Recent studies have described a phenomenon wherein the onset of a peripheral visual stimulus elicits short-latency (textless100 ms) stimulus-locked recruitment (SLR) of neck muscles in nonhuman primates (NHPs), well before any saccadic gaze shift. The SLR is thought to arise from visual responses within the intermediate layers of the superior colliculus (SCi), hence neck muscle recordings may reflect presaccadic activity within the SCi, even in humans. We obtained bilateral intramuscular recordings from splenius capitis (SPL, an ipsilateral head-turning muscle) from 28 human subjects performing leftward or rightward visually guided eye-head gaze shifts. Evidence of an SLR was obtained in 16/55 (29%) of samples; we also observed examples where the SLR was present only unilaterally. We compared these human results with those recorded from a sample of eight NHPs from which recordings of both SPL and deeper suboccipital muscles were available. Using the same criteria, evidence of an SLR was obtained in 8/14 (57%) of SPL recordings, but in 26/29 (90%) of recordings from suboccipital muscles. Thus, both species-specific and muscle- specific factors contribute to the low SLR prevalence in human SPL. Regardless of the presence of the SLR, neck muscle activity in both human SPL and in NHPs became predictive of the reaction time of the ensuing saccade gaze shift ~70 ms after target appearance; such pregaze recruitment likely reflects developing SCi activity, even if the tectoreticulospinal pathway does not reliably relay visually related activity to SPL in humans.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Recent studies have described a phenomenon wherein the onset of a peripheral visual stimulus elicits short-latency (textless100 ms) stimulus-locked recruitment (SLR) of neck muscles in nonhuman primates (NHPs), well before any saccadic gaze shift. The SLR is thought to arise from visual responses within the intermediate layers of the superior colliculus (SCi), hence neck muscle recordings may reflect presaccadic activity within the SCi, even in humans. We obtained bilateral intramuscular recordings from splenius capitis (SPL, an ipsilateral head-turning muscle) from 28 human subjects performing leftward or rightward visually guided eye-head gaze shifts. Evidence of an SLR was obtained in 16/55 (29%) of samples; we also observed examples where the SLR was present only unilaterally. We compared these human results with those recorded from a sample of eight NHPs from which recordings of both SPL and deeper suboccipital muscles were available. Using the same criteria, evidence of an SLR was obtained in 8/14 (57%) of SPL recordings, but in 26/29 (90%) of recordings from suboccipital muscles. Thus, both species-specific and muscle- specific factors contribute to the low SLR prevalence in human SPL. Regardless of the presence of the SLR, neck muscle activity in both human SPL and in NHPs became predictive of the reaction time of the ensuing saccade gaze shift ~70 ms after target appearance; such pregaze recruitment likely reflects developing SCi activity, even if the tectoreticulospinal pathway does not reliably relay visually related activity to SPL in humans. |
Arnulf B A Graf; Richard A Andersen Inferring eye position from populations of lateral intraparietal neurons Journal Article eLife, 2014 (3), pp. 1–13, 2014. @article{Graf2014, title = {Inferring eye position from populations of lateral intraparietal neurons}, author = {Arnulf B A Graf and Richard A Andersen}, doi = {10.7554/eLife.02813}, year = {2014}, date = {2014-01-01}, journal = {eLife}, volume = {2014}, number = {3}, pages = {1--13}, abstract = {Understanding how the brain computes eye position is essential to unraveling high- level visual functions such as eye movement planning, coordinate transformations and stability of spatial awareness. The lateral intraparietal area (LIP) is essential for this process. However, despite decades of research, its contribution to the eye position signal remains controversial. LIP neurons have recently been reported to inaccurately represent eye position during a saccadic eye movement, and to be too slow to support a role in high-level visual functions. We addressed this issue by predicting eye position and saccade direction from the responses of populations of LIP neurons. We found that both signals were accurately predicted before, during and after a saccade. Also, the dynamics of these signals support their contribution to visual functions. These findings provide a principled understanding of the coding of information in populations of neurons within an important node of the cortical network for visual-motor behaviors.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Understanding how the brain computes eye position is essential to unraveling high- level visual functions such as eye movement planning, coordinate transformations and stability of spatial awareness. The lateral intraparietal area (LIP) is essential for this process. However, despite decades of research, its contribution to the eye position signal remains controversial. LIP neurons have recently been reported to inaccurately represent eye position during a saccadic eye movement, and to be too slow to support a role in high-level visual functions. We addressed this issue by predicting eye position and saccade direction from the responses of populations of LIP neurons. We found that both signals were accurately predicted before, during and after a saccade. Also, the dynamics of these signals support their contribution to visual functions. These findings provide a principled understanding of the coding of information in populations of neurons within an important node of the cortical network for visual-motor behaviors. |
Whitney S Griggs; Hidetoshi Amita; Atul Gopal; Okihide Hikosaka Visual neurons in the superior colliculus discriminate many objects by their historical values Journal Article Frontiers in Neuroscience, 12 , pp. 1–15, 2018. @article{Griggs2018, title = {Visual neurons in the superior colliculus discriminate many objects by their historical values}, author = {Whitney S Griggs and Hidetoshi Amita and Atul Gopal and Okihide Hikosaka}, doi = {10.3389/fnins.2018.00396}, year = {2018}, date = {2018-01-01}, journal = {Frontiers in Neuroscience}, volume = {12}, pages = {1--15}, abstract = {The superior colliculus (SC) is an important structure in the mammalian brain that orients the animal towards distinct visual events. Visually-responsive neurons in SC are modulated by visual object features, including size, motion, and color. However, it remains unclear whether SC activity is modulated by non-visual object features, such as the reward value associated with the object. To address this question, three monkeys were trained (textgreater10 days) to saccade to multiple fractal objects, half of which were consistently associated with large reward while other half were associated with small reward. This created historically high-valued (‘good') and low-valued (‘bad') objects. During the neuronal recordings from the SC, the monkeys maintained fixation at the center while the objects were flashed in the receptive field of the neuron without any reward. We found that approximately half of the visual neurons responded more strongly to the good than bad objects. In some neurons, this value-coding remained intact for a long time (textgreater1 year) after the last object-reward association learning. Notably, the neuronal discrimination of reward values started about 100 ms after the appearance of visual objects and lasted for more than 100 ms. These results provide evidence that SC neurons can discriminate objects by their historical (long-term) values. This object value information may be provided by the basal ganglia, especially the circuit originating from the tail of the caudate nucleus. The information may be used by the neural circuits inside SC for motor (saccade) output or may be sent to the circuits outside SC for future behavior.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The superior colliculus (SC) is an important structure in the mammalian brain that orients the animal towards distinct visual events. Visually-responsive neurons in SC are modulated by visual object features, including size, motion, and color. However, it remains unclear whether SC activity is modulated by non-visual object features, such as the reward value associated with the object. To address this question, three monkeys were trained (textgreater10 days) to saccade to multiple fractal objects, half of which were consistently associated with large reward while other half were associated with small reward. This created historically high-valued (‘good') and low-valued (‘bad') objects. During the neuronal recordings from the SC, the monkeys maintained fixation at the center while the objects were flashed in the receptive field of the neuron without any reward. We found that approximately half of the visual neurons responded more strongly to the good than bad objects. In some neurons, this value-coding remained intact for a long time (textgreater1 year) after the last object-reward association learning. Notably, the neuronal discrimination of reward values started about 100 ms after the appearance of visual objects and lasted for more than 100 ms. These results provide evidence that SC neurons can discriminate objects by their historical (long-term) values. This object value information may be provided by the basal ganglia, especially the circuit originating from the tail of the caudate nucleus. The information may be used by the neural circuits inside SC for motor (saccade) output or may be sent to the circuits outside SC for future behavior. |
Diego A Gutnisky; Charles B Beaman; Sergio E Lew; Valentin Dragoi Spontaneous fluctuations in visual cortical responses influence population coding accuracy Journal Article Cerebral Cortex, 27 (2), pp. 1409–1427, 2017. @article{Gutnisky2017, title = {Spontaneous fluctuations in visual cortical responses influence population coding accuracy}, author = {Diego A Gutnisky and Charles B Beaman and Sergio E Lew and Valentin Dragoi}, doi = {10.1093/cercor/bhv312}, year = {2017}, date = {2017-01-01}, journal = {Cerebral Cortex}, volume = {27}, number = {2}, pages = {1409--1427}, abstract = {Information processing in the cerebral cortex depends not only on the nature of incoming stimuli, but also on the state of neuronal networks at the time of stimulation. That is, the same stimulus will be processed differently depending on the neuronal context in which it is received. A major factor that could influence neuronal context is the background, or ongoing neuronal activity before stimulation. In visual cortex, ongoing activity is known to play a critical role in the development of local circuits, yet whether it influences the coding of visual features in adult cortex is unclear. Here, we investigate whether and how the information encoded by individual neurons and populations in primary visual cortex (V1) depends on the ongoing activity before stimulus presentation. We report that when individual neurons are in a "low" prestimulus state, they have a higher capacity to discriminate stimulus features, such as orientation, despite their reduction in evoked responses. By measuring the distribution of prestimulus activity across a population of neurons, we found that network discrimination accuracy is improved in the low prestimulus state. Thus, the distribution of ongoing activity states across the network creates an "internal context" that dynamically filters incoming stimuli to modulate the accuracy of sensory coding. The modulation of stimulus coding by ongoing activity state is consistent with recurrent network models in which ongoing activity dynamically controls the balanced background excitation and inhibition to individual neurons.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Information processing in the cerebral cortex depends not only on the nature of incoming stimuli, but also on the state of neuronal networks at the time of stimulation. That is, the same stimulus will be processed differently depending on the neuronal context in which it is received. A major factor that could influence neuronal context is the background, or ongoing neuronal activity before stimulation. In visual cortex, ongoing activity is known to play a critical role in the development of local circuits, yet whether it influences the coding of visual features in adult cortex is unclear. Here, we investigate whether and how the information encoded by individual neurons and populations in primary visual cortex (V1) depends on the ongoing activity before stimulus presentation. We report that when individual neurons are in a "low" prestimulus state, they have a higher capacity to discriminate stimulus features, such as orientation, despite their reduction in evoked responses. By measuring the distribution of prestimulus activity across a population of neurons, we found that network discrimination accuracy is improved in the low prestimulus state. Thus, the distribution of ongoing activity states across the network creates an "internal context" that dynamically filters incoming stimuli to modulate the accuracy of sensory coding. The modulation of stimulus coding by ongoing activity state is consistent with recurrent network models in which ongoing activity dynamically controls the balanced background excitation and inhibition to individual neurons. |
Diego A Gutnisky; Charles Beaman; Sergio E Lew; Valentin Dragoi Cortical response states for enhanced sensory discrimination Journal Article eLife, 6 , pp. 1–23, 2017. @article{Gutnisky2017a, title = {Cortical response states for enhanced sensory discrimination}, author = {Diego A Gutnisky and Charles Beaman and Sergio E Lew and Valentin Dragoi}, doi = {10.7554/eLife.29226}, year = {2017}, date = {2017-01-01}, journal = {eLife}, volume = {6}, pages = {1--23}, abstract = {Brain activity during wakefulness is characterized by rapid fluctuations in neuronal responses. Whether these fluctuations play any role in modulating the accuracy of behavioral responses is poorly understood. Here, we investigated whether and how trial changes in the population response impact sensory coding in monkey V1 and perceptual performance. Although the responses of individual neurons varied widely across trials, many cells tended to covary with the local population. When population activity was in a 'low' state, neurons had lower evoked responses and correlated variability, yet higher probability to predict perceptual accuracy. The impact of firing rate fluctuations on network and perceptual accuracy was strongest 200-ms before stimulus presentation, and it greatly diminished when the number of cells used to measure the state of the population was decreased. These findings indicate that enhanced perceptual discrimination occurs when population activity is in a 'silent' response mode in which neurons increase information extraction.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Brain activity during wakefulness is characterized by rapid fluctuations in neuronal responses. Whether these fluctuations play any role in modulating the accuracy of behavioral responses is poorly understood. Here, we investigated whether and how trial changes in the population response impact sensory coding in monkey V1 and perceptual performance. Although the responses of individual neurons varied widely across trials, many cells tended to covary with the local population. When population activity was in a 'low' state, neurons had lower evoked responses and correlated variability, yet higher probability to predict perceptual accuracy. The impact of firing rate fluctuations on network and perceptual accuracy was strongest 200-ms before stimulus presentation, and it greatly diminished when the number of cells used to measure the state of the population was decreased. These findings indicate that enhanced perceptual discrimination occurs when population activity is in a 'silent' response mode in which neurons increase information extraction. |
Marcel Jan de Haan; Thomas Brochier; Sonja Grün; Alexa Riehle; Frédéric V Barthélemy Real-time visuomotor behavior and electrophysiology recording setup for use with humans and monkeys Journal Article Journal of Neurophysiology, 120 (2), pp. 539–552, 2018. @article{Haan2018a, title = {Real-time visuomotor behavior and electrophysiology recording setup for use with humans and monkeys}, author = {Marcel Jan de Haan and Thomas Brochier and Sonja Grün and Alexa Riehle and Frédéric V Barthélemy}, doi = {10.1152/jn.00262.2017}, year = {2018}, date = {2018-01-01}, journal = {Journal of Neurophysiology}, volume = {120}, number = {2}, pages = {539--552}, abstract = {Large-scale network dynamics in multiple visuomotor areas is of great interest in the study of eye-hand coordination in both human and monkey. To explore this, it is essential to develop a setup that allows for precise tracking of eye and hand movements. It is desirable that it is able to generate mechanical or visual perturbations of hand trajec- tories so that eye-hand coordination can be studied in a variety of conditions. There are simple solutions that satisfy these requirements for hand movements performed in the horizontal plane while visual stimuli and hand feedback are presented in the vertical plane. How- ever, this spatial dissociation requires cognitive rules for eye-hand coordination different from eye-hand movements performed in the same space, as is the case in most natural conditions. Here we present an innovative solution for the precise tracking of eye and hand movements in a single reference frame. Importantly, our solution allows behavioral explorations under normal and perturbed conditions in both humans and monkeys. It is based on the integration of two noninvasive commercially available systems to achieve online control and synchronous recording of eye (EyeLink) and hand (KINARM) positions during interactive visuomotor tasks. We also present an eye calibration method compatible with different eye trackers that com- pensates for nonlinearities caused by the system's geometry. Our setup monitors the two effectors in real time with high spatial and temporal resolution and simultaneously outputs behavioral and neu- ronal data to an external data acquisition system using a common data format.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Large-scale network dynamics in multiple visuomotor areas is of great interest in the study of eye-hand coordination in both human and monkey. To explore this, it is essential to develop a setup that allows for precise tracking of eye and hand movements. It is desirable that it is able to generate mechanical or visual perturbations of hand trajec- tories so that eye-hand coordination can be studied in a variety of conditions. There are simple solutions that satisfy these requirements for hand movements performed in the horizontal plane while visual stimuli and hand feedback are presented in the vertical plane. How- ever, this spatial dissociation requires cognitive rules for eye-hand coordination different from eye-hand movements performed in the same space, as is the case in most natural conditions. Here we present an innovative solution for the precise tracking of eye and hand movements in a single reference frame. Importantly, our solution allows behavioral explorations under normal and perturbed conditions in both humans and monkeys. It is based on the integration of two noninvasive commercially available systems to achieve online control and synchronous recording of eye (EyeLink) and hand (KINARM) positions during interactive visuomotor tasks. We also present an eye calibration method compatible with different eye trackers that com- pensates for nonlinearities caused by the system's geometry. Our setup monitors the two effectors in real time with high spatial and temporal resolution and simultaneously outputs behavioral and neu- ronal data to an external data acquisition system using a common data format. |
Gerald Hahn; Adrian Ponce-Alvarez; Cyril Monier; Giacomo Benvenuti; Arvind Kumar; Frédéric Chavane; Gustavo Deco; Yves Frégnac Spontaneous cortical activity is transiently poised close to criticality Journal Article PLoS Computational Biology, 13 (5), pp. 1–29, 2017. @article{Hahn2017, title = {Spontaneous cortical activity is transiently poised close to criticality}, author = {Gerald Hahn and Adrian Ponce-Alvarez and Cyril Monier and Giacomo Benvenuti and Arvind Kumar and Frédéric Chavane and Gustavo Deco and Yves Frégnac}, doi = {10.1371/journal.pcbi.1005543}, year = {2017}, date = {2017-01-01}, journal = {PLoS Computational Biology}, volume = {13}, number = {5}, pages = {1--29}, abstract = {Brain activity displays a large repertoire of dynamics across the sleep-wake cycle and even during anesthesia. It was suggested that criticality could serve as a unifying principle underlying the diversity of dynamics. This view has been supported by the observation of spontaneous bursts of cortical activity with scale-invariant sizes and durations, known as neuronal avalanches, in recordings of mesoscopic cortical signals. However, the existence of neuronal avalanches in spiking activity has been equivocal with studies reporting both its presence and absence. Here, we show that signs of criticality in spiking activity can change between synchronized and desynchronized cortical states. We analyzed the spontaneous activity in the primary visual cortex of the anesthetized cat and the awake monkey, and found that neuronal avalanches and thermodynamic indicators of criticality strongly depend on collective synchrony among neurons, LFP fluctuations, and behavioral state. We found that synchronized states are associated to criticality, large dynamical repertoire and prolonged epochs of eye closure, while desynchronized states are associated to sub-criticality, reduced dynamical repertoire, and eyes open conditions. Our results show that criticality in cortical dynamics is not stationary, but fluctuates during anesthesia and between different vigilance states.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Brain activity displays a large repertoire of dynamics across the sleep-wake cycle and even during anesthesia. It was suggested that criticality could serve as a unifying principle underlying the diversity of dynamics. This view has been supported by the observation of spontaneous bursts of cortical activity with scale-invariant sizes and durations, known as neuronal avalanches, in recordings of mesoscopic cortical signals. However, the existence of neuronal avalanches in spiking activity has been equivocal with studies reporting both its presence and absence. Here, we show that signs of criticality in spiking activity can change between synchronized and desynchronized cortical states. We analyzed the spontaneous activity in the primary visual cortex of the anesthetized cat and the awake monkey, and found that neuronal avalanches and thermodynamic indicators of criticality strongly depend on collective synchrony among neurons, LFP fluctuations, and behavioral state. We found that synchronized states are associated to criticality, large dynamical repertoire and prolonged epochs of eye closure, while desynchronized states are associated to sub-criticality, reduced dynamical repertoire, and eyes open conditions. Our results show that criticality in cortical dynamics is not stationary, but fluctuates during anesthesia and between different vigilance states. |
R E Hampson; Ioan Opris; S A Deadwyler Neural correlates of fast pupil dilation in nonhuman primates: Relation to behavioral performance and cognitive workload Journal Article Behavioural Brain Research, 212 (1), pp. 1–11, 2010. @article{Hampson2010, title = {Neural correlates of fast pupil dilation in nonhuman primates: Relation to behavioral performance and cognitive workload}, author = {R E Hampson and Ioan Opris and S A Deadwyler}, doi = {10.1016/j.bbr.2010.03.011}, year = {2010}, date = {2010-01-01}, journal = {Behavioural Brain Research}, volume = {212}, number = {1}, pages = {1--11}, publisher = {Elsevier B.V.}, abstract = {Pupil dilation in humans has been previously shown to correlate with cognitive workload, whereby increased frequency of dilation is associated with increased degree of difficulty of a task. It has been suggested that frontal oculomotor brain areas control cognitively related pupil dilations, but this has not been confirmed due to lack of animal models of cognitive workload and task-related pupil dilation. This is the first report of a wavelet analysis applied to continuous measures of pupil size used to detect the onset of abrupt pupil dilations and the frequency of those dilations in nonhuman primates (NHPs) performing a trial-unique delayed-match-to-sample (DMS) task. A unique finding shows that electrophysiological recordings in the same animals revealed firing of neurons in frontal cortex correlated to different components of pupil dilation during task performance. It is further demonstrated that the frequency of fast pupil dilations (but not rate of eye movements) correlated with cognitive workload during task performance. Such correlations suggest that frontal neuron encoding of pupil dilation provides critical feedback to other brain areas involved in the processing of complex visual information.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Pupil dilation in humans has been previously shown to correlate with cognitive workload, whereby increased frequency of dilation is associated with increased degree of difficulty of a task. It has been suggested that frontal oculomotor brain areas control cognitively related pupil dilations, but this has not been confirmed due to lack of animal models of cognitive workload and task-related pupil dilation. This is the first report of a wavelet analysis applied to continuous measures of pupil size used to detect the onset of abrupt pupil dilations and the frequency of those dilations in nonhuman primates (NHPs) performing a trial-unique delayed-match-to-sample (DMS) task. A unique finding shows that electrophysiological recordings in the same animals revealed firing of neurons in frontal cortex correlated to different components of pupil dilation during task performance. It is further demonstrated that the frequency of fast pupil dilations (but not rate of eye movements) correlated with cognitive workload during task performance. Such correlations suggest that frontal neuron encoding of pupil dilation provides critical feedback to other brain areas involved in the processing of complex visual information. |
Bryan J Hansen; Mircea I Chelaru; Valentin Dragoi Correlated variability in laminar cortical circuits Journal Article Neuron, 76 (3), pp. 590–602, 2012. @article{Hansen2012, title = {Correlated variability in laminar cortical circuits}, author = {Bryan J Hansen and Mircea I Chelaru and Valentin Dragoi}, doi = {10.1016/j.neuron.2012.08.029}, year = {2012}, date = {2012-01-01}, journal = {Neuron}, volume = {76}, number = {3}, pages = {590--602}, publisher = {Elsevier Inc.}, abstract = {Despite the fact that strong trial-to-trial correlated variability in responses has been reported in many cortical areas, recent evidence suggests that neuronal correlations are much lower than previously thought. Here, we used multicontact laminar probes to revisit the issue of correlated variability in primary visual (V1) cortical circuits. We found that correlations between neurons depend strongly on local network context-whereas neurons in the input (granular) layers showed virtually no correlated variability, neurons in the output layers (supragranular and infragranular) exhibited strong correlations. The laminar dependence of noise correlations is consistent with recurrent models in which neurons in the granular layer receive intracortical inputs from nearby cells, whereas supragranular and infragranular layer neurons receive inputs over larger distances. Contrary to expectation that the output cortical layers encode stimulus information most accurately, we found that the input network offers superior discrimination performance compared to the output networks.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Despite the fact that strong trial-to-trial correlated variability in responses has been reported in many cortical areas, recent evidence suggests that neuronal correlations are much lower than previously thought. Here, we used multicontact laminar probes to revisit the issue of correlated variability in primary visual (V1) cortical circuits. We found that correlations between neurons depend strongly on local network context-whereas neurons in the input (granular) layers showed virtually no correlated variability, neurons in the output layers (supragranular and infragranular) exhibited strong correlations. The laminar dependence of noise correlations is consistent with recurrent models in which neurons in the granular layer receive intracortical inputs from nearby cells, whereas supragranular and infragranular layer neurons receive inputs over larger distances. Contrary to expectation that the output cortical layers encode stimulus information most accurately, we found that the input network offers superior discrimination performance compared to the output networks. |
Till S Hartmann; Frank Bremmer; Thomas D Albright; Bart Krekelberg Receptive field positions in area MT during slow eye movements Journal Article Journal of Neuroscience, 31 (29), pp. 10437–10444, 2011. @article{Hartmann2011, title = {Receptive field positions in area MT during slow eye movements}, author = {Till S Hartmann and Frank Bremmer and Thomas D Albright and Bart Krekelberg}, doi = {10.1523/JNEUROSCI.5590-10.2011}, year = {2011}, date = {2011-01-01}, journal = {Journal of Neuroscience}, volume = {31}, number = {29}, pages = {10437--10444}, abstract = {Perceptual stability requires the integration of information across eye movements. We first tested the hypothesis that motion signals are integrated by neurons whose receptive fields (RFs) do not move with the eye but stay fixed in the world. Specifically, we measured the RF properties of neurons in the middle temporal area (MT) of macaques (Macaca mulatta) during the slow phase of optokinetic nystagmus. Using a novel method to estimate RF locations for both spikes and local field potentials, we found that the location on the retina that changed spike rates or local field potentials did not change with eye position; RFs moved with the eye. Second, we tested the hypothesis that neurons link information across eye positions by remapping the retinal location of their RFs to future locations. To test this, we compared RF locations during leftward and rightward slow phases of optokinetic nystagmus. We found no evidence for remapping during slow eye movements; the RF location was not affected by eye-movement direction. Together, our results show that RFs of MT neurons and the aggregate activity reflected in local field potentials are yoked to the eye during slow eye movements. This implies that individual MT neurons do not integrate sensory information from a single position in the world across eye movements. Future research will have to determine whether such integration, and the construction of perceptual stability, takes place in the form of a distributed population code in eye-centered visual cortex or is deferred to downstream areas.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Perceptual stability requires the integration of information across eye movements. We first tested the hypothesis that motion signals are integrated by neurons whose receptive fields (RFs) do not move with the eye but stay fixed in the world. Specifically, we measured the RF properties of neurons in the middle temporal area (MT) of macaques (Macaca mulatta) during the slow phase of optokinetic nystagmus. Using a novel method to estimate RF locations for both spikes and local field potentials, we found that the location on the retina that changed spike rates or local field potentials did not change with eye position; RFs moved with the eye. Second, we tested the hypothesis that neurons link information across eye positions by remapping the retinal location of their RFs to future locations. To test this, we compared RF locations during leftward and rightward slow phases of optokinetic nystagmus. We found no evidence for remapping during slow eye movements; the RF location was not affected by eye-movement direction. Together, our results show that RFs of MT neurons and the aggregate activity reflected in local field potentials are yoked to the eye during slow eye movements. This implies that individual MT neurons do not integrate sensory information from a single position in the world across eye movements. Future research will have to determine whether such integration, and the construction of perceptual stability, takes place in the form of a distributed population code in eye-centered visual cortex or is deferred to downstream areas. |
S A Hassani; M Oemisch; M Balcarras; S Westendorff; S Ardid; M A Van Der Meer; P Tiesinga; T Womelsdorf Scientific Reports, 7 , pp. 1–19, 2017. @article{Hassani2017, title = {A computational psychiatry approach identifies how alpha-2A noradrenergic agonist Guanfacine affects feature-based reinforcement learning in the macaque}, author = {S A Hassani and M Oemisch and M Balcarras and S Westendorff and S Ardid and M A {Van Der Meer} and P Tiesinga and T Womelsdorf}, doi = {10.1038/srep40606}, year = {2017}, date = {2017-01-01}, journal = {Scientific Reports}, volume = {7}, pages = {1--19}, publisher = {Nature Publishing Group}, abstract = {Noradrenaline is believed to support cognitive flexibility through the alpha 2A noradrenergic receptor (a2A-NAR) acting in prefrontal cortex. Enhanced flexibility has been inferred from improved working memory with the a2A-NA agonist Guanfacine. But it has been unclear whether Guanfacine improves specific attention and learning mechanisms beyond working memory, and whether the drug effects can be formalized computationally to allow single subject predictions. We tested and confirmed these suggestions in a case study with a healthy nonhuman primate performing a feature-based reversal learning task evaluating performance using Bayesian and Reinforcement learning models. In an initial dose-testing phase we found a Guanfacine dose that increased performance accuracy, decreased distractibility and improved learning. In a second experimental phase using only that dose we examined the faster feature-based reversal learning with Guanfacine with single-subject computational modeling. Parameter estimation suggested that improved learning is not accounted for by varying a single reinforcement learning mechanism, but by changing the set of parameter values to higher learning rates and stronger suppression of non-chosen over chosen feature information. These findings provide an important starting point for developing nonhuman primate models to discern the synaptic mechanisms of attention and learning functions within the context of a computational neuropsychiatry framework.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Noradrenaline is believed to support cognitive flexibility through the alpha 2A noradrenergic receptor (a2A-NAR) acting in prefrontal cortex. Enhanced flexibility has been inferred from improved working memory with the a2A-NA agonist Guanfacine. But it has been unclear whether Guanfacine improves specific attention and learning mechanisms beyond working memory, and whether the drug effects can be formalized computationally to allow single subject predictions. We tested and confirmed these suggestions in a case study with a healthy nonhuman primate performing a feature-based reversal learning task evaluating performance using Bayesian and Reinforcement learning models. In an initial dose-testing phase we found a Guanfacine dose that increased performance accuracy, decreased distractibility and improved learning. In a second experimental phase using only that dose we examined the faster feature-based reversal learning with Guanfacine with single-subject computational modeling. Parameter estimation suggested that improved learning is not accounted for by varying a single reinforcement learning mechanism, but by changing the set of parameter values to higher learning rates and stronger suppression of non-chosen over chosen feature information. These findings provide an important starting point for developing nonhuman primate models to discern the synaptic mechanisms of attention and learning functions within the context of a computational neuropsychiatry framework. |
Christopher K Hauser; Dantong Zhu; Terrence R Stanford; Emilio Salinas Motor selection dynamics in FEF explain the reaction time variance of saccades to single targets Journal Article eLife, 7 , pp. 1–32, 2018. @article{Hauser2018, title = {Motor selection dynamics in FEF explain the reaction time variance of saccades to single targets}, author = {Christopher K Hauser and Dantong Zhu and Terrence R Stanford and Emilio Salinas}, doi = {10.7554/elife.33456}, year = {2018}, date = {2018-01-01}, journal = {eLife}, volume = {7}, pages = {1--32}, abstract = {In studies of voluntary movement, a most elemental quantity is the reaction time (RT) between the onset of a visual stimulus and a saccade toward it. However, this RT demonstrates extremely high variability which, in spite of extensive research, remains unexplained. It is well established that, when a visual target appears, oculomotor activity gradually builds up until a critical level is reached, at which point a saccade is triggered. Here, based on computational work and single-neuron recordings from monkey frontal eye field (FEF), we show that this rise-to-threshold process starts from a dynamic initial state that already contains other incipient, internally driven motor plans, which compete with the target-driven activity to varying degrees. The ensuing conflict resolution process, which manifests in subtle covariations between baseline activity, build-up rate, and threshold, consists of fundamentally deterministic interactions, and explains the observed RT distributions while invoking only a small amount of intrinsic randomness.As we examine the space around us our eyes move in short steps, looking toward a new location about four times a second. Neurons in a region of the brain called the frontal eye field help initiate these eye movements, which are known as saccades. Each neuron contributes to a saccade with a specific direction and size. Before a saccade, the relevant neurons in the frontal eye field steadily increase their activity. When this activity reaches a critical threshold, the visual system issues a command to move the eyes in the appropriate direction. So a saccade that moves the eyes to the right requires a specific group of neurons to be strongly activated – but, at the same time, the neurons responsible for movement to the left need to be less active.Imagine that you have to move your eyes as quickly as possible to look at a spot of light that appears on a screen. Some of the time your eyes will start to move about 100 milliseconds after the light appears. But on other attempts, your eyes will not start moving until 300 milliseconds after the light came on. What causes this variability?To find out, Hauser et al. recorded from neurons in monkeys trained to perform such a task. When the spot of light appeared many different neurons were active, suggesting there is conflict between the plan that would move the eyes toward the target and plans to look at other locations. That is, when the target appears, the monkey is already thinking of looking somewhere. The time required to resolve this conflict depends on how far apart the target and the competing locations are from one another, and on how much the competing neurons have increased their activity before the target appears.Similar mechanisms are likely to operate when we sit at the dinner table and look for the salt shaker, for example, and so the results presented by Hauser et al. will help us to understand how we direct our attention to different points in space. Understanding how these processes work in more detail will help us to discern what happens when they go wrong, as occurs in attention deficit disorders like ADHD.}, keywords = {}, pubstate = {published}, tppubtype = {article} } In studies of voluntary movement, a most elemental quantity is the reaction time (RT) between the onset of a visual stimulus and a saccade toward it. However, this RT demonstrates extremely high variability which, in spite of extensive research, remains unexplained. It is well established that, when a visual target appears, oculomotor activity gradually builds up until a critical level is reached, at which point a saccade is triggered. Here, based on computational work and single-neuron recordings from monkey frontal eye field (FEF), we show that this rise-to-threshold process starts from a dynamic initial state that already contains other incipient, internally driven motor plans, which compete with the target-driven activity to varying degrees. The ensuing conflict resolution process, which manifests in subtle covariations between baseline activity, build-up rate, and threshold, consists of fundamentally deterministic interactions, and explains the observed RT distributions while invoking only a small amount of intrinsic randomness.As we examine the space around us our eyes move in short steps, looking toward a new location about four times a second. Neurons in a region of the brain called the frontal eye field help initiate these eye movements, which are known as saccades. Each neuron contributes to a saccade with a specific direction and size. Before a saccade, the relevant neurons in the frontal eye field steadily increase their activity. When this activity reaches a critical threshold, the visual system issues a command to move the eyes in the appropriate direction. So a saccade that moves the eyes to the right requires a specific group of neurons to be strongly activated – but, at the same time, the neurons responsible for movement to the left need to be less active.Imagine that you have to move your eyes as quickly as possible to look at a spot of light that appears on a screen. Some of the time your eyes will start to move about 100 milliseconds after the light appears. But on other attempts, your eyes will not start moving until 300 milliseconds after the light came on. What causes this variability?To find out, Hauser et al. recorded from neurons in monkeys trained to perform such a task. When the spot of light appeared many different neurons were active, suggesting there is conflict between the plan that would move the eyes toward the target and plans to look at other locations. That is, when the target appears, the monkey is already thinking of looking somewhere. The time required to resolve this conflict depends on how far apart the target and the competing locations are from one another, and on how much the competing neurons have increased their activity before the target appears.Similar mechanisms are likely to operate when we sit at the dinner table and look for the salt shaker, for example, and so the results presented by Hauser et al. will help us to understand how we direct our attention to different points in space. Understanding how these processes work in more detail will help us to discern what happens when they go wrong, as occurs in attention deficit disorders like ADHD. |
Benjamin Y Hayden; Jack L Gallant Time course of attention reveals different mechanisms for spatial and feature-based attention in area V4 Journal Article Neuron, 47 (5), pp. 637–643, 2005. @article{Hayden2005, title = {Time course of attention reveals different mechanisms for spatial and feature-based attention in area V4}, author = {Benjamin Y Hayden and Jack L Gallant}, doi = {10.1016/j.neuron.2005.07.020}, year = {2005}, date = {2005-01-01}, journal = {Neuron}, volume = {47}, number = {5}, pages = {637--643}, abstract = {Attention can facilitate visual processing, emphasizing specific locations and highlighting stimuli containing specific features. To dissociate the mechanisms of spatial and feature-based attention, we compared the time course of visually evoked responses under different attention conditions. We recorded from single neurons in area V4 during a delayed match-to-sample task that controlled both spatial and feature-based attention. Neuronal responses increased when spatial attention was directed toward the receptive field and were modulated by the identity of the target of feature-based attention. Modulation by spatial attention was weaker during the early portion of the visual response and stronger during the later portion of the response. In contrast, modulation by feature-based attention was relatively constant throughout the response. It appears that stimulus onset transients disrupt spatial attention, but not feature attention. We conclude that spatial attention reflects a combination of stimulus-driven and goal-driven processes, while feature-based attention is purely goal driven.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Attention can facilitate visual processing, emphasizing specific locations and highlighting stimuli containing specific features. To dissociate the mechanisms of spatial and feature-based attention, we compared the time course of visually evoked responses under different attention conditions. We recorded from single neurons in area V4 during a delayed match-to-sample task that controlled both spatial and feature-based attention. Neuronal responses increased when spatial attention was directed toward the receptive field and were modulated by the identity of the target of feature-based attention. Modulation by spatial attention was weaker during the early portion of the visual response and stronger during the later portion of the response. In contrast, modulation by feature-based attention was relatively constant throughout the response. It appears that stimulus onset transients disrupt spatial attention, but not feature attention. We conclude that spatial attention reflects a combination of stimulus-driven and goal-driven processes, while feature-based attention is purely goal driven. |
Benjamin Y Hayden; Michael L Platt Temporal discounting predicts risk sensitivity in rhesus macaques Journal Article Current Biology, 17 (1), pp. 49–53, 2007. @article{Hayden2007, title = {Temporal discounting predicts risk sensitivity in rhesus macaques}, author = {Benjamin Y Hayden and Michael L Platt}, doi = {10.1016/j.cub.2006.10.055}, year = {2007}, date = {2007-01-01}, journal = {Current Biology}, volume = {17}, number = {1}, pages = {49--53}, abstract = {Humans and animals tend both to avoid uncertainty and to prefer immediate over future rewards. The comorbidity of psychiatric disorders such as impulsivity, problem gambling, and addiction suggests that a common mechanism may underlie risk sensitivity and temporal discounting [1-6]. Nonetheless, the precise relationship between these two traits remains largely unknown [3, 5]. To examine whether risk sensitivity and temporal discounting reflect a common process, we recorded choices made by two rhesus macaques in a visual gambling task [7] while we varied the delay between trials. We found that preference for the risky option declined with increasing delay between sequential choices in the task, even when all other task parameters were held constant. These results were quantitatively predicted by a model that assumed that the subjective expected utility of the risky option is evaluated based on the expected time of the larger payoff [5, 6]. The importance of the larger payoff in this model suggests that the salience of larger payoffs played a critical role in determining the value of risky options. These data suggest that risk sensitivity may be a product of other cognitive processes, and specifically that myopia for the future and the salience of jackpots control the propensity to take a gamble.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Humans and animals tend both to avoid uncertainty and to prefer immediate over future rewards. The comorbidity of psychiatric disorders such as impulsivity, problem gambling, and addiction suggests that a common mechanism may underlie risk sensitivity and temporal discounting [1-6]. Nonetheless, the precise relationship between these two traits remains largely unknown [3, 5]. To examine whether risk sensitivity and temporal discounting reflect a common process, we recorded choices made by two rhesus macaques in a visual gambling task [7] while we varied the delay between trials. We found that preference for the risky option declined with increasing delay between sequential choices in the task, even when all other task parameters were held constant. These results were quantitatively predicted by a model that assumed that the subjective expected utility of the risky option is evaluated based on the expected time of the larger payoff [5, 6]. The importance of the larger payoff in this model suggests that the salience of larger payoffs played a critical role in determining the value of risky options. These data suggest that risk sensitivity may be a product of other cognitive processes, and specifically that myopia for the future and the salience of jackpots control the propensity to take a gamble. |
Benjamin Y Hayden; Sarah R Heilbronner; Amrita C Nair; Michael L Platt Cognitive influences on risk-seeking by rhesus macaques Journal Article Judgement and Decision Making, 3 (5), pp. 389–395, 2008. @article{Hayden2008, title = {Cognitive influences on risk-seeking by rhesus macaques}, author = {Benjamin Y Hayden and Sarah R Heilbronner and Amrita C Nair and Michael L Platt}, doi = {10.1016/j.biotechadv.2011.08.021.Secreted}, year = {2008}, date = {2008-01-01}, journal = {Judgement and Decision Making}, volume = {3}, number = {5}, pages = {389--395}, abstract = {Humans and other animals are idiosyncratically sensitive to risk, either preferring or avoiding options having the same value but differing in uncertainty. Many explanations for risk sensitivity rely on the non-linear shape of a hypothesized utility curve. Because such models do not place any importance on uncertainty per se, utility curve-based accounts predict indifference between risky and riskless options that offer the same distribution of rewards. Here we show that monkeys strongly prefer uncertain gambles to alternating rewards with the same payoffs, demonstrating that uncertainty itself contributes to the appeal of risky options. Based on prior observations, we hypothesized that the appeal of the risky option is enhanced by the salience of the potential jackpot. To test this, we subtly manipulated payoffs in a second gambling task. We found that monkeys are more sensitive to small changes in the size of the large reward than to equivalent changes in the size of the small reward, indicating that they attend preferentially to the jackpots. Together, these results challenge utility curve-based accounts of risk sensitivity, and suggest that psychological factors, such as outcome salience and uncertainty itself, contribute to risky decision-making.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Humans and other animals are idiosyncratically sensitive to risk, either preferring or avoiding options having the same value but differing in uncertainty. Many explanations for risk sensitivity rely on the non-linear shape of a hypothesized utility curve. Because such models do not place any importance on uncertainty per se, utility curve-based accounts predict indifference between risky and riskless options that offer the same distribution of rewards. Here we show that monkeys strongly prefer uncertain gambles to alternating rewards with the same payoffs, demonstrating that uncertainty itself contributes to the appeal of risky options. Based on prior observations, we hypothesized that the appeal of the risky option is enhanced by the salience of the potential jackpot. To test this, we subtly manipulated payoffs in a second gambling task. We found that monkeys are more sensitive to small changes in the size of the large reward than to equivalent changes in the size of the small reward, indicating that they attend preferentially to the jackpots. Together, these results challenge utility curve-based accounts of risk sensitivity, and suggest that psychological factors, such as outcome salience and uncertainty itself, contribute to risky decision-making. |
Benjamin Y Hayden; Amrita C Nair; Allison N McCoy; Michael L Platt Posterior cingulate cortex mediates outcome-contingent allocation of behavior Journal Article Neuron, 60 (1), pp. 19–25, 2008. @article{Hayden2008a, title = {Posterior cingulate cortex mediates outcome-contingent allocation of behavior}, author = {Benjamin Y Hayden and Amrita C Nair and Allison N McCoy and Michael L Platt}, doi = {10.1016/j.neuron.2008.09.012}, year = {2008}, date = {2008-01-01}, journal = {Neuron}, volume = {60}, number = {1}, pages = {19--25}, abstract = {Adaptive decision making requires selecting an action and then monitoring its consequences to improve future decisions. The neuronal mechanisms supporting action evaluation and subsequent behavioral modification, however, remain poorly understood. To investigate the contribution of posterior cingulate cortex (CGp) to these processes, we recorded activity of single neurons in monkeys performing a gambling task in which the reward outcome of each choice strongly influenced subsequent choices. We found that CGp neurons signaled reward outcomes in a nonlinear fashion and that outcome-contingent modulations in firing rate persisted into subsequent trials. Moreover, firing rate on any one trial predicted switching to the alternative option on the next trial. Finally, microstimulation in CGp following risky choices promoted a preference reversal for the safe option on the following trial. Collectively, these results demonstrate that CGp directly contributes to the evaluative processes that support dynamic changes in decision making in volatile environments.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Adaptive decision making requires selecting an action and then monitoring its consequences to improve future decisions. The neuronal mechanisms supporting action evaluation and subsequent behavioral modification, however, remain poorly understood. To investigate the contribution of posterior cingulate cortex (CGp) to these processes, we recorded activity of single neurons in monkeys performing a gambling task in which the reward outcome of each choice strongly influenced subsequent choices. We found that CGp neurons signaled reward outcomes in a nonlinear fashion and that outcome-contingent modulations in firing rate persisted into subsequent trials. Moreover, firing rate on any one trial predicted switching to the alternative option on the next trial. Finally, microstimulation in CGp following risky choices promoted a preference reversal for the safe option on the following trial. Collectively, these results demonstrate that CGp directly contributes to the evaluative processes that support dynamic changes in decision making in volatile environments. |
Benjamin Y Hayden; Jack L Gallant Combined effects of spatial and feature-based attention on responses of V4 neurons Journal Article Vision Research, 49 (10), pp. 1182–1187, 2009. @article{Hayden2009, title = {Combined effects of spatial and feature-based attention on responses of V4 neurons}, author = {Benjamin Y Hayden and Jack L Gallant}, doi = {10.1016/j.visres.2008.06.011}, year = {2009}, date = {2009-01-01}, journal = {Vision Research}, volume = {49}, number = {10}, pages = {1182--1187}, publisher = {Elsevier Ltd}, abstract = {Attention is thought to be controlled by a specialized fronto-parietal network that modulates the responses of neurons in sensory and association cortex. However, the principles by which this network affects the responses of these sensory and association neurons remains unknown. In particular, it remains unclear whether different forms of attention, such as spatial and feature-based attention, independently modulate responses of single neurons. We recorded responses of single V4 neurons in a task that controls both forms of attention independently. We find that the combined effects of spatial and feature-based attention can be described as the sum of independent processes with a small super-additive interaction term. This pattern of effects demonstrates that the spatial and feature-based aspects of the attentional control system can independently affect responses of single neurons. These results are consistent with the idea that spatial and feature-based attention are controlled by distinct neural substrates whose effects combine synergistically to influence responses of visual neurons.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Attention is thought to be controlled by a specialized fronto-parietal network that modulates the responses of neurons in sensory and association cortex. However, the principles by which this network affects the responses of these sensory and association neurons remains unknown. In particular, it remains unclear whether different forms of attention, such as spatial and feature-based attention, independently modulate responses of single neurons. We recorded responses of single V4 neurons in a task that controls both forms of attention independently. We find that the combined effects of spatial and feature-based attention can be described as the sum of independent processes with a small super-additive interaction term. This pattern of effects demonstrates that the spatial and feature-based aspects of the attentional control system can independently affect responses of single neurons. These results are consistent with the idea that spatial and feature-based attention are controlled by distinct neural substrates whose effects combine synergistically to influence responses of visual neurons. |
Benjamin Y Hayden; David V Smith; Michael L Platt Electrophysiological correlates of default-mode processing in macaque posterior cingulate cortex Journal Article Proceedings of the National Academy of Sciences, 106 (14), pp. 5948–5953, 2009. @article{Hayden2009a, title = {Electrophysiological correlates of default-mode processing in macaque posterior cingulate cortex}, author = {Benjamin Y Hayden and David V Smith and Michael L Platt}, doi = {10.1073/pnas.0812035106}, year = {2009}, date = {2009-01-01}, journal = {Proceedings of the National Academy of Sciences}, volume = {106}, number = {14}, pages = {5948--5953}, abstract = {During the course of daily activity, our level of engagement with the world varies on a moment-to-moment basis. Although these fluctuations in vigilance have critical consequences for our thoughts and actions, almost nothing is known about the neuronal substrates governing such dynamic variations in task engagement. We investigated the hypothesis that the posterior cingulate cortex (CGp), a region linked to default-mode processing by hemodynamic and metabolic measures, controls such variations. We recorded the activity of single neurons in CGp in 2 macaque monkeys performing simple tasks in which their behavior varied from vigilant to inattentive. We found that firing rates were reliably suppressed during task performance and returned to a higher resting baseline between trials. Importantly, higher firing rates predicted errors and slow behavioral responses, and were also observed during cued rest periods when monkeys were temporarily liberated from exteroceptive vigilance. These patterns of activity were not observed in the lateral intraparietal area, an area linked to the frontoparietal attention network. Our findings provide physiological confirmation that CGp mediates exteroceptive vigilance and are consistent with the idea that CGp is part of the "default network" of brain areas associated with control of task engagement.}, keywords = {}, pubstate = {published}, tppubtype = {article} } During the course of daily activity, our level of engagement with the world varies on a moment-to-moment basis. Although these fluctuations in vigilance have critical consequences for our thoughts and actions, almost nothing is known about the neuronal substrates governing such dynamic variations in task engagement. We investigated the hypothesis that the posterior cingulate cortex (CGp), a region linked to default-mode processing by hemodynamic and metabolic measures, controls such variations. We recorded the activity of single neurons in CGp in 2 macaque monkeys performing simple tasks in which their behavior varied from vigilant to inattentive. We found that firing rates were reliably suppressed during task performance and returned to a higher resting baseline between trials. Importantly, higher firing rates predicted errors and slow behavioral responses, and were also observed during cued rest periods when monkeys were temporarily liberated from exteroceptive vigilance. These patterns of activity were not observed in the lateral intraparietal area, an area linked to the frontoparietal attention network. Our findings provide physiological confirmation that CGp mediates exteroceptive vigilance and are consistent with the idea that CGp is part of the "default network" of brain areas associated with control of task engagement. |
Benjamin Y Hayden; Sarah R Heilbronner; Michael L Platt Ambiguity aversion in rhesus macaques Journal Article Frontiers in Neuroscience, 4 , pp. 1–7, 2010. @article{Hayden2010, title = {Ambiguity aversion in rhesus macaques}, author = {Benjamin Y Hayden and Sarah R Heilbronner and Michael L Platt}, doi = {10.3389/fnins.2010.00166}, year = {2010}, date = {2010-01-01}, journal = {Frontiers in Neuroscience}, volume = {4}, pages = {1--7}, publisher = {10}, address = {doi}, abstract = {People generally prefer risky options, which have fully specified outcome probabilities, to ambiguous options, which have unspecified probabilities. This preference, formalized in economics, is strong enough that people will reliably prefer a risky option to an ambiguous option with a greater expected value. Explanations for ambiguity aversion often invoke uniquely human faculties like language, self-justification, or a desire to avoid public embarrassment. Challenging these ideas, here we demonstrate that a preference for unambiguous options is shared with rhesus macaques. We trained four monkeys to choose between pairs of options that both offered explicitly cued probabilities of large and small juice outcomes. We then introduced occasional trials where one of the options was obscured and examined their resulting preferences; we ran humans in a parallel experiment on a nearly identical task. We found that monkeys reliably preferred risky options to ambiguous ones, even when this bias was costly, closely matching the behavior of humans in the analogous task. Notably, ambiguity aversion varied parametrically with the extent of ambiguity. As expected, ambiguity aversion gradually declined as monkeys learned the underlying probability distribution of rewards. These data indicate that ambiguity aversion reflects fundamental cognitive biases shared with other animals rather than uniquely human factors guiding decisions.}, keywords = {}, pubstate = {published}, tppubtype = {article} } People generally prefer risky options, which have fully specified outcome probabilities, to ambiguous options, which have unspecified probabilities. This preference, formalized in economics, is strong enough that people will reliably prefer a risky option to an ambiguous option with a greater expected value. Explanations for ambiguity aversion often invoke uniquely human faculties like language, self-justification, or a desire to avoid public embarrassment. Challenging these ideas, here we demonstrate that a preference for unambiguous options is shared with rhesus macaques. We trained four monkeys to choose between pairs of options that both offered explicitly cued probabilities of large and small juice outcomes. We then introduced occasional trials where one of the options was obscured and examined their resulting preferences; we ran humans in a parallel experiment on a nearly identical task. We found that monkeys reliably preferred risky options to ambiguous ones, even when this bias was costly, closely matching the behavior of humans in the analogous task. Notably, ambiguity aversion varied parametrically with the extent of ambiguity. As expected, ambiguity aversion gradually declined as monkeys learned the underlying probability distribution of rewards. These data indicate that ambiguity aversion reflects fundamental cognitive biases shared with other animals rather than uniquely human factors guiding decisions. |
Benjamin Y Hayden; Michael L Platt Neurons in anterior cingulate cortex multiplex information about reward and action Journal Article Journal of Neuroscience, 30 (9), pp. 3339–3346, 2010. @article{Hayden2010a, title = {Neurons in anterior cingulate cortex multiplex information about reward and action}, author = {Benjamin Y Hayden and Michael L Platt}, doi = {10.1523/JNEUROSCI.4874-09.2010}, year = {2010}, date = {2010-01-01}, journal = {Journal of Neuroscience}, volume = {30}, number = {9}, pages = {3339--3346}, abstract = {The dorsal anterior cingulate cortex (dACC) is thought to play a critical role in forming associations between rewards and actions. Currently available physiological data, however, remain inconclusive regarding the question of whether dACC neurons carry information linking particular actions to reward or, instead, encode abstract reward information independent of specific actions. Here we show that firing rates of a majority of dACC neurons in a population studied in an eight-option variably rewarded choice task were sensitive to both saccade direction and reward value. Furthermore, the influences of reward and saccade direction on neuronal activity were approximately equal in magnitude over the range of rewards tested and were statistically independent. Our results indicate that dACC neurons multiplex information about both reward and action, endorsing the idea that this area links motivational outcomes to behavior and undermining the notion that its neurons solely contribute to reward processing in the abstract.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The dorsal anterior cingulate cortex (dACC) is thought to play a critical role in forming associations between rewards and actions. Currently available physiological data, however, remain inconclusive regarding the question of whether dACC neurons carry information linking particular actions to reward or, instead, encode abstract reward information independent of specific actions. Here we show that firing rates of a majority of dACC neurons in a population studied in an eight-option variably rewarded choice task were sensitive to both saccade direction and reward value. Furthermore, the influences of reward and saccade direction on neuronal activity were approximately equal in magnitude over the range of rewards tested and were statistically independent. Our results indicate that dACC neurons multiplex information about both reward and action, endorsing the idea that this area links motivational outcomes to behavior and undermining the notion that its neurons solely contribute to reward processing in the abstract. |
Benjamin Y Hayden; David V Smith; Michael L Platt Cognitive control signals in posterior cingulate cortex Journal Article Frontiers in Human Neuroscience, 4 , pp. 1–8, 2010. @article{Hayden2010b, title = {Cognitive control signals in posterior cingulate cortex}, author = {Benjamin Y Hayden and David V Smith and Michael L Platt}, doi = {10.3389/fnhum.2010.00223}, year = {2010}, date = {2010-01-01}, journal = {Frontiers in Human Neuroscience}, volume = {4}, pages = {1--8}, publisher = {10}, address = {doi}, abstract = {Efficiently shifting between tasks is a central function of cognitive control. The role of the default network - a constellation of areas with high baseline activity that declines during task performance - in cognitive control remains poorly understood. We hypothesized that task switching demands cognitive control to shift the balance of processing toward the external world, and therefore predicted that switching between the two tasks would require suppression of activity of neurons within the posterior cingulate cortex (CGp). To test this idea, we recorded the activity of single neurons in CGp, a central node in the default network, in monkeys performing two interleaved tasks. As predicted, we found that basal levels of neuronal activity were reduced following a switch from one task to another and gradually returned to pre-switch baseline on subsequent trials. We failed to observe these effects in lateral intraparietal cortex, part of the dorsal fronto-parietal cortical attention network directly connected to CGp. These findings indicate that suppression of neuronal activity in CGp facilitates cognitive control, and suggest that activity in the default network reflects processes that directly compete with control processes elsewhere in the brain.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Efficiently shifting between tasks is a central function of cognitive control. The role of the default network - a constellation of areas with high baseline activity that declines during task performance - in cognitive control remains poorly understood. We hypothesized that task switching demands cognitive control to shift the balance of processing toward the external world, and therefore predicted that switching between the two tasks would require suppression of activity of neurons within the posterior cingulate cortex (CGp). To test this idea, we recorded the activity of single neurons in CGp, a central node in the default network, in monkeys performing two interleaved tasks. As predicted, we found that basal levels of neuronal activity were reduced following a switch from one task to another and gradually returned to pre-switch baseline on subsequent trials. We failed to observe these effects in lateral intraparietal cortex, part of the dorsal fronto-parietal cortical attention network directly connected to CGp. These findings indicate that suppression of neuronal activity in CGp facilitates cognitive control, and suggest that activity in the default network reflects processes that directly compete with control processes elsewhere in the brain. |
Benjamin Y Hayden; Sarah R Heilbronner; John M Pearson; Michael L Platt Surprise signals in anterior cingulate cortex: Neuronal encoding of unsigned reward prediction errors driving adjustment in behavior Journal Article Journal of Neuroscience, 31 (11), pp. 4178–4187, 2011. @article{Hayden2011, title = {Surprise signals in anterior cingulate cortex: Neuronal encoding of unsigned reward prediction errors driving adjustment in behavior}, author = {Benjamin Y Hayden and Sarah R Heilbronner and John M Pearson and Michael L Platt}, doi = {10.1523/JNEUROSCI.4652-10.2011}, year = {2011}, date = {2011-01-01}, journal = {Journal of Neuroscience}, volume = {31}, number = {11}, pages = {4178--4187}, abstract = {In attentional models of learning, associations between actions and subsequent rewards are stronger when outcomes are surprising, regardless of their valence. Despite the behavioral evidence that surprising outcomes drive learning, neural correlates of unsigned reward prediction errors remain elusive. Here we show that in a probabilistic choice task, trial-to-trial variations in preference track outcome surprisingness. Concordant with this behavioral pattern, responses of neurons in macaque (Macaca mulatta) dorsal anterior cingulate cortex (dACC) to both large and small rewards were enhanced when the outcome was surprising. Moreover, when, on some trials, probabilities were hidden, neuronal responses to rewards were reduced, consistent with the idea that the absence of clear expectations diminishes surprise. These patterns are inconsistent with the idea that dACC neurons track signed errors in reward prediction, as dopamine neurons do. Our results also indicate that dACC neurons do not signal conflict. In the context of other studies of dACC function, these results suggest a link between reward-related modulations in dACC activity and attention and motor control processes involved in behavioral adjustment. More speculatively, these data point to a harmonious integration between reward and learning accounts of ACC function on one hand, and attention and cognitive control accounts on the other.}, keywords = {}, pubstate = {published}, tppubtype = {article} } In attentional models of learning, associations between actions and subsequent rewards are stronger when outcomes are surprising, regardless of their valence. Despite the behavioral evidence that surprising outcomes drive learning, neural correlates of unsigned reward prediction errors remain elusive. Here we show that in a probabilistic choice task, trial-to-trial variations in preference track outcome surprisingness. Concordant with this behavioral pattern, responses of neurons in macaque (Macaca mulatta) dorsal anterior cingulate cortex (dACC) to both large and small rewards were enhanced when the outcome was surprising. Moreover, when, on some trials, probabilities were hidden, neuronal responses to rewards were reduced, consistent with the idea that the absence of clear expectations diminishes surprise. These patterns are inconsistent with the idea that dACC neurons track signed errors in reward prediction, as dopamine neurons do. Our results also indicate that dACC neurons do not signal conflict. In the context of other studies of dACC function, these results suggest a link between reward-related modulations in dACC activity and attention and motor control processes involved in behavioral adjustment. More speculatively, these data point to a harmonious integration between reward and learning accounts of ACC function on one hand, and attention and cognitive control accounts on the other. |
Benjamin Y Hayden; John M Pearson; Michael L Platt Neuronal basis of sequential foraging decisions in a patchy environment Journal Article Nature Neuroscience, 14 (7), pp. 933–939, 2011. @article{Hayden2011a, title = {Neuronal basis of sequential foraging decisions in a patchy environment}, author = {Benjamin Y Hayden and John M Pearson and Michael L Platt}, doi = {10.1038/nn.2856}, year = {2011}, date = {2011-01-01}, journal = {Nature Neuroscience}, volume = {14}, number = {7}, pages = {933--939}, publisher = {Nature Publishing Group}, abstract = {Deciding when to leave a depleting resource to exploit another is a fundamental problem for all decision makers. The neuronal mechanisms mediating patch-leaving decisions remain unknown. We found that neurons in primate (Macaca mulatta) dorsal anterior cingulate cortex, an area that is linked to reward monitoring and executive control, encode a decision variable signaling the relative value of leaving a depleting resource for a new one. Neurons fired during each sequential decision to stay in a patch and, for each travel time, these responses reached a fixed threshold for patch-leaving. Longer travel times reduced the gain of neural responses for choosing to stay in a patch and increased the firing rate threshold mandating patch-leaving. These modulations more closely matched behavioral decisions than any single task variable. These findings portend an understanding of the neural basis of foraging decisions and endorse the unification of theoretical and experimental work in ecology and neuroscience.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Deciding when to leave a depleting resource to exploit another is a fundamental problem for all decision makers. The neuronal mechanisms mediating patch-leaving decisions remain unknown. We found that neurons in primate (Macaca mulatta) dorsal anterior cingulate cortex, an area that is linked to reward monitoring and executive control, encode a decision variable signaling the relative value of leaving a depleting resource for a new one. Neurons fired during each sequential decision to stay in a patch and, for each travel time, these responses reached a fixed threshold for patch-leaving. Longer travel times reduced the gain of neural responses for choosing to stay in a patch and increased the firing rate threshold mandating patch-leaving. These modulations more closely matched behavioral decisions than any single task variable. These findings portend an understanding of the neural basis of foraging decisions and endorse the unification of theoretical and experimental work in ecology and neuroscience. |
Benjamin Y Hayden; Jack L Gallant Working memory and decision processes in visual area V4 Journal Article Frontiers in Neuroscience, 7 , pp. 1–10, 2013. @article{Hayden2013, title = {Working memory and decision processes in visual area V4}, author = {Benjamin Y Hayden and Jack L Gallant}, doi = {10.3389/fnins.2013.00018}, year = {2013}, date = {2013-01-01}, journal = {Frontiers in Neuroscience}, volume = {7}, pages = {1--10}, publisher = {10}, address = {doi}, abstract = {Recognizing and responding to a remembered stimulus requires the coordination of perception, working memory and decision-making. To investigate the role of visual cortex in these processes, we recorded responses of single V4 neurons during performance of a delayed match-to-sample task that incorporates rapid serial visual presentation of natural images. We found that neuronal activity during the delay period after the cue but before the images depends on the identity of the remembered image and that this change persists while distractors appear. This persistent response modulation has been identified as a diagnostic criterion for putative working memory signals; our data thus suggest that working memory may involve reactivation of sensory neurons. When the remembered image reappears in the neuron's receptive field, visually evoked responses are enhanced; this match enhancement is a diagnostic criterion for decision. One model that predicts these data is the matched filter hypothesis, which holds that during search V4 neurons change their tuning so as to match the remembered cue, and thus become detectors for that image. More generally, these results suggest that V4 neurons participate in the perceptual, working memory and decision processes that are needed to perform memory-guided decision-making.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Recognizing and responding to a remembered stimulus requires the coordination of perception, working memory and decision-making. To investigate the role of visual cortex in these processes, we recorded responses of single V4 neurons during performance of a delayed match-to-sample task that incorporates rapid serial visual presentation of natural images. We found that neuronal activity during the delay period after the cue but before the images depends on the identity of the remembered image and that this change persists while distractors appear. This persistent response modulation has been identified as a diagnostic criterion for putative working memory signals; our data thus suggest that working memory may involve reactivation of sensory neurons. When the remembered image reappears in the neuron's receptive field, visually evoked responses are enhanced; this match enhancement is a diagnostic criterion for decision. One model that predicts these data is the matched filter hypothesis, which holds that during search V4 neurons change their tuning so as to match the remembered cue, and thus become detectors for that image. More generally, these results suggest that V4 neurons participate in the perceptual, working memory and decision processes that are needed to perform memory-guided decision-making. |
Sarah R Heilbronner; Benjamin Y Hayden; Michael L Platt Decision salience signals in posterior cingulate cortex Journal Article Frontiers in Neuroscience, 5 , pp. 1–9, 2011. @article{Heilbronner2011, title = {Decision salience signals in posterior cingulate cortex}, author = {Sarah R Heilbronner and Benjamin Y Hayden and Michael L Platt}, doi = {10.3389/fnins.2011.00055}, year = {2011}, date = {2011-01-01}, journal = {Frontiers in Neuroscience}, volume = {5}, pages = {1--9}, publisher = {10}, address = {doi}, abstract = {Despite its phylogenetic antiquity and clinical importance, the posterior cingulate cortex (CGp) remains an enigmatic nexus of attention, memory, motivation, and decision making. Here we show that CGp neurons track decision salience - the degree to which an option differs from a standard - but not the subjective value of a decision. To do this, we recorded the spiking activity of CGp neurons in monkeys choosing between options varying in reward-related risk, delay to reward, and social outcomes, each of which varied in level of decision salience. Firing rates were higher when monkeys chose the risky option, consistent with their risk-seeking preferences, but were also higher when monkeys chose the delayed and social options, contradicting their preferences. Thus, across decision contexts, neuronal activity was uncorrelated with how much monkeys valued a given option, as inferred from choice. Instead, neuronal activity signaled the deviation of the chosen option from the standard, independently of how it differed. The observed decision salience signals suggest a role for CGp in the flexible allocation of neural resources to motivationally significant information, akin to the role of attention in selective processing of sensory inputs.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Despite its phylogenetic antiquity and clinical importance, the posterior cingulate cortex (CGp) remains an enigmatic nexus of attention, memory, motivation, and decision making. Here we show that CGp neurons track decision salience - the degree to which an option differs from a standard - but not the subjective value of a decision. To do this, we recorded the spiking activity of CGp neurons in monkeys choosing between options varying in reward-related risk, delay to reward, and social outcomes, each of which varied in level of decision salience. Firing rates were higher when monkeys chose the risky option, consistent with their risk-seeking preferences, but were also higher when monkeys chose the delayed and social options, contradicting their preferences. Thus, across decision contexts, neuronal activity was uncorrelated with how much monkeys valued a given option, as inferred from choice. Instead, neuronal activity signaled the deviation of the chosen option from the standard, independently of how it differed. The observed decision salience signals suggest a role for CGp in the flexible allocation of neural resources to motivationally significant information, akin to the role of attention in selective processing of sensory inputs. |
Sarah R Heilbronner; Michael L Platt Causal evidence of performance monitoring by neurons in posterior cingulate cortex during learning Journal Article Neuron, 80 (6), pp. 1384–1391, 2013. @article{Heilbronner2013, title = {Causal evidence of performance monitoring by neurons in posterior cingulate cortex during learning}, author = {Sarah R Heilbronner and Michael L Platt}, doi = {10.1016/j.neuron.2013.09.028}, year = {2013}, date = {2013-01-01}, journal = {Neuron}, volume = {80}, number = {6}, pages = {1384--1391}, publisher = {Elsevier Inc.}, abstract = {The posterior cingulate cortex (CGp) is a major hub of the default mode network (DMN), a set of cortical areas with high resting activity that declines during task performance. This relationship suggests that DMN activity contributes to mental processes that are antagonistic to performance. Alternatively, DMN may detect conditions under which performance is poor and marshal cognitive resources for improvement. To test this idea, we recorded activity of CGp neurons in monkeys performing a learning task while varying reward size and novelty. We found that CGp neurons responded to errors, and this activity was magnified by small reward and novel stimuli. Inactivating CGp with muscimol impaired new learning when rewards were small but had no effect when rewards were large; inactivation did not affect performance on well-learned associations. Thus, CGp, and by extension the DMN, may support learning, and possibly other cognitive processes, by monitoring performance and motivating exploration.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The posterior cingulate cortex (CGp) is a major hub of the default mode network (DMN), a set of cortical areas with high resting activity that declines during task performance. This relationship suggests that DMN activity contributes to mental processes that are antagonistic to performance. Alternatively, DMN may detect conditions under which performance is poor and marshal cognitive resources for improvement. To test this idea, we recorded activity of CGp neurons in monkeys performing a learning task while varying reward size and novelty. We found that CGp neurons responded to errors, and this activity was magnified by small reward and novel stimuli. Inactivating CGp with muscimol impaired new learning when rewards were small but had no effect when rewards were large; inactivation did not affect performance on well-learned associations. Thus, CGp, and by extension the DMN, may support learning, and possibly other cognitive processes, by monitoring performance and motivating exploration. |
Sarah R Heilbronner; Benjamin Y Hayden The description-experience gap in risky choice in nonhuman primates Journal Article Psychonomic Bulletin & Review, 23 (2), pp. 593–600, 2016. @article{Heilbronner2016, title = {The description-experience gap in risky choice in nonhuman primates}, author = {Sarah R Heilbronner and Benjamin Y Hayden}, doi = {10.3758/s13423-015-0924-2}, year = {2016}, date = {2016-01-01}, journal = {Psychonomic Bulletin & Review}, volume = {23}, number = {2}, pages = {593--600}, abstract = {Risk attitudes in humans depend on the format used to present the gamble: we are more risk-averse for common gambles in the gains domain whose properties are described to us verbally than for those whose properties we learned about solely through experience. This difference, which constitutes part ofthe description-experience gap,is important, because it highlights the role ofknowledge acquisition in decision-mak- ing. The reasons for the gap remain obscure, but could depend upon uniquely human cognitive abilities, such as those asso- ciated with language. Thus, the gap may or may not extend to nonhuman animals. For this study, rhesus monkeys performed a novel task in which the properties of some gambles were explicitly cued (described), whereas others were learned through previous choices (experienced). Our monkeys displayed a description-experience gap. Overall, monkeys were more risk-seeking for experienced than for described gambles. This difference was observed for a range ofgamble probabilities (from 20% to 80% likelihood of payoff), indicating that it is not limited to low probability events. These results suggest that the description- experience gap does not depend on uniquely human cognitive abilities, such as those associated with lan- guage, and support the idea that epistemic influences on risk attitudes are evolutionarily ancient.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Risk attitudes in humans depend on the format used to present the gamble: we are more risk-averse for common gambles in the gains domain whose properties are described to us verbally than for those whose properties we learned about solely through experience. This difference, which constitutes part ofthe description-experience gap,is important, because it highlights the role ofknowledge acquisition in decision-mak- ing. The reasons for the gap remain obscure, but could depend upon uniquely human cognitive abilities, such as those asso- ciated with language. Thus, the gap may or may not extend to nonhuman animals. For this study, rhesus monkeys performed a novel task in which the properties of some gambles were explicitly cued (described), whereas others were learned through previous choices (experienced). Our monkeys displayed a description-experience gap. Overall, monkeys were more risk-seeking for experienced than for described gambles. This difference was observed for a range ofgamble probabilities (from 20% to 80% likelihood of payoff), indicating that it is not limited to low probability events. These results suggest that the description- experience gap does not depend on uniquely human cognitive abilities, such as those associated with lan- guage, and support the idea that epistemic influences on risk attitudes are evolutionarily ancient. |
James P Herman; Richard J Krauzlis Color-change detection activity in the primate superior colliculus Journal Article eNeuro, 4 (2), pp. 1–16, 2017. @article{Herman2017, title = {Color-change detection activity in the primate superior colliculus}, author = {James P Herman and Richard J Krauzlis}, doi = {10.1523/ENEURO.0046-17.2017}, year = {2017}, date = {2017-01-01}, journal = {eNeuro}, volume = {4}, number = {2}, pages = {1--16}, abstract = {The primate superior colliculus (SC) is a midbrain structure that participates in the control of spatial attention. Previous studies examining the role of the SC in attention have mostly used luminance-based visual features (e.g., motion, contrast) as the stimuli and saccadic eye movements as the behavioral response, both of which are known to modulate the activity of SC neurons. To explore the limits of the SC's involvement in the control of spatial attention, we recorded SC neuronal activity during a task using color, a visual feature dimension not traditionally associated with the SC, and required monkeys to detect threshold-level changes in the saturation of a cued stimulus by releasing a joystick during maintained fixation. Using this color-based spatial attention task, we found substantial cue-related modulation in all categories of visually responsive neurons in the intermediate layers of the SC. Notably, near-threshold changes in color saturation, both increases and decreases, evoked phasic bursts of activity with magnitudes as large as those evoked by stimulus onset. This change-detection activity had two distinctive features: activity for hits was larger than for misses, and the timing of change-detection activity accounted for 67% of joystick release latency, even though it preceded the release by at least 200 ms. We conclude that during attention tasks, SC activity denotes the behavioral relevance of the stimulus regardless of feature dimension and that phasic event-related SC activity is suitable to guide the selection of manual responses as well as saccadic eye movements.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The primate superior colliculus (SC) is a midbrain structure that participates in the control of spatial attention. Previous studies examining the role of the SC in attention have mostly used luminance-based visual features (e.g., motion, contrast) as the stimuli and saccadic eye movements as the behavioral response, both of which are known to modulate the activity of SC neurons. To explore the limits of the SC's involvement in the control of spatial attention, we recorded SC neuronal activity during a task using color, a visual feature dimension not traditionally associated with the SC, and required monkeys to detect threshold-level changes in the saturation of a cued stimulus by releasing a joystick during maintained fixation. Using this color-based spatial attention task, we found substantial cue-related modulation in all categories of visually responsive neurons in the intermediate layers of the SC. Notably, near-threshold changes in color saturation, both increases and decreases, evoked phasic bursts of activity with magnitudes as large as those evoked by stimulus onset. This change-detection activity had two distinctive features: activity for hits was larger than for misses, and the timing of change-detection activity accounted for 67% of joystick release latency, even though it preceded the release by at least 200 ms. We conclude that during attention tasks, SC activity denotes the behavioral relevance of the stimulus regardless of feature dimension and that phasic event-related SC activity is suitable to guide the selection of manual responses as well as saccadic eye movements. |
Todd M Herrington; Nicolas Y Masse; Karim J Hachmeh; Jackson E T Smith; John A Assad; Erik P Cook Journal of Neuroscience, 29 (18), pp. 5793–5805, 2009. @article{Herrington2009, title = {The effect of microsaccades on the correlation between neural activity and behavior in middle temporal, ventral intraparietal, and lateral intraparietal areas}, author = {Todd M Herrington and Nicolas Y Masse and Karim J Hachmeh and Jackson E T Smith and John A Assad and Erik P Cook}, doi = {10.1523/JNEUROSCI.4412-08.2009}, year = {2009}, date = {2009-01-01}, journal = {Journal of Neuroscience}, volume = {29}, number = {18}, pages = {5793--5805}, abstract = {It is widely reported that the activity of single neurons in visual cortex is correlated with the perceptual decision of the subject. The strength of this correlation has implications for the neuronal populations generating the percepts. Here we asked whether microsaccades, which are small, involuntary eye movements, contribute to the correlation between neural activity and behavior. We analyzed data from three different visual detection experiments, with neural recordings from the middle temporal (MT), lateral intraparietal (LIP), and ventral intraparietal (VIP) areas. All three experiments used random dot motion stimuli, with the animals required to detect a transient or sustained change in the speed or strength of motion. We found that microsaccades suppressed neural activity and inhibited detection of the motion stimulus, contributing to the correlation between neural activity and detection behavior. Microsaccades accounted for as much as 19% of the correlation for area MT, 21% for area LIP, and 17% for VIP. While microsaccades only explain part of the correlation between neural activity and behavior, their effect has implications when considering the neuronal populations underlying perceptual decisions.}, keywords = {}, pubstate = {published}, tppubtype = {article} } It is widely reported that the activity of single neurons in visual cortex is correlated with the perceptual decision of the subject. The strength of this correlation has implications for the neuronal populations generating the percepts. Here we asked whether microsaccades, which are small, involuntary eye movements, contribute to the correlation between neural activity and behavior. We analyzed data from three different visual detection experiments, with neural recordings from the middle temporal (MT), lateral intraparietal (LIP), and ventral intraparietal (VIP) areas. All three experiments used random dot motion stimuli, with the animals required to detect a transient or sustained change in the speed or strength of motion. We found that microsaccades suppressed neural activity and inhibited detection of the motion stimulus, contributing to the correlation between neural activity and detection behavior. Microsaccades accounted for as much as 19% of the correlation for area MT, 21% for area LIP, and 17% for VIP. While microsaccades only explain part of the correlation between neural activity and behavior, their effect has implications when considering the neuronal populations underlying perceptual decisions. |
Markus A Hietanen; Nicholas S C Price; Shaun L Cloherty; Kostas Hadjidimitrakis; Michael R Ibbotson Long-term sensorimotor adaptation in the ocular following system of primates Journal Article PLoS ONE, 12 (12), pp. 1–15, 2017. @article{Hietanen2017, title = {Long-term sensorimotor adaptation in the ocular following system of primates}, author = {Markus A Hietanen and Nicholas S C Price and Shaun L Cloherty and Kostas Hadjidimitrakis and Michael R Ibbotson}, doi = {10.1371/journal.pone.0189030}, year = {2017}, date = {2017-01-01}, journal = {PLoS ONE}, volume = {12}, number = {12}, pages = {1--15}, abstract = {The sudden movement of a wide-field image leads to a reflexive eye tracking response referred to as short-latency ocular following. If the image motion occurs soon after a saccade the initial speed of the ocular following is enhanced, a phenomenon known as post-saccadic enhancement. We show in macaque monkeys that repeated exposure to the same stimulus regime over a period of months leads to progressive increases in the initial speeds of ocular following. The improvement in tracking speed occurs for ocular following with and without a prior saccade. As a result of the improvement in ocular following speeds, the influence of post-saccadic enhancement wanes with increasing levels of training. The improvement in ocular following speed following repeated exposure to the same oculomotor task represents a novel form of sensori-motor learning in the context of a reflexive movement.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The sudden movement of a wide-field image leads to a reflexive eye tracking response referred to as short-latency ocular following. If the image motion occurs soon after a saccade the initial speed of the ocular following is enhanced, a phenomenon known as post-saccadic enhancement. We show in macaque monkeys that repeated exposure to the same stimulus regime over a period of months leads to progressive increases in the initial speeds of ocular following. The improvement in tracking speed occurs for ocular following with and without a prior saccade. As a result of the improvement in ocular following speeds, the influence of post-saccadic enhancement wanes with increasing levels of training. The improvement in ocular following speed following repeated exposure to the same oculomotor task represents a novel form of sensori-motor learning in the context of a reflexive movement. |
Ha Hong; Daniel L K Yamins; Najib J Majaj; James J DiCarlo Explicit information for category-orthogonal object properties increases along the ventral stream Journal Article Nature Neuroscience, 19 (4), pp. 613–622, 2016. @article{Hong2016, title = {Explicit information for category-orthogonal object properties increases along the ventral stream}, author = {Ha Hong and Daniel L K Yamins and Najib J Majaj and James J DiCarlo}, doi = {10.1038/nn.4247}, year = {2016}, date = {2016-01-01}, journal = {Nature Neuroscience}, volume = {19}, number = {4}, pages = {613--622}, abstract = {Extensive research has revealed that the ventral visual stream hierarchically builds a robust representation for supporting visual object categorization tasks. We systematically explored the ability of multiple ventral visual areas to support a variety of 'category-orthogonal' object properties such as position, size and pose. For complex naturalistic stimuli, we found that the inferior temporal (IT) population encodes all measured category-orthogonal object properties, including those properties often considered to be low-level features (for example, position), more explicitly than earlier ventral stream areas. We also found that the IT population better predicts human performance patterns across properties. A hierarchical neural network model based on simple computational principles generates these same cross-area patterns of information. Taken together, our empirical results support the hypothesis that all behaviorally relevant object properties are extracted in concert up the ventral visual hierarchy, and our computational model explains how that hierarchy might be built.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Extensive research has revealed that the ventral visual stream hierarchically builds a robust representation for supporting visual object categorization tasks. We systematically explored the ability of multiple ventral visual areas to support a variety of 'category-orthogonal' object properties such as position, size and pose. For complex naturalistic stimuli, we found that the inferior temporal (IT) population encodes all measured category-orthogonal object properties, including those properties often considered to be low-level features (for example, position), more explicitly than earlier ventral stream areas. We also found that the IT population better predicts human performance patterns across properties. A hierarchical neural network model based on simple computational principles generates these same cross-area patterns of information. Taken together, our empirical results support the hypothesis that all behaviorally relevant object properties are extracted in concert up the ventral visual hierarchy, and our computational model explains how that hierarchy might be built. |
Chia-Chun Hung; Cecil C Yen; Jennifer L Ciuchta; Daniel Papoti; Nicholas A Bock; David A Leopold; Afonso C Silva Functional MRI of visual responses in the awake, behaving marmoset Journal Article NeuroImage, 15 (120), pp. 1–11, 2015. @article{Hung2015, title = {Functional MRI of visual responses in the awake, behaving marmoset}, author = {Chia-Chun Hung and Cecil C Yen and Jennifer L Ciuchta and Daniel Papoti and Nicholas A Bock and David A Leopold and Afonso C Silva}, doi = {10.1002/jbmr.2490.OPG-Fc}, year = {2015}, date = {2015-01-01}, journal = {NeuroImage}, volume = {15}, number = {120}, pages = {1--11}, abstract = {The visual brain is composed of interconnected subcortical and cortical structures that receive and process image information originating in the retina. The visual system of nonhuman primates, in particular macaques, has been studied in great detail in order to elucidate principles of human sensation and perception. The common marmoset (Callithrix jacchus) is a small New World monkey of growing interest as a primate model for neuroscience. Marmosets have advantages over macaques because of their small size, lissencephalic cortex, and growing potential for viral and genetic manipulations. Previous anatomical studies and electrophysiological recordings in anesthetized marmosets have shown that this species' cortical visual hierarchy closely resembles that of other primates, including humans. Until now, however, there have been no attempts to systematically study visual responses throughout the marmoset brain using fMRI. Here we show that awake marmosets readily learn to carry out a simple visual task inside the bore of an MRI scanner during functional mapping experiments. Functional scanning at 500$mu$m in-plane resolution in a 30 cm horizontal bore at 7T revealed robust positive blood oxygenation level-dependent (BOLD) fMRI responses to visual stimuli throughout visual cortex and associated subcortical areas. Nonvisual sensory areas showed negative contrasts to visual stimuli compared to the fixation dot only baseline. Structured images of objects and faces led to stronger responses than scrambled control images at stages beyond early visual cortex. Our study establishes functionalMRI mapping of visual responses in awake, behaving marmosets is straightforward and valuable for assessing the functional organization of the primate brain at high resolution.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The visual brain is composed of interconnected subcortical and cortical structures that receive and process image information originating in the retina. The visual system of nonhuman primates, in particular macaques, has been studied in great detail in order to elucidate principles of human sensation and perception. The common marmoset (Callithrix jacchus) is a small New World monkey of growing interest as a primate model for neuroscience. Marmosets have advantages over macaques because of their small size, lissencephalic cortex, and growing potential for viral and genetic manipulations. Previous anatomical studies and electrophysiological recordings in anesthetized marmosets have shown that this species' cortical visual hierarchy closely resembles that of other primates, including humans. Until now, however, there have been no attempts to systematically study visual responses throughout the marmoset brain using fMRI. Here we show that awake marmosets readily learn to carry out a simple visual task inside the bore of an MRI scanner during functional mapping experiments. Functional scanning at 500$mu$m in-plane resolution in a 30 cm horizontal bore at 7T revealed robust positive blood oxygenation level-dependent (BOLD) fMRI responses to visual stimuli throughout visual cortex and associated subcortical areas. Nonvisual sensory areas showed negative contrasts to visual stimuli compared to the fixation dot only baseline. Structured images of objects and faces led to stronger responses than scrambled control images at stages beyond early visual cortex. Our study establishes functionalMRI mapping of visual responses in awake, behaving marmosets is straightforward and valuable for assessing the functional organization of the primate brain at high resolution. |
Chia-Chun Hung; Cecil C Yen; Jennifer L Ciuchta; Daniel Papoti; Nicholas A Bock; David A Leopold; Afonso C Silva Functional mapping of face-selective regions in the extrastriate visual cortex of the marmoset Journal Article Journal of Neuroscience, 35 (3), pp. 1160–1172, 2015. @article{Hung2015a, title = {Functional mapping of face-selective regions in the extrastriate visual cortex of the marmoset}, author = {Chia-Chun Hung and Cecil C Yen and Jennifer L Ciuchta and Daniel Papoti and Nicholas A Bock and David A Leopold and Afonso C Silva}, doi = {10.1523/JNEUROSCI.2659-14.2015}, year = {2015}, date = {2015-01-01}, journal = {Journal of Neuroscience}, volume = {35}, number = {3}, pages = {1160--1172}, abstract = {The cerebral cortex of humans and macaques has specialized regions for processing faces and other visual stimulus categories. It is unknown whether a similar functional organization exists in New World monkeys, such as the common marmoset (Callithrix jacchus), a species of growing interest as a primate model in neuroscience. To address this question, we measured selective neural responses in the brain of four awake marmosets trained to fix their gaze upon images of faces, bodies, objects, and control patterns. In two of the subjects, we measured high gamma-range field potentials from electrocorticography arrays implanted over a large portion of the occipital and inferotemporal cortex. In the other two subjects, we measured BOLD fMRI responses across the entire brain. Both techniques revealed robust, regionally specific patterns of category-selective neural responses. We report that at least six face-selective patches mark the occipitotemporal pathway of the marmoset, with the most anterior patches showing the strongest preference for faces over other stimuli. The similar appearance of these patches to previous findings in macaques and humans, including their apparent arrangement in two parallel pathways, suggests that core elements of the face processing network were present in the common anthropoid primate ancestor living ∼35 million years ago. The findings also identify the marmoset as a viable animal model system for studying specialized neural mechanisms related to high-level social visual perception in humans.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The cerebral cortex of humans and macaques has specialized regions for processing faces and other visual stimulus categories. It is unknown whether a similar functional organization exists in New World monkeys, such as the common marmoset (Callithrix jacchus), a species of growing interest as a primate model in neuroscience. To address this question, we measured selective neural responses in the brain of four awake marmosets trained to fix their gaze upon images of faces, bodies, objects, and control patterns. In two of the subjects, we measured high gamma-range field potentials from electrocorticography arrays implanted over a large portion of the occipital and inferotemporal cortex. In the other two subjects, we measured BOLD fMRI responses across the entire brain. Both techniques revealed robust, regionally specific patterns of category-selective neural responses. We report that at least six face-selective patches mark the occipitotemporal pathway of the marmoset, with the most anterior patches showing the strongest preference for faces over other stimuli. The similar appearance of these patches to previous findings in macaques and humans, including their apparent arrangement in two parallel pathways, suggests that core elements of the face processing network were present in the common anthropoid primate ancestor living ∼35 million years ago. The findings also identify the marmoset as a viable animal model system for studying specialized neural mechanisms related to high-level social visual perception in humans. |
Guilhem Ibos; David J Freedman Dynamic integration of task-relevant visual features in posterior parietal cortex Journal Article Neuron, 83 (6), pp. 1468–1480, 2014. @article{Ibos2014, title = {Dynamic integration of task-relevant visual features in posterior parietal cortex}, author = {Guilhem Ibos and David J Freedman}, doi = {10.1016/j.neuron.2014.08.020}, year = {2014}, date = {2014-01-01}, journal = {Neuron}, volume = {83}, number = {6}, pages = {1468--1480}, publisher = {83}, abstract = {The primate visual system consists of multiple hierarchically organized cortical areas, each specialized for processing distinct aspects of the visual scene. For example, color and form are encoded in ventralpathway areas such as V4 and inferior temporal cortex, while motion is preferentially processed in dorsal pathway areas such as the middletemporal area. Such representations often need to be integrated perceptually to solve tasks that depend on multiple features. We tested the hypothesis that the lateral intraparietal area (LIP) integrates disparate task-relevant visual features by recording from LIP neurons in monkeys trained to identify target stimuli composed of conjunctionsof color and motion features. We show that LIP neurons exhibit integrative representations of both color and motion features when they are taskrelevant and task-dependent shifts of both direction and color tuning. This suggests that LIP plays a role in flexibly integrating task-relevant sensory signals.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The primate visual system consists of multiple hierarchically organized cortical areas, each specialized for processing distinct aspects of the visual scene. For example, color and form are encoded in ventralpathway areas such as V4 and inferior temporal cortex, while motion is preferentially processed in dorsal pathway areas such as the middletemporal area. Such representations often need to be integrated perceptually to solve tasks that depend on multiple features. We tested the hypothesis that the lateral intraparietal area (LIP) integrates disparate task-relevant visual features by recording from LIP neurons in monkeys trained to identify target stimuli composed of conjunctionsof color and motion features. We show that LIP neurons exhibit integrative representations of both color and motion features when they are taskrelevant and task-dependent shifts of both direction and color tuning. This suggests that LIP plays a role in flexibly integrating task-relevant sensory signals. |
Guilhem Ibos; David J Freedman Interaction between spatial and feature attention in posterior parietal cortex Journal Article Neuron, 91 (4), pp. 931–943, 2016. @article{Ibos2016, title = {Interaction between spatial and feature attention in posterior parietal cortex}, author = {Guilhem Ibos and David J Freedman}, doi = {10.1016/j.neuron.2016.07.025}, year = {2016}, date = {2016-01-01}, journal = {Neuron}, volume = {91}, number = {4}, pages = {931--943}, publisher = {Elsevier Inc.}, abstract = {Lateral intraparietal (LIP) neurons encode a vast array of sensory and cognitive variables. Recently, we proposed that the flexibility of feature representations in LIP reflect the bottom-up integration of sensory signals, modulated by feature-based attention (FBA), from upstream feature-selective cortical neurons. Moreover, LIP activity is also strongly modulated by the position of space-based attention (SBA). However, the mechanisms by which SBA and FBA interact to facilitate the representation of task-relevant spatial and non-spatial features in LIP remain unclear. We recorded from LIP neurons during performance of a task that required monkeys to detect specific conjunctions of color, motion direction, and stimulus position. Here we show that FBA and SBA potentiate each other's effect in a manner consistent with attention gating the flow of visual information along the cortical visual pathway. Our results suggest that linear bottom-up integrative mechanisms allow LIP neurons to emphasize task-relevant spatial and non-spatial features.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Lateral intraparietal (LIP) neurons encode a vast array of sensory and cognitive variables. Recently, we proposed that the flexibility of feature representations in LIP reflect the bottom-up integration of sensory signals, modulated by feature-based attention (FBA), from upstream feature-selective cortical neurons. Moreover, LIP activity is also strongly modulated by the position of space-based attention (SBA). However, the mechanisms by which SBA and FBA interact to facilitate the representation of task-relevant spatial and non-spatial features in LIP remain unclear. We recorded from LIP neurons during performance of a task that required monkeys to detect specific conjunctions of color, motion direction, and stimulus position. Here we show that FBA and SBA potentiate each other's effect in a manner consistent with attention gating the flow of visual information along the cortical visual pathway. Our results suggest that linear bottom-up integrative mechanisms allow LIP neurons to emphasize task-relevant spatial and non-spatial features. |
Guilhem Ibos; David J Freedman Sequential sensory and decision processing in posterior parietal cortex Journal Article eLife, 6 , pp. 1–19, 2017. @article{Ibos2017, title = {Sequential sensory and decision processing in posterior parietal cortex}, author = {Guilhem Ibos and David J Freedman}, doi = {10.7554/eLife.23743}, year = {2017}, date = {2017-01-01}, journal = {eLife}, volume = {6}, pages = {1--19}, abstract = {textlessptextgreaterDecisions about the behavioral significance of sensory stimuli often require comparing sensory inference of what we are looking at to internal models of what we are looking for. Here, we test how neuronal selectivity for visual features is transformed into decision-related signals in posterior parietal cortex (area LIP). Monkeys performed a visual matching task that required them to detect target stimuli composed of conjunctions of color and motion-direction. Neuronal recordings from area LIP revealed two main findings. First, the sequential processing of visual features and the selection of target-stimuli suggest that LIP is involved in transforming sensory information into decision-related signals. Second, the patterns of color and motion selectivity and their impact on decision-related encoding suggest that LIP plays a role in detecting target stimuli by comparing bottom-up sensory inputs (what the monkeys were looking at) and top-down cognitive encoding inputs (what the monkeys were looking for).textless/ptextgreater}, keywords = {}, pubstate = {published}, tppubtype = {article} } textlessptextgreaterDecisions about the behavioral significance of sensory stimuli often require comparing sensory inference of what we are looking at to internal models of what we are looking for. Here, we test how neuronal selectivity for visual features is transformed into decision-related signals in posterior parietal cortex (area LIP). Monkeys performed a visual matching task that required them to detect target stimuli composed of conjunctions of color and motion-direction. Neuronal recordings from area LIP revealed two main findings. First, the sequential processing of visual features and the selection of target-stimuli suggest that LIP is involved in transforming sensory information into decision-related signals. Second, the patterns of color and motion selectivity and their impact on decision-related encoding suggest that LIP plays a role in detecting target stimuli by comparing bottom-up sensory inputs (what the monkeys were looking at) and top-down cognitive encoding inputs (what the monkeys were looking for).textless/ptextgreater |
Ameqrane Ilhame; Wattiez Nicolas; Pouget Pierre; Missal Marcus A subanesthetic dose of ketamine in the Rhesus monkey reduces the occurrence of anticipatory saccades Journal Article Psychopharmacology, 232 (19), pp. 3563–3572, 2015. @article{Ilhame2015, title = {A subanesthetic dose of ketamine in the Rhesus monkey reduces the occurrence of anticipatory saccades}, author = {Ameqrane Ilhame and Wattiez Nicolas and Pouget Pierre and Missal Marcus}, doi = {10.1007/s00213-015-4005-z}, year = {2015}, date = {2015-01-01}, journal = {Psychopharmacology}, volume = {232}, number = {19}, pages = {3563--3572}, abstract = {RATIONALE: It has been shown that antagonism of the glutamatergic N-methyl-D-aspartate (NMDA) receptor with subanesthetic doses of ketamine perturbs the perception of elapsed time. Anticipatory eye movements are based on an internal representation of elapsed time. Therefore, the occurrence of anticipatory saccades could be a particularly sensitive indicator of abnormal time perception due to NMDA receptors blockade. OBJECTIVES: The objective of this study was to determine whether the occurrence of anticipatory saccades could be selectively altered by a subanesthetic dose of ketamine. METHODS: Three Rhesus monkeys were trained in a simple visually guided saccadic task with a variable delay. Monkeys were rewarded for making a visually guided saccade at the end of the delay. Premature anticipatory saccades to the future position of the eccentric target initiated before the end of the delay were not rewarded. A subanesthetic dose of ketamine (0.25 mg/kg) or a saline solution of the same volume was injected i.m. during the task. RESULTS: We found that the injected dose of ketamine did not induce sedation or abnormal behavior. However, in ∼4 min, ketamine induced a strong reduction of the occurrence of anticipatory saccades but did not reduce the occurrence of visually guided saccades. CONCLUSION: This unexpected reduction of anticipatory saccade occurrence could be interpreted as resulting from an altered use of the perception of elapsed time during the delay period induced by NMDA receptors antagonism.}, keywords = {}, pubstate = {published}, tppubtype = {article} } RATIONALE: It has been shown that antagonism of the glutamatergic N-methyl-D-aspartate (NMDA) receptor with subanesthetic doses of ketamine perturbs the perception of elapsed time. Anticipatory eye movements are based on an internal representation of elapsed time. Therefore, the occurrence of anticipatory saccades could be a particularly sensitive indicator of abnormal time perception due to NMDA receptors blockade. OBJECTIVES: The objective of this study was to determine whether the occurrence of anticipatory saccades could be selectively altered by a subanesthetic dose of ketamine. METHODS: Three Rhesus monkeys were trained in a simple visually guided saccadic task with a variable delay. Monkeys were rewarded for making a visually guided saccade at the end of the delay. Premature anticipatory saccades to the future position of the eccentric target initiated before the end of the delay were not rewarded. A subanesthetic dose of ketamine (0.25 mg/kg) or a saline solution of the same volume was injected i.m. during the task. RESULTS: We found that the injected dose of ketamine did not induce sedation or abnormal behavior. However, in ∼4 min, ketamine induced a strong reduction of the occurrence of anticipatory saccades but did not reduce the occurrence of visually guided saccades. CONCLUSION: This unexpected reduction of anticipatory saccade occurrence could be interpreted as resulting from an altered use of the perception of elapsed time during the delay period induced by NMDA receptors antagonism. |
Masato Inoue; Motoaki Uchimura; Shigeru Kitazawa Error signals in motor cortices drive adaptation in reaching Journal Article Neuron, 90 (5), pp. 1114–1126, 2016. @article{Inoue2016, title = {Error signals in motor cortices drive adaptation in reaching}, author = {Masato Inoue and Motoaki Uchimura and Shigeru Kitazawa}, doi = {10.1016/j.neuron.2016.04.029}, year = {2016}, date = {2016-01-01}, journal = {Neuron}, volume = {90}, number = {5}, pages = {1114--1126}, publisher = {Elsevier Inc.}, abstract = {Reaching movements are subject to adaptation in response to errors induced by prisms or external perturbations. Motor cortical circuits have been hypothesized to provide execution errors that drive adaptation, but human imaging studies to date have reported that execution errors are encoded in parietal association areas. Thus, little evidence has been uncovered that supports the motor hypothesis. Here, we show that both primary motor and premotor cortices encode information on end-point errors in reaching. We further show that post-movement microstimulation to these regions caused trial-by-trial increases in errors, which subsided exponentially when the stimulation was terminated. The results indicate for the first time that motor cortical circuits provide error signals that drive trial-by-trial adaptation in reaching movements.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Reaching movements are subject to adaptation in response to errors induced by prisms or external perturbations. Motor cortical circuits have been hypothesized to provide execution errors that drive adaptation, but human imaging studies to date have reported that execution errors are encoded in parietal association areas. Thus, little evidence has been uncovered that supports the motor hypothesis. Here, we show that both primary motor and premotor cortices encode information on end-point errors in reaching. We further show that post-movement microstimulation to these regions caused trial-by-trial increases in errors, which subsided exponentially when the stimulation was terminated. The results indicate for the first time that motor cortical circuits provide error signals that drive trial-by-trial adaptation in reaching movements. |
Masato Inoue; Shigeru Kitazawa Motor error in parietal area 5 and target error in area 7 drive distinctive adaptation in reaching Journal Article Current Biology, 28 , pp. 2250–2262, 2018. @article{Inoue2018, title = {Motor error in parietal area 5 and target error in area 7 drive distinctive adaptation in reaching}, author = {Masato Inoue and Shigeru Kitazawa}, doi = {10.1016/j.cub.2018.05.056}, year = {2018}, date = {2018-01-01}, journal = {Current Biology}, volume = {28}, pages = {2250--2262}, abstract = {Errors in reaching drive trial-by-trial adaptation to compensate for the error. Parietal association areas are implicated in error coding, but whether the parietal error signals directly drive adaptation remains unknown. We first examined the activity of neurons in areas 5 and 7 while two monkeys performed rapid target reaching to clarify whether and how the parietal error signals drive adaptation in reaching. We introduced random errors using a motor-driven prism device to augment random motor errors in reaching. Neurons in both regions encoded information on the target position prior to reaching and information on the motor error after reaching. However, post-movement microstimulation caused trial-by-trial adaptation to cancel the motor error only when it was delivered to area 5. By contrast, stimulation to area 7 caused trial-by-trial adaptation so that the reaching endpoint was adjusted toward the target position. We further hypothesized that area 7 would encode target error that is caused by a target jump during the reach, and our results support this hypothesis. Area 7 neurons encoded target error information, but area 5 neurons did not encode this information. These results suggest that area 5 provides signals for adapting to motor errors and that area 7 provides signals to adapt to target errors.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Errors in reaching drive trial-by-trial adaptation to compensate for the error. Parietal association areas are implicated in error coding, but whether the parietal error signals directly drive adaptation remains unknown. We first examined the activity of neurons in areas 5 and 7 while two monkeys performed rapid target reaching to clarify whether and how the parietal error signals drive adaptation in reaching. We introduced random errors using a motor-driven prism device to augment random motor errors in reaching. Neurons in both regions encoded information on the target position prior to reaching and information on the motor error after reaching. However, post-movement microstimulation caused trial-by-trial adaptation to cancel the motor error only when it was delivered to area 5. By contrast, stimulation to area 7 caused trial-by-trial adaptation so that the reaching endpoint was adjusted toward the target position. We further hypothesized that area 7 would encode target error that is caused by a target jump during the reach, and our results support this hypothesis. Area 7 neurons encoded target error information, but area 5 neurons did not encode this information. These results suggest that area 5 provides signals for adapting to motor errors and that area 7 provides signals to adapt to target errors. |
E B Issa; J J DiCarlo Precedence of the eye region in neural processing of faces Journal Article Journal of Neuroscience, 32 (47), pp. 16666–16682, 2012. @article{Issa2012, title = {Precedence of the eye region in neural processing of faces}, author = {E B Issa and J J DiCarlo}, doi = {10.1523/JNEUROSCI.2391-12.2012}, year = {2012}, date = {2012-01-01}, journal = {Journal of Neuroscience}, volume = {32}, number = {47}, pages = {16666--16682}, abstract = {Functional magnetic resonance imaging (fMRI) has revealed multiple subregions in monkey inferior temporal cortex (IT) that are selective for images of faces over other objects. The earliest of these subregions, the posterior lateral face patch (PL), has not been studied previously at the neurophysiological level. Perhaps not surprisingly, we found that PL contains a high concentration of "face-selective" cells when tested with standard image sets comparable to those used previously to define the region at the level of fMRI. However, we here report that several different image sets and analytical approaches converge to show that nearly all face-selective PL cells are driven by the presence of a single eye in the context of a face outline. Most strikingly, images containing only an eye, even when incorrectly positioned in an outline, drove neurons nearly as well as full-face images, and face images lacking only this feature led to longer latency responses. Thus, bottom-up face processing is relatively local and linearly integrates features-consistent with parts-based models-grounding investigation of how the presence of a face is first inferred in the IT face processing hierarchy.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Functional magnetic resonance imaging (fMRI) has revealed multiple subregions in monkey inferior temporal cortex (IT) that are selective for images of faces over other objects. The earliest of these subregions, the posterior lateral face patch (PL), has not been studied previously at the neurophysiological level. Perhaps not surprisingly, we found that PL contains a high concentration of "face-selective" cells when tested with standard image sets comparable to those used previously to define the region at the level of fMRI. However, we here report that several different image sets and analytical approaches converge to show that nearly all face-selective PL cells are driven by the presence of a single eye in the context of a face outline. Most strikingly, images containing only an eye, even when incorrectly positioned in an outline, drove neurons nearly as well as full-face images, and face images lacking only this feature led to longer latency responses. Thus, bottom-up face processing is relatively local and linearly integrates features-consistent with parts-based models-grounding investigation of how the presence of a face is first inferred in the IT face processing hierarchy. |
Peter Janssen; Siddharth Srivastava; Sien Ombelet; Guy A Orban Coding of shape and position in macaque lateral Iintraparietal area Journal Article Journal of Neuroscience, 28 (26), pp. 6679–6690, 2008. @article{Janssen2008, title = {Coding of shape and position in macaque lateral Iintraparietal area}, author = {Peter Janssen and Siddharth Srivastava and Sien Ombelet and Guy A Orban}, doi = {10.1523/JNEUROSCI.0499-08.2008}, year = {2008}, date = {2008-01-01}, journal = {Journal of Neuroscience}, volume = {28}, number = {26}, pages = {6679--6690}, abstract = {The analysis of object shape is critical for both object recognition and grasping. Areas in the intraparietal sulcus of the rhesus monkey are important for the visuomotor transformations underlying actions directed toward objects. The lateral intraparietal (LIP) area has strong anatomical connections with the anterior intraparietal area, which is known to control the shaping of the hand during grasping, and LIP neurons can respond selectively to simple two-dimensional shapes. Here we investigate the shape representation in area LIP of awake rhesus monkeys. Specifically, we determined to what extent LIP neurons are tuned to shape dimensions known to be relevant for grasping and assessed the invariance of their shape preferences with regard to changes in stimulus size and position in the receptive field. Most LIP neurons proved to be significantly tuned to multiple shape dimensions. The population of LIP neurons that were tested showed barely significant size invariance. Position invariance was present in a minority of the neurons tested. Many LIP neurons displayed spurious shape selectivity arising from accidental interactions between the stimulus and the receptive field. We observed pronounced differences in the receptive field profiles determined by presenting two different shapes. Almost all LIP neurons showed spatially selective saccadic activity, but the receptive field for saccades did not always correspond to the receptive field as determined using shapes. Our results demonstrate that a subpopulation of LIP neurons encodes stimulus shape. Furthermore, the shape representation in the dorsal visual stream appears to differ radically from the known representation of shape in the ventral visual stream.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The analysis of object shape is critical for both object recognition and grasping. Areas in the intraparietal sulcus of the rhesus monkey are important for the visuomotor transformations underlying actions directed toward objects. The lateral intraparietal (LIP) area has strong anatomical connections with the anterior intraparietal area, which is known to control the shaping of the hand during grasping, and LIP neurons can respond selectively to simple two-dimensional shapes. Here we investigate the shape representation in area LIP of awake rhesus monkeys. Specifically, we determined to what extent LIP neurons are tuned to shape dimensions known to be relevant for grasping and assessed the invariance of their shape preferences with regard to changes in stimulus size and position in the receptive field. Most LIP neurons proved to be significantly tuned to multiple shape dimensions. The population of LIP neurons that were tested showed barely significant size invariance. Position invariance was present in a minority of the neurons tested. Many LIP neurons displayed spurious shape selectivity arising from accidental interactions between the stimulus and the receptive field. We observed pronounced differences in the receptive field profiles determined by presenting two different shapes. Almost all LIP neurons showed spatially selective saccadic activity, but the receptive field for saccades did not always correspond to the receptive field as determined using shapes. Our results demonstrate that a subpopulation of LIP neurons encodes stimulus shape. Furthermore, the shape representation in the dorsal visual stream appears to differ radically from the known representation of shape in the ventral visual stream. |
Nan Jia; Scott L Brincat; Andrés F Salazar-Gómez; Mikhail Panko; Frank H Guenther; Earl K Miller Decoding of intended saccade direction in an oculomotor brain-computer interface Journal Article Journal of Neural Engineering, 14 (4), pp. 1–13, 2017. @article{Jia2017a, title = {Decoding of intended saccade direction in an oculomotor brain-computer interface}, author = {Nan Jia and Scott L Brincat and Andrés F Salazar-Gómez and Mikhail Panko and Frank H Guenther and Earl K Miller}, doi = {10.1088/1741-2552/aa5a3e}, year = {2017}, date = {2017-01-01}, journal = {Journal of Neural Engineering}, volume = {14}, number = {4}, pages = {1--13}, abstract = {OBJECTIVE: To date, invasive brain-computer interface (BCI) research has largely focused on replacing lost limb functions using signals from of hand/arm areas of motor cortex. However, the oculomotor system may be better suited to BCI applications involving rapid serial selection from spatial targets, such as choosing from a set of possible words displayed on a computer screen in an augmentative and alternative communication (AAC) application. Here we aimed to demonstrate the feasibility of a BCI utilizing the oculomotor system. APPROACH: We developed a chronic intracortical BCI in monkeys to decode intended saccadic eye movement direction using activity from multiple frontal cortical areas. MAIN RESULTS: Intended saccade direction could be decoded in real time with high accuracy, particularly at contralateral locations. Accurate decoding was evident even at the beginning of the BCI session; no extensive BCI experience was necessary. High-frequency (80-500 Hz) local field potential magnitude provided the best performance, even over spiking activity, thus simplifying future BCI applications. Most of the information came from the frontal and supplementary eye fields, with relatively little contribution from dorsolateral prefrontal cortex. SIGNIFICANCE: Our results support the feasibility of high-accuracy intracortical oculomotor BCIs that require little or no practice to operate and may be ideally suited for 'point and click' computer operation as used in most current AAC systems.}, keywords = {}, pubstate = {published}, tppubtype = {article} } OBJECTIVE: To date, invasive brain-computer interface (BCI) research has largely focused on replacing lost limb functions using signals from of hand/arm areas of motor cortex. However, the oculomotor system may be better suited to BCI applications involving rapid serial selection from spatial targets, such as choosing from a set of possible words displayed on a computer screen in an augmentative and alternative communication (AAC) application. Here we aimed to demonstrate the feasibility of a BCI utilizing the oculomotor system. APPROACH: We developed a chronic intracortical BCI in monkeys to decode intended saccadic eye movement direction using activity from multiple frontal cortical areas. MAIN RESULTS: Intended saccade direction could be decoded in real time with high accuracy, particularly at contralateral locations. Accurate decoding was evident even at the beginning of the BCI session; no extensive BCI experience was necessary. High-frequency (80-500 Hz) local field potential magnitude provided the best performance, even over spiking activity, thus simplifying future BCI applications. Most of the information came from the frontal and supplementary eye fields, with relatively little contribution from dorsolateral prefrontal cortex. SIGNIFICANCE: Our results support the feasibility of high-accuracy intracortical oculomotor BCIs that require little or no practice to operate and may be ideally suited for 'point and click' computer operation as used in most current AAC systems. |
Yaoguang Jiang; Gopathy Purushothaman; Vivien A Casagrande The functional asymmetry of ON and OFF channels in the perception of contrast Journal Article Journal of Neurophysiology, 114 , pp. 2816–2829, 2015. @article{Jiang2015a, title = {The functional asymmetry of ON and OFF channels in the perception of contrast}, author = {Yaoguang Jiang and Gopathy Purushothaman and Vivien A Casagrande}, doi = {10.1152/jn.00560.2015}, year = {2015}, date = {2015-01-01}, journal = {Journal of Neurophysiology}, volume = {114}, pages = {2816--2829}, abstract = {To fully understand the relationship between perception and single neural responses, one should take into consideration the early stages of sensory processing. Few studies, however, have directly examined the neural underpinning of visual perception in the lateral geniculate nucleus (LGN), only one synapse away from the retina. In this study we recorded from LGN parvocellular (P) ON-center and OFF-center neurons while monkeys either passively viewed or actively detected a full range of contrasts. We found that OFF neurons were more sensitive in detecting negative contrasts than ON neurons were in detecting positive contrasts. Also, OFF neurons had higher spontaneous activities, higher peak response amplitudes, and were more sustained than ON neurons in their contrast responses. Puzzlingly, OFF neurons failed to show any significant correlations with the monkeys' perceptual choices, despite their greater contrast sensitivities. If, however, choice probabilities were calculated from interspike intervals instead of spike counts (thus taking into account the higher firing rates of OFF neurons), OFF neurons but not ON neurons were significantly correlated with behavioral choices. Taken together, these results demonstrate in awake, behaving animals that: 1) the ON and OFF pathways do not simply mirror each other in their functionality but instead carry qualitatively different types of information, and 2) the responses of ON and OFF neurons can be correlated with perceptual choices even in the absence of physical stimuli and interneuronal correlations.}, keywords = {}, pubstate = {published}, tppubtype = {article} } To fully understand the relationship between perception and single neural responses, one should take into consideration the early stages of sensory processing. Few studies, however, have directly examined the neural underpinning of visual perception in the lateral geniculate nucleus (LGN), only one synapse away from the retina. In this study we recorded from LGN parvocellular (P) ON-center and OFF-center neurons while monkeys either passively viewed or actively detected a full range of contrasts. We found that OFF neurons were more sensitive in detecting negative contrasts than ON neurons were in detecting positive contrasts. Also, OFF neurons had higher spontaneous activities, higher peak response amplitudes, and were more sustained than ON neurons in their contrast responses. Puzzlingly, OFF neurons failed to show any significant correlations with the monkeys' perceptual choices, despite their greater contrast sensitivities. If, however, choice probabilities were calculated from interspike intervals instead of spike counts (thus taking into account the higher firing rates of OFF neurons), OFF neurons but not ON neurons were significantly correlated with behavioral choices. Taken together, these results demonstrate in awake, behaving animals that: 1) the ON and OFF pathways do not simply mirror each other in their functionality but instead carry qualitatively different types of information, and 2) the responses of ON and OFF neurons can be correlated with perceptual choices even in the absence of physical stimuli and interneuronal correlations. |
Yaoguang Jiang; Dmitry Yampolsky; Gopathy Purushothaman; Vivien A Casagrande Perceptual decision related activity in the lateral geniculate nucleus Journal Article Journal of Neurophysiology, 114 (1), pp. 717–735, 2015. @article{Jiang2015b, title = {Perceptual decision related activity in the lateral geniculate nucleus}, author = {Yaoguang Jiang and Dmitry Yampolsky and Gopathy Purushothaman and Vivien A Casagrande}, doi = {10.1152/jn.00068.2015}, year = {2015}, date = {2015-07-01}, journal = {Journal of Neurophysiology}, volume = {114}, number = {1}, pages = {717--735}, publisher = {American Physiological Society Bethesda, MD}, abstract = {Fundamental to neuroscience is the understanding of how the language of neurons relates to behavior. In the lateral geniculate nucleus (LGN), cells show distinct properties such as selectivity for particular wavelengths, increments or decrements in contrast, or preference for fine detail versus rapid motion. No studies, however, have measured how LGN cells respond when an animal is challenged to make a perceptual decision using information within the receptive fields of those LGN cells. In this study we measured neural activity in the macaque LGN during a two alternative forced choice (2AFC) contrast detection task or during a passive fixation task, and found that a small proportion (13.5%) of single LGN parvocellular (P) and magnocellular (M) neurons matched the psychophysical performance of the monkey. The majority of LGN neurons measured in both tasks were not as sensitive as the monkey. The covariation between neural response and behavior (quantified as choice probability) was significantly above chance during active detection, even when there was no external stimulus. Interneuronal correlations and task-related gain modulations were negligible under the same condition. A bottom-up pooling model that compared sensory neural responses to make perceptual choices in the absence of interneuronal correlations could fully explain these results at the level of the LGN, supporting the hypothesis that the perceptual decision pool consists of multiple sensory neurons, and that response fluctuations in these neurons can influence perception.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Fundamental to neuroscience is the understanding of how the language of neurons relates to behavior. In the lateral geniculate nucleus (LGN), cells show distinct properties such as selectivity for particular wavelengths, increments or decrements in contrast, or preference for fine detail versus rapid motion. No studies, however, have measured how LGN cells respond when an animal is challenged to make a perceptual decision using information within the receptive fields of those LGN cells. In this study we measured neural activity in the macaque LGN during a two alternative forced choice (2AFC) contrast detection task or during a passive fixation task, and found that a small proportion (13.5%) of single LGN parvocellular (P) and magnocellular (M) neurons matched the psychophysical performance of the monkey. The majority of LGN neurons measured in both tasks were not as sensitive as the monkey. The covariation between neural response and behavior (quantified as choice probability) was significantly above chance during active detection, even when there was no external stimulus. Interneuronal correlations and task-related gain modulations were negligible under the same condition. A bottom-up pooling model that compared sensory neural responses to make perceptual choices in the absence of interneuronal correlations could fully explain these results at the level of the LGN, supporting the hypothesis that the perceptual decision pool consists of multiple sensory neurons, and that response fluctuations in these neurons can influence perception. |
Kevin Johnston; Michael J Koval; Stephen G Lomber; Stefan Everling Macaque dorsolateral prefrontal cortex does not suppress saccade-related activity in the superior colliculus Journal Article Cerebral Cortex, 24 (5), pp. 1373–1388, 2014. @article{Johnston2014, title = {Macaque dorsolateral prefrontal cortex does not suppress saccade-related activity in the superior colliculus}, author = {Kevin Johnston and Michael J Koval and Stephen G Lomber and Stefan Everling}, doi = {10.1093/cercor/bhs424}, year = {2014}, date = {2014-01-01}, journal = {Cerebral Cortex}, volume = {24}, number = {5}, pages = {1373--1388}, abstract = {Of the many functions ascribed to the dorsolateral prefrontal cortex (DLPFC), the ability to override automatic stimulus-driven behavior is one of the most prominent. This ability has been investigated extensively with the antisaccade task, which requires suppression of saccades toward suddenly appearing visual stimuli. Convergent lines of evidence have supported a model in which the DLPFC suppresses unwanted saccades by inhibiting saccade-related activity in the ipsilateral superior colliculus (SC), a midbrain oculomotor structure. Here, we carried out a direct test of this inhibitory model using unilateral cryogenic deactivation of the DLPFC within the caudal principal sulcus (cPS) and simultaneous single-neuron recording of SC saccade-related neurons in monkeys performing saccades and antisaccades. Contrary to the inhibition model, which predicts that attenuation of inhibition effected by unilateral cPS deactivation should result in activity increases in ipsilateral and decreases in contralateral SC, we observed a delayed onset of saccade-related activity in the ipsilateral SC, and activity increases in the contralateral SC. These effects were mirrored by increased error rates of ipsiversive antisaccades, and reaction times of contraversive saccades. These data challenge the inhibitory model and suggest instead that the primary influence of the DLPFC on the SC is excitatory.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Of the many functions ascribed to the dorsolateral prefrontal cortex (DLPFC), the ability to override automatic stimulus-driven behavior is one of the most prominent. This ability has been investigated extensively with the antisaccade task, which requires suppression of saccades toward suddenly appearing visual stimuli. Convergent lines of evidence have supported a model in which the DLPFC suppresses unwanted saccades by inhibiting saccade-related activity in the ipsilateral superior colliculus (SC), a midbrain oculomotor structure. Here, we carried out a direct test of this inhibitory model using unilateral cryogenic deactivation of the DLPFC within the caudal principal sulcus (cPS) and simultaneous single-neuron recording of SC saccade-related neurons in monkeys performing saccades and antisaccades. Contrary to the inhibition model, which predicts that attenuation of inhibition effected by unilateral cPS deactivation should result in activity increases in ipsilateral and decreases in contralateral SC, we observed a delayed onset of saccade-related activity in the ipsilateral SC, and activity increases in the contralateral SC. These effects were mirrored by increased error rates of ipsiversive antisaccades, and reaction times of contraversive saccades. These data challenge the inhibitory model and suggest instead that the primary influence of the DLPFC on the SC is excitatory. |
Kevin D Johnston; Kevin Barker; David Schaeffer; Lauren Schaeffer; Stefan Everling Methods for chair restraint and training of the common marmoset on oculomotor tasks Journal Article Journal of Neurophysiology, 119 (5), pp. 1636–1646, 2018. @article{Johnston2018, title = {Methods for chair restraint and training of the common marmoset on oculomotor tasks}, author = {Kevin D Johnston and Kevin Barker and David Schaeffer and Lauren Schaeffer and Stefan Everling}, doi = {10.1152/jn.00866.2017}, year = {2018}, date = {2018-01-01}, journal = {Journal of Neurophysiology}, volume = {119}, number = {5}, pages = {1636--1646}, abstract = {The oculomotor system is the most thoroughly understood sensorimotor system in the brain, due in large part to electrophysiological studies carried out in macaque monkeys trained to perform oculomotor tasks. A disadvantage of the macaque model is that many cortical oculomotor areas of interest lie within sulci, making high-density array and laminar recordings impractical. Many techniques of molecular biology developed in rodents, such as optogenetic manipulation of neuronal subtypes, are also limited in this species. The common marmoset (Callithrix jacchus) possesses a smooth cortex, allowing easy access to frontoparietal oculomotor areas, and may bridge the gap between systems neuroscience in macaques and molecular techniques. Techniques for restraint, training, and neural recording in these animals have been well developed in auditory neuroscience. Those for oculomotor neuroscience, however, remain at a relatively early stage. In this article we provide details of a custom-designed restraint chair for marmosets, a combination head restraint/recording chamber allowing access to cortical oculomotor areas and providing stability suitable for eye movement and neural recordings, as well as a training protocol for oculomotor tasks. We additionally report the results of a psychophysical study in marmosets trained to perform a saccade task using these methods, showing that, as in rhesus and humans, marmosets exhibit a “gap effect,” a decrease in reaction time when the fixation stimulus is removed before the onset of a visual saccade target. These results are the first evidence of this effect in marmosets and support the common marmoset model for neurophysiological investigations of oculomotor control.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The oculomotor system is the most thoroughly understood sensorimotor system in the brain, due in large part to electrophysiological studies carried out in macaque monkeys trained to perform oculomotor tasks. A disadvantage of the macaque model is that many cortical oculomotor areas of interest lie within sulci, making high-density array and laminar recordings impractical. Many techniques of molecular biology developed in rodents, such as optogenetic manipulation of neuronal subtypes, are also limited in this species. The common marmoset (Callithrix jacchus) possesses a smooth cortex, allowing easy access to frontoparietal oculomotor areas, and may bridge the gap between systems neuroscience in macaques and molecular techniques. Techniques for restraint, training, and neural recording in these animals have been well developed in auditory neuroscience. Those for oculomotor neuroscience, however, remain at a relatively early stage. In this article we provide details of a custom-designed restraint chair for marmosets, a combination head restraint/recording chamber allowing access to cortical oculomotor areas and providing stability suitable for eye movement and neural recordings, as well as a training protocol for oculomotor tasks. We additionally report the results of a psychophysical study in marmosets trained to perform a saccade task using these methods, showing that, as in rhesus and humans, marmosets exhibit a “gap effect,” a decrease in reaction time when the fixation stimulus is removed before the onset of a visual saccade target. These results are the first evidence of this effect in marmosets and support the common marmoset model for neurophysiological investigations of oculomotor control. |
Helen E Jones; Ian M Andolina; Stewart D Shipp; Daniel L Adams; Javier Cudeiro; Thomas E Salt; Adam M Sillito Figure-ground modulation in awake primate thalamus Journal Article Proceedings of the National Academy of Sciences, 112 (22), pp. 7085–7090, 2015. @article{Jones2015, title = {Figure-ground modulation in awake primate thalamus}, author = {Helen E Jones and Ian M Andolina and Stewart D Shipp and Daniel L Adams and Javier Cudeiro and Thomas E Salt and Adam M Sillito}, doi = {10.1073/pnas.1405162112}, year = {2015}, date = {2015-01-01}, journal = {Proceedings of the National Academy of Sciences}, volume = {112}, number = {22}, pages = {7085--7090}, abstract = {Figure-ground discrimination refers to the perception of an object, the figure, against a nondescript background. Neural mechanisms of figure-ground detection have been associated with feedback interactions between higher centers and primary visual cortex and have been held to index the effect of global analysis on local feature encoding. Here, in recordings from visual thalamus of alert primates, we demonstrate a robust enhancement of neuronal firing when the figure, as opposed to the ground, component of a motion-defined figure-ground stimulus is located over the receptive field. In this paradigm, visual stimulation of the receptive field and its near environs is identical across both conditions, suggesting the response enhancement reflects higher integrative mechanisms. It thus appears that cortical activity generating the higher-order percept of the figure is simultaneously reentered into the lowest level that is anatomically possible (the thalamus), so that the signature of the evolving representation of the figure is imprinted on the input driving it in an iterative process.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Figure-ground discrimination refers to the perception of an object, the figure, against a nondescript background. Neural mechanisms of figure-ground detection have been associated with feedback interactions between higher centers and primary visual cortex and have been held to index the effect of global analysis on local feature encoding. Here, in recordings from visual thalamus of alert primates, we demonstrate a robust enhancement of neuronal firing when the figure, as opposed to the ground, component of a motion-defined figure-ground stimulus is located over the receptive field. In this paradigm, visual stimulation of the receptive field and its near environs is identical across both conditions, suggesting the response enhancement reflects higher integrative mechanisms. It thus appears that cortical activity generating the higher-order percept of the figure is simultaneously reentered into the lowest level that is anatomically possible (the thalamus), so that the signature of the evolving representation of the figure is imprinted on the input driving it in an iterative process. |
Siddhartha Joshi; Yin Li; Rishi M Kalwani; Joshua I Gold Relationships between pupil diameter and neuronal activity in the locus coeruleus, colliculi, and cingulate cortex Journal Article Neuron, 89 (1), pp. 221–234, 2016. @article{Joshi2016, title = {Relationships between pupil diameter and neuronal activity in the locus coeruleus, colliculi, and cingulate cortex}, author = {Siddhartha Joshi and Yin Li and Rishi M Kalwani and Joshua I Gold}, doi = {10.1016/j.neuron.2015.11.028}, year = {2016}, date = {2016-01-01}, journal = {Neuron}, volume = {89}, number = {1}, pages = {221--234}, publisher = {Elsevier Inc.}, abstract = {Changes in pupil diameter that reflect effort and other cognitive factors are often interpreted in terms of the activity of norepinephrine-containing neurons in the brainstem nucleus locus coeruleus (LC), but there is little direct evidence for such a relationship. Here, we show that LC activation reliably anticipates changes in pupil diameter that either fluctuate naturally or are driven by external events during near fixation, as in many psychophysical tasks. This relationship occurs on as fine a temporal and spatial scale as single spikes from single units. However, this relationship is not specific to the LC. Similar relationships, albeit with delayed timing and different reliabilities across sites, are evident in the inferior and superior colliculus and anterior and posterior cingulate cortex. Because these regions are interconnected with the LC, the results suggest that non-luminance-mediated changes in pupil diameter might reflect LC-mediated coordination of neuronal activity throughout some parts of the brain. Joshi et al. found that changes in pupil diameter can reflect neural activity in the locus coeruleus (LC) and, less reliably, several other interconnected structures. The results suggest that LC-mediated arousal may coordinate activity throughout some parts of the brain.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Changes in pupil diameter that reflect effort and other cognitive factors are often interpreted in terms of the activity of norepinephrine-containing neurons in the brainstem nucleus locus coeruleus (LC), but there is little direct evidence for such a relationship. Here, we show that LC activation reliably anticipates changes in pupil diameter that either fluctuate naturally or are driven by external events during near fixation, as in many psychophysical tasks. This relationship occurs on as fine a temporal and spatial scale as single spikes from single units. However, this relationship is not specific to the LC. Similar relationships, albeit with delayed timing and different reliabilities across sites, are evident in the inferior and superior colliculus and anterior and posterior cingulate cortex. Because these regions are interconnected with the LC, the results suggest that non-luminance-mediated changes in pupil diameter might reflect LC-mediated coordination of neuronal activity throughout some parts of the brain. Joshi et al. found that changes in pupil diameter can reflect neural activity in the locus coeruleus (LC) and, less reliably, several other interconnected structures. The results suggest that LC-mediated arousal may coordinate activity throughout some parts of the brain. |
Yoshinao Kajikawa; John F Smiley; Charles E Schroeder Primary generators of visually evoked field potentials recorded in the macaque auditory cortex Journal Article Journal of Neuroscience, 37 (42), pp. 10139–10153, 2017. @article{Kajikawa2017, title = {Primary generators of visually evoked field potentials recorded in the macaque auditory cortex}, author = {Yoshinao Kajikawa and John F Smiley and Charles E Schroeder}, doi = {10.1523/JNEUROSCI.3800-16.2017}, year = {2017}, date = {2017-01-01}, journal = {Journal of Neuroscience}, volume = {37}, number = {42}, pages = {10139--10153}, abstract = {Prior studies have reported “local” field potential (LFP) responses to faces in the macaque auditory cortex and have suggested that such face-LFPs may be substrates of audiovisual integration. However, although field potentials (FPs) may reflect the synaptic currents of neurons near the recording electrode, due to the use of a distant reference electrode, they often reflect those of synaptic activity occurring in distant sites as well. Thus, FP recordings within a given brain region (e.g., auditory cortex) may be “contaminated” by activity generated elsewhere in the brain. To determine whether face responses are indeed generated within macaque auditory cortex, we recorded FPs and concomitant multiunit activity with linear array multielectrodes across auditory cortex in three macaques (one female), and applied current source density (CSD) analysis to the laminar FP profile. CSD analysis revealed no appreciable local generator contribution to the visual FP in auditory cortex, although we did note an increase in the amplitude of visual FP with cortical depth, suggesting that their generators are located below auditory cortex. In the underlying inferotemporal cortex, we found polarity inversions of the main visual FP components accompanied by robust CSD responses and large-amplitude multiunit activity. These results indicate that face-evoked FP responses in auditory cortex are not generated locally but are volume-conducted from other face-responsive regions. In broader terms, our results underscore the caution that, unless far-field contamination is removed, LFPs in general may reflect such “far-field” activity, in addition to, or in absence of, local synaptic responses.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Prior studies have reported “local” field potential (LFP) responses to faces in the macaque auditory cortex and have suggested that such face-LFPs may be substrates of audiovisual integration. However, although field potentials (FPs) may reflect the synaptic currents of neurons near the recording electrode, due to the use of a distant reference electrode, they often reflect those of synaptic activity occurring in distant sites as well. Thus, FP recordings within a given brain region (e.g., auditory cortex) may be “contaminated” by activity generated elsewhere in the brain. To determine whether face responses are indeed generated within macaque auditory cortex, we recorded FPs and concomitant multiunit activity with linear array multielectrodes across auditory cortex in three macaques (one female), and applied current source density (CSD) analysis to the laminar FP profile. CSD analysis revealed no appreciable local generator contribution to the visual FP in auditory cortex, although we did note an increase in the amplitude of visual FP with cortical depth, suggesting that their generators are located below auditory cortex. In the underlying inferotemporal cortex, we found polarity inversions of the main visual FP components accompanied by robust CSD responses and large-amplitude multiunit activity. These results indicate that face-evoked FP responses in auditory cortex are not generated locally but are volume-conducted from other face-responsive regions. In broader terms, our results underscore the caution that, unless far-field contamination is removed, LFPs in general may reflect such “far-field” activity, in addition to, or in absence of, local synaptic responses. |
R M Kalwani; S Joshi; J I Gold Phasic activation of individual neurons in the locus ceruleus/subceruleus complex of monkeys reflects rewarded decisions to go but not stop Journal Article Journal of Neuroscience, 34 (41), pp. 13656–13669, 2014. @article{Kalwani2014, title = {Phasic activation of individual neurons in the locus ceruleus/subceruleus complex of monkeys reflects rewarded decisions to go but not stop}, author = {R M Kalwani and S Joshi and J I Gold}, doi = {10.1523/JNEUROSCI.2566-14.2014}, year = {2014}, date = {2014-01-01}, journal = {Journal of Neuroscience}, volume = {34}, number = {41}, pages = {13656--13669}, abstract = {Neurons in the brainstem nucleus locus ceruleus (LC) often exhibit phasic activation in the context of simple sensory-motor tasks. The functional role of this activation, which leads to the release of norepinephrine throughout the brain, is not yet understood in part because the conditions under which it occurs remain in question. Early studies focused on the relationship of LC phasic activation to salient sensory events, whereas more recent work has emphasized its timing relative to goal-directed behavioral responses, possibly representing the end of a sensory-motor decision process. To better understand the relationship between LC phasic activation and sensory, motor, and decision processing, we recorded spiking activity of neurons in the LC+ (LC and the adjacent, norepinephrine-containing subceruleus nucleus) of monkeys performing a countermanding task. The task required the monkeys to occasionally withhold planned, saccadic eye movements to a visual target. We found that many well isolated LC+ units responded to both the onset of the visual cue instructing the monkey to initiate the saccade and again after saccade onset, even when it was initiated erroneously in the presence of a stop signal. Many of these neurons did not respond to saccades made outside of the task context. In contrast, neither the appearance of the stop signal nor the successful withholding of the saccade elicited an LC+ response. Therefore, LC+ phasic activation encodes sensory and motor events related to decisions to execute, but not withhold, movements, implying a functional role in goal-directed actions, but not necessarily more covert forms of processing.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Neurons in the brainstem nucleus locus ceruleus (LC) often exhibit phasic activation in the context of simple sensory-motor tasks. The functional role of this activation, which leads to the release of norepinephrine throughout the brain, is not yet understood in part because the conditions under which it occurs remain in question. Early studies focused on the relationship of LC phasic activation to salient sensory events, whereas more recent work has emphasized its timing relative to goal-directed behavioral responses, possibly representing the end of a sensory-motor decision process. To better understand the relationship between LC phasic activation and sensory, motor, and decision processing, we recorded spiking activity of neurons in the LC+ (LC and the adjacent, norepinephrine-containing subceruleus nucleus) of monkeys performing a countermanding task. The task required the monkeys to occasionally withhold planned, saccadic eye movements to a visual target. We found that many well isolated LC+ units responded to both the onset of the visual cue instructing the monkey to initiate the saccade and again after saccade onset, even when it was initiated erroneously in the presence of a stop signal. Many of these neurons did not respond to saccades made outside of the task context. In contrast, neither the appearance of the stop signal nor the successful withholding of the saccade elicited an LC+ response. Therefore, LC+ phasic activation encodes sensory and motor events related to decisions to execute, but not withhold, movements, implying a functional role in goal-directed actions, but not necessarily more covert forms of processing. |
Peter Kaposvari; Susheel Kumar; Rufin Vogels Statistical learning signals in macaque inferior temporal cortex Journal Article Cerebral Cortex, 28 (1), pp. 250–266, 2018. @article{Kaposvari2018, title = {Statistical learning signals in macaque inferior temporal cortex}, author = {Peter Kaposvari and Susheel Kumar and Rufin Vogels}, doi = {10.1093/cercor/bhw374}, year = {2018}, date = {2018-01-01}, journal = {Cerebral Cortex}, volume = {28}, number = {1}, pages = {250--266}, abstract = {Humans are sensitive to statistical regularities in their visual environment, but the nature of the underlying neural statistical learning signals still remains to be clarified. As in human behavioral and neuroimaging studies of statistical learning, we exposed rhesus monkeys to a continuous stream of images, presented without interstimulus interval or reward association. The stimulus set consisted of 3 groups of 5 images each (quintets). The stimulus order within each quintet was fixed, but the quintets were presented repeatedly in a random order without interruption. Thus, only transitional probabilities defined quintets of images. Postexposure recordings in inferior temporal (IT) cortex showed an enhanced response to stimuli that violated the exposed sequence. This enhancement was found only for stimuli that were not predicted by the just preceding stimulus, reflecting a temporally adjacent stimulus relationship, and was sensitive to stimulus order. By comparing IT responses with sequences with and without statistical regularities, we observed a short latency, transient response suppression for stimuli of the sequence with regularities, in addition to a later sustained response enhancement to stimuli that violated the sequence with regularities. These findings constrain models of mechanisms underlying neural responses in predictable temporal sequences, such as predictive coding.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Humans are sensitive to statistical regularities in their visual environment, but the nature of the underlying neural statistical learning signals still remains to be clarified. As in human behavioral and neuroimaging studies of statistical learning, we exposed rhesus monkeys to a continuous stream of images, presented without interstimulus interval or reward association. The stimulus set consisted of 3 groups of 5 images each (quintets). The stimulus order within each quintet was fixed, but the quintets were presented repeatedly in a random order without interruption. Thus, only transitional probabilities defined quintets of images. Postexposure recordings in inferior temporal (IT) cortex showed an enhanced response to stimuli that violated the exposed sequence. This enhancement was found only for stimuli that were not predicted by the just preceding stimulus, reflecting a temporally adjacent stimulus relationship, and was sensitive to stimulus order. By comparing IT responses with sequences with and without statistical regularities, we observed a short latency, transient response suppression for stimuli of the sequence with regularities, in addition to a later sustained response enhancement to stimuli that violated the sequence with regularities. These findings constrain models of mechanisms underlying neural responses in predictable temporal sequences, such as predictive coding. |
Kohitij Kar; Bart Krekelberg Testing the assumptions underlying fMRI adaptation using intracortical recordings in area MT Journal Article Cortex, 80 , pp. 21–34, 2016. @article{Kar2016, title = {Testing the assumptions underlying fMRI adaptation using intracortical recordings in area MT}, author = {Kohitij Kar and Bart Krekelberg}, doi = {10.1016/j.cortex.2015.12.011}, year = {2016}, date = {2016-01-01}, journal = {Cortex}, volume = {80}, pages = {21--34}, publisher = {Elsevier Ltd}, abstract = {We investigated how neural activity in the middle temporal area of the macaque monkey changes after 3 sec of exposure to a visual stimulus and used this to gain insight into the assumptions underlying the fMRI adaptation method (fMRIa). We studied both changes in tuning curves following weak and strong motion stimuli (adaptation) and the differences between a first and second exposure to the same stimulus (repetition suppression). Typically, tuning curves had smaller amplitudes and narrower tuning widths after strong adaptation; this was true for single neurons, multi-unit activity (MUA), the evoked local field potential (LFP), as well as gamma band activity. Repetition typically led to reduced responses. This reduction was correlated with direction selectivity and not explained by neural fatigue. Our data, however, warn against a simplistic view of the consequences of adaptation. First, a considerable fraction of neurons and sites showed response enhancements after adaptation, especially when probed with a stimulus that moved opposite to the direction of the adapting stimulus. Second, adaptation was stimulus selective only on a time scale of ∼100 msec. Third, aggregate measures of neural activity (MUA, LFPs) had substantially different adaptation effects. Fourth, there were qualitative differences between our findings in MT and earlier findings in IT cortex. We conclude that selective adaptation effects in fMRIa are relatively easy to miss even when they exist (for instance by presenting stimuli for too long, or because neurons that enhance after adaptation cancel out the effect of neurons that suppress). Moreover, we argue that adaptation should be understood in the context of the computations that a neural circuit perform. Using fMRIa as a tool to uncover neural selectivity requires a better understanding of this circuitry and its consequences for adaptation.}, keywords = {}, pubstate = {published}, tppubtype = {article} } We investigated how neural activity in the middle temporal area of the macaque monkey changes after 3 sec of exposure to a visual stimulus and used this to gain insight into the assumptions underlying the fMRI adaptation method (fMRIa). We studied both changes in tuning curves following weak and strong motion stimuli (adaptation) and the differences between a first and second exposure to the same stimulus (repetition suppression). Typically, tuning curves had smaller amplitudes and narrower tuning widths after strong adaptation; this was true for single neurons, multi-unit activity (MUA), the evoked local field potential (LFP), as well as gamma band activity. Repetition typically led to reduced responses. This reduction was correlated with direction selectivity and not explained by neural fatigue. Our data, however, warn against a simplistic view of the consequences of adaptation. First, a considerable fraction of neurons and sites showed response enhancements after adaptation, especially when probed with a stimulus that moved opposite to the direction of the adapting stimulus. Second, adaptation was stimulus selective only on a time scale of ∼100 msec. Third, aggregate measures of neural activity (MUA, LFPs) had substantially different adaptation effects. Fourth, there were qualitative differences between our findings in MT and earlier findings in IT cortex. We conclude that selective adaptation effects in fMRIa are relatively easy to miss even when they exist (for instance by presenting stimuli for too long, or because neurons that enhance after adaptation cancel out the effect of neurons that suppress). Moreover, we argue that adaptation should be understood in the context of the computations that a neural circuit perform. Using fMRIa as a tool to uncover neural selectivity requires a better understanding of this circuitry and its consequences for adaptation. |
Kohitij Kar; Jacob Duijnhouwer; Bart Krekelberg Transcranial alternating current stimulation attenuates neuronal adaptation Journal Article Journal of Neuroscience, 37 (9), pp. 2325–2335, 2017. @article{Kar2017, title = {Transcranial alternating current stimulation attenuates neuronal adaptation}, author = {Kohitij Kar and Jacob Duijnhouwer and Bart Krekelberg}, doi = {10.1523/JNEUROSCI.2266-16.2016}, year = {2017}, date = {2017-01-01}, journal = {Journal of Neuroscience}, volume = {37}, number = {9}, pages = {2325--2335}, abstract = {We previously showed that brief application of 2 mA (peak-to-peak) transcranial currents alternating at 10 Hz significantly reduces motion adaptation in humans. This is but one of many behavioral studies showing that weak currents applied to the scalp modulate neural processing. Transcranial stimulation has been shown to improve perception, learning, and a range of clinical symptoms. Few studies, however, have measured the neural consequences of transcranial current stimulation. We capitalized on the strong link between motion perception and neural activity in the middle temporal (MT) area of the macaque monkey to study the neural mechanisms that underlie the behavioral consequences of transcranial alternating current stimulation. First, we observed that 2 mA currents generated substantial intracranial fields, which were much stronger in the stimulated hemisphere (0.12 V/m) than on the opposite side of the brain (0.03 V/m). Second, we found that brief application of transcranial alternating current stimulation at 10 Hz reduced spike-frequency adaptation of MT neurons and led to a broadband increase in the power spectrum of local field potentials. Together, these findings provide a direct demonstration that weak electric fields applied to the scalp significantly affect neural processing in the primate brain and that this includes a hitherto unknown mechanism that attenuates sensory adaptation.}, keywords = {}, pubstate = {published}, tppubtype = {article} } We previously showed that brief application of 2 mA (peak-to-peak) transcranial currents alternating at 10 Hz significantly reduces motion adaptation in humans. This is but one of many behavioral studies showing that weak currents applied to the scalp modulate neural processing. Transcranial stimulation has been shown to improve perception, learning, and a range of clinical symptoms. Few studies, however, have measured the neural consequences of transcranial current stimulation. We capitalized on the strong link between motion perception and neural activity in the middle temporal (MT) area of the macaque monkey to study the neural mechanisms that underlie the behavioral consequences of transcranial alternating current stimulation. First, we observed that 2 mA currents generated substantial intracranial fields, which were much stronger in the stimulated hemisphere (0.12 V/m) than on the opposite side of the brain (0.03 V/m). Second, we found that brief application of transcranial alternating current stimulation at 10 Hz reduced spike-frequency adaptation of MT neurons and led to a broadband increase in the power spectrum of local field potentials. Together, these findings provide a direct demonstration that weak electric fields applied to the scalp significantly affect neural processing in the primate brain and that this includes a hitherto unknown mechanism that attenuates sensory adaptation. |
Leor N Katz; Jacob L Yates; Jonathan W Pillow; Alexander C Huk Dissociated functional significance of decision-related activity in the primate dorsal stream Journal Article Nature, 535 , pp. 285–288, 2016. @article{Katz2016, title = {Dissociated functional significance of decision-related activity in the primate dorsal stream}, author = {Leor N Katz and Jacob L Yates and Jonathan W Pillow and Alexander C Huk}, doi = {10.1038/nature18617}, year = {2016}, date = {2016-01-01}, journal = {Nature}, volume = {535}, pages = {285--288}, publisher = {Nature Publishing Group}, abstract = {During decision making, neurons in multiple brain regions exhibit responses that are correlated with decisions. However, it remains uncertain whether or not various forms of decision-related activity are causally related to decision making. Here we address this question by recording and reversibly inactivating the lateral intraparietal (LIP) and middle temporal (MT) areas of rhesus macaques performing a motion direction discrimination task. Neurons in area LIP exhibited firing rate patterns that directly resembled the evidence accumulation process posited to govern decision making, with strong correlations between their response fluctuations and the animal's choices. Neurons in area MT, in contrast, exhibited weak correlations between their response fluctuations and choices, and had firing rate patterns consistent with their sensory role in motion encoding. The behavioural impact of pharmacological inactivation of each area was inversely related to their degree of decision-related activity: while inactivation of neurons in MT profoundly impaired psychophysical performance, inactivation in LIP had no measurable impact on decision-making performance, despite having silenced the very clusters that exhibited strong decision-related activity. Although LIP inactivation did not impair psychophysical behaviour, it did influence spatial selection and oculomotor metrics in a free-choice control task. The absence of an effect on perceptual decision making was stable over trials and sessions and was robust to changes in stimulus type and task geometry, arguing against several forms of compensation. Thus, decision-related signals in LIP do not appear to be critical for computing perceptual decisions, and may instead reflect secondary processes. Our findings highlight a dissociation between decision correlation and causation, showing that strong neuron-decision correlations do not necessarily offer direct access to the neural computations underlying decisions.}, keywords = {}, pubstate = {published}, tppubtype = {article} } During decision making, neurons in multiple brain regions exhibit responses that are correlated with decisions. However, it remains uncertain whether or not various forms of decision-related activity are causally related to decision making. Here we address this question by recording and reversibly inactivating the lateral intraparietal (LIP) and middle temporal (MT) areas of rhesus macaques performing a motion direction discrimination task. Neurons in area LIP exhibited firing rate patterns that directly resembled the evidence accumulation process posited to govern decision making, with strong correlations between their response fluctuations and the animal's choices. Neurons in area MT, in contrast, exhibited weak correlations between their response fluctuations and choices, and had firing rate patterns consistent with their sensory role in motion encoding. The behavioural impact of pharmacological inactivation of each area was inversely related to their degree of decision-related activity: while inactivation of neurons in MT profoundly impaired psychophysical performance, inactivation in LIP had no measurable impact on decision-making performance, despite having silenced the very clusters that exhibited strong decision-related activity. Although LIP inactivation did not impair psychophysical behaviour, it did influence spatial selection and oculomotor metrics in a free-choice control task. The absence of an effect on perceptual decision making was stable over trials and sessions and was robust to changes in stimulus type and task geometry, arguing against several forms of compensation. Thus, decision-related signals in LIP do not appear to be critical for computing perceptual decisions, and may instead reflect secondary processes. Our findings highlight a dissociation between decision correlation and causation, showing that strong neuron-decision correlations do not necessarily offer direct access to the neural computations underlying decisions. |
Katsuhisa Kawaguchi; Stephane Clery; Paria Pourriahi; Lenka Seillier; Ralf M Haefner; Hendrikje Nienborg Differentiating between models of perceptual decision making using pupil size inferred confidence Journal Article Journal of Neuroscience, 38 (41), pp. 8874–8888, 2018. @article{Kawaguchi2018, title = {Differentiating between models of perceptual decision making using pupil size inferred confidence}, author = {Katsuhisa Kawaguchi and Stephane Clery and Paria Pourriahi and Lenka Seillier and Ralf M Haefner and Hendrikje Nienborg}, doi = {10.1523/jneurosci.0735-18.2018}, year = {2018}, date = {2018-01-01}, journal = {Journal of Neuroscience}, volume = {38}, number = {41}, pages = {8874--8888}, abstract = {During perceptual decisions, subjects often rely more strongly on early, rather than late, sensory evidence, even in tasks when both are equally informative about the correct decision. This early psychophysical weighting has been explained by an integration-to-bound decision process, in which the stimulus is ignored after the accumulated evidence reaches a certain bound, or confidence level. Here, we derive predictions about how the average temporal weighting of the evidence depends on a subject's decision confidence in this model. To test these predictions empirically, we devised a method to infer decision confidence from pupil size in 2 male monkeys performing a disparity discrimination task. Our animals' data confirmed the integration-to-bound predictions, with different internal decision bounds and different levels of correlation between pupil size and decision confidence accounting for differences between animals. However, the data were less compatible with two alternative accounts for early psychophysical weighting: attractor dynamics either within the decision area or due to feedback to sensory areas, or a feedforward account due to neuronal response adaptation. This approach also opens the door to using confidence more broadly when studying the neural basis of decision making.}, keywords = {}, pubstate = {published}, tppubtype = {article} } During perceptual decisions, subjects often rely more strongly on early, rather than late, sensory evidence, even in tasks when both are equally informative about the correct decision. This early psychophysical weighting has been explained by an integration-to-bound decision process, in which the stimulus is ignored after the accumulated evidence reaches a certain bound, or confidence level. Here, we derive predictions about how the average temporal weighting of the evidence depends on a subject's decision confidence in this model. To test these predictions empirically, we devised a method to infer decision confidence from pupil size in 2 male monkeys performing a disparity discrimination task. Our animals' data confirmed the integration-to-bound predictions, with different internal decision bounds and different levels of correlation between pupil size and decision confidence accounting for differences between animals. However, the data were less compatible with two alternative accounts for early psychophysical weighting: attractor dynamics either within the decision area or due to feedback to sensory areas, or a feedforward account due to neuronal response adaptation. This approach also opens the door to using confidence more broadly when studying the neural basis of decision making. |
Keisuke Kawasaki; David L Sheinberg Learning to recognize visual objects with microstimulation in inferior temporal cortex Journal Article Journal of Neurophysiology, 100 (1), pp. 197–211, 2008. @article{Kawasaki2008, title = {Learning to recognize visual objects with microstimulation in inferior temporal cortex}, author = {Keisuke Kawasaki and David L Sheinberg}, doi = {10.1152/jn.90247.2008}, year = {2008}, date = {2008-01-01}, journal = {Journal of Neurophysiology}, volume = {100}, number = {1}, pages = {197--211}, abstract = {The malleability of object representations by experience is essential for adaptive behavior. It has been hypothesized that neurons in inferior temporal cortex (IT) in monkeys are pivotal in visual association learning, evidenced by experiments revealing changes in neural selectivity following visual learning, as well as by lesion studies, wherein functional inactivation of IT impairs learning. A critical question remaining to be answered is whether IT neuronal activity is sufficient for learning. To address this question directly, we conducted experiments combining visual classification learning with microstimulation in IT. We assessed the effects of IT microstimulation during learning in cases where the stimulation was exclusively informative, conditionally informative, and informative but not necessary for the classification task. The results show that localized microstimulation in IT can be used to establish visual classification learning, and the same stimulation applied during learning can predictably bias judgments on subsequent recognition. The effect of induced activity can be explained neither by direct stimulation-motor association nor by simple detection of cortical stimulation. We also found that the learning effects are specific to IT stimulation as they are not observed by microstimulation in an adjacent auditory area. Our results add the evidence that the differential activity in IT during visual association learning is sufficient for establishing new associations. The results suggest that experimentally manipulated activity patterns within IT can be effectively combined with ongoing visually induced activity during the formation of new associations.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The malleability of object representations by experience is essential for adaptive behavior. It has been hypothesized that neurons in inferior temporal cortex (IT) in monkeys are pivotal in visual association learning, evidenced by experiments revealing changes in neural selectivity following visual learning, as well as by lesion studies, wherein functional inactivation of IT impairs learning. A critical question remaining to be answered is whether IT neuronal activity is sufficient for learning. To address this question directly, we conducted experiments combining visual classification learning with microstimulation in IT. We assessed the effects of IT microstimulation during learning in cases where the stimulation was exclusively informative, conditionally informative, and informative but not necessary for the classification task. The results show that localized microstimulation in IT can be used to establish visual classification learning, and the same stimulation applied during learning can predictably bias judgments on subsequent recognition. The effect of induced activity can be explained neither by direct stimulation-motor association nor by simple detection of cortical stimulation. We also found that the learning effects are specific to IT stimulation as they are not observed by microstimulation in an adjacent auditory area. Our results add the evidence that the differential activity in IT during visual association learning is sufficient for establishing new associations. The results suggest that experimentally manipulated activity patterns within IT can be effectively combined with ongoing visually induced activity during the formation of new associations. |
Edward L Keller; Kyoung-Min Lee; Se-Woong Park; Jessica A Hill Effect of inactivation of the cortical frontal eye field on saccades generated in a choice response paradigm Journal Article Journal of Neurophysiology, 100 (5), pp. 2726–2737, 2008. @article{Keller2008, title = {Effect of inactivation of the cortical frontal eye field on saccades generated in a choice response paradigm}, author = {Edward L Keller and Kyoung-Min Lee and Se-Woong Park and Jessica A Hill}, doi = {10.1152/jn.90673.2008}, year = {2008}, date = {2008-01-01}, journal = {Journal of Neurophysiology}, volume = {100}, number = {5}, pages = {2726--2737}, abstract = {Previous studies using muscimol inactivations in the frontal eye fields (FEFs) have shown that saccades generated by recall from working memory are eliminated by these lesions, whereas visually guided saccades are relatively spared. In these experiments, we made reversible inactivations in FEFs in alert macaque monkeys and examined the effect on saccades in a choice response task. Our task required monkeys to learn arbitrary pairings between colored stimuli and saccade direction. Following inactivations, the percentage of choice errors increased as a function of the number of alternative (NA) pairings. In contrast, the percentage of dysmetric saccades (saccades that landed in the correct quadrant but were inaccurate) did not vary with NA. Saccade latency increased postlesion but did not increase with NA. We also made simultaneous inactivations in both FEFs. The results following bilateral lesions showed approximately twice as many choice errors. We conclude that the FEFs are involved in the generation of saccades in choice response tasks. The dramatic effect of NA on choice errors, but the lack of an effect of NA on motor errors or response latency, suggests that two types of processing are interrupted by FEF lesions. The first involves the formation of a saccadic intention vector from associate memory inputs, and the second, the execution of the saccade from the intention vector. An alternative interpretation of the first result is that a role of the FEFs may be to suppress incorrect responses. The doubling of choice errors following bilateral FEF lesions suggests that the effect of unilateral lesions is not caused by a general inhibition of the lesioned side by the intact side.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Previous studies using muscimol inactivations in the frontal eye fields (FEFs) have shown that saccades generated by recall from working memory are eliminated by these lesions, whereas visually guided saccades are relatively spared. In these experiments, we made reversible inactivations in FEFs in alert macaque monkeys and examined the effect on saccades in a choice response task. Our task required monkeys to learn arbitrary pairings between colored stimuli and saccade direction. Following inactivations, the percentage of choice errors increased as a function of the number of alternative (NA) pairings. In contrast, the percentage of dysmetric saccades (saccades that landed in the correct quadrant but were inaccurate) did not vary with NA. Saccade latency increased postlesion but did not increase with NA. We also made simultaneous inactivations in both FEFs. The results following bilateral lesions showed approximately twice as many choice errors. We conclude that the FEFs are involved in the generation of saccades in choice response tasks. The dramatic effect of NA on choice errors, but the lack of an effect of NA on motor errors or response latency, suggests that two types of processing are interrupted by FEF lesions. The first involves the formation of a saccadic intention vector from associate memory inputs, and the second, the execution of the saccade from the intention vector. An alternative interpretation of the first result is that a role of the FEFs may be to suppress incorrect responses. The doubling of choice errors following bilateral FEF lesions suggests that the effect of unilateral lesions is not caused by a general inhibition of the lesioned side by the intact side. |
Aarlenne Z Khan; Douglas P Munoz; Naomi Takahashi; Gunnar Blohm; Robert M McPeek Effects of a pretarget distractor on saccade reaction times across space and time in monkeys and humans Journal Article Journal of Vision, 16 (7), pp. 1–20, 2016. @article{Khan2016, title = {Effects of a pretarget distractor on saccade reaction times across space and time in monkeys and humans}, author = {Aarlenne Z Khan and Douglas P Munoz and Naomi Takahashi and Gunnar Blohm and Robert M McPeek}, doi = {10.4330/wjc.v5.i2.12}, year = {2016}, date = {2016-01-01}, journal = {Journal of Vision}, volume = {16}, number = {7}, pages = {1--20}, abstract = {Previous studies have shown that the influence of a behaviorally irrelevant distractor on saccade reaction times (SRTs) varies depending on the temporal and spatial relationship between the distractor and the saccade target. We measured distractor influence on SRTs to a subsequently presented target, varying the spatial location and the timing between the distractor and the target. The distractor appeared at one of four equally eccentric locations, followed by a target (either 50 ms or 200 ms after) at one of 136 different locations encompassing an area of 20° square. We extensively tested two humans and two monkeys on this task to determine interspecies similarities and differences, since monkey neurophysiology is often used to interpret human behavioral findings. Results were similar across species; for the short interval (50 ms), SRTs were shortest to a target presented close to or at the distractor location and increased primarily as a function of the distance from the distractor. There was also an effect of distractor-target direction and visual field. For the long interval (200 ms) the results were inverted; SRTs were longest for short distances between the distractor and target and decreased as a function of distance from distractor. Both SRT patterns were well captured by a two-dimensional dynamic field model with short-distance excitation and long-distance inhibition, based upon known functional connectivity found in the superior colliculus that includes wide-spread excitation and inhibition. Based on these findings, we posit that the different time-dependent patterns of distractor-related SRTs can emerge from the same underlying neuronal mechanisms common to both species.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Previous studies have shown that the influence of a behaviorally irrelevant distractor on saccade reaction times (SRTs) varies depending on the temporal and spatial relationship between the distractor and the saccade target. We measured distractor influence on SRTs to a subsequently presented target, varying the spatial location and the timing between the distractor and the target. The distractor appeared at one of four equally eccentric locations, followed by a target (either 50 ms or 200 ms after) at one of 136 different locations encompassing an area of 20° square. We extensively tested two humans and two monkeys on this task to determine interspecies similarities and differences, since monkey neurophysiology is often used to interpret human behavioral findings. Results were similar across species; for the short interval (50 ms), SRTs were shortest to a target presented close to or at the distractor location and increased primarily as a function of the distance from the distractor. There was also an effect of distractor-target direction and visual field. For the long interval (200 ms) the results were inverted; SRTs were longest for short distances between the distractor and target and decreased as a function of distance from distractor. Both SRT patterns were well captured by a two-dimensional dynamic field model with short-distance excitation and long-distance inhibition, based upon known functional connectivity found in the superior colliculus that includes wide-spread excitation and inhibition. Based on these findings, we posit that the different time-dependent patterns of distractor-related SRTs can emerge from the same underlying neuronal mechanisms common to both species. |
F A Khawaja; James M G Tsui; Christopher C Pack Pattern motion selectivity of spiking outputs and local field potentials in macaque visual cortex Journal Article Journal of Neuroscience, 29 (43), pp. 13702–13709, 2009. @article{Khawaja2009, title = {Pattern motion selectivity of spiking outputs and local field potentials in macaque visual cortex}, author = {F A Khawaja and James M G Tsui and Christopher C Pack}, doi = {10.1523/JNEUROSCI.2844-09.2009}, year = {2009}, date = {2009-01-01}, journal = {Journal of Neuroscience}, volume = {29}, number = {43}, pages = {13702--13709}, abstract = {The dorsal pathway of the primate visual cortex is involved in the processing of motion signals that are useful for perception and behavior. Along this pathway, motion information is first measured by the primary visual cortex (V1), which sends specialized projections to extrastriate regions such as the middle temporal area (MT). Previous work with plaid stimuli has shown that most V1 neurons respond to the individual components of moving stimuli, whereas some MT neurons are capable of estimating the global motion of the pattern. In this work, we show that the majority of neurons in the medial superior temporal area (MST), which receives input from MT, have this pattern-selective property. Interestingly, the local field potentials (LFPs) measured simultaneously with the spikes often exhibit properties similar to that of the presumptive feedforward input to each area: in the high-gamma frequency band, the LFPs in MST are as component selective as the spiking outputs of MT, and MT LFPs have plaid responses that are similar to the spiking outputs of V1. In the lower LFP frequency bands (beta and low gamma), component selectivity is very common, and pattern selectivity is almost entirely absent in both MT and MST. Together, these results suggest a surprisingly strong link between the sensory tuning of cortical LFPs and afferent inputs, with important implications for the interpretation of imaging studies and for models of cortical function.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The dorsal pathway of the primate visual cortex is involved in the processing of motion signals that are useful for perception and behavior. Along this pathway, motion information is first measured by the primary visual cortex (V1), which sends specialized projections to extrastriate regions such as the middle temporal area (MT). Previous work with plaid stimuli has shown that most V1 neurons respond to the individual components of moving stimuli, whereas some MT neurons are capable of estimating the global motion of the pattern. In this work, we show that the majority of neurons in the medial superior temporal area (MST), which receives input from MT, have this pattern-selective property. Interestingly, the local field potentials (LFPs) measured simultaneously with the spikes often exhibit properties similar to that of the presumptive feedforward input to each area: in the high-gamma frequency band, the LFPs in MST are as component selective as the spiking outputs of MT, and MT LFPs have plaid responses that are similar to the spiking outputs of V1. In the lower LFP frequency bands (beta and low gamma), component selectivity is very common, and pattern selectivity is almost entirely absent in both MT and MST. Together, these results suggest a surprisingly strong link between the sensory tuning of cortical LFPs and afferent inputs, with important implications for the interpretation of imaging studies and for models of cortical function. |
Farhan A Khawaja; Liu D Liu; Christopher C Pack Responses of MST neurons to plaid stimuli Journal Article Journal of Neurophysiology, 110 (1), pp. 63–74, 2013. @article{Khawaja2013, title = {Responses of MST neurons to plaid stimuli}, author = {Farhan A Khawaja and Liu D Liu and Christopher C Pack}, doi = {10.1152/jn.00338.2012}, year = {2013}, date = {2013-01-01}, journal = {Journal of Neurophysiology}, volume = {110}, number = {1}, pages = {63--74}, abstract = {The estimation of motion information from retinal input is a fundamental function of the primate dorsal visual pathway. Previous work has shown that this function involves multiple cortical areas, with each area integrating information from its predecessors. Compared with neurons in the primary visual cortex (V1), neurons in the middle temporal (MT) area more faithfully represent the velocity of plaid stimuli, and the observation of this pattern selectivity has led to two-stage models in which MT neurons integrate the outputs of component-selective V1 neurons. Motion integration in these models is generally complemented by motion opponency, which refines velocity selectivity. Area MT projects to a third stage of motion processing, the medial superior temporal (MST) area, but surprisingly little is known about MST responses to plaid stimuli. Here we show that increased pattern selectivity in MST is associated with greater prevalence of the mechanisms implemented by two-stage MT models: Compared with MT neurons, MST neurons integrate motion components to a greater degree and exhibit evidence of stronger motion opponency. Moreover, when tested with more challenging unikinetic plaid stimuli, an appreciable percentage of MST neurons are pattern selective, while such selectivity is rare in MT. Surprisingly, increased motion integration is found in MST even for transparent plaid stimuli, which are not typically integrated perceptually. Thus the relationship between MST and MT is qualitatively similar to that between MT and V1, as repeated application of basic motion mechanisms leads to novel selectivities at each stage along the pathway.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The estimation of motion information from retinal input is a fundamental function of the primate dorsal visual pathway. Previous work has shown that this function involves multiple cortical areas, with each area integrating information from its predecessors. Compared with neurons in the primary visual cortex (V1), neurons in the middle temporal (MT) area more faithfully represent the velocity of plaid stimuli, and the observation of this pattern selectivity has led to two-stage models in which MT neurons integrate the outputs of component-selective V1 neurons. Motion integration in these models is generally complemented by motion opponency, which refines velocity selectivity. Area MT projects to a third stage of motion processing, the medial superior temporal (MST) area, but surprisingly little is known about MST responses to plaid stimuli. Here we show that increased pattern selectivity in MST is associated with greater prevalence of the mechanisms implemented by two-stage MT models: Compared with MT neurons, MST neurons integrate motion components to a greater degree and exhibit evidence of stronger motion opponency. Moreover, when tested with more challenging unikinetic plaid stimuli, an appreciable percentage of MST neurons are pattern selective, while such selectivity is rare in MT. Surprisingly, increased motion integration is found in MST even for transparent plaid stimuli, which are not typically integrated perceptually. Thus the relationship between MST and MT is qualitatively similar to that between MT and V1, as repeated application of basic motion mechanisms leads to novel selectivities at each stage along the pathway. |
Paul S Khayat; Robert Niebergall; Julio C Martinez-Trujillo Attention differentially modulates similar neuronal responses evoked by varying contrast and direction stimuli in area MT. Journal Article Journal of Neuroscience, 30 (6), pp. 2188–2197, 2010. @article{Khayat2010, title = {Attention differentially modulates similar neuronal responses evoked by varying contrast and direction stimuli in area MT.}, author = {Paul S Khayat and Robert Niebergall and Julio C Martinez-Trujillo}, doi = {10.1523/JNEUROSCI.5314-09.2010}, year = {2010}, date = {2010-01-01}, journal = {Journal of Neuroscience}, volume = {30}, number = {6}, pages = {2188--2197}, abstract = {The effects of attention on the responses of visual neurons have been described as a scaling or additive modulation independent of stimulus features and contrast, or as a contrast-dependent modulation. We explored these alternatives by recording neuronal responses in macaque area MT to moving stimuli that evoked similar firing rates but varied in contrast and direction. We presented two identical pairs of stimuli, one inside the neurons' receptive field and the other outside, in the opposite hemifield. One stimulus of each pair always had high contrast and moved in the recorded cell's antipreferred direction (AP pattern), while the other (test pattern) could either move in the cell's preferred direction and vary in contrast, or have the same contrast as the AP pattern and vary in direction. For different stimulus pairs evoking similar responses, switching attention between the two AP patterns, or directing attention from a fixation spot to the AP pattern inside or outside the receptive field, produced a stronger suppression of responses to varying contrast pairs, reaching a maximum ( approximately 20%) at intermediate contrast. For invariable contrast pairs, switching attention from the fixation spot to the AP pattern produced a modulation that ranged from 10% suppression when the test pattern moved in the cells preferred direction to 14% enhancement when it moved in a direction 90 degrees away from that direction. Our results are incompatible with a scaling or additive modulation of MT neurons' response by attention, but support models where spatial and feature-based attention modulate input signals into the area normalization circuit.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The effects of attention on the responses of visual neurons have been described as a scaling or additive modulation independent of stimulus features and contrast, or as a contrast-dependent modulation. We explored these alternatives by recording neuronal responses in macaque area MT to moving stimuli that evoked similar firing rates but varied in contrast and direction. We presented two identical pairs of stimuli, one inside the neurons' receptive field and the other outside, in the opposite hemifield. One stimulus of each pair always had high contrast and moved in the recorded cell's antipreferred direction (AP pattern), while the other (test pattern) could either move in the cell's preferred direction and vary in contrast, or have the same contrast as the AP pattern and vary in direction. For different stimulus pairs evoking similar responses, switching attention between the two AP patterns, or directing attention from a fixation spot to the AP pattern inside or outside the receptive field, produced a stronger suppression of responses to varying contrast pairs, reaching a maximum ( approximately 20%) at intermediate contrast. For invariable contrast pairs, switching attention from the fixation spot to the AP pattern produced a modulation that ranged from 10% suppression when the test pattern moved in the cells preferred direction to 14% enhancement when it moved in a direction 90 degrees away from that direction. Our results are incompatible with a scaling or additive modulation of MT neurons' response by attention, but support models where spatial and feature-based attention modulate input signals into the area normalization circuit. |
Paul S Khayat; Robert Niebergall; Julio C Martinez-Trujillo Frequency-dependent attentional modulation of local field potential signals in macaque area MT Journal Article Journal of Neuroscience, 30 (20), pp. 7037–7048, 2010. @article{Khayat2010a, title = {Frequency-dependent attentional modulation of local field potential signals in macaque area MT}, author = {Paul S Khayat and Robert Niebergall and Julio C Martinez-Trujillo}, doi = {10.1523/JNEUROSCI.0404-10.2010}, year = {2010}, date = {2010-01-01}, journal = {Journal of Neuroscience}, volume = {30}, number = {20}, pages = {7037--7048}, abstract = {Visual attention modulates neuronal responses in primate motion processing area MT. However, whether it modulates the strength local field potentials (LFP-power) within this area remains unexplored, as well as how this modulation relates to the one of the neurons' response. We investigated these issues by simultaneously recording LFPs and neuronal responses evoked by moving random dot patterns of varying direction and contrast in area MT of two male monkeys (Macaca mulatta) during different behavioral conditions. We found that: (1) LFP-power in the gamma (30-120 Hz), but not in the delta (2-4 Hz), (4-8 Hz), alpha (8-12 Hz), beta(1) (12-20 Hz), and beta(2) (20-30 Hz) frequency bands, was tuned for motion direction and contrast, similarly to the neurons' response, (2) shifting attention into a neuron's receptive field (RF) decreased LFP-power in the bands below 30 Hz (except the band), whereas shifting attention to a stimulus motion direction outside the RF had no effect in these bands, (3) LFP-power in the gamma band, however, exhibited both spatial- and motion direction-dependent attentional modulation (increase or decrease), which was highly correlated with the modulation of the neurons' response. These results demonstrate that in area MT, shifting attention into the RFs of neurons in the vicinity of the recording electrode, or to the direction of a moving stimulus located far away from these RFs, distinctively modulates LFP-power in the various frequency bands. They further suggest differences in the neural mechanisms underlying these types of attentional modulation of visual processing.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Visual attention modulates neuronal responses in primate motion processing area MT. However, whether it modulates the strength local field potentials (LFP-power) within this area remains unexplored, as well as how this modulation relates to the one of the neurons' response. We investigated these issues by simultaneously recording LFPs and neuronal responses evoked by moving random dot patterns of varying direction and contrast in area MT of two male monkeys (Macaca mulatta) during different behavioral conditions. We found that: (1) LFP-power in the gamma (30-120 Hz), but not in the delta (2-4 Hz), (4-8 Hz), alpha (8-12 Hz), beta(1) (12-20 Hz), and beta(2) (20-30 Hz) frequency bands, was tuned for motion direction and contrast, similarly to the neurons' response, (2) shifting attention into a neuron's receptive field (RF) decreased LFP-power in the bands below 30 Hz (except the band), whereas shifting attention to a stimulus motion direction outside the RF had no effect in these bands, (3) LFP-power in the gamma band, however, exhibited both spatial- and motion direction-dependent attentional modulation (increase or decrease), which was highly correlated with the modulation of the neurons' response. These results demonstrate that in area MT, shifting attention into the RFs of neurons in the vicinity of the recording electrode, or to the direction of a moving stimulus located far away from these RFs, distinctively modulates LFP-power in the various frequency bands. They further suggest differences in the neural mechanisms underlying these types of attentional modulation of visual processing. |
Paul S Khayat; Julio C Martinez-Trujillo Effects of attention and distractor contrast on the responses of middle temporal area neurons to transient motion direction changes Journal Article European Journal of Neuroscience, 41 (12), pp. 1603–1613, 2015. @article{Khayat2015, title = {Effects of attention and distractor contrast on the responses of middle temporal area neurons to transient motion direction changes}, author = {Paul S Khayat and Julio C Martinez-Trujillo}, doi = {10.1111/ejn.12920}, year = {2015}, date = {2015-01-01}, journal = {European Journal of Neuroscience}, volume = {41}, number = {12}, pages = {1603--1613}, abstract = {The ability of primates to detect transient changes in a visual scene can be influenced by the allocation of attention, as well as by the presence of distractors. We investigated the neural substrates of these effects by recording the responses of neurons in the middle temporal area (MT) of two monkeys while they detected a transient motion direction change in a moving target. We found that positioning a distractor near the target impaired the change-detection performance of the animals. This impairment monotoni- cally decreased as the distractor's contrast decreased. A neural correlate of this effect was a decrease in the ability of MT neu- rons to signal the direction change (detection sensitivity or DS) when a distractor was near the target, both located inside the neuron's receptive field. Moreover, decreasing distractor contrast increased neuronal DS. On the other hand, directing attention away from the target decreased neuronal DS. At the level of individual neurons, we found a negative correlation between the degree of response normalization and the DS. Finally, the intensity of a neuron's response to the change was predictive of the animal's reaction time, suggesting that the activity of our recorded neurons was linked to the animal's detection performance. Our results suggest that the ability of an MT neuron to signal a transient direction change is regulated by the degree of inhibitory drive into the cell. The presence of distractors, their contrast and the allocation of attention influence such inhibitory drive, therefore modulating the ability of the neurons to signal transient changes in stimulus features and consequently behavioral performance.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The ability of primates to detect transient changes in a visual scene can be influenced by the allocation of attention, as well as by the presence of distractors. We investigated the neural substrates of these effects by recording the responses of neurons in the middle temporal area (MT) of two monkeys while they detected a transient motion direction change in a moving target. We found that positioning a distractor near the target impaired the change-detection performance of the animals. This impairment monotoni- cally decreased as the distractor's contrast decreased. A neural correlate of this effect was a decrease in the ability of MT neu- rons to signal the direction change (detection sensitivity or DS) when a distractor was near the target, both located inside the neuron's receptive field. Moreover, decreasing distractor contrast increased neuronal DS. On the other hand, directing attention away from the target decreased neuronal DS. At the level of individual neurons, we found a negative correlation between the degree of response normalization and the DS. Finally, the intensity of a neuron's response to the change was predictive of the animal's reaction time, suggesting that the activity of our recorded neurons was linked to the animal's detection performance. Our results suggest that the ability of an MT neuron to signal a transient direction change is regulated by the degree of inhibitory drive into the cell. The presence of distractors, their contrast and the allocation of attention influence such inhibitory drive, therefore modulating the ability of the neurons to signal transient changes in stimulus features and consequently behavioral performance. |
Ricardo Kienitz; Joscha T Schmiedt; Katharine A Shapcott; Kleopatra Kouroupaki; Richard C Saunders; Michael Christoph Schmid Theta rhythmic neuronal activity and reaction times arising from cortical receptive field interactions during distributed attention Journal Article Current Biology, 28 (15), pp. 2377–2387, 2018. @article{Kienitz2018, title = {Theta rhythmic neuronal activity and reaction times arising from cortical receptive field interactions during distributed attention}, author = {Ricardo Kienitz and Joscha T Schmiedt and Katharine A Shapcott and Kleopatra Kouroupaki and Richard C Saunders and Michael Christoph Schmid}, doi = {10.1016/j.cub.2018.05.086}, year = {2018}, date = {2018-08-01}, journal = {Current Biology}, volume = {28}, number = {15}, pages = {2377--2387}, abstract = {Growing evidence suggests that distributed spatial attention may invoke theta (3–9 Hz) rhythmic sampling processes. The neuronal basis of such attentional sampling is, however, not fully understood. Here we show using array recordings in visual cortical area V4 of two awake macaques that presenting separate visual stimuli to the excitatory center and suppressive surround of neuronal receptive fields (RFs) elicits rhythmic multi-unit activity (MUA)at 3–6 Hz. This neuronal rhythm did not depend on small fixational eye movements. In the context of a distributed spatial attention task, during which the monkeys detected a spatially and temporally uncertain target, reaction times (RTs) exhibited similar rhythmic fluctuations. RTs were fast or slow depend-ing on the target occurrence during high or low MUA, resulting in rhythmic MUA-RT cross-correlations at theta frequencies. These findings show that theta rhythmic neuronal activity can arise from competitiveRF interactions and that this rhythm may result in rhythmic RTs potentially subserving attentional sampling.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Growing evidence suggests that distributed spatial attention may invoke theta (3–9 Hz) rhythmic sampling processes. The neuronal basis of such attentional sampling is, however, not fully understood. Here we show using array recordings in visual cortical area V4 of two awake macaques that presenting separate visual stimuli to the excitatory center and suppressive surround of neuronal receptive fields (RFs) elicits rhythmic multi-unit activity (MUA)at 3–6 Hz. This neuronal rhythm did not depend on small fixational eye movements. In the context of a distributed spatial attention task, during which the monkeys detected a spatially and temporally uncertain target, reaction times (RTs) exhibited similar rhythmic fluctuations. RTs were fast or slow depend-ing on the target occurrence during high or low MUA, resulting in rhythmic MUA-RT cross-correlations at theta frequencies. These findings show that theta rhythmic neuronal activity can arise from competitiveRF interactions and that this rhythm may result in rhythmic RTs potentially subserving attentional sampling. |
Daniel L Kimmel; Dagem Mammo; William T Newsome Tracking the eye non-invasively: Simultaneous comparison of the scleral search coil and optical tracking techniques in the macaque monkey Journal Article Frontiers in Behavioral Neuroscience, 6 , pp. 1–17, 2012. @article{Kimmel2012, title = {Tracking the eye non-invasively: Simultaneous comparison of the scleral search coil and optical tracking techniques in the macaque monkey}, author = {Daniel L Kimmel and Dagem Mammo and William T Newsome}, doi = {10.3389/fnbeh.2012.00049}, year = {2012}, date = {2012-01-01}, journal = {Frontiers in Behavioral Neuroscience}, volume = {6}, pages = {1--17}, publisher = {10}, address = {doi}, abstract = {From human perception to primate neurophysiology, monitoring eye position is critical to the study of vision, attention, oculomotor control, and behavior. Two principal techniques for the precise measurement of eye position-the long-standing sclera-embedded search coil and more recent optical tracking techniques-are in use in various laboratories, but no published study compares the performance of the two methods simultaneously in the same primates. Here we compare two popular systems-a sclera-embedded search coil from C-N-C Engineering and the EyeLink 1000 optical system from SR Research-by recording simultaneously from the same eye in the macaque monkey while the animal performed a simple oculomotor task. We found broad agreement between the two systems, particularly in positional accuracy during fixation, measurement of saccade amplitude, detection of fixational saccades, and sensitivity to subtle changes in eye position from trial to trial. Nonetheless, certain discrepancies persist, particularly elevated saccade peak velocities, post-saccadic ringing, influence of luminance change on reported position, and greater sample-to-sample variation in the optical system. Our study shows that optical performance now rivals that of the search coil, rendering optical systems appropriate for many if not most applications. This finding is consequential, especially for animal subjects, because the optical systems do not require invasive surgery for implantation and repair of search coils around the eye. Our data also allow laboratories using the optical system in human subjects to assess the strengths and limitations of the technique for their own applications.}, keywords = {}, pubstate = {published}, tppubtype = {article} } From human perception to primate neurophysiology, monitoring eye position is critical to the study of vision, attention, oculomotor control, and behavior. Two principal techniques for the precise measurement of eye position-the long-standing sclera-embedded search coil and more recent optical tracking techniques-are in use in various laboratories, but no published study compares the performance of the two methods simultaneously in the same primates. Here we compare two popular systems-a sclera-embedded search coil from C-N-C Engineering and the EyeLink 1000 optical system from SR Research-by recording simultaneously from the same eye in the macaque monkey while the animal performed a simple oculomotor task. We found broad agreement between the two systems, particularly in positional accuracy during fixation, measurement of saccade amplitude, detection of fixational saccades, and sensitivity to subtle changes in eye position from trial to trial. Nonetheless, certain discrepancies persist, particularly elevated saccade peak velocities, post-saccadic ringing, influence of luminance change on reported position, and greater sample-to-sample variation in the optical system. Our study shows that optical performance now rivals that of the search coil, rendering optical systems appropriate for many if not most applications. This finding is consequential, especially for animal subjects, because the optical systems do not require invasive surgery for implantation and repair of search coils around the eye. Our data also allow laboratories using the optical system in human subjects to assess the strengths and limitations of the technique for their own applications. |
Shinichiro Kira; Tianming Yang; Michael N Shadlen A neural implementation of Wald's Sequential Probability Ratio Test Journal Article Neuron, 85 (4), pp. 861–873, 2015. @article{Kira2015, title = {A neural implementation of Wald's Sequential Probability Ratio Test}, author = {Shinichiro Kira and Tianming Yang and Michael N Shadlen}, doi = {10.1016/j.neuron.2015.01.007}, year = {2015}, date = {2015-01-01}, journal = {Neuron}, volume = {85}, number = {4}, pages = {861--873}, publisher = {Elsevier Inc.}, abstract = {Difficult decisions often require evaluation of samples of evidence acquired sequentially. A sensible strategy is to accumulate evidence, weighted by its reliability, until sufficient support is attained. An optimal statistical approach would accumulate evidence in units of logarithms of likelihood ratios (logLR) to a desired level. Studies of perceptual decisions suggest that the brain approximates an analogous procedure, but a direct test of accumulation, in units of logLR, to a threshold in units of cumulative logLR is lacking. We trained rhesus monkeys to make decisions based on a sequence of evanescent, visual cues assigned different logLR, hence different reliability. Firing rates of neurons in the lateral intraparietal area (LIP) reflected the accumulation of logLR and reached a stereotyped level before the monkeys committed to a decision. The monkeys' choices and reaction times, including their variability, were explained by LIP activity in the context of accumulation of logLR to a threshold.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Difficult decisions often require evaluation of samples of evidence acquired sequentially. A sensible strategy is to accumulate evidence, weighted by its reliability, until sufficient support is attained. An optimal statistical approach would accumulate evidence in units of logarithms of likelihood ratios (logLR) to a desired level. Studies of perceptual decisions suggest that the brain approximates an analogous procedure, but a direct test of accumulation, in units of logLR, to a threshold in units of cumulative logLR is lacking. We trained rhesus monkeys to make decisions based on a sequence of evanescent, visual cues assigned different logLR, hence different reliability. Firing rates of neurons in the lateral intraparietal area (LIP) reflected the accumulation of logLR and reached a stereotyped level before the monkeys committed to a decision. The monkeys' choices and reaction times, including their variability, were explained by LIP activity in the context of accumulation of logLR to a threshold. |
Jeffrey T Klein; Michael L Platt Social information signaling by neurons in primate striatum Journal Article Current Biology, 23 , pp. 691–696, 2013. @article{Klein2013, title = {Social information signaling by neurons in primate striatum}, author = {Jeffrey T Klein and Michael L Platt}, doi = {10.1016/j.cub.2013.03.022}, year = {2013}, date = {2013-01-01}, journal = {Current Biology}, volume = {23}, pages = {691--696}, publisher = {Elsevier Ltd}, abstract = {Social decisions depend on reliable information about others. Consequently, social primates are motivated to acquire information about the identity, social status, and reproductive quality of others [1]. Neurophysiological [2] and neuroimaging [3, 4] studies implicate the striatum in the motivational control of behavior. Neuroimaging studies specifically implicate the ventromedial striatum in signaling motivational aspects of social interaction [5]. Despite this evidence, precisely how striatal neurons encode social information remains unknown. Therefore, we probed the activity of single striatal neurons in monkeys choosing between visual social information at the potential expense of fluid reward. We show for the first time that a population of neurons located primarily in medial striatum selectively signals social information. Surprisingly, representation of social information was unrelated to simultaneously expressed social preferences. A largely nonoverlapping population of neurons that was not restricted to the medial striatum signaled information about fluid reward. Our findings demonstrate that information about social context and nutritive reward are maintained largely independently in striatum, even when both influence decisions to execute a single action.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Social decisions depend on reliable information about others. Consequently, social primates are motivated to acquire information about the identity, social status, and reproductive quality of others [1]. Neurophysiological [2] and neuroimaging [3, 4] studies implicate the striatum in the motivational control of behavior. Neuroimaging studies specifically implicate the ventromedial striatum in signaling motivational aspects of social interaction [5]. Despite this evidence, precisely how striatal neurons encode social information remains unknown. Therefore, we probed the activity of single striatal neurons in monkeys choosing between visual social information at the potential expense of fluid reward. We show for the first time that a population of neurons located primarily in medial striatum selectively signals social information. Surprisingly, representation of social information was unrelated to simultaneously expressed social preferences. A largely nonoverlapping population of neurons that was not restricted to the medial striatum signaled information about fluid reward. Our findings demonstrate that information about social context and nutritive reward are maintained largely independently in striatum, even when both influence decisions to execute a single action. |
Steffen Klingenhoefer; Bart Krekelberg Perisaccadic visual perception Journal Article Journal of Vision, 17 (9), pp. 1–14, 2017. @article{Klingenhoefer2017, title = {Perisaccadic visual perception}, author = {Steffen Klingenhoefer and Bart Krekelberg}, doi = {10.1167/17.9.16}, year = {2017}, date = {2017-01-01}, journal = {Journal of Vision}, volume = {17}, number = {9}, pages = {1--14}, abstract = {Primates use frequent, rapid eye movements to sample their visual environment. This is a fruitful strategy to make the best use of the highly sensitive foveal part of the retina, but it requires neural mechanisms to bind the rapidly changing visual input into a single, stable percept. Studies investigating these neural mechanisms have typically assumed that perisaccadic perception in nonhuman primates matches that of humans. We tested this assumption by performing identical experiments in human and nonhuman primates. Our data confirm that perisaccadic visual perception of macaques and humans is qualitatively similar. Specifically, we found a reduction in detectability and mislocalization of targets presented at the time of saccades. We also found substantial differences between human and nonhuman primates. Notably, in nonhuman primates, localization that requires knowledge of eye position was less precise, nonhuman primates detected fewer perisaccadic stimuli, and perisaccadic compression was not towards the saccade target. The qualitative similarities between species support the view that the nonhuman primate is ideally suited to study aspects of brain function-such as those relying on foveal vision-that are uniquely developed in primates. The quantitative differences, however, demonstrate the need for a reassessment of the models purportedly linking neural response changes at the time of saccades with the behavioral phenomena of perisaccadic reduction of detectability and mislocalization.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Primates use frequent, rapid eye movements to sample their visual environment. This is a fruitful strategy to make the best use of the highly sensitive foveal part of the retina, but it requires neural mechanisms to bind the rapidly changing visual input into a single, stable percept. Studies investigating these neural mechanisms have typically assumed that perisaccadic perception in nonhuman primates matches that of humans. We tested this assumption by performing identical experiments in human and nonhuman primates. Our data confirm that perisaccadic visual perception of macaques and humans is qualitatively similar. Specifically, we found a reduction in detectability and mislocalization of targets presented at the time of saccades. We also found substantial differences between human and nonhuman primates. Notably, in nonhuman primates, localization that requires knowledge of eye position was less precise, nonhuman primates detected fewer perisaccadic stimuli, and perisaccadic compression was not towards the saccade target. The qualitative similarities between species support the view that the nonhuman primate is ideally suited to study aspects of brain function-such as those relying on foveal vision-that are uniquely developed in primates. The quantitative differences, however, demonstrate the need for a reassessment of the models purportedly linking neural response changes at the time of saccades with the behavioral phenomena of perisaccadic reduction of detectability and mislocalization. |
Christiaan P Klink; Anna Oleksiak; Martin J M Lankheet; Richard J A van Wezel Intermittent stimulus presentation stabilizes neuronal responses in macaque area MT Journal Article Journal of Neurophysiology, 108 (8), pp. 2101–2114, 2012. @article{Klink2012, title = {Intermittent stimulus presentation stabilizes neuronal responses in macaque area MT}, author = {Christiaan P Klink and Anna Oleksiak and Martin J M Lankheet and Richard J A van Wezel}, doi = {10.1152/jn.00252.2012}, year = {2012}, date = {2012-01-01}, journal = {Journal of Neurophysiology}, volume = {108}, number = {8}, pages = {2101--2114}, abstract = {Repeated stimulation impacts neuronal responses. Here we show how response characteristics of sensory neurons in macaque visual cortex are influenced by the duration of the interruptions during intermittent stimulus presentation. Besides effects on response magnitude consistent with neuronal ad- aptation, the response variability was also systematically influenced. Spike rate variability in motion-sensitive area MT decreased when interruption durations were systematically increased from 250 to 2,000 ms. Activity fluctuations between subsequent trials and Fano factors over full response sequences were both lower with longer interruptions, while spike timing patterns became more regular. These variability changes partially depended on the response magnitude, but another significant effect that was uncorrelated with adaptation-in- duced changes in response magnitude was also present. Reduced response variability was furthermore accompanied by changes in spike-field coherence, pointing to the possibility that reduced spiking variability results from interactions in the local cortical network. While neuronal response stabilization may be a general effect of repeated sensory stimulation, we discuss its potential link with the phenomenon of perceptual stabilization of ambiguous stimuli as a result of interrupted presentation.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Repeated stimulation impacts neuronal responses. Here we show how response characteristics of sensory neurons in macaque visual cortex are influenced by the duration of the interruptions during intermittent stimulus presentation. Besides effects on response magnitude consistent with neuronal ad- aptation, the response variability was also systematically influenced. Spike rate variability in motion-sensitive area MT decreased when interruption durations were systematically increased from 250 to 2,000 ms. Activity fluctuations between subsequent trials and Fano factors over full response sequences were both lower with longer interruptions, while spike timing patterns became more regular. These variability changes partially depended on the response magnitude, but another significant effect that was uncorrelated with adaptation-in- duced changes in response magnitude was also present. Reduced response variability was furthermore accompanied by changes in spike-field coherence, pointing to the possibility that reduced spiking variability results from interactions in the local cortical network. While neuronal response stabilization may be a general effect of repeated sensory stimulation, we discuss its potential link with the phenomenon of perceptual stabilization of ambiguous stimuli as a result of interrupted presentation. |
Jonas Knöll; Jonathan W Pillow; Alexander C Huk Lawful tracking of visual motion in humans, macaques, and marmosets in a naturalistic, continuous, and untrained behavioral context Journal Article Proceedings of the National Academy of Sciences, 115 (44), pp. E10486–E10494, 2018. @article{Knoell2018, title = {Lawful tracking of visual motion in humans, macaques, and marmosets in a naturalistic, continuous, and untrained behavioral context}, author = {Jonas Knöll and Jonathan W Pillow and Alexander C Huk}, doi = {10.1073/pnas.1807192115}, year = {2018}, date = {2018-01-01}, journal = {Proceedings of the National Academy of Sciences}, volume = {115}, number = {44}, pages = {E10486--E10494}, abstract = {Much study of the visual system has focused on how humans and monkeys integrate moving stimuli over space and time. Such assessments of spatiotemporal integration provide fundamental grounding for the interpretation of neurophysiological data, as well as how the resulting neural signals support perceptual deci- sions and behavior. However, the insights supported by classical characterizations of integration performed in humans and rhesus monkeys are potentially limited with respect to both generality and detail: Standard tasks require extensive amounts of training, involve abstract stimulus–response mappings, and depend on combining data across many trials and/or sessions. It is thus of concern that the integration observed in classical tasks involves the recruitment of brain circuits that might not normally subsume natural behaviors, and that quantitative analyses have limited power for characterizing single-trial or single-session processes. Here we bridge these gaps by showing that three primate species (humans, macaques, and marmosets) track the focus of expansion of an optic flow field continuously and without substantial training. This flow-tracking behavior was volitional and reflected substantial temporal integration. Most strikingly, gaze patterns exhibited lawful and nuanced dependencies on random perturbations in the stimulus, such that repetitions of identical flow movies elicited remarkably similar eye movements over long and continuous time periods. These results demonstrate the generality of spatiotemporal integration in natural vision, and offer a means for studying integration outside of artificial tasks while maintaining lawful and highly reliable behavior.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Much study of the visual system has focused on how humans and monkeys integrate moving stimuli over space and time. Such assessments of spatiotemporal integration provide fundamental grounding for the interpretation of neurophysiological data, as well as how the resulting neural signals support perceptual deci- sions and behavior. However, the insights supported by classical characterizations of integration performed in humans and rhesus monkeys are potentially limited with respect to both generality and detail: Standard tasks require extensive amounts of training, involve abstract stimulus–response mappings, and depend on combining data across many trials and/or sessions. It is thus of concern that the integration observed in classical tasks involves the recruitment of brain circuits that might not normally subsume natural behaviors, and that quantitative analyses have limited power for characterizing single-trial or single-session processes. Here we bridge these gaps by showing that three primate species (humans, macaques, and marmosets) track the focus of expansion of an optic flow field continuously and without substantial training. This flow-tracking behavior was volitional and reflected substantial temporal integration. Most strikingly, gaze patterns exhibited lawful and nuanced dependencies on random perturbations in the stimulus, such that repetitions of identical flow movies elicited remarkably similar eye movements over long and continuous time periods. These results demonstrate the generality of spatiotemporal integration in natural vision, and offer a means for studying integration outside of artificial tasks while maintaining lawful and highly reliable behavior. |
Yoshito Kosai; Yasmine El-shamayleh; Amber M Fyall; Anitha Pasupathy The role of visual area V4 in the discrimination of partially occluded shapes Journal Article Journal of Neuroscience, 34 (25), pp. 8570–8584, 2014. @article{Kosai2014, title = {The role of visual area V4 in the discrimination of partially occluded shapes}, author = {Yoshito Kosai and Yasmine El-shamayleh and Amber M Fyall and Anitha Pasupathy}, doi = {10.1523/JNEUROSCI.1375-14.2014}, year = {2014}, date = {2014-01-01}, journal = {Journal of Neuroscience}, volume = {34}, number = {25}, pages = {8570--8584}, abstract = {The primate brain successfully recognizes objects, even when they are partially occluded. To begin to elucidate the neural substrates of this perceptual capacity, we measured the responses of shape-selective neurons in visual area V4 while monkeys discriminated pairs of shapes under varying degrees of occlusion. We found that neuronal shape selectivity always decreased with increasing occlusion level, with some neurons being notably more robust to occlusion than others. The responses of neurons that maintained their selectivity across a wider range of occlusion levels were often sufficiently sensitive to support behavioral performance. Many of these same neurons were distinctively selective for the curvature of local boundary features and their shape tuning was well fit by a model of boundary curvature (curvature-tuned neurons). A significant subset of V4 neurons also signaled the animal's upcoming behavioral choices; these decision signals had short onset latencies that emerged progressively later for higher occlusion levels. The time course of the decision signals in V4 paralleled that of shape selectivity in curvature-tuned neurons: shape selectivity in curvature-tuned neurons, but not others, emerged earlier than the decision signals. These findings provide evidence for the involvement of contour-based mechanisms in the segmentation and recognition of partially occluded objects, consistent with psychophysical theory. Furthermore, they suggest that area V4 participates in the representation of the relevant sensory signals and the generation of decision signals underlying discrimination.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The primate brain successfully recognizes objects, even when they are partially occluded. To begin to elucidate the neural substrates of this perceptual capacity, we measured the responses of shape-selective neurons in visual area V4 while monkeys discriminated pairs of shapes under varying degrees of occlusion. We found that neuronal shape selectivity always decreased with increasing occlusion level, with some neurons being notably more robust to occlusion than others. The responses of neurons that maintained their selectivity across a wider range of occlusion levels were often sufficiently sensitive to support behavioral performance. Many of these same neurons were distinctively selective for the curvature of local boundary features and their shape tuning was well fit by a model of boundary curvature (curvature-tuned neurons). A significant subset of V4 neurons also signaled the animal's upcoming behavioral choices; these decision signals had short onset latencies that emerged progressively later for higher occlusion levels. The time course of the decision signals in V4 paralleled that of shape selectivity in curvature-tuned neurons: shape selectivity in curvature-tuned neurons, but not others, emerged earlier than the decision signals. These findings provide evidence for the involvement of contour-based mechanisms in the segmentation and recognition of partially occluded objects, consistent with psychophysical theory. Furthermore, they suggest that area V4 participates in the representation of the relevant sensory signals and the generation of decision signals underlying discrimination. |
Michael J Koval; Stephen G Lomber; Stefan Everling Prefrontal cortex deactivation in macaques alters activity in the superior colliculus and impairs voluntary control of saccades Journal Article Journal of Neuroscience, 31 (23), pp. 8659–8668, 2011. @article{Koval2011, title = {Prefrontal cortex deactivation in macaques alters activity in the superior colliculus and impairs voluntary control of saccades}, author = {Michael J Koval and Stephen G Lomber and Stefan Everling}, doi = {10.1523/JNEUROSCI.1258-11.2011}, year = {2011}, date = {2011-01-01}, journal = {Journal of Neuroscience}, volume = {31}, number = {23}, pages = {8659--8668}, abstract = {The cognitive control of action requires both the suppression of automatic responses to sudden stimuli and the generation of behavior specified by abstract instructions. Though patient, functional imaging and neurophysiological studies have implicated the dorsolateral prefrontal cortex (dlPFC) in these abilities, the mechanism by which the dlPFC exerts this control remains unknown. Here we examined the functional interaction of the dlPFC with the saccade circuitry by deactivating area 46 of the dlPFC and measuring its effects on the activity of single superior colliculus neurons in monkeys performing a cognitive saccade task. Deactivation of the dlPFC reduced preparatory activity and increased stimulus-related activity in these neurons. These changes in neural activity were accompanied by marked decreases in task performance as evidenced by longer reaction times and more task errors. The results suggest that the dlPFC participates in the cognitive control of gaze by suppressing stimulus-evoked automatic saccade programs.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The cognitive control of action requires both the suppression of automatic responses to sudden stimuli and the generation of behavior specified by abstract instructions. Though patient, functional imaging and neurophysiological studies have implicated the dorsolateral prefrontal cortex (dlPFC) in these abilities, the mechanism by which the dlPFC exerts this control remains unknown. Here we examined the functional interaction of the dlPFC with the saccade circuitry by deactivating area 46 of the dlPFC and measuring its effects on the activity of single superior colliculus neurons in monkeys performing a cognitive saccade task. Deactivation of the dlPFC reduced preparatory activity and increased stimulus-related activity in these neurons. These changes in neural activity were accompanied by marked decreases in task performance as evidenced by longer reaction times and more task errors. The results suggest that the dlPFC participates in the cognitive control of gaze by suppressing stimulus-evoked automatic saccade programs. |
Michael J Koval; Matthew R Hutchison; Stephen G Lomber; Stefan Everling Effects of unilateral deactivations of dorsolateral prefrontal cortex and anterior cingulate cortex on saccadic eye movements Journal Article Journal of Neurophysiology, 111 (4), pp. 787–803, 2014. @article{Koval2014, title = {Effects of unilateral deactivations of dorsolateral prefrontal cortex and anterior cingulate cortex on saccadic eye movements}, author = {Michael J Koval and Matthew R Hutchison and Stephen G Lomber and Stefan Everling}, doi = {10.1152/jn.00626.2013}, year = {2014}, date = {2014-01-01}, journal = {Journal of Neurophysiology}, volume = {111}, number = {4}, pages = {787--803}, abstract = {The dorsolateral prefrontal cortex (dlPFC) and anterior cingulate cortex (ACC) have both been implicated in the cognitive control of saccadic eye movements by single neuron recording studies in nonhuman primates and functional imaging studies in humans, but their relative roles remain unclear. Here, we reversibly deactivated either dlPFC or ACC subregions in macaque monkeys while the animals performed randomly interleaved pro- and antisaccades. In addition, we explored the whole-brain functional connectivity of these two regions by applying a seed-based resting-state functional MRI analysis in a separate cohort of monkeys. We found that unilateral dlPFC deactivation had stronger behavioral effects on saccades than unilateral ACC deactivation, and that the dlPFC displayed stronger functional connectivity with frontoparietal areas than the ACC. We suggest that the dlPFC plays a more prominent role in the preparation of pro- and antisaccades than the ACC.}, keywords = {}, pubstate = {published}, tppubtype = {article} } The dorsolateral prefrontal cortex (dlPFC) and anterior cingulate cortex (ACC) have both been implicated in the cognitive control of saccadic eye movements by single neuron recording studies in nonhuman primates and functional imaging studies in humans, but their relative roles remain unclear. Here, we reversibly deactivated either dlPFC or ACC subregions in macaque monkeys while the animals performed randomly interleaved pro- and antisaccades. In addition, we explored the whole-brain functional connectivity of these two regions by applying a seed-based resting-state functional MRI analysis in a separate cohort of monkeys. We found that unilateral dlPFC deactivation had stronger behavioral effects on saccades than unilateral ACC deactivation, and that the dlPFC displayed stronger functional connectivity with frontoparietal areas than the ACC. We suggest that the dlPFC plays a more prominent role in the preparation of pro- and antisaccades than the ACC. |
Matthew R Krause; Theodoros P Zanos; Bennett A Csorba; Praveen K Pilly; Jaehoon Choe; Matthew E Phillips; Abhishek Datta; Christopher C Pack Transcranial direct current stimulation facilitates associative learning and alters functional connectivity in the primate brain Journal Article Current Biology, 27 (20), pp. 3086–3096, 2017. @article{Krause2017, title = {Transcranial direct current stimulation facilitates associative learning and alters functional connectivity in the primate brain}, author = {Matthew R Krause and Theodoros P Zanos and Bennett A Csorba and Praveen K Pilly and Jaehoon Choe and Matthew E Phillips and Abhishek Datta and Christopher C Pack}, doi = {10.1016/j.cub.2017.09.020}, year = {2017}, date = {2017-01-01}, journal = {Current Biology}, volume = {27}, number = {20}, pages = {3086--3096}, publisher = {Elsevier Ltd.}, abstract = {There has been growing interest in transcranial direct current stimulation (tDCS), a non-invasive technique purported to modulate neural activity via weak, externally applied electric fields. Although some promising preliminary data have been reported for applications ranging from stroke rehabilitation to cognitive enhancement, little is known about how tDCS affects the human brain, and some studies have concluded that it may have no effect at all. Here, we describe a macaque model of tDCS that allows us to simultaneously examine the effects of tDCS on brain activity and behavior. We find that applying tDCS to right prefrontal cortex improves monkeys' performance on an associative learning task. While firing rates do not change within the targeted area, tDCS does induce large low-frequency oscillations in the underlying tissue. These oscillations alter functional connectivity, both locally and between distant brain areas, and these long-range changes correlate with tDCS's effects on behavior. Together, these results are consistent with the idea that tDCS leads to widespread changes in brain activity and suggest that it may be a valuable method for cheaply and non-invasively altering functional connectivity in humans. Krause et al. test transcranial direct current stimulation (tDCS) in a realistic non-human primate model. Stimulation of prefrontal cortex (PFC) improved animals' associative learning while altering coherence between PFC and sensory areas. Their data suggest that tDCS may act by altering long-range connectivity between PFC and other brain areas.}, keywords = {}, pubstate = {published}, tppubtype = {article} } There has been growing interest in transcranial direct current stimulation (tDCS), a non-invasive technique purported to modulate neural activity via weak, externally applied electric fields. Although some promising preliminary data have been reported for applications ranging from stroke rehabilitation to cognitive enhancement, little is known about how tDCS affects the human brain, and some studies have concluded that it may have no effect at all. Here, we describe a macaque model of tDCS that allows us to simultaneously examine the effects of tDCS on brain activity and behavior. We find that applying tDCS to right prefrontal cortex improves monkeys' performance on an associative learning task. While firing rates do not change within the targeted area, tDCS does induce large low-frequency oscillations in the underlying tissue. These oscillations alter functional connectivity, both locally and between distant brain areas, and these long-range changes correlate with tDCS's effects on behavior. Together, these results are consistent with the idea that tDCS leads to widespread changes in brain activity and suggest that it may be a valuable method for cheaply and non-invasively altering functional connectivity in humans. Krause et al. test transcranial direct current stimulation (tDCS) in a realistic non-human primate model. Stimulation of prefrontal cortex (PFC) improved animals' associative learning while altering coherence between PFC and sensory areas. Their data suggest that tDCS may act by altering long-range connectivity between PFC and other brain areas. |
Jens Kremkow; Jianzhong Jin; Stanley J Komban; Yushi Wang; Reza Lashgari; Xiaobing Li; Michael Jansen; Qasim Zaidi; Jose-Manuel Alonso Neuronal nonlinearity explains greater visual spatial resolution for darks than lights Journal Article Proceedings of the National Academy of Sciences, 111 (8), pp. 3170–3175, 2014. @article{Kremkow2014, title = {Neuronal nonlinearity explains greater visual spatial resolution for darks than lights}, author = {Jens Kremkow and Jianzhong Jin and Stanley J Komban and Yushi Wang and Reza Lashgari and Xiaobing Li and Michael Jansen and Qasim Zaidi and Jose-Manuel Alonso}, doi = {10.1073/pnas.1310442111}, year = {2014}, date = {2014-01-01}, journal = {Proceedings of the National Academy of Sciences}, volume = {111}, number = {8}, pages = {3170--3175}, abstract = {Astronomers and physicists noticed centuries ago that visual spatial resolution is higher for dark than light stimuli, but the neuronal mechanisms for this perceptual asymmetry remain unknown. Here we demonstrate that the asymmetry is caused by a neuronal nonlinearity in the early visual pathway. We show that neurons driven by darks (OFF neurons) increase their responses roughly linearly with luminance decrements, independent of the background luminance. However, neurons driven by lights (ON neurons) saturate their responses with small increases in luminance and need bright backgrounds to approach the linearity of OFF neurons. We show that, as a consequence of this difference in linearity, receptive fields are larger in ON than OFF thalamic neurons, and cortical neurons are more strongly driven by darks than lights at low spatial frequencies. This ON/OFF asymmetry in linearity could be demonstrated in the visual cortex of cats, monkeys, and humans and in the cat visual thalamus. Furthermore, in the cat visual thalamus, we show that the neuronal nonlinearity is present at the ON receptive field center of ON-center neurons and ON receptive field surround of OFF-center neurons, suggesting an origin at the level of the photoreceptor. These results demonstrate a fundamental difference in visual processing between ON and OFF channels and reveal a competitive advantage for OFF neurons over ON neurons at low spatial frequencies, which could be important during cortical development when retinal images are blurred by immature optics in infant eyes.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Astronomers and physicists noticed centuries ago that visual spatial resolution is higher for dark than light stimuli, but the neuronal mechanisms for this perceptual asymmetry remain unknown. Here we demonstrate that the asymmetry is caused by a neuronal nonlinearity in the early visual pathway. We show that neurons driven by darks (OFF neurons) increase their responses roughly linearly with luminance decrements, independent of the background luminance. However, neurons driven by lights (ON neurons) saturate their responses with small increases in luminance and need bright backgrounds to approach the linearity of OFF neurons. We show that, as a consequence of this difference in linearity, receptive fields are larger in ON than OFF thalamic neurons, and cortical neurons are more strongly driven by darks than lights at low spatial frequencies. This ON/OFF asymmetry in linearity could be demonstrated in the visual cortex of cats, monkeys, and humans and in the cat visual thalamus. Furthermore, in the cat visual thalamus, we show that the neuronal nonlinearity is present at the ON receptive field center of ON-center neurons and ON receptive field surround of OFF-center neurons, suggesting an origin at the level of the photoreceptor. These results demonstrate a fundamental difference in visual processing between ON and OFF channels and reveal a competitive advantage for OFF neurons over ON neurons at low spatial frequencies, which could be important during cortical development when retinal images are blurred by immature optics in infant eyes. |
Rebecca M Krock; Tirin Moore Visual sensitivity of frontal eye field neurons during the preparation of saccadic eye movements Journal Article Journal of Neurophysiology, 116 (6), pp. 2882–2891, 2016. @article{Krock2016, title = {Visual sensitivity of frontal eye field neurons during the preparation of saccadic eye movements}, author = {Rebecca M Krock and Tirin Moore}, doi = {10.1152/jn.01140.2015}, year = {2016}, date = {2016-01-01}, journal = {Journal of Neurophysiology}, volume = {116}, number = {6}, pages = {2882--2891}, abstract = {Primate vision is continuously disrupted by saccadic eye movements, and yet this disruption goes unperceived. One mechanism thought to reduce perception of this self-generated movement is saccadic suppression, a global loss of visual sensitivity just before, during, and after saccadic eye movements. The frontal eye field (FEF) is a candidate source of neural correlates of saccadic suppression previously observed in visual cortex, because it contributes to the generation of visually guided saccades and modulates visual cortical responses. However, whether the FEF exhibits a perisaccadic reduction in visual sensitivity that could be transmitted to visual cortex is unknown. To determine whether the FEF exhibits a signature of saccadic suppression, we recorded the visual responses of FEF neurons to brief, full-field visual probe stimuli presented during fixation and before onset of saccades directed away from the receptive field in rhesus macaques (Macaca mulatta). We measured visual sensitivity during both epochs and found that it declines before saccade onset. Visual sensitivity was significantly reduced in visual but not visuomotor neurons. This reduced sensitivity was also present in visual neurons with no movement-related modulation during visually guided saccades and thus occurred independently from movement-related activity. Across the population of visual neurons, sensitivity began declining similar to 80 ms before saccade onset. We also observed a similar presaccadic reduction in sensitivity to isoluminant, chromatic stimuli. Our results demonstrate that the signaling of visual information by FEF neurons is reduced during saccade preparation, and thus these neurons exhibit a signature of saccadic suppression.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Primate vision is continuously disrupted by saccadic eye movements, and yet this disruption goes unperceived. One mechanism thought to reduce perception of this self-generated movement is saccadic suppression, a global loss of visual sensitivity just before, during, and after saccadic eye movements. The frontal eye field (FEF) is a candidate source of neural correlates of saccadic suppression previously observed in visual cortex, because it contributes to the generation of visually guided saccades and modulates visual cortical responses. However, whether the FEF exhibits a perisaccadic reduction in visual sensitivity that could be transmitted to visual cortex is unknown. To determine whether the FEF exhibits a signature of saccadic suppression, we recorded the visual responses of FEF neurons to brief, full-field visual probe stimuli presented during fixation and before onset of saccades directed away from the receptive field in rhesus macaques (Macaca mulatta). We measured visual sensitivity during both epochs and found that it declines before saccade onset. Visual sensitivity was significantly reduced in visual but not visuomotor neurons. This reduced sensitivity was also present in visual neurons with no movement-related modulation during visually guided saccades and thus occurred independently from movement-related activity. Across the population of visual neurons, sensitivity began declining similar to 80 ms before saccade onset. We also observed a similar presaccadic reduction in sensitivity to isoluminant, chromatic stimuli. Our results demonstrate that the signaling of visual information by FEF neurons is reduced during saccade preparation, and thus these neurons exhibit a signature of saccadic suppression. |
Satwant Kumar; Ivo D Popivanov; Rufin Vogels Transformation of visual representations across ventral stream body-selective patches Journal Article Cerebral Cortex, 29 (1), pp. 215–229, 2017. @article{Kumar2017, title = {Transformation of visual representations across ventral stream body-selective patches}, author = {Satwant Kumar and Ivo D Popivanov and Rufin Vogels}, doi = {10.1093/cercor/bhx320}, year = {2017}, date = {2017-01-01}, journal = {Cerebral Cortex}, volume = {29}, number = {1}, pages = {215--229}, abstract = {Although the neural processing of visual images of bodies is critical for survival, it is much less well understood than face processing. Functional imaging studies demonstrated body selective regions in primate inferior temporal cortex. To advance our understanding of how the visual brain represents bodies, we compared the representation of animate and inanimate objects in two such body patches with fMRI-guided single unit recordings in rhesus monkeys. We found that the middle Superior Temporal Sulcus body patch (MSB) distinguishes to a greater extent bodies from non-bodies than the anterior Superior Temporal Sulcus body patch (ASB). Importantly, ASB carried more viewpoint-tolerant information about body posture and body identity than MSB, while MSB showed greater orientation selectivity. Combined with previous work on faces, this suggests that an increase in view-tolerant representations, coupled with a refined individuation, along the visual hierarchy is a general property of information processing within the inferior temporal cortex.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Although the neural processing of visual images of bodies is critical for survival, it is much less well understood than face processing. Functional imaging studies demonstrated body selective regions in primate inferior temporal cortex. To advance our understanding of how the visual brain represents bodies, we compared the representation of animate and inanimate objects in two such body patches with fMRI-guided single unit recordings in rhesus monkeys. We found that the middle Superior Temporal Sulcus body patch (MSB) distinguishes to a greater extent bodies from non-bodies than the anterior Superior Temporal Sulcus body patch (ASB). Importantly, ASB carried more viewpoint-tolerant information about body posture and body identity than MSB, while MSB showed greater orientation selectivity. Combined with previous work on faces, this suggests that an increase in view-tolerant representations, coupled with a refined individuation, along the visual hierarchy is a general property of information processing within the inferior temporal cortex. |
Victor de Lafuente; Mehrdad Jazayeri; Michael N Shadlen Representation of accumulating evidence for a decision in two parietal areas Journal Article Journal of Neuroscience, 35 (10), pp. 4306–4318, 2015. @article{Lafuente2015, title = {Representation of accumulating evidence for a decision in two parietal areas}, author = {Victor de Lafuente and Mehrdad Jazayeri and Michael N Shadlen}, doi = {10.1523/JNEUROSCI.2451-14.2015}, year = {2015}, date = {2015-01-01}, journal = {Journal of Neuroscience}, volume = {35}, number = {10}, pages = {4306--4318}, abstract = {Decisions are often made by accumulating evidence for and against the alternatives. The momentary evidence represented by sensory neurons is accumulated by downstream structures to form a decision variable, linking the evolving decision to the formation of a motor plan. When decisions are communicated by eye movements, neurons in the lateral intraparietal area (LIP) represent the accumulation of evidence bearing on the potential targets for saccades. We now show that reach-related neurons from the medial intraparietal area (MIP) exhibit a gradual modulation of their firing rates consistent with the representation of an evolving decision variable. When decisions were communicated by saccades instead of reaches, decision-related activity was attenuated in MIP, whereas LIP neurons were active while monkeys communicated decisions by saccades or reaches. Thus, for decisions communicated by a hand movement, a parallel flow of sensory information is directed to parietal areas MIP and LIP during decision formation.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Decisions are often made by accumulating evidence for and against the alternatives. The momentary evidence represented by sensory neurons is accumulated by downstream structures to form a decision variable, linking the evolving decision to the formation of a motor plan. When decisions are communicated by eye movements, neurons in the lateral intraparietal area (LIP) represent the accumulation of evidence bearing on the potential targets for saccades. We now show that reach-related neurons from the medial intraparietal area (MIP) exhibit a gradual modulation of their firing rates consistent with the representation of an evolving decision variable. When decisions were communicated by saccades instead of reaches, decision-related activity was attenuated in MIP, whereas LIP neurons were active while monkeys communicated decisions by saccades or reaches. Thus, for decisions communicated by a hand movement, a parallel flow of sensory information is directed to parietal areas MIP and LIP during decision formation. |
Rogier Landman; Jitendra Sharma; Mriganka Sur; Robert Desimone Effect of distracting faces on visual selective attention in the monkey Journal Article Proceedings of the National Academy of Sciences, 111 (50), pp. 18037–18042, 2014. @article{Landman2014, title = {Effect of distracting faces on visual selective attention in the monkey}, author = {Rogier Landman and Jitendra Sharma and Mriganka Sur and Robert Desimone}, doi = {10.1073/pnas.1420167111}, year = {2014}, date = {2014-01-01}, journal = {Proceedings of the National Academy of Sciences}, volume = {111}, number = {50}, pages = {18037--18042}, abstract = {In primates, visual stimuli with social and emotional content tend to attract attention. Attention might be captured through rapid, automatic, subcortical processing or guided by slower, more voluntary cortical processing. Here we examined whether irrelevant faces with varied emotional expressions interfere with a covert attention task in macaque monkeys. In the task, the monkeys monitored a target grating in the periphery for a subtle color change while ignoring distracters that included faces appearing elsewhere on the screen. The onset time of distracter faces before the target change, as well as their spatial proximity to the target, was varied from trial to trial. The presence of faces, especially faces with emotional expressions interfered with the task, indicating a competition for attentional resources between the task and the face stimuli. However, this interference was significant only when faces were presented for greater than 200 ms. Emotional faces also affected saccade velocity and reduced pupillary reflex. Our results indicate that the attraction of attention by emotional faces in the monkey takes a considerable amount of processing time, possibly involving cortical–subcortical interactions. Intranasal application of the hormone oxytocin ameliorated the interfering effects of faces. Together these results provide evidence for slow modulation of attention by emotional distracters, which likely involves oxytocinergic brain circuits.}, keywords = {}, pubstate = {published}, tppubtype = {article} } In primates, visual stimuli with social and emotional content tend to attract attention. Attention might be captured through rapid, automatic, subcortical processing or guided by slower, more voluntary cortical processing. Here we examined whether irrelevant faces with varied emotional expressions interfere with a covert attention task in macaque monkeys. In the task, the monkeys monitored a target grating in the periphery for a subtle color change while ignoring distracters that included faces appearing elsewhere on the screen. The onset time of distracter faces before the target change, as well as their spatial proximity to the target, was varied from trial to trial. The presence of faces, especially faces with emotional expressions interfered with the task, indicating a competition for attentional resources between the task and the face stimuli. However, this interference was significant only when faces were presented for greater than 200 ms. Emotional faces also affected saccade velocity and reduced pupillary reflex. Our results indicate that the attraction of attention by emotional faces in the monkey takes a considerable amount of processing time, possibly involving cortical–subcortical interactions. Intranasal application of the hormone oxytocin ameliorated the interfering effects of faces. Together these results provide evidence for slow modulation of attention by emotional distracters, which likely involves oxytocinergic brain circuits. |
Matthew L Leavitt; Florian Pieper; Adam Sachs; Ridha Joober; Julio C Martinez-Trujillo PLoS ONE, 8 (4), pp. 1–11, 2013. @article{Leavitt2013, title = {Structure of spike count correlations reveals functional interactions between neurons in dorsolateral prefrontal cortex area 8a of behaving primates}, author = {Matthew L Leavitt and Florian Pieper and Adam Sachs and Ridha Joober and Julio C Martinez-Trujillo}, doi = {10.1371/journal.pone.0061503}, year = {2013}, date = {2013-01-01}, journal = {PLoS ONE}, volume = {8}, number = {4}, pages = {1--11}, publisher = {10. 1371/journal.pone.0061503}, address = {e61503. doi}, abstract = {Neurons within the primate dorsolateral prefrontal cortex (dlPFC) are clustered in microcolumns according to their visuospatial tuning. One issue that remains poorly investigated is how this anatomical arrangement influences functional interactions between neurons during behavior. To investigate this question we implanted 4 mm×4 mm multielectrode arrays in two macaques' dlPFC area 8a and measured spike count correlations (rsc ) between responses of simultaneously recorded neurons when animals maintained stationary gaze. Positive and negative rsc were significantly higher than predicted by chance across a wide range of inter-neuron distances (from 0.4 to 4 mm). Positive rsc were stronger between neurons with receptive fields (RFs) separated by ≤90° of angular distance and progressively decreased as a function of inter-neuron physical distance. Negative rsc were stronger between neurons with RFs separated by textgreater90° and increased as a function of inter-neuron distance. Our results show that short- and long-range functional interactions between dlPFC neurons depend on the physical distance between them and the relationship between their visuospatial tuning preferences. Neurons with similar visuospatial tuning show positive rsc that decay with inter-neuron distance, suggestive of excitatory interactions within and between adjacent microcolumns. Neurons with dissimilar tuning from spatially segregated microcolumns show negative rsc that increase with inter-neuron distance, suggestive of inhibitory interactions. This pattern of results shows that functional interactions between prefrontal neurons closely follow the pattern of connectivity reported in anatomical studies. Such interactions may be important for the role of the prefrontal cortex in the allocation of attention to targets in the presence of competing distracters.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Neurons within the primate dorsolateral prefrontal cortex (dlPFC) are clustered in microcolumns according to their visuospatial tuning. One issue that remains poorly investigated is how this anatomical arrangement influences functional interactions between neurons during behavior. To investigate this question we implanted 4 mm×4 mm multielectrode arrays in two macaques' dlPFC area 8a and measured spike count correlations (rsc ) between responses of simultaneously recorded neurons when animals maintained stationary gaze. Positive and negative rsc were significantly higher than predicted by chance across a wide range of inter-neuron distances (from 0.4 to 4 mm). Positive rsc were stronger between neurons with receptive fields (RFs) separated by ≤90° of angular distance and progressively decreased as a function of inter-neuron physical distance. Negative rsc were stronger between neurons with RFs separated by textgreater90° and increased as a function of inter-neuron distance. Our results show that short- and long-range functional interactions between dlPFC neurons depend on the physical distance between them and the relationship between their visuospatial tuning preferences. Neurons with similar visuospatial tuning show positive rsc that decay with inter-neuron distance, suggestive of excitatory interactions within and between adjacent microcolumns. Neurons with dissimilar tuning from spatially segregated microcolumns show negative rsc that increase with inter-neuron distance, suggestive of inhibitory interactions. This pattern of results shows that functional interactions between prefrontal neurons closely follow the pattern of connectivity reported in anatomical studies. Such interactions may be important for the role of the prefrontal cortex in the allocation of attention to targets in the presence of competing distracters. |
Matthew L Leavitt; Florian Pieper; Adam J Sachs; Julio C Martinez-Trujillo Correlated variability modifies working memory fidelity in primate prefrontal neuronal ensembles Journal Article Proceedings of the National Academy of Sciences, 114 (12), pp. E2494–E2503, 2017. @article{Leavitt2017a, title = {Correlated variability modifies working memory fidelity in primate prefrontal neuronal ensembles}, author = {Matthew L Leavitt and Florian Pieper and Adam J Sachs and Julio C Martinez-Trujillo}, doi = {10.1073/pnas.1619949114}, year = {2017}, date = {2017-01-01}, journal = {Proceedings of the National Academy of Sciences}, volume = {114}, number = {12}, pages = {E2494--E2503}, abstract = {Neurons in the primate lateral prefrontal cortex (LPFC) encode working memory (WM) representations via sustained firing, a phenomenon hypothesized to arise from recurrent dynamics within ensembles of interconnected neurons. Here, we tested this hypothesis by using microelectrode arrays to examine spike count correlations (rsc) in LPFC neuronal ensembles during a spatial WM task. We found a pattern of pairwise rsc during WM maintenance indicative of stronger coupling between similarly tuned neurons and increased inhibition between dissimilarly tuned neurons. We then used a linear decoder to quantify the effects of the high-dimensional rsc structure on information coding in the neuronal ensembles. We found that the rsc structure could facilitate or impair coding, depending on the size of the ensemble and tuning properties of its constituent neurons. A simple optimization procedure demonstrated that near-maximum decoding performance could be achieved using a relatively small number of neurons. These WM- optimized subensembles were more signal correlation (rsignal)- diverse and anatomically dispersed than predicted by the statistics of the full recorded population of neurons, and they often con- tained neurons that were poorly WM-selective, yet enhanced cod- ing fidelity by shaping the ensemble's rsc structure. We observed a pattern of rsc between LPFC neurons indicative of recurrent dynamics as a mechanism for WM-related activity and that the rsc structure can increase the fidelity ofWM representations. Thus, WM coding in LPFC neuronal ensembles arises from a complex synergy between single neuron coding properties and multidimensional, ensemble-level phenomena.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Neurons in the primate lateral prefrontal cortex (LPFC) encode working memory (WM) representations via sustained firing, a phenomenon hypothesized to arise from recurrent dynamics within ensembles of interconnected neurons. Here, we tested this hypothesis by using microelectrode arrays to examine spike count correlations (rsc) in LPFC neuronal ensembles during a spatial WM task. We found a pattern of pairwise rsc during WM maintenance indicative of stronger coupling between similarly tuned neurons and increased inhibition between dissimilarly tuned neurons. We then used a linear decoder to quantify the effects of the high-dimensional rsc structure on information coding in the neuronal ensembles. We found that the rsc structure could facilitate or impair coding, depending on the size of the ensemble and tuning properties of its constituent neurons. A simple optimization procedure demonstrated that near-maximum decoding performance could be achieved using a relatively small number of neurons. These WM- optimized subensembles were more signal correlation (rsignal)- diverse and anatomically dispersed than predicted by the statistics of the full recorded population of neurons, and they often con- tained neurons that were poorly WM-selective, yet enhanced cod- ing fidelity by shaping the ensemble's rsc structure. We observed a pattern of rsc between LPFC neurons indicative of recurrent dynamics as a mechanism for WM-related activity and that the rsc structure can increase the fidelity ofWM representations. Thus, WM coding in LPFC neuronal ensembles arises from a complex synergy between single neuron coding properties and multidimensional, ensemble-level phenomena. |
Matthew L Leavitt; Florian Pieper; Adam J Sachs; Julio C Martinez-Trujillo A quadrantic bias in prefrontal representation of visual-mnemonic space Journal Article Cerebral Cortex, 28 , pp. 2405–2421, 2018. @article{Leavitt2018, title = {A quadrantic bias in prefrontal representation of visual-mnemonic space}, author = {Matthew L Leavitt and Florian Pieper and Adam J Sachs and Julio C Martinez-Trujillo}, doi = {10.1093/cercor/bhx142}, year = {2018}, date = {2018-01-01}, journal = {Cerebral Cortex}, volume = {28}, pages = {2405--2421}, abstract = {Single neurons in primate dorsolateral prefrontal cortex (dLPFC) are known to encode working memory (WM) representations of visual space. Psychophysical studies have shown that the horizontal and vertical meridians of the visual field can bias spatial information maintained in WM. However, most studies and models have tacitly assumed that dLPFC neurons represent mnemonic space homogenously. The anatomical organization of these representations has also eluded clear parametric description. We investigated these issues by recording from neuronal ensembles in macaque dLPFC with microelectrode arrays while subjects performed an oculomotor delayed-response task. We found that spatial WM representations in macaque dLPFC are biased by the vertical and horizontal meridians of the visual field, dividing mnemonic space into quadrants. This bias is reflected in single neuron firing rates, neuronal ensemble representations, the spike count correlation structure, and eye movement patterns. We also found that dLPFC representations of mnemonic space cluster anatomically in a nonretinotopic manner that partially reflects the organization of visual space. These results provide an explanation for known WM biases, and reveal novel principles of WM representation in prefrontal neuronal ensembles and across the cortical surface, as well as the need to reconceptualize models of WM to accommodate the observed representational biases.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Single neurons in primate dorsolateral prefrontal cortex (dLPFC) are known to encode working memory (WM) representations of visual space. Psychophysical studies have shown that the horizontal and vertical meridians of the visual field can bias spatial information maintained in WM. However, most studies and models have tacitly assumed that dLPFC neurons represent mnemonic space homogenously. The anatomical organization of these representations has also eluded clear parametric description. We investigated these issues by recording from neuronal ensembles in macaque dLPFC with microelectrode arrays while subjects performed an oculomotor delayed-response task. We found that spatial WM representations in macaque dLPFC are biased by the vertical and horizontal meridians of the visual field, dividing mnemonic space into quadrants. This bias is reflected in single neuron firing rates, neuronal ensemble representations, the spike count correlation structure, and eye movement patterns. We also found that dLPFC representations of mnemonic space cluster anatomically in a nonretinotopic manner that partially reflects the organization of visual space. These results provide an explanation for known WM biases, and reveal novel principles of WM representation in prefrontal neuronal ensembles and across the cortical surface, as well as the need to reconceptualize models of WM to accommodate the observed representational biases. |