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!
2013 |
Patrick J. Mineault; Theodoros P. Zanos; Christopher C. Pack Local field potentials reflect multiple spatial scales in V4 Journal Article In: Frontiers in Computational Neuroscience, vol. 7, pp. 21, 2013. @article{Mineault2013,Local field potentials (LFP) reflect the properties of neuronal circuits or columns recorded in a volume around a microelectrode (Buzsáki et al., 2012). The extent of this integration volume has been a subject of some debate, with estimates ranging from a few hundred microns (Katzner et al., 2009; Xing et al., 2009) to several millimeters (Kreiman et al., 2006). We estimated receptive fields (RFs) of multi-unit activity (MUA) and LFPs at an intermediate level of visual processing, in area V4 of two macaques. The spatial structure of LFP receptive fields varied greatly as a function of time lag following stimulus onset, with the retinotopy of LFPs matching that of MUAs at a restricted set of time lags. A model-based analysis of the LFPs allowed us to recover two distinct stimulus-triggered components: an MUA-like retinotopic component that originated in a small volume around the microelectrodes (~350 μm), and a second component that was shared across the entire V4 region; this second component had tuning properties unrelated to those of the MUAs. Our results suggest that the LFP reflects neural activity across multiple spatial scales, which both complicates its interpretation and offers new opportunities for investigating the large-scale structure of network processing. |
Daniel S. Pages; Jennifer M. Groh Looking at the ventriloquist: Visual outcome of eye movements calibrates sound localization Journal Article In: PLoS ONE, vol. 8, no. 8, pp. e72562, 2013. @article{Pages2013,A general problem in learning is how the brain determines what lesson to learn (and what lessons not to learn). For example, sound localization is a behavior that is partially learned with the aid of vision. This process requires correctly matching a visual location to that of a sound. This is an intrinsically circular problem when sound location is itself uncertain and the visual scene is rife with possible visual matches. Here, we develop a simple paradigm using visual guidance of sound localization to gain insight into how the brain confronts this type of circularity. We tested two competing hypotheses. 1: The brain guides sound location learning based on the synchrony or simultaneity of auditory-visual stimuli, potentially involving a Hebbian associative mechanism. 2: The brain uses a 'guess and check' heuristic in which visual feedback that is obtained after an eye movement to a sound alters future performance, perhaps by recruiting the brain's reward-related circuitry. We assessed the effects of exposure to visual stimuli spatially mismatched from sounds on performance of an interleaved auditory-only saccade task. We found that when humans and monkeys were provided the visual stimulus asynchronously with the sound but as feedback to an auditory-guided saccade, they shifted their subsequent auditory-only performance toward the direction of the visual cue by 1.3-1.7 degrees, or 22-28% of the original 6 degree visual-auditory mismatch. In contrast when the visual stimulus was presented synchronously with the sound but extinguished too quickly to provide this feedback, there was little change in subsequent auditory-only performance. Our results suggest that the outcome of our own actions is vital to localizing sounds correctly. Contrary to previous expectations, visual calibration of auditory space does not appear to require visual-auditory associations based on synchrony/simultaneity. |
Christopher J. Peck; Brian Lau; C. Daniel Salzman The primate amygdala combines information about space and value Journal Article In: Nature Neuroscience, vol. 16, no. 3, pp. 340–348, 2013. @article{Peck2013,A stimulus predicting reinforcement can trigger emotional responses, such as arousal, and cognitive ones, such as increased attention toward the stimulus. Neuroscientists have long appreciated that the amygdala mediates spatially nonspecific emotional responses, but it remains unclear whether the amygdala links motivational and spatial representations. To test whether amygdala neurons encode spatial and motivational information, we presented reward-predictive cues in different spatial configurations to monkeys and assessed how these cues influenced spatial attention. Cue configuration and predicted reward magnitude modulated amygdala neural activity in a coordinated fashion. Moreover, fluctuations in activity were correlated with trial-to-trial variability in spatial attention. Thus, the amygdala integrates spatial and motivational information, which may influence the spatial allocation of cognitive resources. These results suggest that amygdala dysfunction may contribute to deficits in cognitive processes normally coordinated with emotional responses, such as the directing of attention toward the location of emotionally relevant stimuli. |
Farhan A. Khawaja; Liu D. Liu; Christopher C. Pack Responses of MST neurons to plaid stimuli Journal Article In: Journal of Neurophysiology, vol. 110, no. 1, pp. 63–74, 2013. @article{Khawaja2013,The estimation of motion information from retinal input is a fundamental function of the primate dorsal visual pathway. Previous work has shown that this function involves multiple cortical areas, with each area integrating information from its predecessors. Compared with neurons in the primary visual cortex (V1), neurons in the middle temporal (MT) area more faithfully represent the velocity of plaid stimuli, and the observation of this pattern selectivity has led to two-stage models in which MT neurons integrate the outputs of component-selective V1 neurons. Motion integration in these models is generally complemented by motion opponency, which refines velocity selectivity. Area MT projects to a third stage of motion processing, the medial superior temporal (MST) area, but surprisingly little is known about MST responses to plaid stimuli. Here we show that increased pattern selectivity in MST is associated with greater prevalence of the mechanisms implemented by two-stage MT models: Compared with MT neurons, MST neurons integrate motion components to a greater degree and exhibit evidence of stronger motion opponency. Moreover, when tested with more challenging unikinetic plaid stimuli, an appreciable percentage of MST neurons are pattern selective, while such selectivity is rare in MT. Surprisingly, increased motion integration is found in MST even for transparent plaid stimuli, which are not typically integrated perceptually. Thus the relationship between MST and MT is qualitatively similar to that between MT and V1, as repeated application of basic motion mechanisms leads to novel selectivities at each stage along the pathway. |
Jeffrey T. Klein; Michael L. Platt Social information signaling by neurons in primate striatum Journal Article In: Current Biology, vol. 23, pp. 691–696, 2013. @article{Klein2013,Social decisions depend on reliable information about others. Consequently, social primates are motivated to acquire information about the identity, social status, and reproductive quality of others [1]. Neurophysiological [2] and neuroimaging [3, 4] studies implicate the striatum in the motivational control of behavior. Neuroimaging studies specifically implicate the ventromedial striatum in signaling motivational aspects of social interaction [5]. Despite this evidence, precisely how striatal neurons encode social information remains unknown. Therefore, we probed the activity of single striatal neurons in monkeys choosing between visual social information at the potential expense of fluid reward. We show for the first time that a population of neurons located primarily in medial striatum selectively signals social information. Surprisingly, representation of social information was unrelated to simultaneously expressed social preferences. A largely nonoverlapping population of neurons that was not restricted to the medial striatum signaled information about fluid reward. Our findings demonstrate that information about social context and nutritive reward are maintained largely independently in striatum, even when both influence decisions to execute a single action. |
Matthew L. Leavitt; Florian Pieper; Adam J. Sachs; Ridha Joober; Julio C. Martinez-Trujillo In: PLoS ONE, vol. 8, no. 4, pp. e61503, 2013. @article{Leavitt2013,Neurons within the primate dorsolateral prefrontal cortex (dlPFC) are clustered in microcolumns according to their visuospatial tuning. One issue that remains poorly investigated is how this anatomical arrangement influences functional interactions between neurons during behavior. To investigate this question we implanted 4 mm×4 mm multielectrode arrays in two macaques' dlPFC area 8a and measured spike count correlations (rsc ) between responses of simultaneously recorded neurons when animals maintained stationary gaze. Positive and negative rsc were significantly higher than predicted by chance across a wide range of inter-neuron distances (from 0.4 to 4 mm). Positive rsc were stronger between neurons with receptive fields (RFs) separated by ≤90° of angular distance and progressively decreased as a function of inter-neuron physical distance. Negative rsc were stronger between neurons with RFs separated by >90° and increased as a function of inter-neuron distance. Our results show that short- and long-range functional interactions between dlPFC neurons depend on the physical distance between them and the relationship between their visuospatial tuning preferences. Neurons with similar visuospatial tuning show positive rsc that decay with inter-neuron distance, suggestive of excitatory interactions within and between adjacent microcolumns. Neurons with dissimilar tuning from spatially segregated microcolumns show negative rsc that increase with inter-neuron distance, suggestive of inhibitory interactions. This pattern of results shows that functional interactions between prefrontal neurons closely follow the pattern of connectivity reported in anatomical studies. Such interactions may be important for the role of the prefrontal cortex in the allocation of attention to targets in the presence of competing distracters. |
Kyoung-Min Lee; Kyung-Ha Ahn The frontal eye fields limit the capacity of visual short-term memory in rhesus monkeys Journal Article In: PLoS ONE, vol. 8, no. 3, pp. e59606, 2013. @article{Lee2013a,The frontal eye fields (FEF) in rhesus monkeys have been implicated in visual short-term memory (VSTM) as well as control of visual attention. Here we examined the importance of the area in the VSTM capacity and the relationship between VSTM and attention, using the chemical inactivation technique and multi-target saccade tasks with or without the need of target-location memory. During FEF inactivation, serial saccades to targets defined by color contrast were unaffected, but saccades relying on short-term memory were impaired when the target count was at the capacity limit of VSTM. The memory impairment was specific to the FEF-coded retinotopic locations, and subject to competition among targets distributed across visual fields. These results together suggest that the FEF plays a crucial role during the entry of information into VSTM, by enabling attention deployment on targets to be remembered. In this view, the memory capacity results from the limited availability of attentional resources provided by FEF: The FEF can concurrently maintain only a limited number of activations to register the targets into memory. When lesions render part of the area unavailable for activation, the number would decrease, further reducing the capacity of VSTM. |
Masayuki Matsumoto; Masahiko Takada Distinct representations of cognitive and motivational signals in midbrain dopamine neurons Journal Article In: Neuron, vol. 79, no. 5, pp. 1011–1024, 2013. @article{Matsumoto2013,Dopamine is essential to cognitive functions. However, despite abundant studies demonstrating that dopamine neuron activity is related to reinforcement and motivation, little is known about what signals dopamine neurons convey to promote cognitive processing. We therefore examined dopamine neuron activity in monkeys performing a delayed matching-to-sample task that required working memory and visual search. We found that dopamine neurons responded to task events associated with cognitive operations. A subset of dopamine neurons were activated by visual stimuli if the monkey had to store the stimuli in working memory. These neurons were located dorsolaterally in the substantia nigra pars compacta, whereas ventromedial dopamine neurons, some in the ventral tegmental area, represented reward prediction signals. Furthermore, dopamine neurons monitored visual search performance, becoming active when the monkey made an internal judgment that the search was successfully completed. Our findings suggest an anatomical gradient of dopamine signals along the dorsolateral-ventromedial axis of the ventral midbrain. |
Richard McFarland; Hettie Roebuck; Yin Yan; Bonaventura Majolo; Wu Li; Kun Guo Social interactions through the eyes of macaques and humans Journal Article In: PLoS ONE, vol. 8, no. 2, pp. e56437, 2013. @article{McFarland2013,Group-living primates frequently interact with each other to maintain social bonds as well as to compete for valuable resources. Observing such social interactions between group members provides individuals with essential information (e.g. on the fighting ability or altruistic attitude of group companions) to guide their social tactics and choice of social partners. This process requires individuals to selectively attend to the most informative content within a social scene. It is unclear how non-human primates allocate attention to social interactions in different contexts, and whether they share similar patterns of social attention to humans. Here we compared the gaze behaviour of rhesus macaques and humans when free-viewing the same set of naturalistic images. The images contained positive or negative social interactions between two conspecifics of different phylogenetic distance from the observer; i.e. affiliation or aggression exchanged by two humans, rhesus macaques, Barbary macaques, baboons or lions. Monkeys directed a variable amount of gaze at the two conspecific individuals in the images according to their roles in the interaction (i.e. giver or receiver of affiliation/aggression). Their gaze distribution to non-conspecific individuals was systematically varied according to the viewed species and the nature of interactions, suggesting a contribution of both prior experience and innate bias in guiding social attention. Furthermore, the monkeys' gaze behavior was qualitatively similar to that of humans, especially when viewing negative interactions. Detailed analysis revealed that both species directed more gaze at the face than the body region when inspecting individuals, and attended more to the body region in negative than in positive social interactions. Our study suggests that monkeys and humans share a similar pattern of role-sensitive, species- and context-dependent social attention, implying a homologous cognitive mechanism of social attention between rhesus macaques and humans. |
Chris A. Rishel; Gang Huang; David J. Freedman Independent category and spatial encoding in parietal cortex Journal Article In: Neuron, vol. 77, no. 5, pp. 969–979, 2013. @article{Rishel2013,The posterior parietal cortex plays a central role in spatial functions, such as spatial attention and saccadic eye movements. However, recent work has increasingly focused on the role of parietal cortex in encoding nonspatial cognitive factors such as visual categories, learned stimulus associations, and task rules. The relationship between spatial encoding and nonspatial cognitive signals in parietal cortex, and whether cognitive signals are robustly encoded in the presence of strong spatial neuronal responses, is unknown. We directly compared nonspatial cognitive and spatial encoding in the lateral intraparietal (LIP) area by training monkeys to perform a visual categorization task during which they made saccades toward or away from LIP response fields (RFs). Here we show that strong saccade-related responses minimally influence robustly encoded category signals in LIP. This suggests that cognitive and spatial signals are encoded independently in LIP and underscores the role of parietal cortex in nonspatial cognitive functions. |
Maria C. Romero; Ilse C. Van Dromme; Peter Janssen The role of binocular disparity in stereoscopic images of objects in the macaque anterior intraparietal area Journal Article In: PLoS ONE, vol. 8, no. 2, pp. e55340, 2013. @article{Romero2013,Neurons in the macaque Anterior Intraparietal area (AIP) encode depth structure in random-dot stimuli defined by gradients of binocular disparity, but the importance of binocular disparity in real-world objects for AIP neurons is unknown. We investigated the effect of binocular disparity on the responses of AIP neurons to images of real-world objects during passive fixation. We presented stereoscopic images of natural and man-made objects in which the disparity information was congruent or incongruent with disparity gradients present in the real-world objects, and images of the same objects where such gradients were absent. Although more than half of the AIP neurons were significantly affected by binocular disparity, the great majority of AIP neurons remained image selective even in the absence of binocular disparity. AIP neurons tended to prefer stimuli in which the depth information derived from binocular disparity was congruent with the depth information signaled by monocular depth cues, indicating that these monocular depth cues have an influence upon AIP neurons. Finally, in contrast to neurons in the inferior temporal cortex, AIP neurons do not represent images of objects in terms of categories such as animate-inanimate, but utilize representations based upon simple shape features including aspect ratio. |
Adam C. Snyder; Michael J. Morais; Matthew A. Smith Variance in population firing rate as a measure of slow time-scale correlation Journal Article In: Frontiers in Computational Neuroscience, vol. 7, pp. 176, 2013. @article{Snyder2013,Correlated variability in the spiking responses of pairs of neurons, also known as spike count correlation, is a key indicator of functional connectivity and a critical factor in population coding. Underscoring the importance of correlation as a measure for cognitive neuroscience research is the observation that spike count correlations are not fixed, but are rather modulated by perceptual and cognitive context. Yet while this context fluctuates from moment to moment, correlation must be calculated over multiple trials. This property undermines its utility as a dependent measure for investigations of cognitive processes which fluctuate on a trial-to-trial basis, such as selective attention. A measure of functional connectivity that can be assayed on a moment-to-moment basis is needed to investigate the single-trial dynamics of populations of spiking neurons. Here, we introduce the measure of population variance in normalized firing rate for this goal. We show using mathematical analysis, computer simulations and in vivo data how population variance in normalized firing rate is inversely related to the latent correlation in the population, and how this measure can be used to reliably classify trials from different typical correlation conditions, even when firing rate is held constant. We discuss the potential advantages for using population variance in normalized firing rate as a dependent measure for both basic and applied neuroscience research. |
Sruthi K. Swaminathan; Nicolas Y. Masse; David J. Freedman A comparison of lateral and medial intraparietal areas during a visual categorization task Journal Article In: Journal of Neuroscience, vol. 33, no. 32, pp. 13157–13170, 2013. @article{Swaminathan2013,Categorization is essential for interpreting sensory stimuli and guiding our actions. Recent studies have revealed robust neuronal category representations in the lateral intraparietal area (LIP). Here, we examine the specialization of LIP for categorization and the roles of other parietal areas by comparing LIP and the medial intraparietal area (MIP) during a visual categorization task. MIP is involved in goal-directed arm movements and visuomotor coordination but has not been implicated in non-motor cognitive functions, such as categorization. As expected, we found strong category encoding in LIP. Interestingly, we also observed category signals in MIP. However, category signals were stronger and appeared with a shorter latency in LIP than MIP. In this task, monkeys indicated whether a test stimulus was a category match to a previous sample with a manual response. Test-period activity in LIP showed category encoding and distinguished between matches and non-matches. In contrast, MIP primarily reflected the match/non-match status of test stimuli, with a strong preference for matches (which required a motor response). This suggests that, although category representations are distributed across parietal cortex, LIP and MIP play distinct roles: LIP appears more involved in the categorization process itself, whereas MIP is more closely tied to decision-related motor actions. |
Tom Theys; Pierpaolo Pani; Johannes Loon; Jan Goffin; Peter Janssen Three-dimensional shape coding in grasping circuits: A comparison between the anterior intraparietal area and ventral premotor area F5a Journal Article In: Journal of Cognitive Neuroscience, vol. 25, no. 3, pp. 352–364, 2013. @article{Theys2013,Depth information is necessary for adjusting the hand to the three-dimensional (3-D) shape of an object to grasp it. The transformation of visual information into appropriate distal motor commands is critically dependent on the anterior intraparietal area (AIP) and the ventral premotor cortex (area F5), particularly the F5p sector. Recent studies have demonstrated that both AIP and the F5a sector of the ventral premotor cortex contain neurons that respond selectively to disparity-defined 3-D shape. To investigate the neural coding of 3-D shape and the behavioral role of 3-D shape-selective neurons in these two areas, we recorded single-cell activity in AIP and F5a during passive fixation of curved surfaces and during grasping of real-world objects. Similar to those in AIP, F5a neurons were either first- or second-order disparity selective, frequently showed selectivity for discrete approximations of smoothly curved surfaces that contained disparity discontinuities, and exhibited mostly monotonic tuning for the degree of disparity variation. Furthermore, in both areas, 3-D shape-selective neurons were colocalized with neurons that were active during grasping of real-world objects. Thus, area AIP and F5a contain highly similar representations of 3-D shape, which is consistent with the proposed transfer of object information from AIP to the motor system through the ventral premotor cortex. |
Michele A. Cox; Michael C. Schmid; Andrew J. Peters; Richard C. Saunders; David A. Leopold; Alexander Maier Receptive field focus of visual area V4 neurons determines responses to illusory surfaces Journal Article In: Proceedings of the National Academy of Sciences, vol. 110, no. 42, pp. 17095–17100, 2013. @article{Cox2013,Illusory figures demonstrate the visual system's ability to infer surfaces under conditions of fragmented sensory input. To investigate the role of midlevel visual area V4 in visual surface completion, we used multielectrode arrays to measure spiking responses to two types of visual stimuli: Kanizsa patterns that induce the perception of an illusory surface and physically similar control stimuli that do not. Neurons in V4 exhibited stronger and sometimes rhythmic spiking responses for the illusion-promoting configurations compared with controls. Moreover, this elevated response depended on the precise alignment of the neuron's peak visual field sensitivity (receptive field focus) with the illusory surface itself. Neurons whose receptive field focus was over adjacent inducing elements, less than 1.5° away, did not show response enhancement to the illusion. Neither receptive field sizes nor fixational eye movements could account for this effect, which was present in both single-unit signals and multiunit activity. These results suggest that the active perceptual completion of surfaces and shapes, which is a fundamental problem in natural visual experience, draws upon the selective enhancement of activity within a distinct subpopulation of neurons in cortical area V4. |
Yuwei Cui; Liu D. Liu; Farhan A. Khawaja; Christopher C. Pack; Daniel A. Butts Diverse suppressive Iinfluences in area MT and selectivity to complex motion features Journal Article In: Journal of Neuroscience, vol. 33, no. 42, pp. 16715–16728, 2013. @article{Cui2013c,Neuronal selectivity results from both excitatory and suppressive inputs to a given neuron. Suppressive influences can often significantly modulate neuronal responses and impart novel selectivity in the context of behaviorally relevant stimuli. In this work, we use a naturalistic optic flow stimulus to explore the responses of neurons in the middle temporal area (MT) of the alert macaque monkey; these responses are interpreted using a hierarchical model that incorporates relevant nonlinear properties of upstream processing in the primary visual cortex (V1). In this stimulus context, MT neuron responses can be predicted from distinct excitatory and suppressive components. Excitation is spatially localized and matches the measured preferred direction of each neuron. Suppression is typically composed of two distinct components: (1) a directionally untuned component, which appears to play the role of surround suppression and normalization; and (2) a direction-selective component, with comparable tuning width as excitation and a distinct spatial footprint that is usually partially overlapping with excitation. The direction preference of this direction-tuned suppression varies widely across MT neurons: approximately one-third have overlapping suppression in the opposite direction as excitation, and many other neurons have suppression with similar direction preferences to excitation. There is also a population of MT neurons with orthogonally oriented suppression. We demonstrate that direction-selective suppression can impart selectivity of MT neurons to more complex velocity fields and that it can be used for improved estimation of the three-dimensional velocity of moving objects. Thus, considering MT neurons in a complex stimulus context reveals a diverse set of computations likely relevant for visual processing in natural visual contexts. |
Thomas Deffieux; Youliana Younan; Nicolas Wattiez; Mickael Tanter; Pierre Pouget; Jean-François Aubry Low-intensity focused ultrasound modulates monkey visuomotor behavior Journal Article In: Current Biology, vol. 23, pp. 2430–2433, 2013. @article{Deffieux2013,In vivo feasibility of using low-intensity focused ultrasound (FUS) to transiently modulate the function of regional brain tissue has been recently tested in anesthetized lagomorphs [1] and rodents [2-4]. Hypothetically, ultrasonic stimulation of the brain possesses several advantages [5]: it does not necessitate surgery or genetic alteration but could ultimately confer spatial resolutions superior to other noninvasive methods. Here, we gauged the ability of noninvasive FUS to causally modulate high-level cognitive behavior. Therefore, we examined how FUS might interfere with prefrontal activity in two awake macaque rhesus monkeys that had been trained to perform an antisaccade (AS) task. We show that ultrasound significantly modulated AS latencies. Such effects proved to be dependent on FUS hemifield of stimulation (relative latency increases most for ipsilateral AS). These results are interpreted in terms of a modulation of saccade inhibition to the contralateral visual field due to the disruption of processing across the frontal eye fields. Our study demonstrates for the first time the feasibility of using FUS stimulation to causally modulate behavior in the awake nonhuman primate brain. This result supports the use of this approach to study brain function. Neurostimulation with ultrasound could be used for exploratory and therapeutic purposes noninvasively, with potentially unprecedented spatial resolution. |
R. Becket Ebitz; Karli K. Watson; Michael L. Platt Oxytocin blunts social vigilance in the rhesus macaque Journal Article In: Proceedings of the National Academy of Sciences, vol. 110, no. 28, pp. 11630–11635, 2013. @article{Ebitz2013,Exogenous application of the neuromodulatory hormone oxytocin (OT) promotes prosocial behavior and can improve social function. It is unclear, however, whether OT promotes prosocial behavior per se, or whether it facilitates social interaction by reducing a state of vigilance toward potential social threats. To disambiguate these two possibilities, we exogenously delivered OT to male rhesus macaques, which have a characteristic pattern of species-typical social vigilance, and examined their performance in three social attention tasks. We first determined that, in the absence of competing task demands or goals, OT increased attention to faces and eyes, as in humans. By contrast, OT reduced species typical social vigilance for unfamiliar, dominant, and emotional faces in two additional tasks. OT eliminated the emergence of a typical state of vigilance when dominant face images were available during a social image choice task. Moreover, OT improved performance on a reward-guided saccade task, despite salient social distractors: OT reduced the interference of unfamiliar faces, particularly emotional ones, when these faces were task irrelevant. Together, these results demonstrate that OT suppresses vigilance toward potential social threats in the rhesus macaque. We hypothesize that a basic role for OT in regulating social vigilance may have facilitated the evolution of prosocial behaviors in humans. |
Christopher D. Fiorillo; Minryung R. Song; Sora R. Yun Multiphasic temporal dynamics in responses of midbrain dopamine neurons to appetitive and aversive stimuli Journal Article In: Journal of Neuroscience, vol. 33, no. 11, pp. 4710–4725, 2013. @article{Fiorillo2013,The transient response of dopamine neurons has been described as reward prediction error (RPE), with activation or suppression by events that are better or worse than expected, respectively. However, at least a minority of neurons are activated by aversive or high-intensity stimuli, casting doubt on the generality of RPE in describing the dopamine signal. To overcome limitations of previous studies, we studied neuronal responses to a wider variety of high-intensity and aversive stimuli, and we quantified and controlled aversiveness through a choice task in which macaques sacrificed juice to avoid aversive stimuli. Whereas most previous work has portrayed the RPE as a single impulse or "phase," here we demonstrate its multiphasic temporal dynamics. Aversive or high-intensity stimuli evoked a triphasic sequence of activation-suppression-activation extending over a period of 40-700 ms. The initial activation at short latencies (40-120 ms) reflected sensory intensity. The influence of motivational value became dominant between 150 and 250 ms, with activation in the case of appetitive stimuli, and suppression in the case of aversive and neutral stimuli. The previously unreported late activation appeared to be a modest "rebound" after strong suppression. Similarly, strong activation by reward was often followed by suppression. We suggest that these "rebounds" may result from overcompensation by homeostatic mechanisms in some cells. Our results are consistent with a realistic RPE, which evolves over time through a dynamic balance of excitation and inhibition. |
Christopher D. Fiorillo; Sora R. Yun; Minryung R. Song Diversity and homogeneity in responses of midbrain dopamine neurons Journal Article In: Journal of Neuroscience, vol. 33, no. 11, pp. 4693–4709, 2013. @article{Fiorillo2013a,Dopamine neurons of the ventral midbrain have been found to signal a reward prediction error that can mediate positive reinforcement. Despite the demonstration of modest diversity at the cellular and molecular levels, there has been little analysis of response diversity in behaving animals. Here we examine response diversity in rhesus macaques to appetitive, aversive, and neutral stimuli having relative motivational values that were measured and controlled through a choice task. First, consistent with previous studies, we observed a continuum of response variability and an apparent absence of distinct clusters in scatter plots, suggesting a lack of statistically discrete subpopulations of neurons. Second, we found that a group of " sensitive " neurons tend to be more strongly suppressed by a variety of stimuli and to be more strongly activated by juice. Third, neurons in the " ventral tier " of substantia nigra were found to have greater suppression, and a subset of these had higher baseline firing rates and late " rebound " activation after suppression. These neurons could belong to a previously identified subgroup of dopamine neurons that express high levels of H-type cation channels but lack calbindin. Fourth, neurons further rostral exhibited greater suppression. Fifth, although we observed weak activation of some neurons by aversive stimuli, this was not associated with their aversiveness. In conclusion, we find a diversity of response properties, distributed along a continuum, within what may be a single functional population of neurons signaling reward prediction error. |
Benjamin Y. Hayden; Jack L. Gallant Working memory and decision processes in visual area V4 Journal Article In: Frontiers in Neuroscience, vol. 7, pp. 18, 2013. @article{Hayden2013,Recognizing and responding to a remembered stimulus requires the coordination of perception, working memory and decision-making. To investigate the role of visual cortex in these processes, we recorded responses of single V4 neurons during performance of a delayed match-to-sample task that incorporates rapid serial visual presentation of natural images. We found that neuronal activity during the delay period after the cue but before the images depends on the identity of the remembered image and that this change persists while distractors appear. This persistent response modulation has been identified as a diagnostic criterion for putative working memory signals; our data thus suggest that working memory may involve reactivation of sensory neurons. When the remembered image reappears in the neuron's receptive field, visually evoked responses are enhanced; this match enhancement is a diagnostic criterion for decision. One model that predicts these data is the matched filter hypothesis, which holds that during search V4 neurons change their tuning so as to match the remembered cue, and thus become detectors for that image. More generally, these results suggest that V4 neurons participate in the perceptual, working memory and decision processes that are needed to perform memory-guided decision-making. |
Sarah R. Heilbronner; Michael L. Platt Causal evidence of performance monitoring by neurons in posterior cingulate cortex during learning Journal Article In: Neuron, vol. 80, no. 6, pp. 1384–1391, 2013. @article{Heilbronner2013,The posterior cingulate cortex (CGp) is a major hub of the default mode network (DMN), a set of cortical areas with high resting activity that declines during task performance. This relationship suggests that DMN activity contributes to mental processes that are antagonistic to performance. Alternatively, DMN may detect conditions under which performance is poor and marshal cognitive resources for improvement. To test this idea, we recorded activity of CGp neurons in monkeys performing a learning task while varying reward size and novelty. We found that CGp neurons responded to errors, and this activity was magnified by small reward and novel stimuli. Inactivating CGp with muscimol impaired new learning when rewards were small but had no effect when rewards were large; inactivation did not affect performance on well-learned associations. Thus, CGp, and by extension the DMN, may support learning, and possibly other cognitive processes, by monitoring performance and motivating exploration. |
Mark M. G. Walton; Seiji Ono; Michael J. Mustari Stimulation of pontine reticular formation in monkeys with strabismus Journal Article In: Investigative Ophthalmology & Visual Science, vol. 54, no. 10, pp. 7125–7136, 2013. @article{Walton2013,PURPOSE: Saccade disconjugacy in strabismus could result from any of a number of factors, including abnormalities of eye muscles, the plant, motoneurons, near response cells, or atypical tuning of neurons in saccade-related areas of the brain. This study was designed to investigate the possibility that saccade disconjugacy in strabismus is associated with abnormalities in paramedian pontine reticular formation (PPRF). METHODS: We applied microstimulation to 22 sites in PPRF and 20 sites in abducens nucleus in three rhesus macaque monkeys (one normal, one esotrope, and one exotrope). RESULTS: When mean velocity was compared between the two eyes, a slight difference was found for 1/5 sites in the normal animal. Significant differences were found for 5/6 sites in an esotrope and 10/11 sites in an exotrope. For five sites in the strabismic monkeys, the directions of evoked movements differed by more than 40° between the two eyes. When stimulation was applied to abducens nucleus (20 sites), the ipsilateral eye moved faster for 4/6 sites in the normal animal and all nine sites in the esotrope. For the exotrope, however, the left eye always moved faster, even for three sites on the right side. For the strabismic animals, stimulation of abducens nucleus often caused a different eye to move faster than stimulation of PPRF. CONCLUSIONS: These data suggest that PPRF is organized at least partly monocularly in strabismus and that disconjugate saccades are at least partly a consequence of unbalanced saccadic commands being sent to the two eyes. |
Wael F. Asaad; Navaneethan Santhanam; Steven McClellan; David J. Freedman High-performance execution of psychophysical tasks with complex visual stimuli in MATLAB Journal Article In: Journal of Neurophysiology, vol. 109, no. 1, pp. 249–260, 2013. @article{Asaad2013,Behavioral, psychological, and physiological experiments often require the ability to present sensory stimuli, monitor and record subjects' responses, interface with a wide range of devices, and precisely control the timing of events within a behavioral task. Here, we describe our recent progress developing an accessible and full-featured software system for controlling such studies using the MATLAB environment. Compared with earlier reports on this software, key new features have been implemented to allow the presentation of more complex visual stimuli, increase temporal precision, and enhance user interaction. These features greatly improve the performance of the system and broaden its applicability to a wider range of possible experiments. This report describes these new features and improvements, current limitations, and quantifies the performance of the system in a real-world experimental setting. |
T. C. Blanchard; John M. Pearson; Benjamin Y. Hayden Postreward delays and systematic biases in measures of animal temporal discounting Journal Article In: Proceedings of the National Academy of Sciences, vol. 110, no. 38, pp. 15491–15496, 2013. @article{Blanchard2013,Intertemporal choice tasks, which pit smaller/sooner rewards against larger/later ones, are frequently used to study time preferences and, by extension, impulsivity and self-control. When used in animals, many trials are strung together in sequence and an adjusting buffer is added after the smaller/sooner option to hold the total duration of each trial constant. Choices of the smaller/sooner option are not reward maximizing and so are taken to indicate that the animal is discounting future rewards. However, if animals fail to correctly factor in the duration of the postreward buffers, putative discounting behavior may instead reflect constrained reward maximization. Here, we report three results consistent with this discounting-free hypothesis. We find that (i) monkeys are insensitive to the association between the duration of postreward delays and their choices; (ii) they are sensitive to the length of postreward delays, although they greatly underestimate them; and (iii) increasing the salience of the postreward delay biases monkeys toward the larger/later option, reducing measured discounting rates. These results are incompatible with standard discounting-based accounts but are compatible with an alternative heuristic model. Our data suggest that measured intertemporal preferences in animals may not reflect impulsivity, or even mental discounting of future options, and that standard human and animal intertemporal choice tasks measure unrelated mental processes. |
Steve W. C. Chang; Jean-François Gariépy; Michael L. Platt Neuronal reference frames for social decisions in primate frontal cortex Journal Article In: Nature Neuroscience, vol. 16, no. 2, pp. 243–250, 2013. @article{Chang2013,Social decisions are crucial for the success of individuals and the groups that they comprise. Group members respond vicariously to benefits obtained by others, and impairments in this capacity contribute to neuropsychiatric disorders such as autism and sociopathy. We examined the manner in which neurons in three frontal cortical areas encoded the outcomes of social decisions as monkeys performed a reward-allocation task. Neurons in the orbitofrontal cortex (OFC) predominantly encoded rewards that were delivered to oneself. Neurons in the anterior cingulate gyrus (ACCg) encoded reward allocations to the other monkey, to oneself or to both. Neurons in the anterior cingulate sulcus (ACCs) signaled reward allocations to the other monkey or to no one. In this network of received (OFC) and foregone (ACCs) reward signaling, ACCg emerged as an important nexus for the computation of shared experience and social reward. Individual and species-specific variations in social decision-making might result from the relative activation and influence of these areas. |
Chih-Yang Chen; Ziad M. Hafed Postmicrosaccadic enhancement of slow eye movements Journal Article In: Journal of Neuroscience, vol. 33, no. 12, pp. 5375–5386, 2013. @article{Chen2013,Active sensation poses unique challenges to sensory systems because moving the sensor necessarily alters the input sensory stream. Sensory input quality is additionally compromised if the sensor moves rapidly, as during rapid eye movements, making the period immediately after the movement critical for recovering reliable sensation. Here, we studied this immediate postmovement interval for the case of microsaccades during fixation, which rapidly jitter the "sensor" exactly when it is being voluntarily stabilized to maintain clear vision. We characterized retinal-image slip in monkeys immediately after microsaccades by analyzing postmovement ocular drifts. We observed enhanced ocular drifts by up to ~28% relative to premicrosaccade levels, and for up to ~50 ms after movement end. Moreover, we used a technique to trigger full-field image motion contingent on real-time microsaccade detection, and we used the initial ocular following response to this motion as a proxy for changes in early visual motion processing caused by microsaccades. When the full-field image motion started during microsaccades, ocular following was strongly suppressed, consistent with detrimental retinal effects of the movements. However, when the motion started after microsaccades, there was up to ~73% increase in ocular following speed, suggesting an enhanced motion sensitivity. These results suggest that the interface between even the smallest possible saccades and "fixation" includes a period of faster than usual image slip, as well as an enhanced responsiveness to image motion, and that both of these phenomena need to be considered when interpreting the pervasive neural and perceptual modulations frequently observed around the time of microsaccades. |
M. Gabriela Costello; Dantong Zhu; Emilio Salinas; Terrence R. Stanford Perceptual modulation of motor-but not visual-responses in the frontal eye field during an urgent-decision task Journal Article In: Journal of Neuroscience, vol. 33, no. 41, pp. 16394–16408, 2013. @article{Costello2013,Neuronal activity in the frontal eye field (FEF) ranges from purely motor (related to saccade production) to purely visual (related to stimulus presence). According to numerous studies, visual responses correlate strongly with early perceptual analysis of the visual scene, including the deployment of spatial attention, whereas motor responses do not. Thus, functionally, the consensus is that visually responsive FEF neurons select a target among visible objects, whereas motor-related neurons plan specific eye movements based on such earlier target selection. However, these conclusions are based on behavioral tasks that themselves promote a serial arrangement of perceptual analysis followed by motor planning. So, is the presumed functional hierarchy in FEF an intrinsic property of its circuitry or does it reflect just one possible mode of operation? We investigate this in monkeys performing a rapid-choice task in which, crucially, motor planning always starts ahead of task-critical perceptual analysis, and the two relevant spatial locations are equally informative and equally likely to be target or distracter. We find that the choice is instantiated in FEF as a competition between oculomotor plans, in agreement with model predictions. Notably, although perception strongly influences the motor neurons, it has little if any measurable impact on the visual cells; more generally, the more dominant the visual response, the weaker the perceptual modulation. The results indicate that, contrary to expectations, during rapid saccadic choices perceptual information may directly modulate ongoing saccadic plans, and this process is not contingent on prior selection of the saccadic goal by visually driven FEF responses. |
2012 |
Ken-ichi Amemori; Ann M. Graybiel Localized microstimulation of primate pregenual cingulate cortex induces negative decision-making Journal Article In: Nature Neuroscience, vol. 15, no. 5, pp. 776–785, 2012. @article{Amemori2012,The pregenual anterior cingulate cortex (pACC) has been implicated in human anxiety disorders and depression, but the circuit-level mechanisms underlying these disorders are unclear. In healthy individuals, the pACC is involved in cost-benefit evaluation. We developed a macaque version of an approach-avoidance decision task used to evaluate anxiety and depression in humans and, with multi-electrode recording and cortical microstimulation, we probed pACC function as monkeys performed this task. We found that the macaque pACC has an opponent process-like organization of neurons representing motivationally positive and negative subjective value. Spatial distribution of these two neuronal populations overlapped in the pACC, except in one subzone, where neurons with negative coding were more numerous. Notably, microstimulation in this subzone, but not elsewhere in the pACC, increased negative decision-making, and this negative biasing was blocked by anti-anxiety drug treatment. This cortical zone could be critical for regulating negative emotional valence and anxiety in decision-making. |
Timothy J. Buschman; Eric L. Denovellis; Cinira Diogo; Daniel Bullock; Earl K. Miller Synchronous oscillatory neural ensembles for rules in the prefrontal cortex Journal Article In: Neuron, vol. 76, no. 4, pp. 838–846, 2012. @article{Buschman2012,Intelligent behavior requires acquiring and following rules. Rules define how our behavior should fit different situations. To understand its neural mechanisms, we simultaneously recorded from multiple electrodes in dorsolateral prefrontal cortex (PFC) while monkeys switched between two rules (respond to color versus orientation). We found evidence that oscillatory synchronization of local field potentials (LFPs) formed neural ensembles representing the rules: there were rule-specific increases in synchrony at " beta" (19-40 Hz) frequencies between electrodes. In addition, individual PFC neurons synchronized to the LFP ensemble corresponding to the current rule (color versus orientation). Furthermore, the ensemble encoding the behaviorally dominant orientation rule showed increased " alpha" (6-16 Hz) synchrony when preparing to apply the alternative (weaker) color rule. This suggests that beta-frequency synchrony selects the relevant rule ensemble, while alpha-frequency synchrony deselects a stronger, but currently irrelevant, ensemble. Synchrony may act to dynamically shape task-relevant neural ensembles out of larger, overlapping circuits. |
Brittany N. Bushnell; Anitha Pasupathy Shape encoding consistency across colors in primate V4 Journal Article In: Journal of Neurophysiology, vol. 108, no. 5, pp. 1299–1308, 2012. @article{Bushnell2012,Neurons in primate cortical area V4 are sensitive to the form and color of visual stimuli. To determine whether form selectivity remains consistent across colors, we studied the responses of single V4 neurons in awake monkeys to a set of two-dimensional shapes presented in two different colors. For each neuron, we chose two colors that were visually distinct and that evoked reliable and different responses. Across neurons, the correlation coefficient between responses in the two colors ranged from -0.03 to 0.93 (median 0.54). Neurons with highly consistent shape responses, i.e., high correlation coefficients, showed greater dispersion in their responses to the different shapes, i.e., greater shape selectivity, and also tended to have less eccentric receptive field locations; among shape-selective neurons, shape consistency ranged from 0.16 to 0.93 (median 0.63). Consistency of shape responses was independent of the physical difference between the stimulus colors used and the strength of neuronal color tuning. Finally, we found that our measurement of shape response consistency was strongly influenced by the number of stimulus repeats: consistency estimates based on fewer than 10 repeats were substantially underestimated. In conclusion, our results suggest that neurons that are likely to contribute to shape perception and discrimination exhibit shape responses that are largely consistent across colors, facilitating the use of simpler algorithms for decoding shape information from V4 neuronal populations. |
X. Cai; Camillo Padoa-Schioppa Neuronal encoding of subjective value in dorsal and ventral anterior cingulate cortex Journal Article In: Journal of Neuroscience, vol. 32, no. 11, pp. 3791–3808, 2012. @article{Cai2012,We examined the activity of individual cells in the primate anterior cingulate cortex during an economic choice task. In the experiments, monkeys chose between different juices offered in variables amounts and subjective values were inferred from the animals' choices. We analyzed neuronal firing rates in relation to a large number of behaviorally relevant variables. We report three main results. First, there were robust differences between the dorsal bank (ACCd) and the ventral bank (ACCv) of the cingulate sulcus. Specifically, neurons in ACCd but not in ACCv were modulated by the movement direction. Furthermore, neurons in ACCd were most active before movement initiation, whereas neurons in ACCv were most active after juice delivery. Second, neurons in both areas encoded the identity and the subjective value of the juice chosen by the animal. In contrast, neither region encoded the value of individual offers. Third, the population of value-encoding neurons in both ACCd and ACCv underwent range adaptation. With respect to economic choice, it is interesting to compare these areas with the orbitofrontal cortex (OFC), previously examined. While neurons in OFC encoded both pre-decision and post-decision variables, neurons in ACCd and ACCv only encoded post-decision variables. Moreover, the encoding of the choice outcome (chosen value and chosen juice) in ACCd and ACCv trailed that found in OFC. These observations indicate that economic decisions (i.e., value comparisons) take place upstream of ACCd and ACCv. The coexistence of choice outcome and movement signals in ACCd suggests that this area constitutes a gateway through which the choice system informs motor systems. |
Steve W. C. Chang; Joseph W. Barter; R. Becket Ebitz; Karli K. Watson; Michael L. Platt Inhaled oxytocin amplifies both vicarious reinforcement and self reinforcement in rhesus macaques (Macaca mulatta) Journal Article In: Proceedings of the National Academy of Sciences, vol. 109, no. 3, pp. 959–964, 2012. @article{Chang2012a,People attend not only to their own experiences, but also to the experiences of those around them. Such social awareness profoundly influences human behavior by enabling observational learning, as well as by motivating cooperation, charity, empathy, and spite. Oxytocin (OT), a neurosecretory hormone synthesized by hypothalamic neurons in the mammalian brain, can enhance affiliation or boost exclusion in different species in distinct contexts, belying any simple mechanistic neural model. Here we show that inhaled OT penetrates the CNS and subsequently enhances the sensitivity of rhesus macaques to rewards occurring to others as well as themselves. Roughly 2 h after inhaling OT, monkeys increased the frequency of prosocial choices associated with reward to another monkey when the alternative was to reward no one. OT also increased attention to the recipient monkey as well as the time it took to render such a decision. In contrast, within the first 2 h following inhalation, OT increased selfish choices associated with delivery of reward to self over a reward to the other monkey, without affecting attention or decision latency. Despite the differences in species typical social behavior, exogenous, inhaled OT causally promotes social donation behavior in rhesus monkeys, as it does in more egalitarian and monogamous ones, like prairie voles and humans, when there is no perceived cost to self. These findings potentially implicate shared neural mechanisms. |
Jan Churan; Daniel Guitton; Christopher C. Pack Perisaccadic remapping and rescaling of visual responses in macaque superior colliculus Journal Article In: PLoS ONE, vol. 7, no. 12, pp. e52195, 2012. @article{Churan2012,Visual neurons have spatial receptive fields that encode the positions of objects relative to the fovea. Because foveate animals execute frequent saccadic eye movements, this position information is constantly changing, even though the visual world is generally stationary. Interestingly, visual receptive fields in many brain regions have been found to exhibit changes in strength, size, or position around the time of each saccade, and these changes have often been suggested to be involved in the maintenance of perceptual stability. Crucial to the circuitry underlying perisaccadic changes in visual receptive fields is the superior colliculus (SC), a brainstem structure responsible for integrating visual and oculomotor signals. In this work we have studied the time-course of receptive field changes in the SC. We find that the distribution of the latencies of SC responses to stimuli placed outside the fixation receptive field is bimodal: The first mode is comprised of early responses that are temporally locked to the onset of the visual probe stimulus and stronger for probes placed closer to the classical receptive field. We suggest that such responses are therefore consistent with a perisaccadic rescaling, or enhancement, of weak visual responses within a fixed spatial receptive field. The second mode is more similar to the remapping that has been reported in the cortex, as responses are time-locked to saccade onset and stronger for stimuli placed in the postsaccadic receptive field location. We suggest that these two temporal phases of spatial updating may represent different sources of input to the SC. |
Maria C. Romero; Ilse C. Van Dromme; Peter Janssen Responses to two-dimensional shapes in the macaque anterior intraparietal area Journal Article In: European Journal of Neuroscience, vol. 36, no. 3, pp. 2324–2334, 2012. @article{Romero2012,Neurons in the macaque dorsal visual stream respond to the visual presentation of objects in the context of a grasping task and to three-dimensional (3D) surfaces defined by binocular disparity, but little is known about the neural representation of two-dimensional (2D) shape in the dorsal stream. We recorded the activity of single neurons in the macaque anterior intraparietal area (AIP), which is known to be crucial for grasping, during the presentation of images of objects and silhouette, outline and line-drawing versions of these images (contour stimuli). The vast majority of AIP neurons responding selectively to 2D images were also selective for at least one of the contour stimuli with the same boundary shape, suggesting that the boundary is sufficient for the image selectivity of most AIP neurons. Furthermore, a subset of these neurons with foveal receptive fields generally preserved the shape preference across positions, whereas for more than half of the AIP population the center of the receptive field was at a parafoveal location with less tolerance to changes in stimulus position. AIP neurons frequently exhibited shape selectivity across different stimulus sizes. These results demonstrate that AIP neurons encode not only 3D but also 2D shape features. |
Octavio Ruiz; Michael A. Paradiso Macaque V1 representations in natural and reduced visual contexts: Spatial and temporal properties and influence of saccadic eye movements Journal Article In: Journal of Neurophysiology, vol. 108, no. 1, pp. 324–333, 2012. @article{Ruiz2012,Vision in natural situations is different from the paradigms generally used to study vision in the laboratory. In natural vision, stimuli usually appear in a receptive field as the result of saccadic eye movements rather than suddenly flashing into view. The stimuli themselves are rich with meaningful and recognizable objects rather than simple abstract patterns. In this study we examined the sensitivity of neurons in macaque area V1 to saccades and to complex background contexts. Using a variety of visual conditions, we find that natural visual response patterns are unique. Compared with standard laboratory situations, in more natural vision V1 responses have longer latency, slower time course, delayed orientation selectivity, higher peak selectivity, and lower amplitude. Furthermore, the influences of saccades and background type (complex picture vs. uniform gray) interact to give a distinctive, and presumably more natural, response pattern. While in most of the experiments natural images were used as background, we find that similar synthetic unnatural background stimuli produce nearly identical responses (i.e., complexity matters more than "naturalness"). These findings have important implications for our understanding of vision in more natural situations. They suggest that with the saccades used to explore complex images, visual context ("surround effects") would have a far greater effect on perception than in standard experiments with stimuli flashed on a uniform background. Perceptual thresholds for contrast and orientation should also be significantly different in more natural situations. |
NaYoung So; Veit Stuphorn Supplementary eye field encodes reward prediction error Journal Article In: Journal of Neuroscience, vol. 32, no. 9, pp. 2950–2963, 2012. @article{So2012,The outcomes of many decisions are uncertain and therefore need to be evaluated. We studied this evaluation process by recording neuronal activity in the supplementary eye field (SEF) during an oculomotor gambling task. While the monkeys awaited the outcome, SEF neurons represented attributes of the chosen option, namely, its expected value and the uncertainty of this value signal. After the gamble result was revealed, a number of neurons reflected the actual reward outcome. Other neurons evaluated the outcome by encoding the difference between the reward expectation represented during the delay period and the actual reward amount (i.e., the reward prediction error). Thus, SEF encodes not only reward prediction error but also all the components necessary for its computation: the expected and the actual outcome. This suggests that SEF might actively evaluate value-based decisions in the oculomotor domain, independent of other brain regions. |
Sruthi K. Swaminathan; David J. Freedman Preferential encoding of visual categories in parietal cortex compared with prefrontal cortex Journal Article In: Nature Neuroscience, vol. 15, no. 2, pp. 315–320, 2012. @article{Swaminathan2012,The ability to recognize the behavioral relevance, or category membership, of sensory stimuli is critical for interpreting the meaning of events in our environment. Neurophysiological studies of visual categorization have found categorical representations of stimuli in prefrontal cortex (PFC), an area that is closely associated with cognitive and executive functions. Recent studies have also identified neuronal category signals in parietal areas that are typically associated with visual-spatial processing. It has been proposed that category-related signals in parietal cortex and other visual areas may result from 'top-down' feedback from PFC. We directly compared neuronal activity in the lateral intraparietal (LIP) area and PFC in monkeys performing a visual motion categorization task. We found that LIP showed stronger, more reliable and shorter latency category signals than PFC. These findings suggest that LIP is strongly involved in visual categorization and argue against the idea that parietal category signals arise as a result of feedback from PFC during this task. |
Tom Theys; Siddharth Srivastava; Johannes Loon; Jan Goffin; Peter Janssen Selectivity for three-dimensional contours and surfaces in the anterior intraparietal area Journal Article In: Journal of Neurophysiology, vol. 107, no. 3, pp. 995–1008, 2012. @article{Theys2012,The macaque anterior intraparietal area (AIP) is crucial for visually guided grasping. AIP neurons respond during the visual presentation of real-world objects and encode the depth profile of disparity-defined curved surfaces. We investigated the neural representation of curved surfaces in AIP using a stimulus-reduction approach. The stimuli consisted of three-dimensional (3-D) shapes curved along the horizontal axis, the vertical axis, or both the horizontal and the vertical axes of the shape. The depth profile was defined solely by binocular disparity that varied along either the boundary or the surface of the shape or along both the boundary and the surface of the shape. The majority of AIP neurons were selective for curved boundaries along the horizontal or the vertical axis, and neural selectivity emerged at short latencies. Stimuli in which disparity varied only along the surface of the shape (with zero disparity on the boundaries) evoked selectivity in a smaller proportion of AIP neurons and at considerably longer latencies. AIP neurons were not selective for 3-D surfaces composed of anticorrelated disparities. Thus the neural selectivity for object depth profile in AIP is present when only the boundary is curved in depth, but not for disparity in anticorrelated stereograms. |
Patrick J. Mineault; Farhan A. Khawaja; Daniel A. Butts; Christopher C. Pack Hierarchical processing of complex motion along the primate dorsal visual pathway Journal Article In: Proceedings of the National Academy of Sciences, vol. 109, no. 16, pp. E972–E980, 2012. @article{Mineault2012,Neurons in the medial superior temporal (MST) area of the primate visual cortex respond selectively to complex motion patterns defined by expansion, rotation, and deformation. Consequently they are often hypothesized to be involved in important behavioral functions, such as encoding the velocities of moving objects and surfaces relative to the observer. However, the computations underlying such selectivity are unknown. In this work we have developed a unique, naturalistic motion stimulus and used it to probe the complex selectivity of MST neurons. The resulting data were then used to estimate the properties of the feed-forward inputs to each neuron. This analysis yielded models that successfully accounted for much of the observed stimulus selectivity, provided that the inputs were combined via a nonlinear integration mechanism that approximates a multiplicative interaction among MST inputs. In simulations we found that this type of integration has the functional role of improving estimates of the 3D velocity of moving objects. As this computation is of general utility for detecting complex stimulus features, we suggest that it may represent a fundamental aspect of hierarchical sensory processing. |
Ryan E. B. Mruczek; David L. Sheinberg Stimulus selectivity and response latency in putative inhibitory and excitatory neurons of the primate inferior temporal cortex Journal Article In: Journal of Neurophysiology, vol. 108, no. 10, pp. 2725–2736, 2012. @article{Mruczek2012,The cerebral cortex is composed of many distinct classes of neurons. Numerous studies have demonstrated corresponding differences in neuronal properties across cell types, but these comparisons have largely been limited to conditions outside of awake, behaving animals. Thus the functional role of the various cell types is not well understood. Here, we investigate differences in the functional properties of two widespread and broad classes of cells in inferior temporal cortex of macaque monkeys: inhibitory interneurons and excitatory projection cells. Cells were classified as putative inhibitory or putative excitatory neurons on the basis of their extracellular waveform characteristics (e.g., spike duration). Consistent with previous intracellular recordings in cortical slices, putative inhibitory neurons had higher spontaneous firing rates and higher stimulus-evoked firing rates than putative excitatory neurons. Additionally, putative excitatory neurons were more susceptible to spike waveform adaptation following very short interspike intervals. Finally, we compared two functional properties of each neuron's stimulus-evoked response: stimulus selectivity and response latency. First, putative excitatory neurons showed stronger stimulus selectivity compared with putative inhibitory neurons. Second, putative inhibitory neurons had shorter response latencies compared with putative excitatory neurons. Selectivity differences were maintained and latency differences were enhanced during a visual search task emulating more natural viewing conditions. Our results suggest that short-latency inhibitory responses are likely to sculpt visual processing in excitatory neurons, yielding a sparser visual representation. |
Ioan Opris; Robert E. Hampson; Greg A. Gerhardt; Theodore W. Berger; Sam A. Deadwyler Columnar processing in primate pFC: Evidence for executive control microcircuits Journal Article In: Journal of Cognitive Neuroscience, vol. 24, no. 12, pp. 2334–2347, 2012. @article{Opris2012,A common denominator for many cognitive disorders of human brain is the disruption of neural activity within pFC, whose structural basis is primarily interlaminar (columnar) microcircuits or "minicolumns." The importance of this brain region for executive decision-making has been well documented; however, because of technological constraints, the minicolumnar basis is not well understood. Here, via implementation of a unique conformal multielectrode recording array, the role of interlaminar pFC minicolumns in the executive control of task-related target selection is demonstrated in nonhuman primates performing a visuomotor DMS task. The results reveal target-specific, interlaminar correlated firing during the decision phase of the trial between multielectrode recording array-isolated minicolumnar pairs of neurons located in parallel in layers 2/3 and layer 5 of pFC. The functional significance of individual pFC minicolumns (separated by 40 μm) was shown by reduced correlated firing between cell pairs within single minicolumns on error trials with inappropriate target selection. To further demonstrate dependence on performance, a task-disrupting drug (cocaine) was administered in the middle of the session, which also reduced interlaminar firing in minicolumns that fired appropriately in the early (nondrug) portion of the session. The results provide a direct demonstration of task-specific, real-time columnar processing in pFC indicating the role of this type of microcircuit in executive control of decision-making in primate brain. |
Jessica M. Phillips; Stefan Everling Neural activity in the macaque putamen associated with saccades and behavioral outcome Journal Article In: PLoS ONE, vol. 7, no. 12, pp. e51596, 2012. @article{Phillips2012,It is now widely accepted that the basal ganglia nuclei form segregated, parallel loops with neocortical areas. The prevalent view is that the putamen is part of the motor loop, which receives inputs from sensorimotor areas, whereas the caudate, which receives inputs from frontal cortical eye fields and projects via the substantia nigra pars reticulata to the superior colliculus, belongs to the oculomotor loop. Tracer studies in monkeys and functional neuroimaging studies in human subjects, however, also suggest a potential role for the putamen in oculomotor control. To investigate the role of the putamen in saccadic eye movements, we recorded single neuron activity in the caudal putamen of two rhesus monkeys while they alternated between short blocks of pro- and anti-saccades. In each trial, the instruction cue was provided after the onset of the peripheral stimulus, thus the monkeys could either generate an immediate response to the stimulus based on the internal representation of the rule from the previous trial, or alternatively, could await the visual rule-instruction cue to guide their saccadic response. We found that a subset of putamen neurons showed saccade-related activity, that the preparatory mode (internally- versus externally-cued) influenced the expression of task-selectivity in roughly one third of the task-modulated neurons, and further that a large proportion of neurons encoded the outcome of the saccade. These results suggest that the caudal putamen may be part of the neural network for goal-directed saccades, wherein the monitoring of saccadic eye movements, context and performance feedback may be processed together to ensure optimal behavioural performance and outcomes are achieved during ongoing behaviour. |
Elsie Premereur; Wim Vanduffel; Peter Janssen Local field potential activity associated with temporal expectations in the macaque lateral intraparietal area Journal Article In: Journal of Cognitive Neuroscience, vol. 24, no. 6, pp. 1314–1330, 2012. @article{Premereur2012,Oscillatory brain activity is attracting increasing interest in cognitive neuroscience. Numerous EEG (magnetoencephalography) and local field potential (LFP) measurements have related cognitive functions to different types of brain oscillations, but the functional significance of these rhythms remains poorly understood. Despite its proven value, LFP activity has not been extensively tested in the macaque lateral intraparietal area (LIP), which has been implicated in a wide variety of cognitive control processes. We recorded action potentials and LFPs in area LIP during delayed eye movement tasks and during a passive fixation task, in which the time schedule was fixed so that temporal expectations about task-relevant cues could be formed. LFP responses in the gamma band discriminated reliably between saccade targets and distractors inside the receptive field (RF). Alpha and beta responses were much less strongly affected by the presence of a saccade target, however, but rose sharply in the waiting period before the go signal. Surprisingly, conditions without visual stimulation of the LIP-RF-evoked robust LFP responses in every frequency band—most prominently in those below 50 Hz—precisely time-locked to the expected time of stimulus onset in the RF. These results indicate that in area LIP, oscillations in the LFP, which reflect synaptic input and local network activity, are tightly coupled to the temporal expectation of task-relevant cues. |
Elsie Premereur; Wim Vanduffel; Pieter R. Roelfsema; Peter Janssen Frontal eye field microstimulation induces task-dependent gamma oscillations in the lateral intraparietal area Journal Article In: Journal of Neurophysiology, vol. 108, no. 5, pp. 1392–1402, 2012. @article{Premereur2012a,Macaque frontal eye fields (FEF) and the lateral intraparietal area (LIP) are high-level oculomotor control centers that have been implicated in the allocation of spatial attention. Electrical microstimulation of macaque FEF elicits functional magnetic resonance imaging (fMRI) activations in area LIP, but no study has yet investigated the effect of FEF microstimulation on LIP at the single-cell or local field potential (LFP) level. We recorded spiking and LFP activity in area LIP during weak, subthreshold microstimulation of the FEF in a delayed-saccade task. FEF microstimulation caused a highly time- and frequency-specific, task-dependent increase in gamma power in retinotopically corresponding sites in LIP: FEF microstimulation produced a significant increase in LIP gamma power when a saccade target appeared and remained present in the LIP receptive field (RF), whereas less specific increases in alpha power were evoked by FEF microstimulation for saccades directed away from the RF. Stimulating FEF with weak currents had no effect on LIP spike rates or on the gamma power during memory saccades or passive fixation. These results provide the first evidence for task-dependent modulations of LFPs in LIP caused by top-down stimulation of FEF. Since the allocation and disengagement of spatial attention in visual cortex have been associated with increases in gamma and alpha power, respectively, the effects of FEF microstimulation on LIP are consistent with the known effects of spatial attention. |
M. Victoria Puig; Earl K. Miller The role of prefrontal dopamine D1 receptors in the neural mechanisms of associative learning Journal Article In: Neuron, vol. 74, no. 5, pp. 874–886, 2012. @article{Puig2012,Dopamine is thought to play a major role in learning. However, while dopamine D1 receptors (D1Rs) in the prefrontal cortex (PFC) have been shown to modulate working memory-related neural activity, their role in the cellular basis of learning is unknown. We recorded activity from multiple electrodes while injecting the D1R antagonist SCH23390 in the lateral PFC as monkeys learned visuomotor associations. Blocking D1Rs impaired learning of novel associations and decreased cognitive flexibility but spared performance of already familiar associations. This suggests a greater role for prefrontal D1Rs in learning new, rather than performing familiar, associations. There was a corresponding greater decrease in neural selectivity and increase in alpha and beta oscillations in local field potentials for novel than for familiar associations. Our results suggest that weak stimulation of D1Rs observed in aging and psychiatric disorders may impair learning and PFC function by reducing neural selectivity and exacerbating neural oscillations associated with inattention and cognitive deficits. |
Braden A. Purcell; Pauline K. Weigand; Jeffrey D. Schall Supplementary eye field during visual search: Salience, cognitive control, and performance monitoring Journal Article In: Journal of Neuroscience, vol. 32, no. 30, pp. 10273–10285, 2012. @article{Purcell2012,How supplementary eye field (SEF) contributes to visual search is unknown. Inputs from cortical and subcortical structures known to represent visual salience suggest that SEF may serve as an additional node in this network. This hypothesis was tested by recording action potentials and local field potentials (LFPs) in two monkeys performing an efficient pop-out visual search task. Target selection modulation, tuning width, and response magnitude of spikes and LFP in SEF were compared with those in frontal eye field. Surprisingly, only ~2% of SEF neurons and ~8% of SEF LFP sites selected the location of the search target. The absence of salience in SEF may be due to an absence of appropriate visual afferents, which suggests that these inputs are a necessary anatomical feature of areas representing salience. We also tested whether SEF contributes to overcoming the automatic tendency to respond to a primed color when the target identity switches during priming of pop-out. Very few SEF neurons or LFP sites modulated in association with performance deficits following target switches. However, a subset of SEF neurons and LFPs exhibited strong modulation following erroneous saccades to a distractor. Altogether, these results suggest that SEF plays a limited role in controlling ongoing visual search behavior, but may play a larger role in monitoring search performance. |
Robert M. G. Reinhart; Richard P. Heitz; Braden A. Purcell; Pauline K. Weigand; Jeffrey D. Schall; Geoffrey F. Woodman Homologous mechanisms of visuospatial working memory maintenance in macaque and human: Properties and sources Journal Article In: Journal of Neuroscience, vol. 32, no. 22, pp. 7711–7722, 2012. @article{Reinhart2012,Although areas of frontal cortex are thought to be critical for maintaining information in visuospatial working memory, the event-related potential (ERP) index of maintenance is found over posterior cortex in humans. In the present study, we reconcile these seemingly contradictory findings. Here, we show that macaque monkeys and humans exhibit the same posterior ERP signature of working memory maintenance that predicts the precision of the memory-based behavioral responses. In addition, we show that the specific pattern of rhythmic oscillations in the alpha band, recently demonstrated to underlie the human visual working memory ERP component, is also present in monkeys. Next, we concurrently recorded intracranial local field potentials from two prefrontal and another frontal cortical area to determine their contribution to the surface potential indexing maintenance. The local fields in the two prefrontal areas, but not the cortex immediately posterior, exhibited amplitude modulations, timing, and relationships to behavior indicating that they contribute to the generation of the surface ERP component measured from the distal posterior electrodes. Rhythmic neural activity in the theta and gamma bands during maintenance provided converging support for the engagement of the same brain regions. These findings demonstrate that nonhuman primates have homologous electrophysiological signatures of visuospatial working memory to those of humans and that a distributed neural network, including frontal areas, underlies the posterior ERP index of visuospatial working memory maintenance. |
Daniel L. Kimmel; Dagem Mammo; William T. Newsome Tracking the eye non-invasively: Simultaneous comparison of the scleral search coil and optical tracking techniques in the macaque monkey Journal Article In: Frontiers in Behavioral Neuroscience, vol. 6, pp. 49, 2012. @article{Kimmel2012,From human perception to primate neurophysiology, monitoring eye position is critical to the study of vision, attention, oculomotor control, and behavior. Two principal techniques for the precise measurement of eye position-the long-standing sclera-embedded search coil and more recent optical tracking techniques-are in use in various laboratories, but no published study compares the performance of the two methods simultaneously in the same primates. Here we compare two popular systems-a sclera-embedded search coil from C-N-C Engineering and the EyeLink 1000 optical system from SR Research-by recording simultaneously from the same eye in the macaque monkey while the animal performed a simple oculomotor task. We found broad agreement between the two systems, particularly in positional accuracy during fixation, measurement of saccade amplitude, detection of fixational saccades, and sensitivity to subtle changes in eye position from trial to trial. Nonetheless, certain discrepancies persist, particularly elevated saccade peak velocities, post-saccadic ringing, influence of luminance change on reported position, and greater sample-to-sample variation in the optical system. Our study shows that optical performance now rivals that of the search coil, rendering optical systems appropriate for many if not most applications. This finding is consequential, especially for animal subjects, because the optical systems do not require invasive surgery for implantation and repair of search coils around the eye. Our data also allow laboratories using the optical system in human subjects to assess the strengths and limitations of the technique for their own applications. |
P. Christiaan Klink; Anna Oleksiak; Martin J. Lankheet; Richard J. A. Wezel Intermittent stimulus presentation stabilizes neuronal responses in macaque area MT Journal Article In: Journal of Neurophysiology, vol. 108, no. 8, pp. 2101–2114, 2012. @article{Klink2012,Repeated stimulation impacts neuronal responses. Here we show how response characteristics of sensory neurons in macaque visual cortex are influenced by the duration of the interruptions during intermittent stimulus presentation. Besides effects on response magnitude consistent with neuronal ad- aptation, the response variability was also systematically influenced. Spike rate variability in motion-sensitive area MT decreased when interruption durations were systematically increased from 250 to 2,000 ms. Activity fluctuations between subsequent trials and Fano factors over full response sequences were both lower with longer interruptions, while spike timing patterns became more regular. These variability changes partially depended on the response magnitude, but another significant effect that was uncorrelated with adaptation-in- duced changes in response magnitude was also present. Reduced response variability was furthermore accompanied by changes in spike-field coherence, pointing to the possibility that reduced spiking variability results from interactions in the local cortical network. While neuronal response stabilization may be a general effect of repeated sensory stimulation, we discuss its potential link with the phenomenon of perceptual stabilization of ambiguous stimuli as a result of interrupted presentation. |
Anders Ledberg; Anna Montagnini; Richard Coppola; Steven L. Bressler Reduced variability of ongoing and evoked cortical activity leads to improved behavioral performance Journal Article In: PLoS ONE, vol. 7, no. 8, pp. e43166, 2012. @article{Ledberg2012,Sensory responses of the brain are known to be highly variable, but the origin and functional relevance of this variability have long remained enigmatic. Using the variable foreperiod of a visual discrimination task to assess variability in the primate cerebral cortex, we report that visual evoked response variability is not only tied to variability in ongoing cortical activity, but also predicts mean response time. We used cortical local field potentials, simultaneously recorded from widespread cortical areas, to gauge both ongoing and visually evoked activity. Trial-to-trial variability of sensory evoked responses was strongly modulated by foreperiod duration and correlated both with the cortical variability before stimulus onset as well as with response times. In a separate set of experiments we probed the relation between small saccadic eye movements, foreperiod duration and manual response times. The rate of eye movements was modulated by foreperiod duration and eye position variability was positively correlated with response times. Our results indicate that when the time of a sensory stimulus is predictable, reduction in cortical variability before the stimulus can improve normal behavioral function that depends on the stimulus. |
Kyoung-Min Lee; Kyung-Ha Ahn; Edward L. Keller Saccade generation by the frontal eye fields in Rhesus monkeys is separable from visual detection and bottom-up attention shift Journal Article In: PLoS ONE, vol. 7, no. 6, pp. e39886, 2012. @article{Lee2012a,The frontal eye fields (FEF), originally identified as an oculomotor cortex, have also been implicated in perceptual functions, such as constructing a visual saliency map and shifting visual attention. Further dissecting the area's role in the transformation from visual input to oculomotor command has been difficult because of spatial confounding between stimuli and responses and consequently between intermediate cognitive processes, such as attention shift and saccade preparation. Here we developed two tasks in which the visual stimulus and the saccade response were dissociated in space (the extended memory-guided saccade task), and bottom-up attention shift and saccade target selection were independent (the four-alternative delayed saccade task). Reversible inactivation of the FEF in rhesus monkeys disrupted, as expected, contralateral memory-guided saccades, but visual detection was demonstrated to be intact at the same field. Moreover, saccade behavior was impaired when a bottom-up shift of attention was not a prerequisite for saccade target selection, indicating that the inactivation effect was independent of the previously reported dysfunctions in bottom-up attention control. These findings underscore the motor aspect of the area's functions, especially in situations where saccades are generated by internal cognitive processes, including visual short-term memory and long-term associative memory. |
Bram-Ernst Verhoef; Rufin Vogels; Peter Janssen Inferotemporal cortex subserves three-dimensional structure categorization Journal Article In: Neuron, vol. 73, no. 1, pp. 171–182, 2012. @article{Verhoef2012,We perceive real-world objects as three-dimensional (3D), yet it is unknown which brain area underlies our ability to perceive objects in this way. The macaque inferotemporal (IT) cortex contains neurons that respond selectively to 3D structures defined by binocular disparity. To examine the causal role of IT in the categorization of 3D structures, we electrically stimulated clusters of IT neurons with a similar 3D-structure preference while monkeys performed a 3D-structure categorization task. Microstimulation of 3D-structure-selective IT clusters caused monkeys to choose the preferred structure of the 3D-structure-selective neurons considerably more often. Microstimulation in IT also accelerated the monkeys' choice for the preferred structure, while delaying choices corresponding to the nonpreferred structure of a given site. These findings reveal that 3D-structure-selective neurons in IT contribute to the categorization of 3D objects. How and where 3D shape perception arises from neuronal activity of neurons remains an unanswered question. Verhoef etal. find that manipulating the activity of neurons in the temporal lobe can influence the performance of monkeys performing a 3D shape categorization task. |
Chin-An Wang; Susan E. Boehnke; Brian J. White; Douglas P. Munoz Microstimulation of the monkey superior colliculus induces pupil dilation without evoking saccades Journal Article In: Journal of Neuroscience, vol. 32, no. 11, pp. 3629–3636, 2012. @article{Wang2012c,The orienting reflex is initiated by a salient stimulus and facilitates quick, appropriate action. It involves a rapid shift of the eyes, head, and attention and other physiological responses such as changes in heart rate and transient pupil dilation. The SC is a critical structure in the midbrain that selects incoming stimuli based on saliency and relevance to coordinate orienting behaviors, particularly gaze shifts, but its causal role in pupil dilation remains poorly understood in mammals. Here, we examined the role of the primate SC in the control of pupil dynamics. While requiring monkeys to keep their gaze fixed, we delivered weak electrical microstimulation to the SC, so that saccadic eye movements were not evoked. Pupil size increased transiently after microstimulation of the intermediate SC layers (SCi) and the size of evoked pupil dilation was larger on a dim versus bright background. In contrast, microstimulation of the superficial SC layers did not cause pupil dilation. Thus, the SCi is directly involved not only in shifts of gaze and attention, but also in pupil dilation as part of the orienting reflex, and the function of pupil dilation may be related to increasing visual sensitivity. The shared neural mechanisms suggest that pupil dilation may be associated with covert attention. |
Karli K. Watson; Michael L. Platt Social signals in primate orbitofrontal cortex Journal Article In: Current Biology, vol. 22, no. 23, pp. 2268–2273, 2012. @article{Watson2012,Primate evolution produced an increased capacity to respond flexibly to varying social contexts as well as expansion of the prefrontal cortex [1, 2]. Despite this association, how prefrontal neurons respond to social information remains virtually unknown. People with damage to their orbitofrontal cortex (OFC) struggle to recognize facial expressions [3, 4], make poor social judgments [5, 6], and frequently make social faux pas [7, 8]. Here we test explicitly whether neurons in primate OFC signal social information and, if so, how such signals compare with responses to primary fluid rewards. We find that OFC neurons distinguish images that belong to socially defined categories, such as female perinea and faces, as well as the social dominance of those faces. These modulations signaled both how much monkeys valued these pictures and their interest in continuing to view them. Far more neurons signaled social category than signaled fluid value, despite the stronger impact of fluid reward on monkeys' choices. These findings indicate that OFC represents both the motivational value and attentional priority of other individuals, thus contributing to both the acquisition of information about others and subsequent social decisions. Our results betray a fundamental disconnect between preferences expressed through overt choice, which were primarily driven by the desire for more fluid, and preferential neuronal processing, which favored social computations. |
Luke Woloszyn; David L. Sheinberg Effects of long-term visual experience on responses of distinct classes of single units in inferior temporal cortex Journal Article In: Neuron, vol. 74, no. 1, pp. 193–205, 2012. @article{Woloszyn2012,Primates can learn to recognize a virtually limitless number of visual objects. A candidate neural substrate for this adult plasticity is the inferior temporal cortex (ITC). Using a large stimulus set, we explored the impact that long-term experience has on the response properties of two classes of neurons in ITC: broad-spiking (putative excitatory) cells and narrow-spiking (putative inhibitory) cells. We found that experience increased maximum responses of putative excitatory neurons but had the opposite effect on maximum responses of putative inhibitory neurons, an observation that helps to reconcile contradictory reports regarding the presence and direction of this effect. In addition, we found that experience reduced the average stimulus-evoked response in both cell classes, but this decrease was much more pronounced in putative inhibitory units. This latter finding supports a potentially critical role of inhibitory neurons in detecting and initiating the cascade of events underlying adult neural plasticity in ITC. Woloszyn and Sheinberg show that long-term visual experience enhances activity of putative excitatory neurons in inferior temporal cortex but decreases global activity of putative inhibitory neurons. These findings help reconcile conflicting views of the influence of visual experience on activity in IT cortex. |
Kyoko Yoshida; Nobuhito Saito; Atsushi Iriki; Masaki Isoda Social error monitoring in macaque frontal cortex Journal Article In: Nature Neuroscience, vol. 15, no. 9, pp. 1307–1312, 2012. @article{Yoshida2012,Although much learning occurs through direct experience of errors, humans and other animals can learn from the errors of other individuals. The medial frontal cortex (MFC) processes self-generated errors, but the neuronal architecture and mechanisms underlying the monitoring of others' errors are poorly understood. Exploring such mechanisms is important, as they underlie observational learning and allow adaptive behavior in uncertain social environments. Using two paired monkeys that monitored each other's action for their own action selection, we identified a group of neurons in the MFC that exhibited a substantial activity increase that was associated with another's errors. Nearly half of these neurons showed activity changes consistent with general reward-omission signals, whereas the remaining neurons specifically responded to another's erroneous actions. These findings indicate that the MFC contains a dedicated circuit for monitoring others' mistakes during social interactions. |
Heng Zou; Hermann J. Muller; Zhuanghua Shi Non-spatial sounds regulate eye movements and enhance visual search Journal Article In: Journal of Vision, vol. 12, no. 5, pp. 2–2, 2012. @article{Zou2012,Spatially uninformative sounds can enhance visual search when the sounds are synchronized with color changes of the visual target, a phenomenon referred to as "pip-and-pop" effect (van der Burg, Olivers, Bronkhorst, & Theeuwes, 2008). The present study investigated the relationship of this effect to changes in oculomotor scanning behavior induced by the sounds. The results revealed sound events to increase fixation durations upon their occurrence and to decrease the mean number of saccades. More specifically, spatially uninformative sounds facilitated the orientation of ocular scanning away from already scanned display regions not containing a target (Experiment 1) and enhanced search performance even on target-absent trials (Experiment 2). Facilitation was also observed when the sounds were presented 100 ms prior to the target or at random (Experiment 3). These findings suggest that non-spatial sounds cause a general freezing effect on oculomotor scanning behavior, an effect which in turn benefits visual search performance by temporally and spatially extended information sampling. |
T. S. Davis; R. A. Parker; Paul A. House; E. Bagley; S. Wendelken; R. A. Normann; Bradley Greger Spatial and temporal characteristics of V1 microstimulation during chronic implantation of a microelectrode array in a behaving macaque Journal Article In: Journal of Neural Engineering, vol. 9, no. 6, pp. 1–12, 2012. @article{Davis2012,OBJECTIVE: It has been hypothesized that a vision prosthesis capable of evoking useful visual percepts can be based upon electrically stimulating the primary visual cortex (V1) of a blind human subject via penetrating microelectrode arrays. As a continuation of earlier work, we examined several spatial and temporal characteristics of V1 microstimulation. APPROACH: An array of 100 penetrating microelectrodes was chronically implanted in V1 of a behaving macaque monkey. Microstimulation thresholds were measured using a two-alternative forced choice detection task. Relative locations of electrically-evoked percepts were measured using a memory saccade-to-target task. MAIN RESULTS: The principal finding was that two years after implantation we were able to evoke behavioural responses to electric stimulation across the spatial extent of the array using groups of contiguous electrodes. Consistent responses to stimulation were evoked at an average threshold current per electrode of 204 ± 49 µA (mean ± std) for groups of four electrodes and 91 ± 25 µA for groups of nine electrodes. Saccades to electrically-evoked percepts using groups of nine electrodes showed that the animal could discriminate spatially distinct percepts with groups having an average separation of 1.6 ± 0.3 mm (mean ± std) in cortex and 1.0° ± 0.2° in visual space. Significance. These results demonstrate chronic perceptual functionality and provide evidence for the feasibility of a cortically-based vision prosthesis for the blind using penetrating microelectrodes. |
Sarah L. Eagleman; Valentin Dragoi Image sequence reactivation in awake V4 networks Journal Article In: Proceedings of the National Academy of Sciences, vol. 109, no. 47, pp. 19450–19455, 2012. @article{Eagleman2012,In the absence of sensory input, neuronal networks are far from being silent. Whether spontaneous changes in ongoing activity reflect previous sensory experience or stochastic fluctuations in brain activity is not well understood. Here we describe reactivation of stimulus-evoked activity in awake visual cortical networks. We found that continuous exposure to randomly flashed image sequences induces reactivation in macaque V4 cortical networks in the absence of visual stimulation. This reactivation of previously evoked activity is stimulus-specific, occurs only in the same temporal order as the original response, and strengthens with increased stimulus exposures. Importantly, cells exhibiting significant reactivation carry more information about the stimulus than cells that do not reactivate. These results demonstrate a surprising degree of experience-dependent plasticity in visual cortical networks as a result of repeated exposure to unattended information. We suggest that awake reactivation in visual cortex may underlie perceptual learning by passive stimulus exposure. |
Bryan J. Hansen; Mircea I. Chelaru; Valentin Dragoi Correlated variability in laminar cortical circuits Journal Article In: Neuron, vol. 76, no. 3, pp. 590–602, 2012. @article{Hansen2012,Despite the fact that strong trial-to-trial correlated variability in responses has been reported in many cortical areas, recent evidence suggests that neuronal correlations are much lower than previously thought. Here, we used multicontact laminar probes to revisit the issue of correlated variability in primary visual (V1) cortical circuits. We found that correlations between neurons depend strongly on local network context-whereas neurons in the input (granular) layers showed virtually no correlated variability, neurons in the output layers (supragranular and infragranular) exhibited strong correlations. The laminar dependence of noise correlations is consistent with recurrent models in which neurons in the granular layer receive intracortical inputs from nearby cells, whereas supragranular and infragranular layer neurons receive inputs over larger distances. Contrary to expectation that the output cortical layers encode stimulus information most accurately, we found that the input network offers superior discrimination performance compared to the output networks. |
Elias B. Issa; James J. DiCarlo Precedence of the eye region in neural processing of faces Journal Article In: Journal of Neuroscience, vol. 32, no. 47, pp. 16666–16682, 2012. @article{Issa2012,Functional magnetic resonance imaging (fMRI) has revealed multiple subregions in monkey inferior temporal cortex (IT) that are selective for images of faces over other objects. The earliest of these subregions, the posterior lateral face patch (PL), has not been studied previously at the neurophysiological level. Perhaps not surprisingly, we found that PL contains a high concentration of "face-selective" cells when tested with standard image sets comparable to those used previously to define the region at the level of fMRI. However, we here report that several different image sets and analytical approaches converge to show that nearly all face-selective PL cells are driven by the presence of a single eye in the context of a face outline. Most strikingly, images containing only an eye, even when incorrectly positioned in an outline, drove neurons nearly as well as full-face images, and face images lacking only this feature led to longer latency responses. Thus, bottom-up face processing is relatively local and linearly integrates features-consistent with parts-based models-grounding investigation of how the presence of a face is first inferred in the IT face processing hierarchy. |
2011 |
C. D. Fiorillo Transient activation of midbrain dopamine neurons by reward risk Journal Article In: Neuroscience, vol. 197, pp. 162–171, 2011. @article{Fiorillo2011,Dopamine neurons of the ventral midbrain are activated transiently following stimuli that predict future reward. This response has been shown to signal the expected value of future reward, and there is strong evidence that it drives positive reinforcement of stimuli and actions associated with reward in accord with reinforcement learning models. Behavior is also influenced by reward uncertainty, or risk, but it is not known whether the transient response of dopamine neurons is sensitive to reward risk. To investigate this, monkeys were trained to associate distinct visual stimuli with certain or uncertain volumes of juice of nearly the same expected value. In a choice task, monkeys preferred the stimulus predicting an uncertain (risky) reward outcome. In a Pavlovian task, in which the neuronal responses to each stimulus could be measured in isolation, it was found that dopamine neurons were more strongly activated by the stimulus associated with reward risk. Given extensive evidence that dopamine drives reinforcement, these results strongly suggest that dopamine neurons can reinforce risk-seeking behavior (gambling), at least under certain conditions. Risk-seeking behavior has the virtue of promoting exploration and learning, and these results support the hypothesis that dopamine neurons represent the value of exploration. |
Davis M. Glasser; James M. G. Tsui; Christopher C. Pack; Duje Tadin Perceptual and neural consequences of rapid motion adaptation Journal Article In: Proceedings of the National Academy of Sciences, vol. 108, no. 45, pp. E1080–E1088, 2011. @article{Glasser2011,Nervous systems adapt to the prevailing sensory environment, and the consequences of this adaptation can be observed in the responses of single neurons and in perception. Given the variety of timescales underlying events in the natural world, determining the temporal characteristics of adaptation is important to understanding how perception adjusts to its sensory environment. Previous work has shown that neural adaptation can occur on a timescale of milliseconds, but perceptual adaptation has generally been studied over relatively long timescales, typically on the order of seconds. This disparity raises important questions. Can perceptual adaptation be observed at brief, functionally relevant timescales? And if so, how do its properties relate to the rapid adaptation seen in cortical neurons? We address these questions in the context of visual motion processing, a perceptual modality characterized by rapid temporal dynamics. We demonstrate objectively that 25 ms of motion adaptation is sufficient to generate a motion aftereffect, an illusory sensation of movement experienced when a moving stimulus is replaced by a stationary pattern. This rapid adaptation occurs regardless of whether the adapting motion is perceived. In neurophysiological recordings from the middle temporal area of primate visual cortex, we find that brief motion adaptation evokes direction-selective responses to subsequently presented stationary stimuli. A simple model shows that these neural responses can explain the consequences of rapid perceptual adaptation. Overall, we show that the motion aftereffect is not merely an intriguing perceptual illusion, but rather a reflection of rapid neural and perceptual processes that can occur essentially every time we experience motion. |
Till S. Hartmann; Frank Bremmer; Thomas D. Albright; Bart Krekelberg Receptive field positions in area MT during slow eye movements Journal Article In: Journal of Neuroscience, vol. 31, no. 29, pp. 10437–10444, 2011. @article{Hartmann2011,Perceptual stability requires the integration of information across eye movements. We first tested the hypothesis that motion signals are integrated by neurons whose receptive fields (RFs) do not move with the eye but stay fixed in the world. Specifically, we measured the RF properties of neurons in the middle temporal area (MT) of macaques (Macaca mulatta) during the slow phase of optokinetic nystagmus. Using a novel method to estimate RF locations for both spikes and local field potentials, we found that the location on the retina that changed spike rates or local field potentials did not change with eye position; RFs moved with the eye. Second, we tested the hypothesis that neurons link information across eye positions by remapping the retinal location of their RFs to future locations. To test this, we compared RF locations during leftward and rightward slow phases of optokinetic nystagmus. We found no evidence for remapping during slow eye movements; the RF location was not affected by eye-movement direction. Together, our results show that RFs of MT neurons and the aggregate activity reflected in local field potentials are yoked to the eye during slow eye movements. This implies that individual MT neurons do not integrate sensory information from a single position in the world across eye movements. Future research will have to determine whether such integration, and the construction of perceptual stability, takes place in the form of a distributed population code in eye-centered visual cortex or is deferred to downstream areas. |
Benjamin Y. Hayden; Sarah R. Heilbronner; John M. Pearson; Michael L. Platt Surprise signals in anterior cingulate cortex: Neuronal encoding of unsigned reward prediction errors driving adjustment in behavior Journal Article In: Journal of Neuroscience, vol. 31, no. 11, pp. 4178–4187, 2011. @article{Hayden2011,In attentional models of learning, associations between actions and subsequent rewards are stronger when outcomes are surprising, regardless of their valence. Despite the behavioral evidence that surprising outcomes drive learning, neural correlates of unsigned reward prediction errors remain elusive. Here we show that in a probabilistic choice task, trial-to-trial variations in preference track outcome surprisingness. Concordant with this behavioral pattern, responses of neurons in macaque (Macaca mulatta) dorsal anterior cingulate cortex (dACC) to both large and small rewards were enhanced when the outcome was surprising. Moreover, when, on some trials, probabilities were hidden, neuronal responses to rewards were reduced, consistent with the idea that the absence of clear expectations diminishes surprise. These patterns are inconsistent with the idea that dACC neurons track signed errors in reward prediction, as dopamine neurons do. Our results also indicate that dACC neurons do not signal conflict. In the context of other studies of dACC function, these results suggest a link between reward-related modulations in dACC activity and attention and motor control processes involved in behavioral adjustment. More speculatively, these data point to a harmonious integration between reward and learning accounts of ACC function on one hand, and attention and cognitive control accounts on the other. |
Benjamin Y. Hayden; John M. Pearson; Michael L. Platt Neuronal basis of sequential foraging decisions in a patchy environment Journal Article In: Nature Neuroscience, vol. 14, no. 7, pp. 933–939, 2011. @article{Hayden2011a,Deciding when to leave a depleting resource to exploit another is a fundamental problem for all decision makers. The neuronal mechanisms mediating patch-leaving decisions remain unknown. We found that neurons in primate (Macaca mulatta) dorsal anterior cingulate cortex, an area that is linked to reward monitoring and executive control, encode a decision variable signaling the relative value of leaving a depleting resource for a new one. Neurons fired during each sequential decision to stay in a patch and, for each travel time, these responses reached a fixed threshold for patch-leaving. Longer travel times reduced the gain of neural responses for choosing to stay in a patch and increased the firing rate threshold mandating patch-leaving. These modulations more closely matched behavioral decisions than any single task variable. These findings portend an understanding of the neural basis of foraging decisions and endorse the unification of theoretical and experimental work in ecology and neuroscience. |
Sarah R. Heilbronner; Benjamin Y. Hayden; Michael L. Platt Decision salience signals in posterior cingulate cortex Journal Article In: Frontiers in Neuroscience, vol. 5, pp. 55, 2011. @article{Heilbronner2011,Despite its phylogenetic antiquity and clinical importance, the posterior cingulate cortex (CGp) remains an enigmatic nexus of attention, memory, motivation, and decision making. Here we show that CGp neurons track decision salience - the degree to which an option differs from a standard - but not the subjective value of a decision. To do this, we recorded the spiking activity of CGp neurons in monkeys choosing between options varying in reward-related risk, delay to reward, and social outcomes, each of which varied in level of decision salience. Firing rates were higher when monkeys chose the risky option, consistent with their risk-seeking preferences, but were also higher when monkeys chose the delayed and social options, contradicting their preferences. Thus, across decision contexts, neuronal activity was uncorrelated with how much monkeys valued a given option, as inferred from choice. Instead, neuronal activity signaled the deviation of the chosen option from the standard, independently of how it differed. The observed decision salience signals suggest a role for CGp in the flexible allocation of neural resources to motivationally significant information, akin to the role of attention in selective processing of sensory inputs. |
David M. Milstein; Michael C. Dorris The relationship between saccadic choice and reaction times with manipulations of target value Journal Article In: Frontiers in Neuroscience, vol. 5, pp. 122, 2011. @article{Milstein2011,Choosing the option with the highest expected value (EV; reward probability × reward magnitude) maximizes the intake of reward under conditions of uncertainty. However, human economic choices indicate that our value calculation has a subjective component whereby probability and reward magnitude are not linearly weighted. Using a similar economic framework, our goal was to characterize how subjective value influences the generation of simple motor actions. Specifically, we hypothesized that attributes of saccadic eye movements could provide insight into how rhesus monkeys, a well-studied animal model in cognitive neuroscience, subjectively value potential visual targets. In the first experiment, monkeys were free to choose by directing a saccade toward one of two simultaneously displayed targets, each of which had an uncertain outcome. In this task, choices were more likely to be allocated toward the higher valued target. In the second experiment, only one of the two possible targets appeared on each trial. In this task, saccadic reaction times (SRTs) decreased toward the higher valued target. Reward magnitude had a much stronger influence on both choices and SRTs than probability, whose effect was observed only when reward magnitude was similar for both targets. Across EV blocks, a strong relationship was observed between choice preferences and SRTs. However, choices tended to maximize at skewed values whereas SRTs varied more continuously. Lastly, SRTs were unchanged when all reward magnitudes were 1×, 1.5×, and 2× their normal amount, indicating that saccade preparation was influenced by the relative value of the targets rather than the absolute value of any single-target. We conclude that value is not only an important factor( )for deliberative decision making in primates, but also for the selection and preparation of simple motor actions, such as saccadic eye movements. More precisely, our results indicate that, under conditions of uncertainty, saccade choices and reaction times are influenced by the relative expected subjective value of potential movements. |
Robert Niebergall; Paul S. Khayat; Stefan Treue; Julio C. Martinez-Trujillo Multifocal attention filters targets from distracters within and beyond primate mt neurons' receptive field boundaries Journal Article In: Neuron, vol. 72, no. 6, pp. 1067–1079, 2011. @article{Niebergall2011,Visual attention has been classically described as a spotlight that enhances the processing of a behaviorally relevant object. However, in many situations, humans and animals must simultaneously attend to several relevant objects separated by distracters. To account for this ability, various models of attention have been proposed including splitting of the attentional spotlight into multiple foci, zooming of the spotlight over a region of space, and switching of the spotlight among objects. We investigated this controversial issue by recording neuronal activity in visual area MT of two macaques while they attended to two translating objects that circumvented a third distracter object located inside the neurons' receptive field. We found that when the attended objects passed through or nearby the receptive field, neuronal responses to the distracter were either decreased or remained unaltered. These results demonstrate that attention can split into multiple spotlights corresponding to relevant objects while filtering out interspersed distracters. |
Robert Niebergall; Paul S. Khayat; Stefan Treue; Julio C. Martinez-Trujillo Expansion of MT neurons excitatory receptive fields during covert attentive tracking Journal Article In: Journal of Neuroscience, vol. 31, no. 43, pp. 15499–15510, 2011. @article{Niebergall2011a,Primates can attentively track moving objects while keeping gaze stationary. The neural mechanisms underlying this ability are poorly understood. We investigated this issue by recording responses of neurons in area MT of two rhesus monkeys while they performed two different tasks. During the Attend-Fixation task, two moving random dot patterns (RDPs) translated across a screen at the same speed and in the same direction while the animals directed gaze to a fixation spot and detected a change in its luminance. During the Tracking task, the animals kept gaze on the fixation spot and attentively tracked the two RDPs to report a change in the local speed of one of the patterns' dots. In both conditions, neuronal responses progressively increased as the RDPs entered the neurons' receptive field (RF), peaked when they reached its center, and decreased as they translated away. This response profile was well described by a Gaussian function with its center of gravity indicating the RF center and its flanks the RF excitatory borders. During Tracking, responses were increased relative to Attend-Fixation, causing the Gaussian profiles to expand. Such increases were proportionally larger in the RF periphery than at its center, and were accompanied by a decrease in the trial-to-trial response variability (Fano factor) relative to Attend-Fixation. These changes resulted in an increase in the neurons' performance at detecting targets at longer distances from the RF center. Our results show that attentive tracking dynamically changes MT neurons' RF profiles, ultimately improving the neurons' ability to encode the tracked stimulus features. |
Shinji Nishimoto; Jack L. Gallant A three-dimensional spatiotemporal receptive field model explains responses of area MT neurons to naturalistic movies Journal Article In: Journal of Neuroscience, vol. 31, no. 41, pp. 14551–14564, 2011. @article{Nishimoto2011,Area MT has been an important target for studies of motion processing. However, previous neurophysiological studies of MT have used simple stimuli that do not contain many of the motion signals that occur during natural vision. In this study we sought to determine whether views of area MT neurons developed using simple stimuli can account for MT responses under more naturalistic conditions. We recorded responses from macaque area MT neurons during stimulation with naturalistic movies. We then used a quantitative modeling framework to discover which specific mechanisms best predict neuronal responses under these challenging conditions. We find that the simplest model that accurately predicts responses of MT neurons consists of a bank of V1-like filters, each followed by a compressive nonlinearity, a divisive nonlinearity, and linear pooling. Inspection of the fit models shows that the excitatory receptive fields of MT neurons tend to lie on a single plane within the three-dimensional spatiotemporal frequency domain, and suppressive receptive fields lie off this plane. However, most excitatory receptive fields form a partial ring in the plane and avoid low temporal frequencies. This receptive field organization ensures that most MT neurons are tuned for velocity but do not tend to respond to ambiguous static textures that are aligned with the direction of motion. In sum, MT responses to naturalistic movies are largely consistent with predictions based on simple stimuli. However, models fit using naturalistic stimuli reveal several novel properties of MT receptive fields that had not been shown in prior experiments. |
Anna Oleksiak; P. Christiaan Klink; Albert Postma; Ineke J. M. Ham; Martin J. Lankheet; Richard J. A. Wezel Spatial summation in macaque parietal area 7a follows a winner-take-all rule Journal Article In: Journal of Neurophysiology, vol. 105, no. 3, pp. 1150–1158, 2011. @article{Oleksiak2011,While neurons in posterior parietal cortex have been found to signal the presence of a salient stimulus among multiple items in a display, spatial summation within their receptive field in the absence of an attentional bias has never been investigated. This information, however, is indispensable when one investigates the mechanisms of spatial attention and competition between multiple visual objects. To examine the spatial summation rule in parietal area 7a neurons, we trained rhesus monkeys to fixate on a central cross while two identical stimuli were briefly displayed in a neuron's receptive field. The response to a pair of dots was compared with the responses to the same dots when they were presented individually. The scaling and power parameters of a generalized summation algorithm varied greatly, both across neurons and across combinations of stimulus locations. However, the averaged response of the recorded population of 7a neurons was consistent with a winner-take-all rule for spatial summation. A control experiment where a monkey covertly attended to both stimuli simultaneously suggests that attention introduces additional competition by facilitating the less optimal stimulus. Thus an averaging stage is introduced between ∼ 200 and 300 ms of the response to a pair of stimuli. In short, the summation algorithm over the population of area 7a neurons carries the signature of a winner-take-all operation, with spatial attention possibly influencing the temporal dynamics of stimulus competition, that is the moment that the "winner" takes "victory" over the "loser" stimulus. |
Elsie Premereur; Wim Vanduffel; Peter Janssen Functional heterogeneity of macaque lateral intraparietal neurons Journal Article In: Journal of Neuroscience, vol. 31, no. 34, pp. 12307–12317, 2011. @article{Premereur2011,The macaque lateral intraparietal area (LIP) has been implicated in manycognitive processes, ranging from saccade planning and spatial attention to timing and categorization. Importantly, different research groups have used different criteria for including LIP neurons in their studies. While some research groups have selected LIP neurons based on the presence of memory-delay activity, other research groups have used other criteria such as visual, presaccadic, and/or memory activity. We recorded from LIP neurons that were selected based on spatially selective saccadic activity but regardless ofmemory-delay activity in macaque monkeys. To test anticipatory climbing activity, we used a delayed visually guided saccade task with a unimodal schedule ofgo-times, for which the conditional probability that the go-signal will occur rises monotonically as a function of time. A subpopulation of LIP neurons showed anticipatory activity that mimicked the subjective hazard rate ofthe go-signal when the animal was planning a saccade toward the receptive field. Alarge subgroup ofLIP neurons, however, did not modulate their firing rates according to the subjective hazard function. These non-anticipatory neurons were strongly influenced by salient visual stimuli appearing in their receptive field, but less so by the direction ofthe impending saccade. Thus, LIP contains a heterogeneous population ofneurons related to saccade planning or visual salience, and these neurons are spatially intermixed.Our results suggest that between-study differences in neuronal selectionmayhave contributed significantly to the findings of different research groups with respect to the functional role ofarea LIP. |
Narcisse P. Bichot; Matthew T. Heard; Robert Desimone Stimulation of the nucleus accumbens as behavioral reward in awake behaving monkeys Journal Article In: Journal of Neuroscience Methods, vol. 199, no. 2, pp. 265–272, 2011. @article{Bichot2011,It has been known that monkeys will repeatedly press a bar for electrical stimulation in several different brain structures. We explored the possibility of using electrical stimulation in one such structure, the nucleus accumbens, as a substitute for liquid reward in animals performing a complex task, namely visual search. The animals had full access to water in the cage at all times on days when stimulation was used to motivate them. Electrical stimulation was delivered bilaterally at mirror locations in and around the accumbens, and the animals' motivation to work for electrical stimulation was quantified by the number of trials they performed correctly per unit of time. Acute mapping revealed that stimulation over a large area successfully supported behavioral performance during the task. Performance improved with increasing currents until it reached an asymptotic, theoretically maximal level. Moreover, stimulation with chronically implanted electrodes showed that an animal's motivation to work for electrical stimulation was at least equivalent to, and often better than, when it worked for liquid reward while on water control. These results suggest that electrical stimulation in the accumbens is a viable method of reward in complex tasks. Because this method of reward does not necessitate control over water or food intake, it may offer an alternative to the traditional liquid or food rewards in monkeys, depending on the goals and requirements of the particular research project. |
Brittany N. Bushnell; Philip J. Harding; Yoshito Kosai; Wyeth Bair; Anitha Pasupathy Equiluminance cells in visual cortical area V4 Journal Article In: Journal of Neuroscience, vol. 31, no. 35, pp. 12398–12412, 2011. @article{Bushnell2011,We report a novel class of V4 neuron in the macaque monkey that responds selectively to equiluminant colored form. These "equiluminance" cells stand apart because they violate the well established trend throughout the visual system that responses are minimal at low luminance contrast and grow and saturate as contrast increases. Equiluminance cells, which compose ∼22% of V4, exhibit the opposite behavior: responses are greatest near zero contrast and decrease as contrast increases. While equiluminance cells respond preferentially to equiluminant colored stimuli, strong hue tuning is not their distinguishing feature-some equiluminance cells do exhibit strong unimodal hue tuning, but many show little or no tuning for hue. We find that equiluminance cells are color and shape selective to a degree comparable with other classes of V4 cells with more conventional contrast response functions. Those more conventional cells respond equally well to achromatic luminance and equiluminant color stimuli, analogous to color luminance cells described in V1. The existence of equiluminance cells, which have not been reported in V1 or V2, suggests that chromatically defined boundaries and shapes are given special status in V4 and raises the possibility that form at equiluminance and form at higher contrasts are processed in separate channels in V4. |
Brittany N. Bushnell; Philip J. Harding; Yoshito Kosai; Anitha Pasupathy Partial occlusion modulates contour-based shape encoding in primate area V4 Journal Article In: Journal of Neuroscience, vol. 31, no. 11, pp. 4012–4024, 2011. @article{Bushnell2011a,Past studies of shape coding in visual cortical area V4 have demonstrated that neurons can accurately represent isolated shapes in terms of their component contour features. However, rich natural scenes contain many partially occluded objects, which have "accidental" contours at the junction between the occluded and occluding objects. These contours do not represent the true shape of the occluded object and are known to be perceptually discounted. To discover whether V4 neurons differentially encode accidental contours, we studied the responses of single neurons in fixating monkeys to complex shapes and contextual stimuli presented either in isolation or adjoining each other to provide a percept of partial occlusion. Responses to preferred contours were suppressed when the adjoining context rendered those contours accidental. The observed suppression was reversed when the partial occlusion percept was compromised by introducing a small gap between the component stimuli. Control experiments demonstrated that these results likely depend on contour geometry at T-junctions and cannot be attributed to mechanisms based solely on local color/luminance contrast, spatial proximity of stimuli, or the spatial frequency content of images. Our findings provide novel insights into how occluded objects, which are fundamental to complex visual scenes, are encoded in area V4. They also raise the possibility that the weakened encoding of accidental contours at the junction between objects could mark the first step of image segmentation along the ventral visual pathway. |
Steve W. C. Chang; Amy A. Winecoff; Michael L. Platt Vicarious reinforcement in rhesus macaques (Macaca mulatta) Journal Article In: Frontiers in Neuroscience, vol. 5, pp. 27, 2011. @article{Chang2011,What happens to others profoundly influences our own behavior. Such other-regarding outcomes can drive observational learning, as well as motivate cooperation, charity, empathy, and even spite. Vicarious reinforcement may serve as one of the critical mechanisms mediating the influence of other-regarding outcomes on behavior and decision-making in groups. Here we show that rhesus macaques spontaneously derive vicarious reinforcement from observing rewards given to another monkey, and that this reinforcement can motivate them to subsequently deliver or withhold rewards from the other animal. We exploited Pavlovian and instrumental conditioning to associate rewards to self (M1) and/or rewards to another monkey (M2) with visual cues. M1s made more errors in the instrumental trials when cues predicted reward to M2 compared to when cues predicted reward to M1, but made even more errors when cues predicted reward to no one. In subsequent preference tests between pairs of conditioned cues, M1s preferred cues paired with reward to M2 over cues paired with reward to no one. By contrast, M1s preferred cues paired with reward to self over cues paired with reward to both monkeys simultaneously. Rates of attention to M2 strongly predicted the strength and valence of vicarious reinforcement. These patterns of behavior, which were absent in non-social control trials, are consistent with vicarious reinforcement based upon sensitivity to observed, or counterfactual, outcomes with respect to another individual. Vicarious reward may play a critical role in shaping cooperation and competition, as well as motivating observational learning and group coordination in rhesus macaques, much as it does in humans. We propose that vicarious reinforcement signals mediate these behaviors via homologous neural circuits involved in reinforcement learning and decision-making. |
Jan Churan; Daniel Guitton; Christopher C. Pack Context dependence of receptive field remapping in superior colliculus Journal Article In: Journal of Neurophysiology, vol. 106, no. 4, pp. 1862–1874, 2011. @article{Churan2011,Our perception of the positions of objects in our surroundings is surprisingly unaffected by movements of the eyes, head, and body. This suggests that the brain has a mechanism for maintaining perceptual stability, based either on the spatial relationships among visible objects or internal copies of its own motor commands. Strong evidence for the latter mechanism comes from the remapping of visual receptive fields that occurs around the time of a saccade. Remapping occurs when a single neuron responds to visual stimuli placed presaccadically in the spatial location that will be occupied by its receptive field after the completion of a saccade. Although evidence for remapping has been found in many brain areas, relatively little is known about how it interacts with sensory context. This interaction is important for understanding perceptual stability more generally, as the brain may rely on extraretinal signals or visual signals to different degrees in different contexts. Here, we have studied the interaction between visual stimulation and remapping by recording from single neurons in the superior colliculus of the macaque monkey, using several different visual stimulus conditions. We find that remapping responses are highly sensitive to low-level visual signals, with the overall luminance of the visual background exerting a particularly powerful influence. Specifically, although remapping was fairly common in complete darkness, such responses were usually decreased or abolished in the presence of modest background illumination. Thus the brain might make use of a strategy that emphasizes visual landmarks over extraretinal signals whenever the former are available. |
Adam J. Sachs; Paul S. Khayat; Robert Niebergall; Julio C. Martinez-Trujillo A metric-based analysis of the contribution of spike timing to contrast and motion direction coding by single neurons in macaque area MT Journal Article In: Brain Research, vol. 1368, pp. 163–184, 2011. @article{Sachs2011,Spike timing is thought to contribute to the coding of motion direction information by neurons in macaque area MT. Here, we examined whether spike timing also contributes to the coding of stimulus contrast. We applied a metric-based approach to spike trains fired by MT neurons in response to stimuli that varied in contrast, or direction. We assessed the performance of three metrics, Dspikeand Dproduct(containing spike count and timing information), and the spike count metric Dcount. We analyzed responses elicited during the first 200 msec of stimulus presentation from 205 neurons. For both contrast and direction, the large majority of neurons showed the highest mutual information using Dspike, followed by Dproduct, and Dcount. This was corroborated by the performance of a theoretical observer model at discriminating contrast and direction using the three metrics. Our results demonstrate that spike timing can contribute to contrast coding in MT neurons, and support previous reports of its potential contribution to direction coding. Furthermore, they suggest that a combination of spike count with periodic and non-periodic spike timing information (contained in Dspike, but not in Dproductand Dcountwhich are insensitive to spike counts and timing respectively) provides the largest coding advantage in spike trains fired by MT neurons during contrast and direction discrimination. |
Navid G. Sadeghi; Vani Pariyadath; Sameer Apte; David M. Eagleman; Erik P. Cook Neural correlates of subsecond time distortion in the middle temporal area of visual cortex Journal Article In: Journal of Cognitive Neuroscience, vol. 23, no. 12, pp. 3829–3840, 2011. @article{Sadeghi2011,How does the brain represent the passage of time at the subsecond scale? Although different conceptual models for time perception have been proposed, its neurophysiological basis remains unknown. We took advantage of a visual duration illusion produced by stimulus novelty to link changes in cortical activity in monkeys with distortions of duration perception in humans. We found that human subjects perceived the duration of a subsecond motion pulse with a novel direction longer than a motion pulse with a repeated direction. Recording from monkeys viewing identical motion stimuli but performing a different behavioral task, we found that both the duration and amplitude of the neural response in the middle temporal area of visual cortex were positively correlated with the degree of novelty of the motion direction. In contrast to previous accounts that attribute distortions in duration perception to changes in the speed of a putative internal clock, our results suggest that the known adaptive properties of neural activity in visual cortex contributes to subsecond temporal distortions. |
Swetha Shankar; Dino P. Massoglia; Dantong Zhu; M. Gabriela Costello; Terrence R. Stanford; Emilio Salinas Tracking the temporal evolution of a perceptual judgment using a compelled-response task Journal Article In: Journal of Neuroscience, vol. 31, no. 23, pp. 8406–8421, 2011. @article{Shankar2011,Choice behavior and its neural correlates have been intensely studied with tasks in which a subject makes a perceptual judgment and indicates the result with a motor action. Yet a question crucial for relating behavior to neural activity remains unresolved: what fraction of a subject's reaction time (RT) is devoted to the perceptual evaluation step, as opposed to executing the motor report? Making such timing measurements accurately is complicated because RTs reflect both sensory and motor processing, and because speed and accuracy may be traded. To overcome these problems, we designed the compelled-saccade task, a two-alternative forced-choice task in which the instruction to initiate a saccade precedes the appearance of the relevant sensory information. With this paradigm, it is possible to track perceptual performance as a function of the amount of time during which sensory information is available to influence a subject's choice. The result-the tachometric curve-directly reveals a subject's perceptual processing capacity independently of motor demands. Psychophysical data, together with modeling and computer-simulation results, reveal that task performance depends on three separable components: the timing of the motor responses, the speed of the perceptual evaluation, and additional cognitive factors. Each can vary quickly, from one trial to the next, or can show stable, longer-term changes. This novel dissociation between sensory and motor processes yields a precise metric of how perceptual capacity varies under various experimental conditions and serves to interpret choice-related neuronal activity as perceptual, motor, or both. |
Joo-Hyun Song; Robert D. Rafal; Robert M. McPeek Deficits in reach target selection during inactivation of the midbrain superior colliculus Journal Article In: Proceedings of the National Academy of Sciences, vol. 108, no. 51, pp. E1433–E1440, 2011. @article{Song2011,Purposive action requires the selection of a single movement goal from multiple possibilities. Neural structures involved in movement planning and execution often exhibit activity related to target selection. A key question is whether this activity is specific to the type of movement produced by the structure, perhaps consisting of a competition among effector-specific movement plans, or whether it constitutes a more abstract, effector-independent selection signal. Here, we show that temporary focal inactivation of the primate superior colliculus (SC), an area involved in eye-movement target selection and execution, causes striking target selection deficits for reaching movements, which cannot be readily explained as a simple impairment in visual perception or motor execution. This indicates that target selection activity in the SC does not simply represent a competition among eye-movement goals and, instead, suggests that the SC contributes to a more general purpose priority map that influences target selection for other actions, such as reaches. |
K. Torab; T. S. Davis; D. J. Warren; Paul A. House; R. A. Normann; Bradley Greger In: Journal of Neural Engineering, vol. 8, no. 3, pp. 1–13, 2011. @article{Torab2011,We hypothesize that a visual prosthesis capable of evoking high-resolution visual perceptions can be produced using high-electrode-count arrays of penetrating microelectrodes implanted into the primary visual cortex of a blind human subject. To explore this hypothesis, and as a prelude to human psychophysical experiments, we have conducted a set of experiments in primary visual cortex (V1) of non-human primates using chronically implanted Utah Electrode Arrays (UEAs). The electrical and recording properties of implanted electrodes, the high-resolution visuotopic organization of V1, and the stimulation levels required to evoke behavioural responses were measured. The impedances of stimulated electrodes were found to drop significantly immediately following stimulation sessions, but these post-stimulation impedances returned to pre-stimulation values by the next experimental session. Two months of periodic microstimulation at currents of up to 96 µA did not impair the mapping of receptive fields from local field potentials or multi-unit activity, or impact behavioural visual thresholds of light stimuli that excited regions of V1 that were implanted with UEAs. These results demonstrate that microstimulation at the levels used did not cause functional impairment of the electrode array or the neural tissue. However, microstimulation with current levels ranging from 18 to 76 µA (46 ± 19 µA, mean ± std) was able to elicit behavioural responses on eight out of 82 systematically stimulated electrodes. We suggest that the ability of microstimulation to evoke phosphenes and elicit a subsequent behavioural response may depend on several factors: the location of the electrode tips within the cortical layers of V1, distance of the electrode tips to neuronal somata, and the inability of nonhuman primates to recognize and respond to a generalized set of evoked percepts. |
James M. G. Tsui; Christopher C. Pack Contrast sensitivity of MT receptive field centers and surrounds Journal Article In: Journal of Neurophysiology, vol. 106, no. 4, pp. 1888–1900, 2011. @article{Tsui2011,Neurons throughout the visual system have receptive fields with both excitatory and suppressive components. The latter are responsible for a phenomenon known as surround suppression, in which responses decrease as a stimulus is extended beyond a certain size. Previous work has shown that surround suppression in the primary visual cortex depends strongly on stimulus contrast. Such complex center-surround interactions are thought to relate to a variety of functions, although little is known about how they affect responses in the extrastriate visual cortex. We have therefore examined the interaction of center and surround in the middle temporal (MT) area of the macaque (Macaca mulatta) extrastriate cortex by recording neuronal responses to stimuli of different sizes and contrasts. Our findings indicate that surround suppression in MT is highly contrast dependent, with the strongest suppression emerging unexpectedly at intermediate stimulus contrasts. These results can be explained by a simple model that takes into account the nonlinear contrast sensitivity of the neurons that provide input to MT. The model also provides a qualitative link to previous reports of a topographic organization of area MT based on clusters of neurons with differing surround suppression strength. We show that this organization can be detected in the gamma-band local field potentials (LFPs) and that the model parameters can predict the contrast sensitivity of these LFP responses. Overall our results show that surround suppression in area MT is far more common than previously suspected, highlighting the potential functional importance of the accumulation of nonlinearities along the dorsal visual pathway. |
Joris Vangeneugden; Patrick A. De Maziere; Marc M. Van Hulle; Tobias Jaeggli; Luc Van Van Gool; Rufin Vogels Distinct mechanisms for coding of visual actions in macaque temporal cortex Journal Article In: Journal of Neuroscience, vol. 31, no. 2, pp. 385–401, 2011. @article{Vangeneugden2011,Temporal cortical neurons are known to respond to visual dynamic-action displays. Many human psychophysical and functional imaging studies examining biological motion perception have used treadmill walking, in contrast to previous macaque single-cell studies. We assessed the coding of locomotion in rhesus monkey (Macacamulatta) temporal cortex using movies of stationary walkers,varying both form and motion (i.e.,different facing directions) or varying only the frame sequence (i.e.,forward vs backward walking). The majority of superiortemporal sulcus and inferior temporal neurons were selective for facing direction, whereas a minority distinguished forward from backward walking. Support vector machines using the temporal cortical population responses as input classified facing direction well, but forward and backward walking less so. Classification performance for the latter improved markedly when the within-action response modulation was considered, reflecting differences in momentarybody poses within the locomotion sequences. Responses to static pose presentations predicted the responses during the course of the action. Analyses of the responses to walking sequences wherein the start frame was varied across trials showed that some neurons also carried a snapshot sequence signal. Such sequence information was present in neurons that responded to static snapshot presen- tations and in neurons that required motion. Our data suggest that actions area nalyzed by temporal cortical neurons using distinct mechanisms. Most neurons predominantly signal momentary pose. In addition, temporal cortical neurons, including those responding to static pose, are sensitive to pose sequence, which can contribute to the signaling oflearned action sequences. |
B. -E. Verhoef; Rufin Vogels; Peter Janssen Synchronization between the end stages of the dorsal and the ventral visual stream Journal Article In: Journal of Neurophysiology, vol. 105, no. 5, pp. 2030–2042, 2011. @article{Verhoef2011,The end stage areas of the ventral (IT) and the dorsal (AIP) visual streams encode the shape of disparity-defined three-dimensional (3D) surfaces. Recent anatomical tracer studies have found direct reciprocal connections between the 3D-shape selective areas in IT and AIP. Whether these anatomical connections are used to facilitate 3D-shape perception is still unknown. We simultaneously recorded multi-unit activity (MUA) and local field potentials in IT and AIP while monkeys discriminated between concave and convex 3D shapes and measured the degree to which the activity in IT and AIP synchronized during the task. We observed strong beta-band synchronization between IT and AIP preceding stimulus onset that decreased shortly after stimulus onset and became modulated by stereo-signal strength and stimulus contrast during the later portion of the stimulus period. The beta-coherence modulation was unrelated to task-difficulty, regionally specific, and dependent on the MUA selectivity of the pairs of sites under study. The beta-spike-field coherence in AIP predicted the upcoming choice of the monkey. Several convergent lines of evidence suggested AIP as the primary source of the AIP-IT synchronized activity. The synchronized beta activity seemed to occur during perceptual anticipation and when the system has stabilized to a particular perceptual state but not during active visual processing. Our findings demonstrate for the first time that synchronized activity exists between the end stages of the dorsal and ventral stream during 3D-shape discrimination. |
Ye Wang; Bogdan F. Iliescu; Jianfu Ma; Kresimir Josic; Valentin Dragoi Adaptive changes in neuronal synchronization in macaque V4 Journal Article In: Journal of Neuroscience, vol. 31, no. 37, pp. 13204–13213, 2011. @article{Wang2011b,A fundamental property of cortical neurons is the capacity to exhibit adaptive changes or plasticity. Whether adaptive changes in cortical responses are accompanied by changes in synchrony between individual neurons and local population activity in sensory cortex is unclear. This issue is important as synchronized neural activity is hypothesized to play an important role in propagating information in neuronal circuits. Here, we show that rapid adaptation (300 ms) to a stimulus of fixed orientation modulates the strength of oscillatory neuronal synchronization in macaque visual cortex (area V4) and influences the ability of neurons to distinguish small changes in stimulus orientation. Specifically, rapid adaptation increases the synchronization of individual neuronal responses with local population activity in the gamma frequency band (30-80 Hz). In contrast to previous reports that gamma synchronization is associated with an increase in firing rates in V4, we found that the postadaptation increase in gamma synchronization is associated with a decrease in neuronal responses. The increase in gamma-band synchronization after adaptation is functionally significant as it is correlated with an improvement in neuronal orientation discrimination performance. Thus, adaptive synchronization between the spiking activity of individual neurons and their local population can enhance temporally insensitive, rate-based-coding schemes for sensory discrimination. |
Zheng Wang; Anna W. Roe Trial-to-trial noise cancellation of cortical field potentials in awake macaques by autoregression model with exogenous input (ARX) Journal Article In: Journal of Neuroscience Methods, vol. 194, no. 2, pp. 266–273, 2011. @article{Wang2011a,Gamma band synchronization has drawn increasing interest with respect to its potential role in neuronal encoding strategy and behavior in awake, behaving animals. However, contamination of these recordings by power line noise can confound the analysis and interpretation of cortical local field potential (LFP). Existing denoising methods are plagued by inadequate noise reduction, inaccuracies, and even introduction of new noise components. To carefully and more completely remove such contamination, we propose an automatic method based on the concept of adaptive noise cancellation that utilizes the correlative features of common noise sources, and implement with AutoRegressive model with eXogenous Input (ARX). We apply this technique to both simulated data and LFPs recorded in the primary visual cortex of awake macaque monkeys. The analyses here demonstrate a greater degree of accurate noise removal than conventional notch filters. Our method leaves desired signal intact and does not introduce artificial noise components. Application of this method to awake monkey V1 recordings reveals a significant power increase in the gamma range evoked by visual stimulation. Our findings suggest that the ARX denoising procedure will be an important pre-processing step in the analysis of large volumes of cortical LFP data as well as high frequency (gamma-band related) electroencephalography/magnetoencephalography (EEG/MEG) applications, one which will help to convincingly dissociate this notorious artifact from gamma-band activity. |
Ben D. B. Willmore; James A. Mazer; Jack L. Gallant Sparse coding in striate and extrastriate visual cortex Journal Article In: Journal of Neurophysiology, vol. 105, no. 6, pp. 2907–2919, 2011. @article{Willmore2011,Theoretical studies of mammalian cortex argue that efficient neural codes should be sparse. However, theoretical and experimental studies have used different definitions of the term "sparse" leading to three assumptions about the nature of sparse codes. First, codes that have high lifetime sparseness require few action potentials. Second, lifetime-sparse codes are also population-sparse. Third, neural codes are optimized to maximize lifetime sparseness. Here, we examine these assumptions in detail and test their validity in primate visual cortex. We show that lifetime and population sparseness are not necessarily correlated and that a code may have high lifetime sparseness regardless of how many action potentials it uses. We measure lifetime sparseness during presentation of natural images in three areas of macaque visual cortex, V1, V2, and V4. We find that lifetime sparseness does not increase across the visual hierarchy. This suggests that the neural code is not simply optimized to maximize lifetime sparseness. We also find that firing rates during a challenging visual task are higher than theoretical values based on metabolic limits and that responses in V1, V2, and V4 are well-described by exponential distributions. These findings are consistent with the hypothesis that neurons are optimized to maximize information transmission subject to metabolic constraints on mean firing rate. |
Huihui Zhou; Robert Desimone Feature-based attention in the Frontal Eye Field and area V4 during visual search Journal Article In: Neuron, vol. 70, no. 6, pp. 1205–1217, 2011. @article{Zhou2011,When we search for a target in a crowded visual scene, we often use the distinguishing features of the target, such as color or shape, to guide our attention and eye movements. To investigate the neural mechanisms of feature-based attention, we simultaneously recorded neural responses in the frontal eye field (FEF) and area V4 while monkeys performed a visual search task. The responses of cells in both areas were modulated by feature attention, independent of spatial attention, and the magnitude of response enhancement was inversely correlated with the number of saccades needed to find the target. However, an analysis of the latency of sensory and attentional influences on responses suggested that V4 provides bottom-up sensory information about stimulus features, whereas the FEF provides a top-down attentional bias toward target features that modulates sensory processing in V4 and that could be used to guide the eyes to a searched-for target. |
Hamed Zivari Adab; Rufin Vogels Practicing coarse orientation discrimination improves orientation signals in macaque cortical area V4 Journal Article In: Current Biology, vol. 21, no. 19, pp. 1661–1666, 2011. @article{ZivariAdab2011,Practice improves the performance in visual tasks, but mechanisms underlying this adult brain plasticity are unclear. Single-cell studies reported no [1], weak [2], or moderate [3, 4] perceptual learning-related changes in macaque visual areas V1 and V4, whereas none were found in middle temporal (MT) [5]. These conflicting results and modeling of human (e.g., [6, 7]) and monkey data [8] suggested that changes in the readout of visual cortical signals underlie perceptual learning, rather than changes in these signals. In the V4 learning studies, monkeys discriminated small differences in orientation, whereas in the MT study, the animals discriminated opponent motion directions. Analogous to the latter study, we trained monkeys to discriminate static orthogonal orientations masked by noise. V4 neurons showed robust increases in their capacity to discriminate the trained orientations during the course of the training. This effect was observed during discrimination and passive fixation but specifically for the trained orientations. The improvement in neural discrimination was due to decreased response variability and an increase of the difference between the mean responses for the two trained orientations. These findings demonstrate that perceptual learning in a coarse discrimination task indeed can change the response properties of a cortical sensory area. |
Michael J. Koval; Stephen G. Lomber; Stefan Everling Prefrontal cortex deactivation in macaques alters activity in the superior colliculus and impairs voluntary control of saccades Journal Article In: Journal of Neuroscience, vol. 31, no. 23, pp. 8659–8668, 2011. @article{Koval2011,The cognitive control of action requires both the suppression of automatic responses to sudden stimuli and the generation of behavior specified by abstract instructions. Though patient, functional imaging and neurophysiological studies have implicated the dorsolateral prefrontal cortex (dlPFC) in these abilities, the mechanism by which the dlPFC exerts this control remains unknown. Here we examined the functional interaction of the dlPFC with the saccade circuitry by deactivating area 46 of the dlPFC and measuring its effects on the activity of single superior colliculus neurons in monkeys performing a cognitive saccade task. Deactivation of the dlPFC reduced preparatory activity and increased stimulus-related activity in these neurons. These changes in neural activity were accompanied by marked decreases in task performance as evidenced by longer reaction times and more task errors. The results suggest that the dlPFC participates in the cognitive control of gaze by suppressing stimulus-evoked automatic saccade programs. |
Alexander Maier; Christopher J. Aura; David A. Leopold Infragranular sources of sustained local field potential responses in macaque primary visual cortex Journal Article In: Journal of Neuroscience, vol. 31, no. 6, pp. 1971–1980, 2011. @article{Maier2011,A local field potential (LFP) response can be measured throughout the visual cortex in response to the abrupt appearance of a visual stimulus. Averaging LFP responses to many stimulus presentations isolates transient, phase-locked components of the response that are consistent from trial to trial. However, stimulus responses are also composed of sustained components, which differ in their phase from trial to trial and therefore must be evaluated using other methods, such as computing the power of the response of each trial before averaging. Here, we investigate the basis of phase-locked and non-phase-locked LFP responses in the primary visual cortex of the macaque monkey using a novel variant of current source density (CSD) analysis. We applied a linear array of electrode contacts spanning the thickness of the cortex to measure the LFP and compute band-limited CSD power to identify the laminar sites of persistent current exchange that may be the basis of sustained visual LFP responses. In agreement with previous studies, we found a short-latency phase-locked current sink, thought to correspond to thalamocortical input to layer 4C. In addition, we found a prominent non-phase-locked component of the CSD that persisted as long as the stimulus was physically present. The latter was relatively broadband, lasted throughout the stimulus presentation, and was centered ∼500 μm deeper than the initial current sink. These findings demonstrate a fundamental difference in the neural mechanisms underlying the initial and sustained processing of simple visual stimuli in the V1 microcircuit. |
2010 |
Paul S. Khayat; Robert Niebergall; Julio C. Martinez-Trujillo Attention differentially modulates similar neuronal responses evoked by varying contrast and direction stimuli in area MT. Journal Article In: Journal of Neuroscience, vol. 30, no. 6, pp. 2188–2197, 2010. @article{Khayat2010,The effects of attention on the responses of visual neurons have been described as a scaling or additive modulation independent of stimulus features and contrast, or as a contrast-dependent modulation. We explored these alternatives by recording neuronal responses in macaque area MT to moving stimuli that evoked similar firing rates but varied in contrast and direction. We presented two identical pairs of stimuli, one inside the neurons' receptive field and the other outside, in the opposite hemifield. One stimulus of each pair always had high contrast and moved in the recorded cell's antipreferred direction (AP pattern), while the other (test pattern) could either move in the cell's preferred direction and vary in contrast, or have the same contrast as the AP pattern and vary in direction. For different stimulus pairs evoking similar responses, switching attention between the two AP patterns, or directing attention from a fixation spot to the AP pattern inside or outside the receptive field, produced a stronger suppression of responses to varying contrast pairs, reaching a maximum ( approximately 20%) at intermediate contrast. For invariable contrast pairs, switching attention from the fixation spot to the AP pattern produced a modulation that ranged from 10% suppression when the test pattern moved in the cells preferred direction to 14% enhancement when it moved in a direction 90 degrees away from that direction. Our results are incompatible with a scaling or additive modulation of MT neurons' response by attention, but support models where spatial and feature-based attention modulate input signals into the area normalization circuit. |
Paul S. Khayat; Robert Niebergall; Julio C. Martinez-Trujillo Frequency-dependent attentional modulation of local field potential signals in macaque area MT Journal Article In: Journal of Neuroscience, vol. 30, no. 20, pp. 7037–7048, 2010. @article{Khayat2010a,Visual attention modulates neuronal responses in primate motion processing area MT. However, whether it modulates the strength local field potentials (LFP-power) within this area remains unexplored, as well as how this modulation relates to the one of the neurons' response. We investigated these issues by simultaneously recording LFPs and neuronal responses evoked by moving random dot patterns of varying direction and contrast in area MT of two male monkeys (Macaca mulatta) during different behavioral conditions. We found that: (1) LFP-power in the gamma (30-120 Hz), but not in the delta (2-4 Hz), (4-8 Hz), alpha (8-12 Hz), beta(1) (12-20 Hz), and beta(2) (20-30 Hz) frequency bands, was tuned for motion direction and contrast, similarly to the neurons' response, (2) shifting attention into a neuron's receptive field (RF) decreased LFP-power in the bands below 30 Hz (except the band), whereas shifting attention to a stimulus motion direction outside the RF had no effect in these bands, (3) LFP-power in the gamma band, however, exhibited both spatial- and motion direction-dependent attentional modulation (increase or decrease), which was highly correlated with the modulation of the neurons' response. These results demonstrate that in area MT, shifting attention into the RFs of neurons in the vicinity of the recording electrode, or to the direction of a moving stimulus located far away from these RFs, distinctively modulates LFP-power in the various frequency bands. They further suggest differences in the neural mechanisms underlying these types of attentional modulation of visual processing. |
Alexander Maier; Geoffrey K. Adams; Christopher Aura; David A. Leopold Distinct superficial and deep laminar domains of activity in the visual cortex during rest and stimulation Journal Article In: Frontiers in Systems Neuroscience, vol. 4, pp. 1–11, 2010. @article{Maier2010,Spatial patterns of spontaneous neural activity at rest have previously been associated with specific networks in the brain, including those pertaining to the functional architecture of the primary visual cortex (V1). However, despite the prominent anatomical differences between cortical layers, little is known about the laminar pattern of spontaneous activity in V1. We address this topic by investigating the amplitude and coherence of ongoing local field potential (LFP) signals measured from different layers in V1 of macaque monkeys during rest and upon presentation of a visual stimulus. We used a linear microelectrode array to measure LFP signals at multiple, evenly spaced positions throughout the cortical thickness. Analyzing both the mean LFP amplitudes and between-contact LFP coherences, we identified two distinct zones of activity, roughly corresponding to superficial and deep layers, divided by a sharp transition near the bottom of layer 4. The LFP signals within each laminar zone were highly coherent, whereas those between zones were not. This functional compartmentalization was found not only during rest, but also when the receptive field was stimulated during a visual task. These results demonstrate the existence of distinct superficial and deep functional domains of coherent LFP activity in V1 that may reflect the intrinsic interplay of V1 microcircuitry with cortical and subcortical targets, respectively. |
Xiaomo Chen; Katherine Wilson Scangos; Veit Stuphorn Supplementary motor area exerts proactive and reactive control of arm movements Journal Article In: Journal of Neuroscience, vol. 30, no. 44, pp. 14657–14675, 2010. @article{Chen2010,Adaptive behavior requires the ability to flexibly control actions. This can occur either proactively to anticipate task requirements, or reactively in response to sudden changes. Here we report neuronal activity in the supplementary motor area (SMA) that is correlated with both forms of behavioral control. Single-unit and multiunit activity and intracranial local field potentials (LFPs) were recorded in macaque monkeys during a stop-signal task, which elicits both proactive and reactive behavioral control. The LFP power in high- (60-150 Hz) and low- (25-40 Hz) frequency bands was significantly correlated with arm movement reaction time, starting before target onset. Multiunit and single-unit activity also showed a significant regression with reaction time. In addition, LFPs and multiunit and single-unit activity changed their activity level depending on the trial history, mirroring adjustments on the behavioral level. Together, these findings indicate that neuronal activity in the SMA exerts proactive control of arm movements by adjusting the level of motor readiness. On trials when the monkeys successfully canceled arm movements in response to an unforeseen stop signal, the LFP power, particularly in a low (10-50 Hz) frequency range, increased early enough to be causally related to the inhibition of the arm movement on those trials. This indicated that neuronal activity in the SMA is also involved in response inhibition in reaction to sudden task changes. Our findings indicate, therefore, that SMA plays a role in the proactive control of motor readiness and the reactive inhibition of unwanted movements. |
T. M. Desrochers; D. Z. Jin; N. D. Goodman; Ann M. Graybiel Optimal habits can develop spontaneously through sensitivity to local cost Journal Article In: Proceedings of the National Academy of Sciences, vol. 107, no. 47, pp. 20512–20517, 2010. @article{Desrochers2010,Habits and rituals are expressed universally across animal species. These behaviors are advantageous in allowing sequential behaviors to be performed without cognitive overload, and appear to rely on neural circuits that are relatively benign but vulnerable to takeover by extreme contexts, neuropsychiatric sequelae, and processes leading to addiction. Reinforcement learning (RL) is thought to underlie the formation of optimal habits. However, this theoretic formulation has principally been tested experimentally in simple stimulus-response tasks with relatively few available responses. We asked whether RL could also account for the emergence of habitual action sequences in realistically complex situations in which no repetitive stimulus-response links were present and in which many response options were present. We exposed naïve macaque monkeys to such experimental conditions by introducing a unique free saccade scan task. Despite the highly uncertain conditions and no instruction, the monkeys developed a succession of stereotypical, self-chosen saccade sequence patterns. Remarkably, these continued to morph for months, long after session-averaged reward and cost (eye movement distance) reached asymptote. Prima facie, these continued behavioral changes appeared to challenge RL. However, trial-by-trial analysis showed that pattern changes on adjacent trials were predicted by lowered cost, and RL simulations that reduced the cost reproduced the monkeys' behavior. Ultimately, the patterns settled into stereotypical saccade sequences that minimized the cost of obtaining the reward on average. These findings suggest that brain mechanisms underlying the emergence of habits, and perhaps unwanted repetitive behaviors in clinical disorders, could follow RL algorithms capturing extremely local explore/exploit tradeoffs. |
Robert E. Hampson; Ioan Opris; S. A. Deadwyler Neural correlates of fast pupil dilation in nonhuman primates: Relation to behavioral performance and cognitive workload Journal Article In: Behavioural Brain Research, vol. 212, no. 1, pp. 1–11, 2010. @article{Hampson2010,Pupil dilation in humans has been previously shown to correlate with cognitive workload, whereby increased frequency of dilation is associated with increased degree of difficulty of a task. It has been suggested that frontal oculomotor brain areas control cognitively related pupil dilations, but this has not been confirmed due to lack of animal models of cognitive workload and task-related pupil dilation. This is the first report of a wavelet analysis applied to continuous measures of pupil size used to detect the onset of abrupt pupil dilations and the frequency of those dilations in nonhuman primates (NHPs) performing a trial-unique delayed-match-to-sample (DMS) task. A unique finding shows that electrophysiological recordings in the same animals revealed firing of neurons in frontal cortex correlated to different components of pupil dilation during task performance. It is further demonstrated that the frequency of fast pupil dilations (but not rate of eye movements) correlated with cognitive workload during task performance. Such correlations suggest that frontal neuron encoding of pupil dilation provides critical feedback to other brain areas involved in the processing of complex visual information. |