Non-Human Primate Eye-Tracking Publications
All EyeLink eye tracker non-human primate research publications up until 2024 (with some early 2025s) are listed below by year. You can search the eye-tracking publications using keywords such as Temporal Cortex, Macaque, Antisaccade, etc. You can also search for individual author names. If we missed any EyeLink non-human primate articles, please email us!
2016 |
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 In: Nature, vol. 535, pp. 285–288, 2016. @article{Katz2016,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. |
Aarlenne Zein 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 In: Journal of Vision, vol. 16, no. 7, pp. 1–20, 2016. @article{Khan2016,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. |
Rebecca M. Krock; Tirin Moore Visual sensitivity of frontal eye field neurons during the preparation of saccadic eye movements Journal Article In: Journal of Neurophysiology, vol. 116, no. 6, pp. 2882–2891, 2016. @article{Krock2016,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. |
Noah M. Ledbetter; Charles D. Chen; Ilya E. Monosov Multiple Mechanisms for Processing Reward Uncertainty in the Primate Basal Forebrain Journal Article In: Journal of Neuroscience, vol. 36, no. 30, pp. 7852–7864, 2016. @article{Ledbetter2016,The ability to use information about the uncertainty of future outcomes is critical for adaptive behavior in an uncertain world.Weshow that the basal forebrain (BF) contains at least two distinct neural-coding strategies to support this capacity. The dorsal-lateral BF, including the ventral pallidum (VP), contains reward-sensitive neurons, some of which are selectively suppressed by uncertain-reward predictions (U-). In contrast, the medial BF (mBF) contains reward-sensitive neurons, some of which are selectively enhanced (U+) by uncertain-reward predictions. In a two-alternative choice-task, U- neurons were selectively suppressed while monkeys chose uncertain options over certain options. During the same choice-epoch, U+ neurons signaled the subjective reward value of the choice options. Additionally, after the choice was reported, U+ neurons signaled reward uncertainty until the choice outcome. We suggest that uncertainty-related suppression of VP may participate in the mediation of uncertainty-seeking actions, whereas uncertainty-related enhancement of the mBF may direct cognitive resources to monitor and learn from uncertain-outcomes. |
Liu D. Liu; Ralf M. Haefner; Christopher C. Pack A neural basis for the spatial suppression of visual motion perception Journal Article In: eLife, vol. 5, pp. 1–20, 2016. @article{Liu2016c,In theory, sensory perception should be more accurate when more neurons contribute to the representation of a stimulus. However, psychophysical experiments that use larger stimuli to activate larger pools of neurons sometimes report impoverished perceptual performance. To determine the neural mechanisms underlying these paradoxical findings, we trained monkeys to discriminate the direction of motion of visual stimuli that varied in size across trials, while simultaneously recording from populations of motion-sensitive neurons in cortical area MT. We used the resulting data to constrain a computational model that explained the behavioral data as an interaction of three main mechanisms: noise correlations, which prevented stimulus information from growing with stimulus size; neural surround suppression, which decreased sensitivity for large stimuli; and a read-out strategy that emphasized neurons with receptive fields near the stimulus center. These results suggest that paradoxical percepts reflect tradeoffs between sensitivity and noise in neuronal populations. |
Lu Liu; Liang She; Ming Chen; Tianyi Liu; Haidong D. Lu; Yang Dan; Mu-ming Poo Spatial structure of neuronal receptive field in awake monkey secondary visual cortex (V2) Journal Article In: Proceedings of the National Academy of Sciences, vol. 113, no. 7, pp. 1913–1918, 2016. @article{Liu2016d,Visual processing depends critically on the receptive field (RF) properties of visual neurons. However, comprehensive characterization of RFs beyond the primary visual cortex (V1) remains a challenge. Here we report fine RF structures in secondary visual cortex (V2) of awake macaque monkeys, identified through a projection pursuit regression analysis of neuronal responses to natural images. We found that V2 RFs could be broadly classified as V1-like (typical Gabor-shaped subunits), ultralong (subunits with high aspect ratios), or complex-shaped (subunits with multiple oriented components). Furthermore, single-unit recordings from functional domains identified by intrinsic optical imaging showed that neurons with ultralong RFs were primarily localized within pale stripes, whereas neurons with complex-shaped RFs were more concentrated in thin stripes. Thus, by combining single-unit recording with optical imaging and a computational approach, we identified RF subunits underlying spatial feature selectivity of V2 neurons and demonstrated the functional organization of these RF properties. |
Mikael Lundqvist; Jonas Rose; Pawel Herman; Scott L. Brincat; Timothy J. Buschman; Earl K. Miller Gamma and beta bursts underlie working memory Journal Article In: Neuron, vol. 90, no. 1, pp. 152–164, 2016. @article{Lundqvist2016,Working memory is thought to result from sustained neuron spiking. However, computational models suggest complex dynamics with discrete oscillatory bursts. We analyzed local field potential (LFP) and spiking from the prefrontal cortex (PFC) of monkeys performing a working memory task. There were brief bursts of narrow-band gamma oscillations (45–100 Hz), varied in time and frequency, accompanying encoding and re-activation of sensory information. They appeared at a minority of recording sites associated with spiking reflecting the to-be-remembered items. Beta oscillations (20–35 Hz) also occurred in brief, variable bursts but reflected a default state interrupted by encoding and decoding. Only activity of neurons reflecting encoding/decoding correlated with changes in gamma burst rate. Thus, gamma bursts could gate access to, and prevent sensory interference with, working memory. This supports the hypothesis that working memory is manifested by discrete oscillatory dynamics and spiking, not sustained activity. |
2015 |
Bram-Ernst Verhoef; Rufin Vogels; Peter Janssen; Leonardo Chelazzi Effects of microstimulation in the anterior intraparietal area during three-dimensional shape categorization Journal Article In: PLoS ONE, vol. 10, no. 8, pp. e0136543, 2015. @article{Verhoef2015,The anterior intraparietal area (AIP) of rhesus monkeys is part of the dorsal visual stream and contains neurons whose visual response properties are commensurate with a role in three-dimensional (3D) shape perception. Neuronal responses in AIP signal the depth structure of disparity-defined 3D shapes, reflect the choices of monkeys while they categorize 3D shapes, and mirror the behavioral variability across different stimulus conditions during 3D-shape categorization. However, direct evidence for a role of AIP in 3D-shape perception has been lacking. We trained rhesus monkeys to categorize disparity-defined 3D shapes and examined AIP's contribution to 3D-shape categorization by microstimulating in clusters of 3D-shape selective AIP neurons during task performance. We find that microstimulation effects on choices (monkey M1) and reaction times (monkey M1 and M2) depend on the 3D-shape preference of the stimulated site. Moreover, electrical stimulation of the same cells, during either the 3D-shape-categorization task or a saccade task, could affect behavior differently. Interestingly, in one monkey we observed a strong correlation between the strength of choice-related AIP activity (choice probabilities) and the influence of microstimulation on 3D-shape-categorization behavior (choices and reaction time). These findings propose AIP as part of the network responsible for 3D-shape perception. The results also show that the anterior intraparietal cortex contains cells with different tuning properties, i.e. 3D-shape- or saccade-related, that can be dynamically read out depending on the requirements of the task at hand. |
Yaoguang Jiang; Dmitry Yampolsky; Gopathy Purushothaman; Vivien A. Casagrande Perceptual decision related activity in the lateral geniculate nucleus Journal Article In: Journal of Neurophysiology, vol. 114, no. 1, pp. 717–735, 2015. @article{Jiang2015,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. |
Mehrdad Jazayeri; Michael N. Shadlen A Neural Mechanism for Sensing and Reproducing a Time Interval Journal Article In: Current Biology, vol. 25, no. 20, pp. 2599–2609, 2015. @article{Jazayeri2015,Timing plays a crucial role in sensorimotor function. However, the neural mechanisms that enable the brain to flexibly measure and reproduce time intervals are not known. We recorded neural activity in parietal cortex of monkeys in a time reproduction task. Monkeys were trained to measure and immediately afterward reproduce different sample intervals. While measuring an interval, neural responses had a nonlinear profile that increased with the duration of the sample interval. Activity was reset during the transition from measurement to production and was followed by a ramping activity whose slope encoded the previously measured sample interval. We found that firing rates at the end of the measurement epoch were correlated with both the slope of the ramp and the monkey's corresponding production interval on a trial-by-trial basis. Analysis of response dynamics further linked the rate of change of firing rates in the measurement epoch to the slope of the ramp in the production epoch. These observations suggest that, during time reproduction, an interval is measured prospectively in relation to the desired motor plan to reproduce that interval. |
Yaoguang Jiang; Gopathy Purushothaman; Vivien A. Casagrande The functional asymmetry of ON and OFF channels in the perception of contrast Journal Article In: Journal of Neurophysiology, vol. 114, pp. 2816–2829, 2015. @article{Jiang2015a,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. |
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 In: Proceedings of the National Academy of Sciences, vol. 112, no. 22, pp. 7085–7090, 2015. @article{Jones2015,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. |
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 In: European Journal of Neuroscience, vol. 41, no. 12, pp. 1603–1613, 2015. @article{Khayat2015,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. |
Shinichiro Kira; Tianming Yang; Michael N. Shadlen A neural implementation of Wald's Sequential Probability Ratio Test Journal Article In: Neuron, vol. 85, no. 4, pp. 861–873, 2015. @article{Kira2015,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. |
Thomas Zhihao Luo; John H. R. Maunsell Neuronal modulations in visual cortex are associated with only one of multiple components of attention Journal Article In: Neuron, vol. 86, no. 5, pp. 1182–1188, 2015. @article{Luo2015,Neuronal signals related to visual attention are found in widespread brain regions, and these signals are generally assumed to participate in a common mechanism of attention. However, the behavioral effects of attention in detection can be separated into two distinct components: spatially selective shifts in either the criterion or sensitivity of the subject. Here we show that a paradigm used by many single-neuron studies of attention conflates behavioral changes in the subject's criterion and sensitivity. Then, using a task designed to dissociate these two components, we found that multiple aspects of attention-related neuronal modulations in area V4 of monkey visual cortex corresponded to behavioral shifts in sensitivity, but not criterion. This result suggests that separate components of attention are associated with signals in different brain regions and that attention is not a unitary process in the brain, but instead consists of distinct neurobiological mechanisms. Luo and Maunsell show that the neuronal modulations in visual cortex correspond to only one of multiple components of attention. This result suggests that different brain structures underlie separate mechanisms of attention and that attention is not a unitary process in the brain, but instead consists of distinct neurobiological mechanisms. |
Najib J. Majaj; Ha Hong; Ethan A. Solomon; James J. DiCarlo Simple learned weighted sums of inferior temporal neuronal firing rates accurately predict human core object recognition performance Journal Article In: Journal of Neuroscience, vol. 35, no. 39, pp. 13402–13418, 2015. @article{Majaj2015,To go beyond qualitative models of the biological substrate of object recognition, we ask: can a single ventral stream neuronal linking hypothesis quantitatively account for core object recognition performance over a broad range of tasks? We measured human performance in 64 object recognition tests using thousands ofchallenging images that explore shape similarity and identity preserving object variation. We then used multielectrode arrays to measure neuronal population responses to those same images in visual areas V4 and inferior temporal (IT) cortex ofmonkeys and simulated V1 population responses. We tested leading candidate linking hypotheses and control hypotheses, each postulating how ventral stream neuronal responses underlie object recognition behavior. Specifically, for each hypothesis, we computed the predicted performance on the 64 tests and compared it with the measured pattern ofhuman performance. All tested hypotheses based on low- and mid-level visually evoked activity (pixels, V1, and V4) were very poor predictors ofthe human behavioral pattern. However, simple learned weighted sums of distributed average IT firing rates exactly predicted the behavioral pattern. More elaborate linking hypotheses relying on IT trial-by-trial correlational structure, finer IT temporal codes, or ones that strictly respect the known spatial substructures ofIT (“face patches”) did not improve predictive power. Although these results do not reject those more elaborate hypotheses, they suggest a simple, sufficient quantitative model: each object recognition task is learned from the spatially distributed mean firing rates (100 ms) of ~60,000 IT neurons and is executed as a simple weighted sum ofthose firing rates. |
J. Patrick Mayo; Amie R. DiTomasso; Marc A. Sommer; Matthew A. Smith Dynamics of visual receptive fields in the macaque frontal eye field Journal Article In: Journal of Neurophysiology, vol. 114, no. 6, pp. 3201–3210, 2015. @article{Mayo2015,Neuronal receptive fields (RFs) provide the foundation for understanding systems-level sensory processing. In early visual areas, investigators have mapped RFs in detail using stochastic stimuli and sophisticated analytical approaches. Much less is known about RFs in prefrontal cortex. Visual stimuli used for mapping RFs in prefrontal cortex tend to cover a small range of spatial and temporal parameters, making it difficult to understand their role in visual processing. To address these shortcomings, we implemented a generalized linear model to measure the RFs of neurons in the macaque frontal eye field (FEF) in response to sparse, full-field stimuli. Our high-resolution, probabilistic approach tracked the evolution of RFs during passive fixation, and we validated our results against conventional measures. We found that FEF neurons exhibited a surprising level of sensitivity to stimuli presented as briefly as 10 ms or to multiple dots presented simultaneously, suggesting that FEF visual responses are more precise than previously appreciated. FEF RF spatial structures were largely maintained over time and between stimulus conditions. Our results demonstrate that the application of probabilistic RF mapping to FEF and similar association areas is an important tool for clarifying the neuronal mechanisms of cognition. |
Ken-ichi Amemori; Satoko Amemori; Ann M. Graybiel Motivation and affective judgments differentially recruit neurons in the primate dorsolateral prefrontal and anterior cingulate cortex Journal Article In: Journal of Neuroscience, vol. 35, no. 5, pp. 1939–1953, 2015. @article{Amemori2015a,The judgment of whether to accept or to reject an offer is determined by positive and negative affect related to the offer, but affect also induces motivational responses. Rewarding and aversive cues influence the firing rates of many neurons in primate prefrontal and cingulate neocortical regions, but it still is unclear whether neurons in these regions are related to affective judgment or to motivation.To address this issue, we recorded simultaneously the neuronal spike activities of single units in the dorsolateral prefrontal cortex (dlPFC) and the anterior cingulate cortex (ACC) of macaque monkeys as they performed approach–avoidance (Ap–Av) and approach–approach (Ap–Ap) decision-making tasks that can behaviorally dissociate affective judgment and motivation. Notably, neurons having activity correlated with motivational condition could be distinguished from neurons having activity related to affective judgment, especially in the Ap–Av task. Although many neurons in both regions exhibited similar, selective patterns of task-related activity, we found a larger proportion of neurons activated in low motivational conditions in the dlPFC than in the ACC, and the onset of this activity was signifi- cantly earlier in the dlPFC than in the ACC. Furthermore, the temporal onsets of affective judgment represented by neuronal activities were significantly slower in the low motivational conditions than in the other conditions. These findings suggest that motivation and affective judgment both recruit dlPFC and ACC neurons but with differential degrees of involvement and timing. |
Satoko Amemori; Ken-ichi Amemori; Margaret L. Cantor; Ann M. Graybiel A non-invasive head-holding device for chronic neural recordings in awake behaving monkeys Journal Article In: Journal of Neuroscience Methods, vol. 240, pp. 154–160, 2015. @article{Amemori2015,Background: We have developed a novel head-holding device for behaving non-human primates that affords stability suitable for reliable chronic electrophysiological recording experiments. The device is completely non-invasive, and thus avoids the risk of infection and other complications that can occur with the use of conventional, surgically implanted head-fixation devices. New method: The device consists of a novel non-invasive head mold and bar clamp holder, and is customized to the shape of each monkey's head. The head-holding device that we introduce, combined with our recording system and reflection-based eye-tracking system, allows for chronic behavioral experiments and single-electrode or multi-electrode recording, as well as manipulation of brain activity. Results and comparison with existing methods: With electrodes implanted chronically in multiple brain regions, we could record neural activity from cortical and subcortical structures with stability equal to that recorded with conventional head-post fixation. Consistent with the non-invasive nature of the device, we could record neural signals for more than two years with a single implant. Importantly, the monkeys were able to hold stable eye fixation positions while held by this device, demonstrating the possibility of analyzing eye movement data with only the gentle restraint imposed by the non-invasive head-holding device. Conclusions: We show that the head-holding device introduced here can be extended to the head holding of smaller animals, and note that it could readily be adapted for magnetic resonance brain imaging over extended periods of time. |
Jalal K. Baruni; Brian Lau; C. Daniel Salzman Reward expectation differentially modulates attentional behavior and activity in visual area V4 Journal Article In: Nature Neuroscience, vol. 18, no. 11, pp. 1656–1663, 2015. @article{Baruni2015,Neural activity in visual area V4 is enhanced when attention is directed into neuronal receptive fields. However, the source of this enhancement is unclear, as most physiological studies have manipulated attention by changing the absolute reward associated with a particular location as well as its value relative to other locations. We trained monkeys to discriminate the orientation of two stimuli presented simultaneously in different hemifields while we independently varied the reward magnitude associated with correct discrimination at each location. Behavioral measures of attention were controlled by the relative value of each location. By contrast, neurons in V4 were consistently modulated by absolute reward value, exhibiting increased activity, increased gamma-band power and decreased trial-to-trial variability whenever receptive field locations were associated with large rewards. These data challenge the notion that the perceptual benefits of spatial attention rely on increased signal-to-noise in V4. Instead, these benefits likely derive from downstream selection mechanisms. |
Narcisse P. Bichot; Matthew T. Heard; Ellen M. DeGennaro; Robert Desimone A source for feature-based attention in the prefrontal cortex Journal Article In: Neuron, vol. 88, no. 4, pp. 832–844, 2015. @article{Bichot2015,In cluttered scenes, we can use feature-based attention to quickly locate a target object. To understand how feature attention is used to find and select objects for action, we focused on the ventral prearcuate (VPA) region of prefrontal cortex. In a visual search task, VPA cells responded selectively to search cues, maintained their feature selectivity throughout the delay and subsequent saccades, and discriminated the search target in their receptive fields with a time course earlier than in FEF or IT cortex. Inactivation of VPA impaired the animals' ability to find targets, and simultaneous recordings in FEF revealed that the effects of feature attention were eliminated while leaving the effects of spatial attention in FEF intact. Altogether, the results suggest that VPA neurons compute the locations of objects with the features sought and send this information to FEF to guide eye movements to those relevant stimuli. |
Tommy C. Blanchard; Benjamin Y. Hayden Monkeys are more patient in a foraging task than in a standard intertemporal choice task Journal Article In: PLoS ONE, vol. 10, no. 2, pp. e0117057, 2015. @article{Blanchard2015,Studies of animal impulsivity generally find steep subjective devaluation, or discounting, of delayed rewards - often on the order of a 50% reduction in value in a few seconds. Because such steep discounting is highly disfavored in evolutionary models of time preference, we hypothesize that discounting tasks provide a poor measure of animals' true time preferences. One prediction of this hypothesis is that estimates of time preferences based on these tasks will lack external validity, i.e. fail to predict time preferences in other contexts. We examined choices made by four rhesus monkeys in a computerized patch-leaving foraging task interleaved with a standard intertemporal choice task. Monkeys were significantly more patient in the foraging task than in the intertemporal choice task. Patch-leaving behavior was well fit by parameter-free optimal foraging equations but poorly fit by the hyperbolic discount parameter obtained from the intertemporal choice task. Day-to-day variation in time preferences across the two tasks was uncorrelated with each other. These data are consistent with the conjecture that seemingly impulsive behavior in animals is an artifact of their difficulty understanding the structure of intertemporal choice tasks, and support the idea that animals are more efficient rate maximizers in the multi-second range than intertemporal choice tasks would suggest. |
Tommy C. Blanchard; Caleb E. Strait; Benjamin Y. Hayden Ramping ensemble activity in dorsal anterior cingulate neurons during persistent commitment to a decision Journal Article In: Journal of Neurophysiology, vol. 114, no. 4, pp. 2439–2449, 2015. @article{Blanchard2015a,We frequently need to commit to a choice to achieve our goals; however, the neural processes that keep us motivated in pursuit of delayed goals remain obscure. We examined ensemble responses of neurons in macaque dorsal anterior cingulate cortex (dACC), an area previously implicated in self-control and persistence, in a task that requires commitment to a choice to obtain a reward. After reward receipt, dACC neurons signaled reward amount with characteristic ensemble firing rate patterns; during the delay in anticipation of the reward, ensemble activity smoothly and gradually came to resemble the postreward pattern. On the subset of risky trials, in which a reward was anticipated with 50% certainty, ramping ensemble activity evolved to the pattern associated with the anticipated reward (and not with the anticipated loss) and then, on loss trials, took on an inverted form anticorrelated with the form associated with a win. These findings enrich our knowledge of reward processing in dACC and may have broader implications for our understanding of persistence and self-control. |
Scott L. Brincat; Earl K. Miller Frequency-specific hippocampal-prefrontal interactions during associative learning Journal Article In: Nature Neuroscience, vol. 18, no. 4, pp. 576–581, 2015. @article{Brincat2015,Much of our knowledge of the world depends on learning associations (for example, face-name), for which the hippocampus (HPC) and prefrontal cortex (PFC) are critical. HPC-PFC interactions have rarely been studied in monkeys, whose cognitive and mnemonic abilities are akin to those of humans. We found functional differences and frequency-specific interactions between HPC and PFC of monkeys learning object pair associations, an animal model of human explicit memory. PFC spiking activity reflected learning in parallel with behavioral performance, whereas HPC neurons reflected feedback about whether trial-and-error guesses were correct or incorrect. Theta-band HPC-PFC synchrony was stronger after errors, was driven primarily by PFC to HPC directional influences and decreased with learning. In contrast, alpha/beta-band synchrony was stronger after correct trials, was driven more by HPC and increased with learning. Rapid object associative learning may occur in PFC, whereas HPC may guide neocortical plasticity by signaling success or failure via oscillatory synchrony in different frequency bands. |
Aaron L. Cecala; Ivan Smalianchuk; Sanjeev B. Khanna; Matthew A. Smith; Neeraj J. Gandhi Context cue-dependent saccadic adaptation in rhesus macaques cannot be elicited using color Journal Article In: Journal of Neurophysiology, vol. 114, no. 1, pp. 570–584, 2015. @article{Cecala2015,When the head does not move, rapid movements of the eyes called saccades are used to redirect the line of sight. Saccades are defined by a series of metrical and kinematic (evolution of a movement as a function of time) relationships. For example, the amplitude of a saccade made from one visual target to another is roughly 90% of the distance between the initial fixation point (T0) and the peripheral target (T1). However, this stereotypical relationship between saccade amplitude and initial retinal error (T1-T0) may be altered, either increased or decreased, by surreptitiously displacing a visual target during an ongoing saccade. This form of motor learning (called saccadic adaptation) has been described in both humans and monkeys. Recent experiments in humans and monkeys have suggested that internal (proprioceptive) and external (target shape, color, and/or motion) cues may be used to produce context-dependent adaptation. We tested the hypothesis that an external contextual cue (target color) could be used to evoke differential gain (actual saccade/initial retinal error) states in rhesus monkeys. We did not observe differential gain states correlated with target color regardless of whether targets were displaced along the same vector as the primary saccade or perpendicular to it. Furthermore, this observation held true regardless of whether adaptation trials using various colors and intrasaccade target displacements were randomly intermixed or presented in short or long blocks of trials. These results are consistent with hypotheses that state that color cannot be used as a contextual cue and are interpreted in light of previous studies of saccadic adaptation in both humans and monkeys. |
Jason L. Chan; Michael J. Koval; Thilo Womelsdorf; Stephen G. Lomber; Stefan Everling Dorsolateral prefrontal cortex deactivation in monkeys reduces preparatory beta and gamma power in the superior colliculus Journal Article In: Cerebral Cortex, vol. 25, no. 12, pp. 4704–4714, 2015. @article{Chan2015,Cognitive control requires the selection and maintenance of task-relevant stimulus-response associations, or rules. The dorsolateral prefrontal cortex (DLPFC) has been implicated by lesion, functional imaging, and neurophysiological studies to be involved in encoding rules, but the mechanisms by which it modulates other brain areas are poorly understood. Here, the functional relationship of the DLPFC with the superior colliculus (SC) was investigated by bilaterally deactivating the DLPFC while recording local field potentials (LFPs) in the SC in monkeys performing an interleaved pro- and antisaccade task. Event-related LFPs showed differences between pro- and antisaccades and responded prominently to stimulus presentation. LFP power after stimulus onset was higher for correct saccades than erroneous saccades. Deactivation of the DLPFC did not affect stimulus onset related LFP activity, but reduced high beta (20-30 Hz) and high gamma (60-150 Hz) power during the preparatory period for both pro- and antisaccades. Spike rate during the preparatory period was positively correlated with gamma power and this relationship was attenuated by DLPFC deactivation. These results suggest that top-down control of the SC by the DLPFC may be mediated by beta oscillations. |
Steve W. C. Chang; Nicholas A. Fagan; Koji Toda; Amanda V. Utevsky; John M. Pearson; Michael L. Platt Neural mechanisms of social decision-making in the primate amygdala Journal Article In: Proceedings of the National Academy of Sciences, vol. 112, no. 52, pp. 16012–16017, 2015. @article{Chang2015,SignificanceMaking social decisions requires evaluation of benefits and costs to self and others. Long associated with emotion and vigilance, neurons in primate amygdala also signal reward and punishment as well as information about the faces and eyes of others. Here we show that neurons in the basolateral amygdala signal the value of rewards for self and others when monkeys make social decisions. These value-mirroring neurons reflected monkeys tendency to make prosocial decisions on a momentary as well as long-term basis. We also found that delivering the social peptide oxytocin into basolateral amygdala enhances both prosocial tendencies and attention to the recipients of prosocial decisions. Our findings endorse the amygdala as a critical neural nexus regulating social decisions. Social decisions require evaluation of costs and benefits to oneself and others. Long associated with emotion and vigilance, the amygdala has recently been implicated in both decision-making and social behavior. The amygdala signals reward and punishment, as well as facial expressions and the gaze of others. Amygdala damage impairs social interactions, and the social neuropeptide oxytocin (OT) influences human social decisions, in part, by altering amygdala function. Here we show in monkeys playing a modified dictator game, in which one individual can donate or withhold rewards from another, that basolateral amygdala (BLA) neurons signaled social preferences both across trials and across days. BLA neurons mirrored the value of rewards delivered to self and others when monkeys were free to choose but not when the computer made choices for them. We also found that focal infusion of OT unilaterally into BLA weakly but significantly increased both the frequency of prosocial decisions and attention to recipients for context-specific prosocial decisions, endorsing the hypothesis that OT regulates social behavior, in part, via amygdala neuromodulation. Our findings demonstrate both neurophysiological and neuroendocrinological connections between primate amygdala and social decisions. |
Evy Cleeren; Cindy Casteels; Karolien Goffin; Peter Janssen; Wim Van Paesschen Ictal perfusion changes associated with seizure progression in the amygdala kindling model in the rhesus monkey Journal Article In: Epilepsia, vol. 56, no. 9, pp. 1366–1375, 2015. @article{Cleeren2015,OBJECTIVE: Amygdala kindling is a widely used animal model for studying mesial temporal lobe epileptogenesis. In the macaque monkey, electrical amygdala kindling develops slowly and provides an opportunity for investigating ictal perfusion changes during epileptogenesis. METHODS: Two rhesus monkeys were electrically kindled through chronically implanted electrodes in the right amygdala over a period of 16 and 17 months. Ictal perfusion single photon emission computed tomography (SPECT) imaging was performed during each of the four predefined clinical stages. RESULTS: Afterdischarge duration increased slowly over 477 days for monkey K and 515 days for monkey S (18 ± 8 s in stage I; 52 ± 13 s in stage IV). During this time, the animals progressed through four clinical stages ranging from interrupting ongoing behavior to bilateral convulsions. Ictal SPECT perfusion imaging showed well-localized but widely distributed regions of hyperperfusion and hypoperfusion, in both cortical and subcortical structures, at every seizure stage. A large portion of the ictal network was involved in the early stages of epileptogenesis and subsequently expanded over time as seizure severity evolved. SIGNIFICANCE: Our data indicate that the different mesial temporal lobe seizure types occur within a common network affecting several parts of the brain, and that seizure severity may be determined by seizure-induced epileptogenesis within a bihemispheric network that is implicated from the start of the process. |
Mojtaba Seyedhosseini; S. Shushruth; Tyler Davis; Jennifer M. Ichida; Paul A. House; Bradley Greger; Alessandra Angelucci; Tolga Tasdizen Informative features of local field potential signals in primary visual cortex during natural image stimulation Journal Article In: Journal of Neurophysiology, vol. 113, no. 5, pp. 1520–1532, 2015. @article{Seyedhosseini2015,The local field potential (LFP) is of growing importance in neurophysiology as a metric of network activity and as a readout signal for use in brain-machine interfaces. However, there are uncertainties regarding the kind and visual field extent of information carried by LFP signals, and the specific features of the LFP signal conveying such information, especially under naturalistic conditions. To address these questions, we recorded LFP responses to natural images in V1 of awake and anesthetized macaques using Utah multielectrode arrays. First, we show that it is possible to identify presented natural images from the LFP responses they evoke using trained Gabor wavelet (GW) models. Since GW models were devised to explain the spiking responses of V1 cells, this finding suggests that local spiking activity and LFPs (thought to reflect primarily local synaptic activity) carry similar visual information. Second, models trained on scalar metrics, like evoked LFP response range, provide robust image identification, supporting the informative nature of even simple LFP features. Third, image identification is robust only for the first 300ms following image presentation, and image information is not restricted to any of the spectral bands. This suggests that the short latency broadband LFP response carries most information during natural scene viewing. Finally, best image identification was achieved by GW models incorporating information at the scale of ~0.5° in size and trained using 4 different orientations. This suggests that during natural image viewing LFPs carry stimulus-specific information at spatial scales corresponding to few orientation columns in macaque V1. |
Heida M. Sigurdardottir; David L. Sheinberg The effects of short-term and long-term learning on the responses of lateral intraparietal neurons to visually presented objects Journal Article In: Journal of Cognitive Neuroscience, vol. 27, no. 7, pp. 1360–1375, 2015. @article{Sigurdardottir2015,The lateral intraparietal area (LIP) is thought to play an important role in the guidance of where to look and pay attention. LIP can also respond selectively to differently shaped objects. We sought to understand to what extent short-term and long-term experience with visual orienting determines the responses of LIP to objects of different shapes. We taught monkeys to arbitrarily associate centrally presented objects of various shapes with orienting either toward or away from a preferred spatial location of a neuron. The training could last for less than a single day or for several months. We found that neural responses to objects are affected by such experience, but that the length of the learning period determines how this neural plasticity manifests. Short-term learning affects neural responses to objects, but these effects are only seen relatively late after visual onset; at this time, the responses to newly learned objects resemble those of familiar objects that share their meaning or arbitrary association. Long-term learning affects the earliest bottom–up responses to visual objects. These responses tend to be greater for objects that have been associated with looking toward, rather than away from, LIP neurons' preferred spatial locations. Responses to objects can nonetheless be distinct, although they have been similarly acted on in the past and will lead to the same orienting behavior in the future. Our results therefore indicate that a complete experience-driven override of LIP object responses may be difficult or impossible. We relate these results to behavioral work on visual attention. |
Adam C. Snyder; Michael J. Morais; Cory M. Willis; Matthew A. Smith Global network influences on local functional connectivity Journal Article In: Nature Neuroscience, vol. 18, no. 5, pp. 736–743, 2015. @article{Snyder2015a,A central neuroscientific pursuit is understanding neuronal interactions that support computations underlying cognition and behavior. Although neurons interact across disparate scales, from cortical columns to whole-brain networks, research has been restricted to one scale at a time. We measured local interactions through multi-neuronal recordings while accessing global networks using scalp electroencephalography (EEG) in rhesus macaques. We measured spike count correlation, an index of functional connectivity with computational relevance, and EEG oscillations, which have been linked to various cognitive functions. We found a non-monotonic relationship between EEG oscillation amplitude and spike count correlation, contrary to the intuitive expectation of a direct relationship. With a widely used network model, we replicated these findings by incorporating a private signal targeting inhibitory neurons, a common mechanism proposed for gain modulation. Finally, we found that spike count correlation explained nonlinearities in the relationship between EEG oscillations and response time in a spatial selective attention task. |
Adam C. Snyder; Matthew A. Smith Stimulus-dependent spiking relationships with the EEG Journal Article In: Journal of Neurophysiology, vol. 114, no. 3, pp. 1468–1482, 2015. @article{Snyder2015,The development and refinement of noninvasive techniques for imaging neural activity is of paramount importance for human neuroscience. Currently, the most accessible and popular technique is electroencephalography (EEG). However, nearly all of what we know about the neural events that underlie EEG signals is based on inference, because of the dearth of studies that have simultaneously paired EEG recordings with direct recordings of single neurons. From the perspective of electrophysiologists there is growing interest in understanding how spiking activ- ity coordinates with large-scale cortical networks. Evidence from recordings at both scales highlights that sensory neurons operate in very distinct states during spontaneous and visually evoked activity, which appear to form extremes in a continuum of coordination in neural networks. We hypothesized that individual neurons have idio- syncratic relationships to large-scale network activity indexed by EEG signals, owing to the neurons' distinct computational roles within the local circuitry. We tested this by recording neuronal populations in visual area V4 of rhesus macaques while we simultaneously recorded EEG. We found substantial heterogeneity in the timing and strength of spike-EEG relationships and that these relationships became more diverse during visual stimulation compared with the spontaneous state. The visual stimulus apparently shifts V4 neurons from a state in which they are relatively uniformly embedded in large-scale network activity to a state in which their distinct roles within the local population are more prominent, suggesting that the specific way in which individual neurons relate to EEG signals may hold clues regarding their computational roles. |
Joo-Hyun Song; Robert M. McPeek Neural correlates of target selection for reaching movements in superior colliculus Journal Article In: Journal of Neurophysiology, vol. 113, no. 5, pp. 1414–1422, 2015. @article{Song2015,We recently demonstrated that inactivation of the primate superior colliculus (SC) causes a deficit in target selection for arm-reaching movements when the reach target is located in the inactivated field (Song JH, Rafal RD, McPeek RM. Proc Natl Acad Sci USA 108: E1433–E1440, 2011). This is consistent with the notion that the SC is part of a general-purpose target selection network beyond eye movements. To understand better the role of SC activity in reach target selection, we examined how individual SC neurons in the intermediate layers discriminate a reach target from distractors. Monkeys reached to touch a color oddball target among distractors while maintaining fixation. We found that many SC neurons robustly discriminate the goal of the reaching movement before the onset of the reach even though no saccade is made. To identify these cells in the context of conventional SC cell classification schemes, we also recorded visual, delay-period, and saccade-related responses in a delayed saccade task. On average, SC cells that discriminated the reach target from distractors showed significantly higher visual and delay-period activity than nondiscriminating cells, but there was no significant difference in saccade-related activity. Whereas a majority of SC neurons that discriminated the reach target showed significant delay-period activity, all nondiscriminating cells lacked such activity. We also found that some cells without delay-period activity did discriminate the reach target from distractors. We conclude that the majority of intermediate-layer SC cells discriminate a reach target from distractors, consistent with the idea that the SC contains a priority map used for effector-independent target selection. |
Caleb E. Strait; Brianna J. Sleezer; Benjamin Y. Hayden Signatures of value comparison in ventral striatum neurons Journal Article In: PLoS Biology, vol. 13, no. 6, pp. 1–22, 2015. @article{Strait2015,The ventral striatum (VS), like its cortical afferents, is closely associated with processing of rewards, but the relative contributions of striatal and cortical reward systems remains unclear. Most theories posit distinct roles for these structures, despite their similarities. We compared responses of VS neurons to those of ventromedial prefrontal cortex (vmPFC) Area 14 neurons, recorded in a risky choice task. Five major response patterns observed in vmPFC were also observed in VS: (1) offer value encoding, (2) value difference encoding, (3) preferential encoding of chosen relative to unchosen value, (4) a correlation between residual variance in responses and choices, and (5) prominent encoding of outcomes. We did observe some differences as well; in particular, preferential encoding of the chosen option was stronger and started earlier in VS than in vmPFC. Nonetheless, the close match between vmPFC and VS suggests that cortex and its striatal targets make overlapping contributions to economic choice. |
Jessica Taubert; Goedele Van Belle; Wim Vanduffel; Bruno Rossion; Rufin Vogels The effect of face inversion for neurons inside and outside fMRI-defined face-selective cortical regions Journal Article In: Journal of Neurophysiology, vol. 113, no. 5, pp. 1644–1655, 2015. @article{Taubert2015,It is widely believed that face processing in the primate brain occurs in a network of category-selective cortical regions. Combined functional MRI (fMRI)-single-cell recording studies in macaques have identified high concentrations of neurons that respond more to faces than objects within face-selective patches. However, cells with a preference for faces over objects are also found scattered throughout inferior temporal (IT) cortex, raising the question whether face-selective cells inside and outside of the face patches differ functionally. Here, we compare the properties of face-selective cells inside and outside of face-selective patches in the IT cortex by means of an image manipulation that reliably disrupts behavior toward face processing: inversion. We recorded IT neurons from two fMRI-defined face-patches (ML and AL) and a region outside of the face patches (herein labeled OUT) during upright and inverted face stimulation. Overall, turning faces upside down reduced the firing rate of face-selective cells. However, there were differences among the recording regions. First, the reduced neuronal response for inverted faces was independent of stimulus position, relative to fixation, in the face-selective patches (ML and AL) only. Additionally, the effect of inversion for face-selective cells in ML, but not those in AL or OUT, was impervious to whether the neurons were initially searched for using upright or inverted stimuli. Collectively, these results show that face-selective cells differ in their functional characteristics depending on their anatomicofunctional location, suggesting that upright faces are preferably coded by face-selective cells inside but not outside of the fMRI-defined face-selective regions of the posterior IT cortex. |
Jessica Taubert; Goedele Van Belle; Wim Vanduffel; Bruno Rossion; Rufin Vogels Neural correlate of the Thatcher face illusion in a monkey face-selective patch Journal Article In: Journal of Neuroscience, vol. 35, no. 27, pp. 9872–9878, 2015. @article{Taubert2015a,Compelling evidence that our sensitivity to facial structure is conserved across the primate order comes from studies of the “Thatcher face illusion”: humans and monkeys notice changes in the orientation of facial features (e.g., the eyes) only when faces are upright, not when faces are upside down. Although it is presumed that face perception in primates depends on face-selective neurons in the inferior temporal (IT) cortex, it is not known whether these neurons respond differentially to upright faces with inverted features. Using microelectrodes guided by functional MRI mapping, we recorded cell responses in three regions of monkey IT cortex.Wereport an interaction in the middle lateral face patch (ML) between the global orientation of a face and the local orientation of its eyes, a response profile consistent with the perception of the Thatcher illusion. This increased sensitivity to eye orientation in upright faces resisted changes in screen location and was not found among face-selective neurons in other areas of IT cortex, including neurons in another face-selective region, the anterior lateral face patch. We conclude that the Thatcher face illusion is correlated with a pattern of activity in the ML that encodes faces according to a flexible holistic template. |
Jon Touryan; James A. Mazer Linear and non-linear properties of feature selectivity in V4 neurons Journal Article In: Frontiers in Systems Neuroscience, vol. 9, pp. 82, 2015. @article{Touryan2015,Extrastriate area V4 is a critical component of visual form processing in both humans and non-human primates. Previous studies have shown that the tuning properties of V4 neurons demonstrate an intermediate level of complexity that lies between the narrow band orientation and spatial frequency tuning of neurons in primary visual cortex and the highly complex object selectivity seen in inferotemporal neurons. However, the nature of feature selectivity within this cortical area is not well understood, especially in the context of natural stimuli. Specifically, little is known about how the tuning properties of V4 neurons, measured in isolation, translate to feature selectivity within natural scenes. In this study, we assessed the degree to which preferences for natural image components can readily be inferred from classical orientation and spatial frequency tuning functions. Using a psychophysically-inspired method we isolated and identified the specific visual "driving features" occurring in natural scene photographs that reliably elicited spiking activity from single V4 neurons. We then compared the measured driving features to those predicted based on the spectral receptive field (SRF), estimated from responses to narrowband sinusoidal grating stimuli. This approach provided a quantitative framework for assessing the degree to which linear feature selectivity was preserved during natural vision. First, we found evidence of both spectrally and spatially tuned suppression within the receptive field, neither of which were present in the linear SRF. Second, we found driving features that were stable during translation of the image across the receptive field (due to small fixational eye movements). The degree of translation invariance fell along a continuum, with some cells showing nearly complete invariance across the receptive field and others exhibiting little to no position invariance. This form of limited translation invariance could indicate that a subset of V4 neurons are insensitive to small fixational eye movements, supporting perceptual stability during natural vision. |
Ilse C. Van Dromme; Wim Vanduffel; Peter Janssen The relation between functional magnetic resonance imaging activations and single-cell selectivity in the macaque intraparietal sulcus Journal Article In: NeuroImage, vol. 113, pp. 86–100, 2015. @article{VanDromme2015,Previous functional magnetic resonance (fMRI) studies in humans and monkeys have demonstrated that the anterior intraparietal sulcus (IPS) is sensitive to the depth structure defined by binocular disparity. However, in the macaque monkey, a single large activation was measured in the anterior lateral bank of the IPS, whereas in human subjects two separate regions were sensitive to depth structure from disparity. We performed fMRI and single-cell experiments in the same animals, in a large number of recording sites in the lateral bank of the IPS. The fMRI interaction effect between the factors curvature (curved or flat) and disparity (stereo or control) correctly predicted the location of higher-order disparity selective neurons that encoded the depth structure of objects. However the large region in the IPS activated by depth structure consisted of two patches of higher-order disparity-selective neurons, one in the anterior IPS and one located more posteriorly, surrounded by regions lacking such selectivity. Thus the IPS region activated by curved surfaces consists of at least two patches of higher-order disparity selective neurons, which may reconcile previous fMRI studies in monkeys and humans. |
Taihei Ninomiya; Kacie Dougherty; David C. Godlove; Jeffrey D. Schall; Alexander Maier Microcircuitry of agranular frontal cortex: Contrasting laminar connectivity between occipital and frontal areas Journal Article In: Journal of Neurophysiology, vol. 113, no. 9, pp. 3242–3255, 2015. @article{Ninomiya2015,Neocortex is striking in its laminar architecture. Tracer studies have uncovered anatomical connectivity among laminae, but the functional connectivity between laminar compartments is still largely unknown. Such functional connectivity can be discerned through spontaneous neural correlations during rest. Previous work demonstrated a robust pattern of mesoscopic resting-state connectivity in macaque primary visual cortex (V1) through interlaminar cross-frequency coupling. Here we investigated whether this pattern generalizes to other cortical areas by comparing resting-state laminar connectivity between V1 and the supplementary eye field (SEF), a frontal area lacking a granular layer 4 (L4). Local field potentials (LFPs) were recorded with linear microelectrode arrays from all laminae of granular V1 and agranular SEF while monkeys rested in darkness. We found substantial differences in the relationship between the amplitude of gamma-band (>30 Hz) LFP and the phase of alpha-band (7-14 Hz) LFP between these areas. In V1, gamma amplitudes in L2/3 and L5 were coupled with alpha-band LFP phase in L5, as previously described. In contrast, in SEF phase-amplitude coupling was prominent within L3 and much weaker across layers. These results suggest that laminar interactions in agranular SEF are unlike those in granular V1. Thus the intrinsic functional connectivity of the cortical microcircuit does not seem to generalize across cortical areas. |
Shogo Ohmae; Toshimitsu Takahashi; Xiaofeng Lu; Yasunori Nishimori; Yasushi Kodaka; Ichiro Takashima; Shigeru Kitazawa Decoding the timing and target locations of saccadic eye movements from neuronal activity in macaque oculomotor areas Journal Article In: Journal of Neural Engineering, vol. 12, no. 3, pp. 1–21, 2015. @article{Ohmae2015,OBJECTIVE: The control of movement timing has been a significant challenge for brain-machine interfaces (BMIs). As a first step toward developing a timing-based BMI, we aimed to decode movement timing and target locations in a visually guided saccadic eye movement task using the activity of neurons in the primate frontal eye field (FEF) and supplementary eye field (SEF). APPROACH: For this purpose, we developed a template-matching method that could recruit a variety of neurons in these areas. MAIN RESULTS: As a result, we were able to achieve a favorable estimation of saccade onset: for example, data from 20 randomly sampled FEF neurons or 40 SEF neurons achieved a median estimation error of ∼10 ms with an interquartile range less than 50 ms (± ∼25 ms). In the best case, seven simultaneously recorded SEF neurons using a multi-electrode array achieved a comparable accuracy (10 ± 30 ms). The method was significantly better than a heuristic method that used only a group of movement cells with sharp discharges at the onset of saccades. The estimation of target location was less accurate but still favorable, especially when we estimated target location at a timing of 200 ms after the onset of saccade: the method was able to discriminate 16 targets with an accuracy of 90%, which differed not only in their directions (eight directions) but also in amplitude (10/20°) when we used data from 61 randomly sampled FEF neurons. SIGNIFICANCE: The results show that the timing, amplitude and direction of saccades can be decoded from neuronal activity in the FEF and SEF and further suggest that timing-based BMIs can be developed by decoding timing information using the template-matching method. |
Ivo D. Popivanov; Jan Jastorff; Wim Vanduffel; Rufin Vogels Tolerance of macaque middle STS body patch neurons to shape-preserving stimulus transformations Journal Article In: Journal of Cognitive Neuroscience, vol. 27, no. 5, pp. 1001–1016, 2015. @article{Popivanov2015,Functional imaging studies in human and nonhuman primates have demonstrated regions in the brain that show category selectivity for faces or (headless) bodies. Recent fMRI-guided single unit studies of the macaque face category-selective regions have increased our understanding of the response properties of single neurons in these face patches. However, much less is known about the response properties of neurons in the fMRI- defined body category-selective regions (“body patches”). Recently, we reported that the majority of single neurons in one fMRI-defined body patch, the mid-STS body patch, responded more strongly to bodies compared with other objects. Here we assessed the tolerance of these neurons' responses and stimulus preference for shape-preserving image transformations. After mapping the receptive field of the single neurons, we found that their stimulus preference showed a high degree of tolerance for changes in the position and size of the stimulus. However, their response strongly depended on the in-plane orientation of a body. The selectivity ofmost neurons was, to a large degree, preserved when silhouettes were presented instead of the original textured and shaded images, suggesting that mainly shape-based features are driving these neurons. In a human psychophysical study, we showed that the information present in silhouettes is largely sufficient for body versus nonbody categorization. These data suggest that mid-STS body patch neurons respond predominantly to oriented shape features that are prevalent in images of bodies. Their responses can inform position- and retinal size-invariant body categorization and discrimination based on shape. |
M. Victoria Puig; Earl K. Miller Neural substrates of dopamine D2 receptor modulated executive functions in the monkey prefrontal cortex Journal Article In: Cerebral Cortex, vol. 25, no. 9, pp. 2980–2987, 2015. @article{Puig2015,Dopamine D2 receptors (D2R) play a major role in cognition, mood and motor movements. Their blockade by antipsychotic drugs reduces hallucinatory and delusional behaviors in schizophrenia, but often fails to alleviate affective and cognitive dysfunctions. The prefrontal cortex (PFC) expresses D2R and is altered in schizophrenia. We investigated how D2R modulate behavior and PFC function in monkeys. Two monkeys learned new and performed highly familiar visuomotor associations, where each cue was associated with a saccade to a right or left target. We recorded neural spikes and local field potentials from multiple electrodes while injecting the D2R antagonist eticlopride in the lateral PFC. Blocking prefrontal D2R impaired associative learning and cognitive flexibility, reduced motivation, but left the performance of familiar associations intact. Eticlopride reduced saccade-direction selectivity of prefrontal neurons, leading to a decrease in neural information about the associations, and an increase in alpha oscillations. These results, together with our recent study using a D1R antagonist, suggest that D1R and D2R in the primate lateral PFC cooperate to modulate several executive functions. Our findings help to gain insight into why antipsychotic drugs, with strong antagonistic actions on D2R, fail to ameliorate cognitive and emotional deficits in schizophrenia. |
Rishi Rajalingham; Kailyn Schmidt; James J. DiCarlo Comparison of object recognition behavior in human and monkey Journal Article In: Journal of Neuroscience, vol. 35, no. 35, pp. 12127–12136, 2015. @article{Rajalingham2015,Although the rhesus monkey is used widely as an animal model of human visual processing, it is not known whether invariant visual object recognition behavior is quantitatively comparable across monkeys and humans. To address this question, we systematically compared the core object recognition behavior of two monkeys with that of human subjects. To test true object recognition behavior (rather than image matching), we generated several thousand naturalistic synthetic images of 24 basic-level objects with high variation in viewing parameters and image background. Monkeys were trained to perform binary object recognition tasks on a match-to-sample paradigm. Data from 605 human subjects performing the same tasks on Mechanical Turk were aggregated to characterize "pooled human" object recognition behavior, as well as 33 separate Mechanical Turk subjects to characterize individual human subject behavior. Our results show that monkeys learn each new object in a few days, after which they not only match mean human performance but show a pattern of object confusion that is highly correlated with pooled human confusion patterns and is statistically indistinguishable from individual human subjects. Importantly, this shared human and monkey pattern of 3D object confusion is not shared with low-level visual representations (pixels, V1+; models of the retina and primary visual cortex) but is shared with a state-of-the-art computer vision feature representation. Together, these results are consistent with the hypothesis that rhesus monkeys and humans share a common neural shape representation that directly supports object perception. |
Supriya Ray; Stephen J. Heinen A mechanism for decision rule discrimination by supplementary eye field neurons Journal Article In: Experimental Brain Research, vol. 233, no. 2, pp. 459–476, 2015. @article{Ray2015,A decision to select an action from alternatives is often guided by rules that flexibly map sensory inputs to motor outputs when certain conditions are satisfied. However, the neural mechanisms underlying rule-based decision making remain poorly understood. Two complementary types of neurons in the supplementary eye field (SEF) of macaques have been identified that modulate activity differentially to interpret rules in an ocular go–nogo task, which stipulates that the animal either visually pursue a moving object if it intersects a visible zone (‘go'), or maintain fixation if it does not (‘nogo'). These neurons discriminate between go and nogo rule-states by increasing activity to signal their preferred (agonist) rule-state and decreasing activity to signal their non-preferred (antagonist) rule-state. In the current study, we found that SEF neurons decrease activity in anticipation of the antagonist rule-state, and do so more rapidly when the rule-state is easier to predict. This rapid decrease in activity could underlie a process of elimination in which trajectories that do not invoke the preferred rule-state receive no further computational resources. Furthermore, discrimination between difficult and easy trials in the antagonist rule-state occurs prior to when discrimination within the agonist rule-state occurs. A winner-take-all like model that incorporates a pair of mutually inhibited integrators to accumulate evidence in favor of either the decision to pursue or the decision to continue fixation accounts for the observed neural phenomena. |
Bram-Ernst Verhoef; Pascal Michelet; Rufin Vogels; Peter Janssen Choice-related activity in the anterior intraparietal area during 3-D structure categorization Journal Article In: Journal of Cognitive Neuroscience, vol. 27, pp. 1104–1115, 2015. @article{Verhoef2015a,The anterior intraparietal area (AIP) of macaques contains neurons that signal the depth structure of disparity-defined 3-D shapes. Previous studies have suggested that AIP's depth information is used for sensorimotor transformations related to the efficient grasping of 3-D objects. We trained monkeys to categorize disparity-defined 3-D shapes and examined whether neuronal activity in AIP may also underlie pure per- ceptual categorization behavior. We first show that neurons with a similar 3-D shape preference cluster in AIP. We then demonstrate that the monkeys' 3-D shape discrimination perfor- mance depends on the position in depth of the stimulus and that this performance difference is reflected in the activity of AIP neurons. We further reveal correlations between the neuronal activity in AIP and the subject's subsequent choices and RTs during 3-D shape categorization. Our findings propose AIP as an important processing stage for 3-D shape perception. |
Mark M. G. Walton; Michael J. Mustari Abnormal tuning of saccade-related cells in pontine reticular formation of strabismic monkeys Journal Article In: Journal of Neurophysiology, vol. 114, no. 2, pp. 857–868, 2015. @article{Walton2015,Strabismus is a common disorder, char- acterized by a chronic misalignment of the eyes and numerous visual and oculomotor abnormalities. For example, saccades are often highly disconjugate. For humans with pattern strabismus, the horizontal and vertical disconjugacies vary with eye position. In monkeys, manipula- tions that disturb binocular vision during the first several weeks of life result in a chronic strabismus with characteristics that closely match those in human patients. Early onset strabismus is associated with altered binocular sensitivity of neurons in visual cortex. Here we test the hypothesis that brain stem circuits specific to saccadic eye movements are abnormal. We targeted the pontine paramedian reticular formation, a structure that directly projects to the ipsilateral abducens nucleus. In normal animals, neurons in this structure are characterized by a high- frequency burst of spikes associated with ipsiversive saccades. We recorded single-unit activity from 84 neurons from four monkeys (two normal, one exotrope, and one esotrope), while they made saccades to a visual target on a tangent screen. All 24 neurons recorded from the normal animals had preferred directions within 30° of pure horizontal. For the strabismic animals, the distribution of preferred directions was normal on one side of the brain, but highly variable on the other. In fact, 12/60 neurons recorded from the strabismic animals preferred vertical saccades. Many also had unusually weak or strong bursts. These data suggest that the loss of corresponding binocular vision during infancy impairs the development of normal tuning characteristics for saccade- related neurons in brain stem. |
Mark M. G. Walton; Michael J. Mustari; Christy L. Willoughby; Linda K. McLoon Abnormal activity of neurons in abducens nucleus of strabismic monkeys Journal Article In: Investigative Ophthalmology & Visual Science, vol. 56, no. 1, pp. 10–19, 2015. @article{Walton2015a,PURPOSE: Infantile strabismus is characterized by persistent misalignment of the eyes. Mounting evidence suggests that the disorder is associated with abnormalities at the neural level, but few details are known. This study investigated the signals carried by abducens neurons in monkeys with experimentally induced strabismus. We wanted to know whether the firing rates of individual neurons are exclusively related to the position and velocity of one eye and whether the overall level of activity of the abducens nucleus was in the normal range. METHODS: We recorded 58 neurons in right and left abducens nuclei while strabismic monkeys (one esotrope and one exotrope) performed a saccade task. We analyzed the firing rates associated with static horizontal eye position and saccades by fitting the data with a dynamic equation that included position and velocity terms for each eye. Results were compared to previously published data in normal monkeys. RESULTS: For both strabismic monkeys the overall tonic activity was 50 to 100 spikes/s lower, for every suprathreshold eye position, than what has previously been reported for normal monkeys. This was mostly the result of lower baseline activity; the slopes of rate-position curves were similar to those in previous reports in normal monkeys. The saccade velocity sensitivities were similar to those of normal monkeys, 0.35 for the esotrope and 0.40 for the exotrope. For most neurons the firing rate was more closely related to the position and velocity of the ipsilateral eye. CONCLUSIONS: These data suggest that strabismus can be associated with reduced neural activity in the abducens nucleus. |
Ye Wang; Valentin Dragoi Rapid learning in visual cortical networks Journal Article In: eLife, vol. 4, no. AUGUST2015, pp. 1–16, 2015. @article{Wang2015b,Although changes in brain activity during learning have been extensively examined at the single neuron level, the coding strategies employed by cell populations remain mysterious. We examined cell populations in macaque area V4 during a rapid form of perceptual learning that emerges within tens of minutes. Multiple single units and LFP responses were recorded as monkeys improved their performance in an image discrimination task. We show that the increase in behavioral performance during learning is predicted by a tight coordination of spike timing with local population activity. More spike-LFP theta synchronization is correlated with higher learning performance, while high-frequency synchronization is unrelated with changes in performance, but these changes were absent once learning had stabilized and stimuli became familiar, or in the absence of learning. These findings reveal a novel mechanism of plasticity in visual cortex by which elevated low-frequency synchronization between individual neurons and local population activity accompanies the improvement in performance during learning. |
Jianbo Xiao; Xin Huang Distributed and dynamic neural encoding of multiple motion directions of transparently moving stimuli in cortical area MT Journal Article In: Journal of Neuroscience, vol. 35, no. 49, pp. 16180–16198, 2015. @article{Xiao2015,Segmenting visual scenes into distinct objects and surfaces is a fundamental visual function. To better understand the underlying neural mechanism, we investigated how neurons in the middle temporal cortex (MT) of macaque monkeys represent overlapping random-dot stimuli moving transparently in slightly different directions. It has been shown that the neuronal response elicited by two stimuli approximately follows the average of the responses elicited by the constituent stimulus components presented alone. In this scheme of response pooling, the ability to segment two simultaneously presented motion directions is limited by the width of the tuning curve to motion in a single direction. We found that, although the population-averaged neuronal tuning showed response averaging, subgroups of neurons showed distinct patterns of response tuning and were capable of representing component directions that were separated by a small angle—less than the tuning width to unidirectional stimuli. One group of neurons preferentially represented the component direction at a specific side of the bidirectional stimuli, weighting one stimulus component more strongly than the other. Another group of neurons pooled the component responses nonlinearly and showed two separate peaks in their tuning curves even when the average of the component responses was unimodal. We also show for the first time that the direction tuning of MT neurons evolved from initially representing the vector-averaged direction of slightly different stimuli to gradually representing the component directions. Our results reveal important neural processes underlying image segmentation and suggest that information about slightly different stimulus com- ponents is computed dynamically and distributed across neurons. |
Theodoros P. Zanos; Patrick J. Mineault; Konstantinos T. Nasiotis; Daniel Guitton; Christopher C. Pack A sensorimotor role for traveling waves in primate visual cortex Journal Article In: Neuron, vol. 85, no. 3, pp. 615–627, 2015. @article{Zanos2015,Traveling waves of neural activity are frequently observed to occur in concert with the presentation of a sensory stimulus or the execution of a movement. Although such waves have been studied for decades, little is known about their function. Here we show that traveling waves in the primate extrastriate visual cortex provide a means of integrating sensory and motor signals. Specifically, we describe a traveling wave of local field potential (LFP) activity in cortical area V4 of macaque monkeys that is triggered by the execution of saccadic eye movements. These waves sweep across the V4 retinotopic map, following a consistent path from the foveal to the peripheral representations of space; their amplitudes correlate with the direction and size of each saccade. Moreover, these waves are associated with a reorganization of the postsaccadic neuronal firing patterns, which follow a similar retinotopic progression, potentially prioritizing the processing of behaviorally relevant stimuli. |
Victor Lafuente; Mehrdad Jazayeri; Michael N. Shadlen Representation of accumulating evidence for a decision in two parietal areas Journal Article In: Journal of Neuroscience, vol. 35, no. 10, pp. 4306–4318, 2015. @article{Lafuente2015,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. |
Caroline B. Drucker; Monica L. Carlson; Koji Toda; Nicholas K. DeWind; Michael L. Platt Non-invasive primate head restraint using thermoplastic masks. Journal Article In: Journal of Neuroscience Methods, vol. 253, pp. 90–100, 2015. @article{Drucker2015,Background: The success of many neuroscientific studies depends upon adequate head fixation of awake, behaving animals. Typically, this is achieved by surgically affixing a head-restraint prosthesis to the skull. New Method: Here we report the use of thermoplastic masks to non-invasively restrain monkeys' heads. Mesh thermoplastic sheets become pliable when heated and can then be molded to an individual monkey's head. After cooling, the custom mask retains this shape indefinitely for day-to-day use. Results: We successfully trained rhesus macaques (Macaca mulatta) to perform cognitive tasks while wearing thermoplastic masks. Using these masks, we achieved a level of head stability sufficient for high-resolution eye-tracking and intracranial electrophysiology. Comparison with Existing Method: Compared with traditional head-posts, we find that thermoplastic masks perform at least as well during infrared eye-tracking and single-neuron recordings, allow for clearer magnetic resonance image acquisition, enable freer placement of a transcranial magnetic stimulation coil, and impose lower financial and time costs on the lab.Conclusions: We conclude that thermoplastic masks are a viable non-invasive form of primate head restraint that enable a wide range of neuroscientific experiments. |
R. Becket Ebitz; Michael L. Platt Neuronal activity in primate dorsal anterior cingulate cortex signals Task conflict and predicts adjustments in pupil-linked arousal Journal Article In: Neuron, vol. 85, no. 3, pp. 628–640, 2015. @article{Ebitz2015,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. |
Samanthi C. Goonetilleke; Leor N. Katz; Daniel K. Wood; Chao Gu; Alexander C. Huk; Brian D. Corneil In: Journal of Neurophysiology, vol. 114, no. 2, pp. 902–913, 2015. @article{Goonetilleke2015,Recent studies have described a phenomenon wherein the onset of a peripheral visual stimulus elicits short-latency (<100 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. |
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 In: NeuroImage, vol. 15, no. 120, pp. 1–11, 2015. @article{Hung2015,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 500μm 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 In: Journal of Neuroscience, vol. 35, no. 3, pp. 1160–1172, 2015. @article{Hung2015a,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. |
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 In: Psychopharmacology, vol. 232, no. 19, pp. 3563–3572, 2015. @article{Ilhame2015,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. |
2014 |
Douglas A. Ruff; Marlene R. Cohen Attention can either increase or decrease spike count correlations in visual cortex Journal Article In: Nature Neuroscience, vol. 17, no. 11, pp. 1591–1597, 2014. @article{Ruff2014,Visual attention enhances the responses of visual neurons that encode the attended location. Several recent studies have shown that attention also decreases correlations between fluctuations in the responses of pairs of neurons (termed spike count correlation or r(SC)). These results are consistent with two hypotheses. First, attention-related changes in rate and r(SC) might be linked (perhaps through a common mechanism), with attention always decreasing r(SC). Second, attention might either increase or decrease r(SC), possibly depending on the role of the neurons in the behavioral task. We recorded simultaneously from dozens of neurons in area V4 while monkeys performed a discrimination task. We found strong evidence in favor of the second hypothesis, showing that attention can flexibly increase or decrease correlations depending on whether the neurons provide evidence for the same or opposite choices. These results place important constraints on models of the neuronal mechanisms underlying cognitive factors. |
Maria C. Romero; Pierpaolo Pani; Peter Janssen Coding of shape features in the macaque anterior intraparietal area Journal Article In: Journal of Neuroscience, vol. 34, no. 11, pp. 4006–4021, 2014. @article{Romero2014,The exquisite ability of primates to grasp and manipulate objects relies on the transformation of visual information into motor com- mands. To this end, the visual system extracts object affordances that can be used to program and execute the appropriate grip. The macaque anterior intraparietal (AIP) area hasbeen implicated in the extraction ofaffordances for the purpose ofgrasping. Neurons in the AIP area respond during visually guided grasping and to the visual presentation ofobjects. A subset ofAIP neurons is also activated by two-dimensional images ofobjects and even by outline contours defining the object shape, but it is unknown how AIP neurons actually represent object shape. In this study, we used a stimulus reduction approach to determine the minimum effective shape feature evoking AIP responses. AIP neurons responding to outline shapes also responded selectively to very small fragment stimuli measuring only 1–2°. This fragment selectivity could not be explained bydifferences in eyemovementsor simple orientation selectivity, but proved to be highly dependent on the relative position ofthe stimulus in the receptive field. Our findings challenge the current understanding ofthe AIP area as a critical stage in the dorsal stream for the extraction ofobject affordances. |
Arani Roy; Stephen V. Shepherd; Michael L. Platt Reversible inactivation of pSTS suppresses social gaze following in the macaque (Macaca mulatta) Journal Article In: Social Cognitive and Affective Neuroscience, vol. 9, no. 2, pp. 209–217, 2014. @article{Roy2014,Humans and other primates shift their attention to follow the gaze of others [gaze following (GF)]. This behavior is a foundational component of joint attention, which is severely disrupted in neurodevelopmental disorders such as autism and schizophrenia. Both cortical and subcortical pathways have been implicated in GF, but their contributions remain largely untested. While the proposed subcortical pathway hinges crucially on the amygdala, the cortical pathway is thought to require perceptual processing by a region in the posterior superior temporal sulcus (pSTS). To determine whether pSTS is necessary for typical GF behavior, we engaged rhesus macaques in a reward discrimination task confounded by leftward- and rightward-facing social distractors following saline or muscimol injections into left pSTS. We found that reversible inactivation of left pSTS with muscimol strongly suppressed GF, as assessed by reduced influence of observed gaze on target choices and saccadic reaction times. These findings demonstrate that activity in pSTS is required for normal GF by primates. |
Douglas A. Ruff; Marlene R. Cohen Attention can increase or decrease spike count correlations between pairs of neurons depending on their role in a task Journal Article In: Nature Neuroscience, vol. 17, no. 11, pp. 1591–1597, 2014. @article{Ruff2014a,Visual attention enhances the responses of visual neurons that encode the attended location. Several recent studies showed that attention also decreases correlations between fluctuations in the responses of pairs of neurons (termed spike count correlation or rSC). The previous results are consistent with two hypotheses. Attention–related changes in rate and rSC might be linked (perhaps through a common mechanism), so that attention always decreases rSC. Alternately, attention might either increase or decrease rSC, possibly depending on the role the neurons play in the behavioral task. We recorded simultaneously from dozens of neurons in area V4 while monkeys performed a discrimination task. We found strong evidence in favor of the second hypothesis, showing that attention can flexibly increase or decrease correlations, depending on whether the neurons provide evidence for the same or opposite perceptual decisions. These results place important constraints on models of the neuronal mechanisms underlying cognitive factors. |
Patrick T. Sadtler; Kristin M. Quick; Matthew D. Golub; Steven M. Chase; Stephen I. Ryu; Elizabeth C. Tyler-Kabara; Byron M. Yu; Aaron P. Batista Neural constraints on learning Journal Article In: Nature, vol. 512, pp. 423–426, 2014. @article{Sadtler2014,Learning, whether motor, sensory or cognitive, requires networks of neurons to generate new activity patterns. As some behaviours are easier to learn than others, we asked if some neural activity patterns are easier to generate than others. Here we investigate whether an existing network constrains the patterns that a subset of its neurons is capable of exhibiting, and if so, what principles define this constraint. We employed a closed-loop intracortical brain-computer interface learning paradigm in which Rhesus macaques (Macaca mulatta) controlled a computer cursor by modulating neural activity patterns in the primary motor cortex. Using the brain-computer interface paradigm, we could specify and alter how neural activity mapped to cursor velocity. At the start of each session, we observed the characteristic activity patterns of the recorded neural population. The activity of a neural population can be represented in a high-dimensional space (termed the neural space), wherein each dimension corresponds to the activity of one neuron. These characteristic activity patterns comprise a low-dimensional subspace (termed the intrinsic manifold) within the neural space. The intrinsic manifold presumably reflects constraints imposed by the underlying neural circuitry. Here we show that the animals could readily learn to proficiently control the cursor using neural activity patterns that were within the intrinsic manifold. However, animals were less able to learn to proficiently control the cursor using activity patterns that were outside of the intrinsic manifold. These results suggest that the existing structure of a network can shape learning. On a timescale of hours, it seems to be difficult to learn to generate neural activity patterns that are not consistent with the existing network structure. These findings offer a network-level explanation for the observation that we are more readily able to learn new skills when they are related to the skills that we already possess. |
Nicholas A. Steinmetz; Tirin Moore Eye movement preparation modulates neuronal responses in area V4 when dissociated from attentional demands Journal Article In: Neuron, vol. 83, no. 2, pp. 496–506, 2014. @article{Steinmetz2014,We examined whether the preparation of saccadic eye movements, when behaviorally dissociated from covert attention, modulates activity within visual cortex. We measured single-neuron and local field potential (LFP) responses to visual stimuli in area V4 while monkeys covertly attended a stimulus at one location and prepared saccades to a potential target at another. In spite of the irrelevance of visual information at the saccade target, visual activity at that location was modulated at least as much as, and often more than, activity at the covertly attended location. Modulations of activity at the attended and saccade target locations were qualitatively similar and included increased response magnitude, stimulus selectivity, and spiking reliability, as well as increased gamma and decreased low-frequency power of LFPs. These results demonstrate that saccade preparation is sufficient to modulate visual cortical representations and suggest that the interrelationship of oculomotor and attention-related mechanisms extends to posterior visual cortex. |
Chess Stetson; Richard A. Andersen The parietal reach region selectively anti-synchronizes with dorsal premotor cortex during planning Journal Article In: Journal of Neuroscience, vol. 34, no. 36, pp. 11948–11958, 2014. @article{Stetson2014,Recent reports have indicated that oscillations shared across distant cortical regions can enhance their connectivity, but do coherent oscillations ever diminish connectivity? We investigated oscillatory activity in two distinct reach-related regions in the awake behaving monkey (Macaca mulatta): the parietal reach region (PRR) and the dorsal premotor cortex (PMd). PRR and PMd were found to oscillate at similar frequencies (beta, 15–30 Hz) during periods of fixation and movement planning. At first glance, the stronger oscillator of the two, PRR, would seem to drive the weaker, PMd. However, a more fine-grained measure, the partial spike-field coherence, revealed a different relationship. Relative to global beta-band activity in the brain, action potentials in PRR anti-synchronize with PMd oscillations. These data suggest that, rather than driving PMd during planning, PRR neurons fire in such a way that they are less likely to communicate information to PMd. |
Caleb E. Strait; Tommy C. Blanchard; Benjamin Y. Hayden Reward value comparison via mutual inhibition in ventromedial prefrontal cortex Journal Article In: Neuron, vol. 82, no. 6, pp. 1357–1366, 2014. @article{Strait2014,Recent theories suggest that reward-based choice reflects competition between value signals in the ventromedial prefrontal cortex (vmPFC). We tested this idea by recording vmPFC neurons while macaques performed a gambling task with asynchronous offer presentation. We found that neuronal activity shows four patterns consistent with selection via mutual inhibition: (1) correlated tuning for probability and reward size, suggesting that vmPFC carries an integrated value signal; (2) anti-correlated tuning curves for the two options, suggesting mutual inhibition; (3) neurons rapidly come to signal the value of the chosen offer, suggesting the circuit serves to produce a choice; and (4) after regressing out the effects of option values, firing rates still could predict choice-a choice probability signal. In addition, neurons signaled gamble outcomes, suggesting that vmPFC contributes to both monitoring and choice processes. These data suggest a possible mechanism for reward-based choice and endorse the centrality of vmPFC in that process. |
R. Becket Ebitz; John M. Pearson; Michael L. Platt Pupil size and social vigilance in rhesus macaques Journal Article In: Frontiers in Neuroscience, vol. 8, pp. 100, 2014. @article{Ebitz2014,Complex natural environments favor the dynamic alignment of neural processing between goal-relevant stimuli and conflicting but biologically salient stimuli like social competitors or predators. The biological mechanisms that regulate dynamic changes in vigilance have not been fully elucidated. Arousal systems that ready the body to respond adaptively to threat may contribute to dynamic regulation of vigilance. Under conditions of constant luminance, pupil diameter provides a peripheral index of arousal state. Although pupil size varies with the processing of goal-relevant stimuli, it remains unclear whether pupil size also predicts attention to biologically salient objects and events like social competitors, whose presence interferes with current goals. Here we show that pupil size in rhesus macaques both reflects the biological salience of task-irrelevant social distractors and predicts vigilance for these stimuli. We measured pupil size in monkeys performing a visual orienting task in which distractors-monkey faces and phase-scrambled versions of the same images-could appear in a congruent, incongruent, or neutral position relative to a rewarded target. Baseline pupil size under constant illumination predicted distractor interference, consistent with the hypothesis that pupil-linked arousal mechanisms regulate task engagement and distractibility. Notably, pupil size also predicted enhanced vigilance for social distractors, suggesting that pupil-linked arousal may adjust the balance of processing resources between goal-relevant and biologically important stimuli. The magnitude of pupil constriction in response to distractors closely tracked distractor interference, saccade planning and the social relevance of distractors, endorsing the idea that the pupillary light response is modulated by attention. These findings indicate that pupil size indexes dynamic changes in attention evoked by both the social environment and arousal. |
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 In: Journal of Neuroscience, vol. 34, no. 15, pp. 5355–5369, 2014. @article{Godlove2014,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. |
Alina Graf; Richard A. Andersen Inferring eye position from populations of lateral intraparietal neurons Journal Article In: eLife, vol. 2014, no. 3, pp. 1–13, 2014. @article{Graf2014,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. |
Guilhem Ibos; David J. Freedman Dynamic integration of task-relevant visual features in posterior parietal cortex Journal Article In: Neuron, vol. 83, no. 6, pp. 1468–1480, 2014. @article{Ibos2014,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. |
Kevin D. 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 In: Cerebral Cortex, vol. 24, no. 5, pp. 1373–1388, 2014. @article{Johnston2014,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. |
R. M. Kalwani; Siddhartha Joshi; Joshua 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 In: Journal of Neuroscience, vol. 34, no. 41, pp. 13656–13669, 2014. @article{Kalwani2014,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. |
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 In: Journal of Neuroscience, vol. 34, no. 25, pp. 8570–8584, 2014. @article{Kosai2014,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; R. Matthew Hutchison; Stephen G. Lomber; Stefan Everling Effects of unilateral deactivations of dorsolateral prefrontal cortex and anterior cingulate cortex on saccadic eye movements Journal Article In: Journal of Neurophysiology, vol. 111, no. 4, pp. 787–803, 2014. @article{Koval2014,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. |
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 In: Proceedings of the National Academy of Sciences, vol. 111, no. 8, pp. 3170–3175, 2014. @article{Kremkow2014,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. |
Rogier Landman; Jitendra Sharma; Mriganka Sur; Robert Desimone Effect of distracting faces on visual selective attention in the monkey Journal Article In: Proceedings of the National Academy of Sciences, vol. 111, no. 50, pp. 18037–18042, 2014. @article{Landman2014,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. |
Hamed Zivari Adab; Ivo D. Popivanov; Wim Vanduffel; Rufin Vogels Perceptual learning of simple stimuli modifies stimulus representations in posterior inferior temporal cortex Journal Article In: Journal of Cognitive Neuroscience, vol. 26, no. 10, pp. 2187–2200, 2014. @article{Adab2014,Practicing simple visual detection and discrimination tasks improves performance, a signature of adult brain plasticity. The neural mechanisms that underlie these changes in performance are still unclear. Previously, we reported that practice in discriminating the orientation of noisy gratings (coarse orientation discrimination) increased the ability of single neurons in the early visual area V4 to discriminate the trained stimuli. Here, we ask whether practice in this task also changes the stimulus tuning properties of later visual cortical areas, despite the use of simple grating stimuli. To identify candidate areas, we used fMRI to map activations to noisy gratings in trained rhesus monkeys, revealing a region in the posterior inferior temporal (PIT) cortex. Subsequent single unit record- ings in PIT showed that the degree of orientation selectivity was similar to that of area V4 and that the PIT neurons discriminated the trained orientations better than the untrained orientations. Unlike in previous single unit studies of perceptual learning in early visual cortex, more PIT neurons preferred trained compared with untrained orientations. The effects of training on the responses to the grating stimuli were also present when the animals were performing a difficult orthogo- nal task in which the grating stimuli were task-irrelevant, suggesting that the training effect does not need attention to be expressed. The PIT neurons could support orientation discrimination at low signal-to-noise levels. These findings suggest that extensive practice in discriminating simple grating stimuli not only affects early visual cortex but also changes the stimulus tuning of a late visual cortical area. |
Mari Anzai; Soich Nagao Motor learning in common marmosets: Vestibulo-ocular reflex adaptation and its sensitivity to inhibitors of Purkinje cell long-term depression Journal Article In: Neuroscience Research, vol. 83, pp. 33–42, 2014. @article{Anzai2014,Adaptation of the horizontal vestibulo-ocular reflex (HVOR) provides an experimental model for cerebellum-dependent motor learning. We developed an eye movement measuring system and a paradigm for induction of HVOR adaptation for the common marmoset. The HVOR gain in dark measured by 10° (peak-to-peak amplitude) and 0.11-0.5. Hz turntable oscillation was around unity. The gain-up and gain-down HVOR adaptation was induced by 1. h of sustained out-of-phase and in-phase 10°-0.33. Hz combined turntable-screen oscillation in the light, respectively. To examine the role of long-term depression (LTD) of parallel fiber-Purkinje cell synapses, we intraperitonially applied T-588 or nimesulide, which block the induction of LTD in vitro or in vivo preparations, 1. h before the test of HVOR adaptation. T-588 (3 and 5. mg/kg body weight) did not affect nonadapted HVOR gains, and impaired both gain-up and gain-down HVOR adaptation. Nimesulide (3 and 6. mg/kg) did not affect nonadapted HVOR gains, and impaired gain-up HVOR adaptation dose-dependently; however, it very little affected gain-down HVOR adaptation. These findings are consistent with the results of our study of nimesulide on the adaptation of horizontal optokinetic response in mice (. Le et al., 2010), and support the view that LTD underlies HVOR adaptation. |
Dong-Hyun Baek; Jeyeon Lee; Hang Byeon; Hoseok Choi; In Young Kim; Kyoung-Min Lee; James Jungho Pak; Dong Pyo Jang; Sang-Hoon Lee A thin film polyimide mesh microelectrode for chronic epidural electrocorticography recording with enhanced contactability Journal Article In: Journal of Neural Engineering, vol. 11, no. 4, pp. 1–10, 2014. @article{Baek2014,Objective. Epidural electrocorticography (ECoG) activity may be more reliable and stable than single-unit-activity or local field potential. Invasive brain computer interface (BCI) devices are limited by mechanical mismatching and cellular reactive responses due to differences in the elastic modulus and the motion of stiff electrodes. We propose a mesh-shaped electrode to enhance the contactability between surface of dura and electrode. Approach. We designed a polyimide (PI) electrode with a mesh pattern for more conformal contact with a curved surface. We compared the contact capability of mesh PI electrodes with conventionally used sheet PI electrode. The electrical properties of the mesh PI electrode were evaluated for four weeks. We recorded the epidural ECoG (eECoG) activity on the surface of rhesus monkey brains while they performed a saccadic task for four months. Main results. The mesh PI electrode showed good contact with the agarose brain surface, as evaluated by visual inspection and signal measurement. It was about 87% accurate in predicting the direction of saccade eye movement. Significance. Our results indicate that the mesh PI electrode was flexible and good contact on the curved surface and can record eECoG activity maintaining close contact to dura, which was proved by in vivo and in vitro test. |
T. C. Blanchard; Benjamin Y. Hayden Neurons in dorsal anterior cingulate cortex signal postdecisional variables in a foraging task Journal Article In: Journal of Neuroscience, vol. 34, no. 2, pp. 646–655, 2014. @article{Blanchard2014,The dorsal anterior cingulate cortex (dACC) is a key hub of the brain's executive control system. Although a great deal is known about its role in outcome monitoring and behavioral adjustment, whether and how it contributes to the decision process remain unclear. Some theories suggest that dACC neurons track decision variables (e.g., option values) that feed into choice processes and is thus "predecisional." Other theories suggest that dACC activity patterns differ qualitatively depending on the choice that is made and is thus "postdecisional." To compare these hypotheses, we examined responses of 124 dACC neurons in a simple foraging task in which monkeys accepted or rejected offers of delayed rewards. In this task, options that vary in benefit (reward size) and cost (delay) appear for 1 s; accepting the option provides the cued reward after the cued delay. To get at dACC neurons' contributions to decisions, we focused on responses around the time of choice, several seconds before the reward and the end of the trial. We found that dACC neurons signal the foregone value of the rejected option, a postdecisional variable. Neurons also signal the profitability (that is, the relative value) of the offer, but even these signals are qualitatively different on accept and reject decisions, meaning that they are also postdecisional. These results suggest that dACC can be placed late in the decision process and also support models that give it a regulatory role in decision, rather than serving as a site of comparison. |
Tommy C. Blanchard; Andreas Wilke; Benjamin Y. Hayden Hot-hand bias in rhesus monkeys Journal Article In: Journal of Experimental Psychology: Animal Behavior Processes, vol. 40, no. 3, pp. 280–286, 2014. @article{Blanchard2014a,Human decision-makers often exhibit the hot-hand phenomenon, a tendency to perceive positive serial autocorrelations in independent sequential events. The term is named after the observation that basketball fans and players tend to perceive streaks of high accuracy shooting when they are demonstrably absent. That is, both observing fans and participating players tend to hold the belief that a player's chance of hitting a shot are greater following a hit than following a miss. We hypothesize that this bias reflects a strong and stable tendency among primates (including humans) to perceive positive autocorrelations in temporal sequences, that this bias is an adaptation to clumpy foraging environments, and that it may even be ecologically rational. Several studies support this idea in humans, but a stronger test would be to determine whether nonhuman primates also exhibit a hot-hand bias. Here we report behavior of 3 monkeys performing a novel gambling task in which correlation between sequential gambles (i.e., temporal clumpiness) is systematically manipulated. We find that monkeys have better performance (meaning, more optimal behavior) for clumped (positively correlated) than for dispersed (negatively correlated) distributions. These results identify and quantify a new bias in monkeys' risky decisions, support accounts that specifically incorporate cognitive biases into risky choice, and support the suggestion that the hot-hand phenomenon is an evolutionary ancient bias. |
Tommy C. Blanchard; Lauren S. Wolfe; Ivo Vlaev; Joel S. Winston; Benjamin Y. Hayden Biases in preferences for sequences of outcomes in monkeys Journal Article In: Cognition, vol. 130, no. 3, pp. 289–299, 2014. @article{Blanchard2014b,Movies, vacations, and meals are all examples of events composed of a sequence of smaller events. How do we go from our evaluations of each scene in a movie to an evaluation of the sequence as a wholeα In theory, we should simply average the values of the individual events. In practice, however, we are biased towards sequences where each element tends to be better than the previous, where the last value is large, and we overweight the best (or worst) part of the sequence. To study how general these biases are we examined monkeys' preferences for sequences of rewards in a novel reward repeat task. Monkeys were first given a sequence of rewards and then chose between repeating the sequence or receiving a standard comparator sequence. We found that, like humans, monkeys overweight events that happen later in a sequence, so much so that adding a small reward to the end of a sequence can paradoxically reduce its value. Monkeys were also biased towards sequences with large peak values (the highest value in the sequence), but only following a working memory challenge, suggesting that this preference may be driven by memory limitations. These results demonstrate the cross-species nature of biases in preferences for sequences of outcomes. In addition, monkeys' consistent preference for sequences in which large values occur later challenges the generality of discounting models of intertemporal choice in animals. |
Charles F. Cadieu; Ha Hong; Daniel L. K. Yamins; Nicolas Pinto; Diego Ardila; Ethan A. Solomon; Najib J. Majaj; James J. DiCarlo Deep neural networks rival the representation of primate IT cortex for core visual object recognition Journal Article In: PLoS Computational Biology, vol. 10, no. 12, pp. e1003963, 2014. @article{Cadieu2014,The primate visual system achieves remarkable visual object recognition performance even in brief presentations, and under changes to object exemplar, geometric transformations, and background variation (a.k.a. core visual object recognition). This remarkable performance is mediated by the representation formed in inferior temporal (IT) cortex. In parallel, recent advances in machine learning have led to ever higher performing models of object recognition using artificial deep neural networks (DNNs). It remains unclear, however, whether the representational performance of DNNs rivals that of the brain. To accurately produce such a comparison, a major difficulty has been a unifying metric that accounts for experimental limitations, such as the amount of noise, the number of neural recording sites, and the number of trials, and computational limitations, such as the complexity of the decoding classifier and the number of classifier training examples. In this work, we perform a direct comparison that corrects for these experimental limitations and computational considerations. As part of our methodology, we propose an extension of ‘‘kernel analysis'' that measures the generalization accuracy as a function of representational complexity. Our evaluations show that, unlike previous bio-inspired models, the latest DNNs rival the representational performance of IT cortex on this visual object recognition task. Furthermore, we show that models that perform well on measures of representational performance also perform well on measures of representational similarity to IT, and on measures of predicting individual IT multi-unit responses. Whether these DNNs rely on computational mechanisms similar to the primate visual system is yet to be determined, but, unlike all previous bio- inspired models, that possibility cannot be ruled out merely on representational performance grounds. |
Xinying Cai; Camillo Padoa-Schioppa Contributions of orbitofrontal and lateral prefrontal cortices to economic choice and the good-to-action transformation Journal Article In: Neuron, vol. 81, no. 5, pp. 1140–1151, 2014. @article{Cai2014,Previous work indicates that economic decisions can be made independently of the visuomotor contingencies of the choice task (space of goods). However, the neuronal mechanisms through which the choice outcome (the chosen good) is transformed into a suitable action plan remain poorly understood. Here we show that neurons in lateral prefrontal cortex reflect the early stages of this good-to-action transformation. Monkeys chose between different juices. The experimental design dissociated in space and time the presentation of the offers and the saccade targets associated with them. We recorded from the orbital, ventrolateral, and dorsolateral prefrontal cortices (OFC, LPFCv, and LPFCd, respectively). Prior to target presentation, neurons in both LPFCv and LPFCd encoded the choice outcome in goods space. After target presentation, they gradually came to encode the location of the targets and the upcoming action plan. Consistent with the anatomical connectivity, all spatial and action-related signals emerged in LPFCv before LPFCd. |
Michael Colombo; James S. Magnuson Eye movements reveal planning in humans: A comparison with Scarf and Colombo's (2009) monkeys Journal Article In: Journal of Experimental Psychology: Animal Learning and Cognition, vol. 40, no. 2, pp. 178–184, 2014. @article{Colombo2014,On sequential response tasks, a long pause preceding the first response is thought to reflect participants taking time to plan a sequence of responses. By tracking the eye movements of two monkeys (Macaca fascicularis), Scarf and Colombo (2009, Eye Movements During List Execution Reveal No Planning in Monkeys [Macaca fascicularis], Journal of Experimental Psychology: Animal Behavior Processes, Vol. 35, pp. 587–592) demonstrated that, at least with respect to monkeys, the long pause preceding the first response is not necessarily the product of planning. In the present experiment, we tracked the eye movements of adult humans using the paradigm employed by Scarf and Colombo and found that, in contrast to monkeys, the pause preceding the first item is indicative of planning in humans. These findings highlight the fact that similar response time profiles, displayed by human and nonhuman animals, do not necessarily reflect similar underlying cognitive operations. |
Siavash Vaziri; Eric T. Carlson; Zhihong Wang; Charles E. Connor A channel for 3D environmental shape in anterior inferotemporal cortex Journal Article In: Neuron, vol. 84, no. 1, pp. 55–62, 2014. @article{Vaziri2014,Inferotemporal cortex (IT) has long been studied as asingle pathway dedicated to object vision, but connectivity analysis reveals anatomically distinct channels, through ventral superior temporal sulcus (STSv) and dorsal/ventral inferotemporal gyrus (TEd, TEv). Here, we report a major functional distinction between channels. We studied individual IT neurons in monkeys viewing stereoscopic 3D images projected on a large screen. We used adaptive stimuli to explore neural tuning for 3D abstract shapes ranging in scale and topology from small, closed, bounded objects to large, open, unbounded environments (landscape-like surfaces and cave-like interiors). In STSv, most neurons were more responsive to objects, as expected. In TEd, surprisingly, most neurons were more responsive to 3D environmental shape. Previous studies have localized environmental information to posterior cortical modules. Our results show it is also channeled through anterior IT, where extensive cross-connections between STSv and TEd could integrate object and environmental shape information. |
Chin-An Wang; Douglas P. Munoz Modulation of stimulus contrast on the human pupil orienting response Journal Article In: European Journal of Neuroscience, vol. 40, no. 5, pp. 2822–2832, 2014. @article{Wang2014,The sudden appearance of a novel stimulus initiates a series of responses to orient the body for appropriate actions, including not only shifts of gaze and attention, but also transient pupil dilation. Modulation of pupil dynamics by stimulus properties is less understood, although its effects on other components of orienting have been extensively explored. Microstimulation of the superior colliculus evoked transient pupil dilation, and the initial component of pupil dilation evoked by microstimulation was similar to that elicited by the presentation of salient sensory stimuli, suggesting a coordinated role of the superior colliculus on this behavior, although evidence in humans is yet to be established. To examine pupil orienting responses in humans, we presented visual stimuli while participants fixated on a central visual spot. Transient pupil dilation in humans was elicited after presentation of a visual stimulus in the periphery. The evoked pupil responses were modulated systematically by stimulus contrast, with faster and larger pupil responses triggered by higher contrast stimuli. The pupil response onset latencies for high contrast stimuli were similar to those produced by the light reflex and significantly faster than the darkness reflex, suggesting that the initial component of pupil dilation is probably mediated by inhibition of the parasympathetic pathway. The contrast modulation was pronounced under different levels of baseline pupil size. Together, our results demonstrate visual contrast modulation on the orienting pupil response in humans. |
Jianbo Xiao; Yu-Qiong Niu; Steven Wiesner; Xin Huang Normalization of neuronal responses in cortical area MT across signal strengths and motion directions Journal Article In: Journal of Neurophysiology, vol. 112, no. 6, pp. 1291–1306, 2014. @article{Xiao2014,Multiple visual stimuli are common in natural scenes, yet it remains unclear how multiple stimuli interact to influence neuronal responses. We investigated this question by manipulating relative signal strengths of two stimuli moving simultaneously within the receptive fields (RFs) of neurons in the extrastriate middle temporal (MT) cortex. Visual stimuli were overlapping random-dot patterns moving in two directions separated by 90°. We first varied the motion coherence of each random-dot pattern and characterized, across the direction tuning curve, the relationship between neuronal responses elicited by bidirectional stimuli and by the constituent motion components. The tuning curve for bidirectional stimuli showed response normalization and can be accounted for by a weighted sum of the responses to the motion components. Allowing nonlinear, multiplicative interaction between the two component responses significantly improved the data fit for some neurons, and the interaction mainly had a suppressive effect on the neuronal response. The weighting of the component responses was not fixed but dependent on relative signal strengths. When two stimulus components moved at different coherence levels, the response weight for the higher-coherence component was significantly greater than that for the lower-coherence component. We also varied relative luminance levels of two coherently moving stimuli and found that MT response weight for the higher-luminance component was also greater. These results suggest that competition between multiple stimuli within a neuron's RF depends on relative signal strengths of the stimuli and that multiplicative nonlinearity may play an important role in shaping the response tuning for multiple stimuli. |
Daniel L. K. Yamins; Ha Hong; Charles F. Cadieu; Ethan A. Solomon; Darren Seibert; James J. DiCarlo Performance-optimized hierarchical models predict neural responses in higher visual cortex Journal Article In: Proceedings of the National Academy of Sciences, vol. 111, no. 23, pp. 8619–8624, 2014. @article{Yamins2014,The ventral visual stream underlies key human visual object recognition abilities. However, neural encoding in the higher areas of the ventral stream remains poorly understood. Here, we describe a modeling approach that yields a quantitatively accurate model of inferior temporal (IT) cortex, the highest ventral cortical area. Using high-throughput computational techniques, we discovered that, within a class of biologically plausible hierarchical neural network models, there is a strong correlation between a model's categorization performance and its ability to predict individual IT neural unit response data. To pursue this idea, we then identified a high-performing neural network that matches human performance on a range of recognition tasks. Critically, even though we did not constrain this model to match neural data, its top output layer turns out to be highly predictive of IT spiking responses to complex naturalistic images at both the single site and population levels. Moreover, the model's intermediate layers are highly predictive of neural responses in the V4 cortex, a midlevel visual area that provides the dominant cortical input to IT. These results show that performance optimization - applied in a biologically appropriate model class - can be used to build quantitative predictive models of neural processing. |
David B. T. McMahon; Igor V. Bondar; Olusoji A. T. Afuwape; David C. Ide; David A. Leopold One month in the life of a neuron: longitudinal single-unit electrophysiology in the monkey visual system Journal Article In: Journal of Neurophysiology, vol. 112, no. 7, pp. 1748–1762, 2014. @article{McMahon2014,Conventional recording methods generally preclude following the activity of the same neurons in awake animals across days. This limits our ability to systematically investigate the principles of neuronal specialization, or to study phenomena that evolve over multiple days such as experience-dependent plasticity. To redress this shortcoming, we developed a drivable, chronically implanted microwire recording preparation that allowed us to follow visual responses in inferotemporal (IT) cortex in awake behaving monkeys across multiple days, and in many cases across months. The microwire bundle and other implanted components were MRI compatible and thus permitted in the same animals both functional imaging and long-term recording from multiple neurons in deep structures within a region the approximate size of one voxel (<1 mm). The distinct patterns of stimulus selectivity observed in IT neurons, together with stable features in spike waveforms and interspike interval distributions, allowed us to track individual neurons across weeks and sometimes months. The long-term consistency of visual responses shown here permits large-scale mappings of neuronal properties using massive image libraries presented over the course of days. We demonstrate this possibility by screening the visual responses of single neurons to a set of 10,000 stimuli. |
David B. T. McMahon; Adam P. Jones; Igor V. Bondar; David A. Leopold Face-selective neurons maintain consistent visual responses across months Journal Article In: Proceedings of the National Academy of Sciences, vol. 111, no. 22, pp. 8251–8256, 2014. @article{McMahon2014a,Face perception in both humans and monkeys is thought to depend on neurons clustered in discrete, specialized brain regions. Because primates are frequently called upon to recognize and remember new individuals, the neuronal representation of faces in the brain might be expected to change over time. The functional properties of neurons in behaving animals are typically assessed over time periods ranging from minutes to hours, which amounts to a snapshot compared to a lifespan of a neuron. It therefore remains unclear how neuronal properties observed on a given day predict that same neuron's activity months or years later. Here we show that the macaque inferotemporal cortex contains face-selective cells that show virtually no change in their patterns of visual responses over time periods as long as one year. Using chronically implanted microwire electrodes guided by functional MRI targeting, we obtained distinct profiles of selectivity for face and nonface stimuli that served as fingerprints for individual neurons in the anterior fundus (AF) face patch within the superior temporal sulcus. Longitudinal tracking over a series of daily recording sessions revealed that face-selective neurons maintain consistent visual response profiles across months-long time spans despite the influence of ongoing daily experience. We propose that neurons in the AF face patch are specialized for aspects of face perception that demand stability as opposed to plasticity. |
David Méary; Zhihan Li; Wu Li; Kun Guo; Olivier Pascalis Seeing two faces together: Preference formation in humans and rhesus macaques Journal Article In: Animal Cognition, vol. 17, no. 5, pp. 1107–1119, 2014. @article{Meary2014,Humans, great apes and old world monkeys show selective attention to faces depending on conspecificity, familiarity, and social status supporting the view that primates share similar face processing mechanisms. Although many studies have been done on face scanning strategy in monkeys and humans, the mechanisms influencing viewing preference have received little attention. To determine how face categories influence viewing preference in humans and rhesus macaques (Macaca mulatta), we performed two eye-tracking experiments using a visual preference task whereby pairs of faces from different species were presented simultaneously. The results indicated that viewing time was significantly influenced by the pairing of the face categories. Humans showed a strong bias towards an own-race face in an Asian-Caucasian condition. Rhesus macaques directed more attention towards non-human primate faces when they were paired with human faces, regardless of the species. When rhesus faces were paired with faces from Barbary macaques (Macaca sylvanus) or chimpanzees (Pan troglodytes), the novel species' faces attracted more attention. These results indicate that monkeys' viewing preferences, as assessed by a visual preference task, are modulated by several factors, species and dominance being the most influential. |
Diego Mendoza-Halliday; Santiago Torres; Julio C. Martinez-Trujillo Sharp emergence of feature-selective sustained activity along the dorsal visual pathway Journal Article In: Nature Neuroscience, vol. 17, no. 9, pp. 1255–1262, 2014. @article{MendozaHalliday2014,Sustained activity encoding visual working memory representations has been observed in several cortical areas of primates. Where along the visual pathways this activity emerges remains unknown. Here we show in macaques that sustained spiking activity encoding memorized visual motion directions is absent in direction-selective neurons in early visual area middle temporal (MT). However, it is robustly present immediately downstream, in multimodal association area medial superior temporal (MST), as well as and in the lateral prefrontal cortex (LPFC). This sharp emergence of sustained activity along the dorsal visual pathway suggests a functional boundary between early visual areas, which encode sensory inputs, and downstream association areas, which additionally encode mnemonic representations. Moreover, local field potential oscillations in MT encoded the memorized directions and, in the low frequencies, were phase-coherent with LPFC spikes. This suggests that LPFC sustained activity modulates synaptic activity in MT, a putative top-down mechanism by which memory signals influence stimulus processing in early visual cortex. |
Paul G. Middlebrooks; Jeffrey D. Schall Response inhibition during perceptual decision making in humans and macaques Journal Article In: Attention, Perception, & Psychophysics, vol. 76, no. 2, pp. 353–366, 2014. @article{Middlebrooks2014,Response inhibition in stop signal tasks has been explained as the outcome of a race between GO and STOP processes (e.g., Logan, 1981). Response choice in two-alternative perceptual categorization tasks has been explained as the outcome of an accumulation of evidence for the alternative responses. To begin unifying these two powerful investigation frameworks, we obtained data from humans and macaque monkeys performing a stop signal task with responses guided by perceptual categorization and variable degrees of difficulty, ranging from low to high accuracy. Comparable results across species reinforced the validity of this animal model. Response times and errors increased with categorization difficulty. The probability of failing to inhibit responses on stop signal trials increased with stop signal delay, and the response times for failed stop signal trials were shorter than those for trials with no stop signal. Thus, the Logan race model could be applied to estimate the duration of the stopping process. We found that the duration of the STOP process did not vary across a wide range of discrimination accuracies. This is consistent with the functional, and possibly mechanistic, independence of choice and inhibition mechanisms. |
Tania Ortuno; Kenneth L. Grieve; Ricardo Cao; Javier Cudeiro; Casto Rivadulla Bursting thalamic responses in awake monkey contribute to visual detection and are modulated by corticofugal feedback Journal Article In: Frontiers in Behavioral Neuroscience, vol. 8, pp. 198, 2014. @article{Ortuno2014,The lateral geniculate nucleus is the gateway for visual information en route to the visual cortex. Neural activity is characterized by the existence of two firing modes: burst and tonic. Originally associated with sleep, bursts have now been postulated to be a part of the normal visual response, structured to increase the probability of cortical activation, able to act as a "wake-up" call to the cortex. We investigated a potential role for burst in the detection of novel stimuli by recording neuronal activity in the lateral geniculate nucleus (LGN) of behaving monkeys during a visual detection task. Our results show that bursts are often the neuron's first response, and are more numerous in the response to attended target stimuli than to unattended distractor stimuli. Bursts are indicators of the task novelty, as repetition decreased bursting. Because the primary visual cortex is the major modulatory input to the LGN, we compared the results obtained in control conditions with those observed when cortical activity was reduced by TMS. This cortical deactivation reduced visual response related bursting by 90%. These results highlight a novel role for the thalamus, able to code higher order image attributes as important as novelty early in the thalamo-cortical conversation. |
Xiaochuan Pan; Hongwei Fan; Kosuke Sawa; Ichiro Tsuda; Minoru Tsukada; Masamichi Sakagami Reward inference by primate prefrontal and striatal neurons Journal Article In: Journal of Neuroscience, vol. 34, no. 4, pp. 1380–1396, 2014. @article{Pan2014a,The brain contains multiple yet distinct systems involved in reward prediction. To understand the nature of these processes, we recorded single-unit activity from the lateral prefrontal cortex (LPFC) and the striatum in monkeys performing a reward inference task using an asymmetric reward schedule. We found that neurons both in the LPFC and in the striatum predicted reward values for stimuli that had been previously well experienced with set reward quantities in the asymmetric reward task. Importantly, these LPFC neurons could predict the reward value of a stimulus using transitive inference even when the monkeys had not yet learned the stimulus–reward association directly; whereas these striatal neurons did not show such an ability. Nevertheless, because there were two set amounts of reward (large and small), the selected striatal neurons were able to exclusively infer the reward value (e.g., large) of one novel stimulus from a pair after directly experiencing the alternative stimulus with the other reward value (e.g., small). Our results suggest that although neurons that predict reward value for old stimuli in the LPFC could also do so for new stimuli via transitive inference, those in the striatum could only predict reward for new stimuli via exclusive inference. Moreover, the striatum showed more complex functions than was surmised previously for model-free learning. |
Pierpaolo Pani; Tom Theys; Maria C. Romero; Peter Janssen Grasping execution and grasping observation activity of single neurons in the macaque anterior intraparietal area Journal Article In: Journal of Cognitive Neuroscience, vol. 26, no. 10, pp. 2342–2355, 2014. @article{Pani2014,Primates use vision to guide their actions in everyday life. Visually guided object grasping is known to rely on a network of cortical areas located in the parietal and premotor cortex. We recorded in the anterior intraparietal area (AIP), an area in the dorsal visual stream that is critical for object grasping and densely connected with the premotor cortex, while monkeys were grasping objects under visual guidance and during passive fixation of videos of grasping actions from the first-person perspective. All AIP neurons in this study responded during grasping execution in the light, that is, became more active after the hand had started to move toward the object and during grasping in the dark. More than half of these AIP neurons responded during the observation of a video of the same grasping actions on a display. Furthermore, these AIP neurons responded as strongly during passive fixation of movements of a hand on a scrambled background and to a lesser extent to a shape appearing within the visual field near the object. Therefore, AIP neurons responding during grasping execution also respond during passive observation of grasping actions and most of them even during passive observation of movements of a simple shape in the visual field. |
C. A. Patterson; Jacob Duijnhouwer; S. C. Wissig; B. Krekelberg; Adam Kohn Similar adaptation effects in primary visual cortex and area MT of the macaque monkey under matched stimulus conditions Journal Article In: Journal of Neurophysiology, vol. 111, no. 6, pp. 1203–1213, 2014. @article{Patterson2014,Recent stimulus history, or adaptation, can alter neuronal response properties. Adaptation effects have been characterized in a number of visually responsive structures, from the retina to higher visual cortex. However, it remains unclear whether adaptation effects across stages of the visual system take a similar form in response to a particular sensory event. This is because studies typically probe a single structure or cortical area, using a stimulus ensemble chosen to provide potent drive to the cells of interest. Here we adopt an alternative approach and compare adaptation effects in primary visual cortex (V1) and area MT using identical stimulus ensembles. Previous work has suggested these areas adjust to recent stimulus drive in distinct ways. We show that this is not the case: adaptation effects in V1 and MT can involve weak or strong loss of responsivity and shifts in neuronal preference toward or away from the adapter, depending on stimulus size and adaptation duration. For a particular stimulus size and adaptation duration, however, effects are similar in nature and magnitude in V1 and MT. We also show that adaptation effects in MT of awake animals depend strongly on stimulus size. Our results suggest that the strategies for adjusting to recent stimulus history depend more strongly on adaptation duration and stimulus size than on the cortical area. Moreover, they indicate that different levels of the visual system adapt similarly to recent sensory experience. |
Ivo D. Popivanov; Jan Jastorff; Wim Vanduffel; Rufin Vogels Heterogeneous single-unit selectivity in an fMRI-defined body-selective patch Journal Article In: Journal of Neuroscience, vol. 34, no. 1, pp. 95–111, 2014. @article{Popivanov2014,Although the visual representation of bodies is essential for reproduction, survival, and social communication, little is known about the mechanisms of body recognition at the single neuron level. Imaging studies showed body-category selective regions in the primate occipitotemporal cortex, but it is difficult to infer the stimulus selectivities of the neurons from the population activity measured in these fMRI studies. To overcome this, we recorded single unit activity and local field potentials (LFPs) in the middle superior temporal sulcus body patch, defined by fMRI in the same rhesus monkeys. Both the spiking activity, averaged across single neurons, and LFP gamma power in this body patch was greater for bodies (including monkey bodies, human bodies, mammals, and birds) compared with other objects, which fits the fMRI activation. Single neurons responded to a small proportion of body images. Thus, the category selectivity at the population level resulted from averaging responses of a heterogeneous population of single units. Despite such strong within-category selectivity at the single unit level, two distinct clusters, bodies and nonbodies, were present when analyzing the responses at the population level, and a classifier that was trained using the responses to a subset of images was able to classify novel images of bodies with high accuracy. The body-patch neurons showed strong selectivity for individual body parts at different orientations. Overall, these data suggest that single units in the fMRI-defined body patch are biased to prefer bodies over nonbody objects, including faces, with a strong selectivity for individual body images. |
Elsie Premereur; Wim Vanduffel; Peter Janssen The effect of FEF microstimulation on the responses of neurons in the lateral intraparietal area Journal Article In: Journal of Cognitive Neuroscience, vol. 26, no. 8, pp. 1672–1684, 2014. @article{Premereur2014,The macaque FEFs and the lateral intraparietal area (LIP) are high-level cortical areas involved in both spatial attention and oculomotor behavior. Stimulating FEF at a level below the threshold for evoking saccades increases fMRI activity and gamma power in area LIP, but the precise effect exerted by the FEF on LIP neurons is unknown. In our study, we recorded LIP single-unit activity during a visually guided saccade task with a peripherally presented go signal during microstimulation of FEF. We found that FEF microstimulation increased the LIP spike rate imme- diately after the highly salient go signal inside the LIP receptive field when both target and go signal were presented inside the receptive field, and no other possible go cues were present on the screen. The effect of FEF microstimulation on the LIP response was positive until at least 800msec aftermicrostimulation had ceased, but reversed for longer trial durations. Therefore, FEF microstimulation can modulate the LIP spike rate only when attention is selectively directed toward the stimulated location. These results provide the first direct evidence for LIP spike rate modulations caused by FEF microstimulation, thus showing that FEF activity can be the source of top–down control ofarea LIP. |
A. P. Raghuraman; Camillo Padoa-Schioppa Integration of multiple determinants in the neuronal computation of economic values Journal Article In: Journal of Neuroscience, vol. 34, no. 35, pp. 11583–11603, 2014. @article{Raghuraman2014,Economic goods may vary on multiple dimensions (determinants). A central conjecture in decision neuroscience is that choices between goods are made by comparing subjective values computed through the integration of all relevant determinants. Previous work identified three groups of neurons in the orbitofrontal cortex (OFC) of monkeys engaged in economic choices: (1) offer value cells, which encode the value of individual offers; (2) chosen value cells, which encode the value of the chosen good; and (3) chosen juice cells, which encode the identity of the chosen good. In principle, these populations could be sufficient to generate a decision. Critically, previous work did not assess whether offer value cells (the putative input to the decision) indeed encode subjective values as opposed to physical properties of the goods, and/or whether offer value cells integrate multiple determinants. To address these issues, we recorded from the OFC while monkeys chose between risky outcomes. Confirming previous observations, three populations of neurons encoded the value of individual offers, the value of the chosen option, and the value-independent choice outcome. The activity of both offer value cells and chosen value cells encoded values defined by the integration of juice quantity and probability. Furthermore, both populations reflected the subjective risk attitude of the animals. We also found additional groups of neurons encoding the risk associated with a particular option, the risky nature of the chosen option, and whether the trial outcome was positive or negative. These results provide substantial support for the conjecture described above and for the involvement of OFC in good-based decisions. |