EyeLink Eye Trackers in Non-Human Primate Publications

@article{Johnston2024,

title = {Semi-orthogonal subspaces for value mediate a tradeoff between binding and generalization},

author = {W. Jeffrey Johnston and Justin M. Fine and Seng Bum Michael Yoo and R. Becket Ebitz and Benjamin Y. Hayden},

doi = {10.1038/s41593-024-01758-5},

year  = {2024},

date = {2024-01-01},

journal = {Nature Neuroscience},

volume = {27},

pages = {2218–2230},

publisher = {Springer US},

abstract = {When choosing between options, we must associate their values with the actions needed to select them. We hypothesize that the brain solves this binding problem through neural population subspaces. Here, in macaques performing a choice task, we show that neural populations in five reward-sensitive regions encode the values of offers presented on the left and right in distinct subspaces. This encoding is sufficient to bind offer values to their locations while preserving abstract value information. After offer presentation, all areas encode the value of the first and second offers in orthogonal subspaces; this orthogonalization also affords binding. Our binding-by-subspace hypothesis makes two new predictions confirmed by the data. First, behavioral errors should correlate with spatial, but not temporal, neural misbinding. Second, behavioral errors should increase when offers have low or high values, compared to medium values, even when controlling for value difference. Together, these results support the idea that the brain uses semi-orthogonal subspaces to bind features.},

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}

@article{Jurewicz2024,

title = {Irrational choices via a curvilinear representational geometry for value},

author = {Katarzyna Jurewicz and Brianna J. Sleezer and Priyanka S. Mehta and Benjamin Y. Hayden and R. Becket Ebitz},

doi = {10.1038/s41467-024-49568-4},

year  = {2024},

date = {2024-01-01},

journal = {Nature Communications},

volume = {15},

number = {1},

pages = {1–15},

publisher = {Springer US},

abstract = {We make decisions by comparing values, but it is not yet clear how value is represented in the brain. Many models assume, if only implicitly, that the representational geometry of value is linear. However, in part due to a historical focus on noisy single neurons, rather than neuronal populations, this hypothesis has not been rigorously tested. Here, we examine the representational geometry of value in the ventromedial prefrontal cortex (vmPFC), a part of the brain linked to economic decision-making, in two male rhesus macaques. We find that values are encoded along a curved manifold in vmPFC. This curvilinear geometry predicts a specific pattern of irrational decision-making: that decision-makers will make worse choices when an irrelevant, decoy option is worse in value, compared to when it is better. We observe this type of irrational choices in behavior. Together, these results not only suggest that the representational geometry of value is nonlinear, but that this nonlinearity could impose bounds on rational decision-making.},

keywords = {},

pubstate = {published},

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}

@article{Kim2024b,

title = {Neural correlates of crowding in macaque area V4},

author = {Taekjun Kim and Anitha Pasupathy},

doi = {10.1523/JNEUROSCI.2260-23.2024},

year  = {2024},

date = {2024-01-01},

journal = {The Journal of Neuroscience},

volume = {44},

number = {24},

pages = {1—-16},

abstract = {Visual crowding refers to the phenomenon where a target object that is easily identifiable in isolation becomes difficult to recognize when surrounded by other stimuli (distractors). Many psychophysical studies have investigated this phenomenon and proposed alternative models for the underlying mechanisms. One prominent hypothesis, albeit with mixed psychophysical support, posits that crowding arises from the loss of information due to pooled encoding of features from target and distractor stimuli in the early stages of cortical visual processing. However, neurophysiological studies have not rigorously tested this hypothesis. We studied the responses of single neurons in macaque (one male, one female) area V4, an intermediate stage of the object-processing pathway, to parametrically designed crowded displays and texture statistics-matched metameric counterparts. Our investigations reveal striking parallels between how crowding parameters—number, distance, and position of distractors—influence human psychophysical performance and V4 shape selectivity. Importantly, we also found that enhancing the salience of a target stimulus could alleviate crowding effects in highly cluttered scenes, and this could be temporally protracted reflecting a dynamical process. Thus, a pooled encoding of nearby stimuli cannot explain the observed responses, and we propose an alternative model where V4 neurons preferentially encode salient stimuli in crowded displays. Overall, we conclude that the magnitude of crowding effects is determined not just by the number of distractors and target–distractor separation but also by the relative salience of targets versus distractors based on their feature attributes—the similarity of distractors and the contrast between target and distractor stimuli.},

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pubstate = {published},

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}

@article{Laamerad2024,

title = {Decision-related activity and movement selection in primate visual cortex},

author = {Pooya Laamerad and Liu D. Liu and Christopher C. Pack},

doi = {10.1126/sciadv.adk7214},

year  = {2024},

date = {2024-01-01},

journal = {Science Advances},

volume = {10},

number = {22},

pages = {1–12},

abstract = {Fluctuations in the activity of sensory neurons often predict perceptual decisions. This connection can be quantified with a metric called choice probability (CP), and there is a longstanding debate about whether CP reflects a causal influence on decisions or an echo of decision-making activity elsewhere in the brain. Here, we show that CP can reflect a third variable, namely, the movement used to indicate the decision. In a standard visual motion discrimination task, neurons in the middle temporal (MT) area of primate cortex responded more strongly during trials that involved a saccade toward their receptive fields. This variability accounted for much of the CP observed across the neuronal population, and it arose through training. Moreover, pharmacological inactivation of MT biased behavioral responses away from the corresponding visual field locations. These results demonstrate that training on a task with fixed sensorimotor contingencies introduces movement-related activity in sensory brain regions and that this plasticity can shape the neural circuitry of perceptual decision-making.},

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pubstate = {published},

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}

@article{Larry2024,

title = {Organization of reward and movement signals in the basal ganglia and cerebellum},

author = {Noga Larry and Gil Zur and Mati Joshua},

doi = {10.1038/s41467-024-45921-9},

year  = {2024},

date = {2024-01-01},

journal = {Nature Communications},

volume = {15},

number = {1},

pages = {1–13},

publisher = {Springer US},

abstract = {The basal ganglia and the cerebellum are major subcortical structures in the motor system. The basal ganglia have been cast as the reward center of the motor system, whereas the cerebellum is thought to be involved in adjusting sensorimotor parameters. Recent findings of reward signals in the cerebellum have challenged this dichotomous view. To compare the basal ganglia and the cerebellum directly, we recorded from oculomotor regions in both structures from the same monkeys. We partitioned the trial-by-trial variability of the neurons into reward and eye-movement signals to compare the coding across structures. Reward expectation and movement signals were the most pronounced in the output structure of the basal ganglia, intermediate in the cerebellum, and the smallest in the input structure of the basal ganglia. These findings suggest that reward and movement information is sharpened through the basal ganglia, resulting in a higher signal-to-noise ratio than in the cerebellum.},

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pubstate = {published},

tppubtype = {article}

}

@article{Liu2024i,

title = {Assessing perceptual chromatic equiluminance using a reflexive pupillary response},

author = {Ye Liu and Bridget W. Mahony and Xiaochun Wang and Pierre M. Daye and Wei Wang and Patrick Cavanagh and Pierre Pouget and Ian Max Andolina},

doi = {10.1038/s41598-024-51982-z},

year  = {2024},

date = {2024-01-01},

journal = {Scientific Reports},

volume = {14},

number = {1},

pages = {1–12},

publisher = {Nature Publishing Group UK},

abstract = {Equiluminant stimuli help assess the integrity of colour perception and the relationship of colour to other visual features. As a result of individual variation, it is necessary to calibrate experimental visual stimuli to suit each individual's unique equiluminant ratio. Most traditional methods rely on training observers to report their subjective equiluminance point. Such paradigms cannot easily be implemented on pre-verbal or non-verbal observers. Here, we present a novel Pupil Frequency-Tagging Method (PFTM) for detecting a participant's unique equiluminance point without verbal instruction and with minimal training. PFTM analyses reflexive pupil oscillations induced by slow (< 2 Hz) temporal alternations between coloured stimuli. Two equiluminant stimuli will induce a similar pupil dilation response regardless of colour; therefore, an observer's equiluminant point can be identified as the luminance ratio between two colours for which the oscillatory amplitude of the pupil at the tagged frequency is minimal. We compared pupillometry-based equiluminance ratios to those obtained with two established techniques in humans: minimum flicker and minimum motion. In addition, we estimated the equiluminance point in non-human primates, demonstrating that this new technique can be successfully employed in non-verbal subjects.},

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pubstate = {published},

tppubtype = {article}

}

@article{Ma2024c,

title = {Effects of ketamine on frontoparietal interactions in a rule-based antisaccade task in macaque monkeys},

author = {Liya Ma and Nupur Katyare and Kevin Johnston and Stefan Everling},

doi = {10.1523/JNEUROSCI.1018-23.2024},

year  = {2024},

date = {2024-01-01},

journal = {Journal of Neuroscience},

volume = {44},

number = {50},

pages = {1–19},

abstract = {Cognitive control is engaged by working memory processes and high-demand situations like antisaccade, where one must suppress a prepotent response. While it is known to be supported by the frontoparietal control network, how intra- and interareal dynamics contribute to cognitive control processes remains unclear. N-Methyl-D-aspartate glutamate receptors (NMDARs) play a key role in prefrontal dynamics that support cognitive control. NMDAR antagonists, such as ketamine, are known to alter task-related prefrontal activities and impair cognitive performance. However, the role of NMDAR in cognitive control-related frontoparietal dynamics remains underexplored. Here, we simultaneously recorded local field potentials and single-unit activities from the lateral prefrontal (lPFC) and posterior parietal cortices (PPC) in two male macaque monkeys during a rule-based antisaccade task, with both rule-visible (RV) and rule-memorized (RM) conditions. In addition to altering the E/I balance in both areas, ketamine had a negative impact on rule coding in true oscillatory activities. It also reduced frontoparietal coherence in a frequency- and rule-dependent manner. Granger prediction analysis revealed that ketamine induced an overall reduction in bidirectional connectivity. Among antisaccade trials, a greater reduction in lPFC–PPC connectivity during the delay period preceded a greater delay in saccadic onset under the RM condition and a greater deficit in performance under the RV condition. Lastly, ketamine compromised rule coding in lPFC neurons in both RV and RM conditions and in PPC neurons only in the RV condition. Our findings demonstrate the utility of acute NMDAR antagonists in understanding the mechanisms through which frontoparietal dynamics support cognitive control processes.},

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}

@article{MendozaHalliday2024a,

title = {Dissociable neuronal substrates of visual feature attention and working memory},

author = {Diego Mendoza-Halliday and Haoran Xu and Frederico A. C. Azevedo and Robert Desimone},

doi = {10.1016/j.neuron.2023.12.007},

year  = {2024},

date = {2024-01-01},

journal = {Neuron},

volume = {112},

number = {5},

pages = {850–863},

publisher = {The Authors},

abstract = {Attention and working memory (WM) are distinct cognitive functions, yet given their close interactions, it is often assumed that they share the same neuronal mechanisms. We show that in macaques performing a WM-guided feature attention task, the activity of most neurons in areas middle temporal (MT), medial superior temporal (MST), lateral intraparietal (LIP), and posterior lateral prefrontal cortex (LPFC-p) displays attentional modulation or WM coding and not both. One area thought to play a role in both functions is LPFC-p. To test this, we optogenetically inactivated LPFC-p bilaterally during different task periods. Attention period inactivation reduced attentional modulation in LPFC-p, MST, and LIP neurons and impaired task performance. In contrast, WM period inactivation did not affect attentional modulation or performance and minimally affected WM coding. Our results suggest that feature attention and WM have dissociable neuronal substrates and that LPFC-p plays a critical role in feature attention, but not in WM.},

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pubstate = {published},

tppubtype = {article}

}

@article{Narmashiri2024,

title = {Value-based search efficiency is encoded in the substantia nigra reticulata firing rate, spiking irregularity and local field potential},

author = {Abdolvahed Narmashiri and Mojtaba Abbaszadeh and Mohammad Hossein Nadian and Ali Ghazizadeh},

doi = {10.1523/JNEUROSCI.1033-23.2023},

year  = {2024},

date = {2024-01-01},

journal = {The Journal of Neuroscience},

volume = {44},

number = {6},

pages = {1–12},

abstract = {Recent results show that valuable objects can pop out in visual search, yet its neural mechanisms remain unexplored. Given the role of substantia nigra reticulata (SNr) in object value memory and control of gaze, we recorded its single-unit activity while male macaque monkeys engaged in efficient or inefficient search for a valuable target object among low-value objects. The results showed that efficient search was concurrent with stronger inhibition and higher spiking irregularity in the target-present (TP) compared with the target-absent (TA) trials in SNr. Importantly, the firing rate differentiation of TP and TA trials happened within ∼100 ms of display onset, and its magnitude was significantly correlated with the search times and slopes (search efficiency). Time–frequency analyses of local field potential (LFP) after display onset revealed significant modulations of the gamma band power with search efficiency. The greater reduction of SNr firing in TP trials in efficient search can create a stronger disinhibition of downstream superior colliculus, which in turn can facilitate saccade to obtain valuable targets in competitive environments.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Neupane2024,

title = {Mental navigation in the primate entorhinal cortex},

author = {Sujaya Neupane and Ila Fiete and Mehrdad Jazayeri},

doi = {10.1038/s41586-024-07557-z},

year  = {2024},

date = {2024-01-01},

journal = {Nature},

volume = {630},

number = {8017},

pages = {704–711},

publisher = {Springer US},

abstract = {A cognitive map is a suitably structured representation that enables novel computations using previous experience; for example, planning a new route in a familiar space. Work in mammals has found direct evidence for such representations in the presence of exogenous sensory inputs in both spatial and non-spatial domains. Here we tested a foundational postulate of the original cognitive map theory: that cognitive maps support endogenous computations without external input. We recorded from the entorhinal cortex of monkeys in a mental navigation task that required the monkeys to use a joystick to produce one-dimensional vectors between pairs of visual landmarks without seeing the intermediate landmarks. The ability of the monkeys to perform the task and generalize to new pairs indicated that they relied on a structured representation of the landmarks. Task-modulated neurons exhibited periodicity and ramping that matched the temporal structure of the landmarks and showed signatures of continuous attractor networks. A continuous attractor network model of path integration14 augmented with a Hebbian-like learning mechanism provided an explanation of how the system could endogenously recall landmarks. The model also made an unexpected prediction that endogenous landmarks transiently slow path integration, reset the dynamics and thereby reduce variability. This prediction was borne out in a reanalysis of firing rate variability and behaviour. Our findings link the structured patterns of activity in the entorhinal cortex to the endogenous recruitment of a cognitive map during mental navigation.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Nigam2024,

title = {Predictions enable top-down pattern separation in the macaque face-processing hierarchy},

author = {Tarana Nigam and Caspar M. Schwiedrzik},

doi = {10.1038/s41467-024-51543-y},

year  = {2024},

date = {2024-01-01},

journal = {Nature Communications},

volume = {15},

number = {1},

pages = {1–13},

publisher = {Springer US},

abstract = {Distinguishing faces requires well distinguishable neural activity patterns. Contextual information may separate neural representations, leading to enhanced identity recognition. Here, we use functional magnetic resonance imaging to investigate how predictions derived from contextual information affect the separability of neural activity patterns in the macaque face-processing system, a 3-level processing hierarchy in ventral visual cortex. We find that in the presence of predictions, early stages of this hierarchy exhibit well separable and high-dimensional neural geometries resembling those at the top of the hierarchy. This is accompanied by a systematic shift of tuning properties from higher to lower areas, endowing lower areas with higher-order, invariant representations instead of their feedforward tuning properties. Thus, top-down signals dynamically transform neural representations of faces into separable and high-dimensional neural geometries. Our results provide evidence how predictive context transforms flexible representational spaces to optimally use the computational resources provided by cortical processing hierarchies for better and faster distinction of facial identities.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Ninomiya2024,

title = {Dynamic spatial representation of self and others' actions in the macaque frontal cortex},

author = {Taihei Ninomiya and Masaki Isoda},

year  = {2024},

date = {2024-01-01},

journal = {Proceedings of the National Academy of Sciences},

volume = {121},

number = {31},

pages = {1–10},

abstract = {Modulation of neuronal firing rates by the spatial locations of physical objects is a widespread phenomenon in the brain. However, little is known about how neuronal responses to the actions of biological entities are spatially tuned and whether such spatially tuned responses are affected by social contexts. These issues are of key importance for understanding the neural basis of embodied social cognition, such as imitation and perspectivetaking. Here, we show that spatial representation of actions can be dynamically changed depending on others' social relevance and agents of action. Monkeys performed a turn-taking choice task with a real monkey partner sitting face-to-face or a filmed partner in prerecorded videos. Three rectangular buttons (left, center, and right) were positioned in front of the subject and partner as their choice targets. We recorded from single neurons in two frontal nodes in the social brain, the ventral premotor cortex (PMv) and the medial prefrontal cortex (MPFC). When the partner was filmed rather than real, spatial preference for partner-actions was markedly diminished in MPFC, but not PMv, neurons. This social context-dependent modulation in the MPFC was also evident for self- actions. Strikingly, a subset of neurons in both areas switched their spatial preference between self-actions and partner-actions in a diametrically opposite manner. This observation suggests that these cortical areas are associated with coordinate transformation in ways consistent with an actor- centered perspective-taking coding scheme. The PMv may subserve such functions in context-independent manners, whereas the MPFC may do so primarily in social contexts.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Noroozi2024,

title = {Frontotemporal network contribution to occluded face processing},

author = {Jalaledin Noroozi and Ehsan Rezayat and Mohammad-Reza A. Dehaqan},

year  = {2024},

date = {2024-01-01},

journal = {Proceedings of the National Academy of Sciences},

volume = {121},

number = {48},

pages = {1–12},

abstract = {Primates are known for their exceptional ability to recognize faces. However, we still have much to learn about how their brains process faces when they are partially hidden. When we cover parts of a face, it affects how our brains respond, even though we still perceive the face as a whole. This suggests that complex brain networks are at work in understanding partially hidden faces. To explore this further, we studied two brain regions, the ventrolateral prefrontal cortex (vlPFC) and the inferior temporal cortex (ITC), while showing primate images of faces with parts occluded. We found that vlPFC neurons were more active when faces were partially covered, while ITC neurons preferred fully visible faces. Interestingly, the ITC seemed to process occluded faces in a separate phase after the vlPFC responded. Our research revealed a coordinated effort between these brain regions based on the level of facial obstruction. Specifically, the vlPFC seemed to play a crucial role, driving the representation of occluded faces in the later phase of ITC processing. Importantly, we also found that the brain processes occluded faces differently from those that are fully visible, suggesting specialized mechanisms for handling these situations. These findings high-light the importance of feedback from the vlPFC in understanding occluded faces in the ITC region of the brain. Understanding these neural processes not only enhances our understanding of how primates perceive faces but also provides insights into broader aspects of visual cognition.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Panichello2024,

title = {Intermittent rate coding and cue-specific ensembles support working memory},

author = {Matthew F. Panichello and Donatas Jonikaitis and Yu Jin Oh and Shude Zhu and Ethan B. Trepka and Tirin Moore},

doi = {10.1038/s41586-024-08139-9},

year  = {2024},

date = {2024-01-01},

journal = {Nature},

volume = {636},

pages = {1–26},

publisher = {Springer US},

abstract = {Persistent, memorandum-specific neuronal spiking activity has long been hypothesized to underlie working memory1,2. However, emerging evidence suggests a potential role for ‘activity-silent' synaptic mechanisms3–5. This issue remains controversial because evidence for either view has largely relied either on datasets that fail to capture single-trial population dynamics or on indirect measures of neuronal spiking. We addressed this controversy by examining the dynamics of mnemonic information on single trials obtained from large, local populations of lateral prefrontal neurons recorded simultaneously in monkeys performing a working memory task. Here we show that mnemonic information does not persist in the spiking activity of neuronal populations during memory delays, but instead alternates between coordinated ‘On' and ‘Off' states. At the level of single neurons, Off states are driven by both a loss of selectivity for memoranda and a return of firing rates to spontaneous levels. Further exploiting the large-scale recordings used here, we show that mnemonic information is available in the patterns of functional connections among neuronal ensembles during Off states. Our results suggest that intermittent periods of memorandum-specific spiking coexist with synaptic mechanisms to support working memory.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Pattadkal2024,

title = {Interactions between saccades and smooth pursuit eye movements in marmosets},

author = {Jagruti J. Pattadkal and Carrie Barr and Nicholas J. Priebe},

doi = {10.1523/ENEURO.0027-24.2024},

year  = {2024},

date = {2024-01-01},

journal = {eNeuro},

volume = {11},

number = {6},

pages = {1–11},

abstract = {Animals use a combination of eye movements to track moving objects. These different eye movements need to be coordinated for successful tracking, requiring interactions between the systems involved. Here, we study the interaction between the saccadic and smooth pursuit eye movement systems in marmosets. Using a single-target pursuit task, we show that saccades cause an enhancement in pursuit following a saccade. Using a two-target pursuit task, we show that this enhancement in pursuit is selective toward the motion of the target selected by the saccade, irrespective of any biases in pursuit prior to the saccade. These experiments highlight the similarities in the functioning of saccadic and smooth pursuit eye movement systems across primates.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Peysakhovich2024,

title = {Primate superior colliculus is causally engaged in abstract higher-order cognition},

author = {Barbara Peysakhovich and Ou Zhu and Stephanie M. Tetrick and Vinay Shirhatti and Alessandra A. Silva and Sihai Li and Guilhem Ibos and Matthew C. Rosen and W. Jeffrey and David J. Freedman},

doi = {10.1038/s41593-024-01744-x},

year  = {2024},

date = {2024-01-01},

journal = {Nature Neuroscience},

volume = {27},

pages = {1999–2008},

publisher = {Springer US},

abstract = {The superior colliculus is an evolutionarily conserved midbrain region that is thought to mediate spatial orienting, including saccadic eye movements and covert spatial attention. Here, we reveal a role for the superior colliculus in higher-order cognition, independent of its role in spatial orienting. We trained rhesus macaques to perform an abstract visual categorization task that involved neither instructed eye movements nor differences in covert attention. We compared neural activity in the superior colliculus and the posterior parietal cortex, a region previously shown to causally contribute to abstract category decisions. The superior colliculus exhibits robust encoding of learned visual categories, which is stronger than in the posterior parietal cortex and arises at a similar latency in the two areas. Moreover, inactivation of the superior colliculus markedly impaired animals' category decisions. These results demonstrate that the primate superior colliculus mediates abstract, higher-order cognitive processes that have traditionally been attributed to the neocortex. Categorization},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Pi2024,

title = {The olivary input to the cerebellum dissociates sensory events from movement plans},

author = {Jay S. Pi and Mohammad Amin Fakharian and Paul Hage and Ehsan Sedaghat-Nejad and Salomon Z. Muller and Reza Shadmehr},

year  = {2024},

date = {2024-01-01},

journal = {Proceedings of the National Academy of Sciences},

volume = {121},

number = {17},

pages = {2024},

abstract = {Neurons in the inferior olive are thought to anatomically organize the Purkinje cells (P-cells) of the cerebellum into computational modules, but what is computed by each module? Here, we designed a saccade task in marmosets that dissociated sensory events from motor events and then recorded the complex and simple spikes of hundreds of P-cells. We found that when a visual target was presented at a random location, the olive reported the direction of that sensory event to one group of P- cells, but not to a seond group. However, just before movement onset, it reported the direction of the planned movement to both groups, even if that movement was not toward the target. At the end of the movement if the subject experienced an error but chose to withhold the corrective movement, only the first group received information about the sensory prediction error. We organized the P-cells based on the information content of their olivary input and found that in the group that received sensory information, the simple spikes were suppressed during fixation, then produced a burst before saccade onset in a direction consistent with assisting the movement. In the second group, the simple spikes were not suppressed during fixation but burst near saccade deceleration in a direction consistent with stopping the movement. Thus, the olive differentiated the P-cells based on whether they would receive sensory or motor information, and this defined their contributions to control of movements as well as holding still.},

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pubstate = {published},

tppubtype = {article}

}

@article{Ramezanpour2024,

title = {Low-cost, portable, easy-to-use kiosks to facilitate home-cage testing of nonhuman primates during vision-based behavioral tasks},

author = {Hamidreza Ramezanpour and Christopher Giverin and Kohitij Kar},

doi = {10.1152/jn.00397.2023},

year  = {2024},

date = {2024-01-01},

journal = {Journal of Neurophysiology},

volume = {132},

number = {3},

pages = {666–677},

abstract = {Nonhuman primates (NHPs), especially rhesus macaques, have significantly contributed to our understanding of the neural computations underlying human vision. Besides the established homologies in the visual brain areas between these species and our ability to probe detailed neural mechanisms in monkeys at multiple scales, NHPs' ability to perform human-like visual behavior makes them an extremely appealing animal model of human vision. Traditionally, such behavioral studies have been conducted in controlled laboratory settings, offering experimenters tight control over variables like luminance, eye movements, and auditory interference. However, in-lab experiments have several constraints, including limited experimental time, the need for dedicated human experimenters, additional lab space requirements, invasive surgeries for headpost implants, and extra time and training for chairing and head restraints. To overcome these limitations, we propose adopting home-cage behavioral training and testing of NHPs, enabling the administration of many vision-based behavioral tasks simultaneously across multiple monkeys with reduced human personnel requirements, no NHP head restraint, and monkeys' unrestricted access to experiments. In this article, we present a portable, low-cost, easy-to-use kiosk system developed to conduct home-cage vision-based behavioral tasks in NHPs. We provide details of its operation and build to enable more open-source development of this technology. Furthermore, we present validation results using behavioral measurements performed in the lab and in NHP home cages, demonstrating the system's reliability and potential to enhance the efficiency and flexibility of NHP behavioral research.},

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pubstate = {published},

tppubtype = {article}

}

@article{Rima2024,

title = {A chinrest-based approach to measure eye movements and experimental task engagement in macaques with minimal restraint},

author = {Samy Rima and Jennifer Greilsamer and Marcus Haag and Jaime Cadena-Valencia and Morgan Sansonnens and Andrea Francovich and Florian Lanz and Andrina Zbinden and Alessandra Bergadano and Michael Christopher Schmid},

doi = {10.1016/j.jneumeth.2024.110173},

year  = {2024},

date = {2024-01-01},

journal = {Journal of Neuroscience Methods},

volume = {408},

pages = {1–8},

publisher = {Elsevier B.V.},

abstract = {Background: The use of Rhesus macaques in vision research is crucial due to their visual system's similarity to humans. While invasive techniques have been the norm, there has been a shift towards non-invasive methods, such as facemasks and head molds, to enhance animal welfare and address ethical concerns. New Method: We present a non-invasive, 3D-printed chinrest with infrared sensors, adapted from canine research, allowing for accurate eye movement measurements and voluntary animal participation in experiments. Results: The chinrest method showed a 16% and 28% increase in average trial numbers for Monkey 1 and Monkey 2, respectively, compared to the traditional headpost method. The engagement was high, with monkeys performing over 500 trials per session and initiating a new trial after an average intertrial interval of approximately 1 second. The hit rate improved by about 10% for Monkey 1 in the chinrest condition, and the fixation precision, measured by the standard deviation of gaze positions, was significantly better in the chinrest condition, with Monkey 1 showing a reduction in fixation imprecision from 0.26° to 0.17° in the X-axis. Comparison with Existing Methods: The chinrest approach showed significant improvements in trial engagement and reduction in aborted trials due to fixation breaks, indicating less stress and potentially improved data quality compared to previous non-invasive methods. Conclusions: The chinrest method offers a significant advancement in primate cognitive testing by allowing for precise data collection while addressing animal welfare concerns, possibly leading to better scientific outcomes and a paradigm shift in primate research methodologies.},

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tppubtype = {article}

}

@article{RodriguezDeliz2024,

title = {Development of radial frequency pattern perception in macaque monkeys},

author = {C. L. Rodríguez Deliz and Gerick M. Lee and Brittany N. Bushnell and Najib J. Majaj and J. Anthony Movshon and Lynne Kiorpes},

doi = {10.1167/jov.24.6.6},

year  = {2024},

date = {2024-01-01},

journal = {Journal of Vision},

volume = {24},

number = {6},

pages = {1–17},

abstract = {Infant primates see poorly, and most perceptual functions mature steadily beyond early infancy. Behavioral studies on human and macaque infants show that global form perception, as measured by the ability to integrate contour information into a coherent percept, improves dramatically throughout the first several years after birth. However, it is unknown when sensitivity to curvature and shape emerges in early life or how it develops. We studied the development of shape sensitivity in 18 macaques, aged 2 months to 10 years. Using radial frequency stimuli, circular targets whose radii are modulated sinusoidally, we tested monkeys' ability to radial frequency stimuli from circles as a function of the depth and frequency of sinusoidal modulation. We implemented a new four-choice oddity task and compared the resulting data with that from a traditional two-alternative forced choice task. We found that radial frequency pattern perception was measurable at the youngest age tested (2 months). Behavioral performance at all radial frequencies improved with age. Performance was better for higher radial frequencies, suggesting the developing visual system prioritizes processing of fine visual details that are ecologically relevant. By using two complementary methods, we were able to capture a comprehensive developmental trajectory for shape perception.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Roshanaei2024,

title = {Working memory expedites the processing of visual signals within the extrastriate cortex},

author = {Majid Roshanaei and Zahra Bahmani and Kelsey Clark and Mohammad Reza Daliri and Behrad Noudoost},

doi = {10.1016/j.isci.2024.110489},

year  = {2024},

date = {2024-01-01},

journal = {iScience},

volume = {27},

number = {8},

pages = {1–12},

publisher = {The Author(s)},

abstract = {Working memory is the ability to maintain information in the absence of sensory input. In this study, we investigated how working memory benefits processing in visual areas. Using a measure of phase consistency to detect the arrival time of visual signals to the middle temporal (MT) area, we assessed the impact of working memory on the speed of sensory processing. We recorded from MT neurons in two monkeys during a spatial working memory task with visual probes. When the memorized location closely matches the receptive field center of the recording site, visual input arrives sooner, but if the memorized location does not match the receptive field center then the arrival of visual information is delayed. Thus, working memory expedites the arrival of visual input in MT. These results reveal that even in the absence of firing rate changes, working memory can still benefit the processing of information within sensory areas.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Sajedin2023,

title = {Information content and temporal structure of face selective local field potentials frequency bands in IT cortex},

author = {Atena Sajedin and Sina Salehi and Hossein Esteky},

doi = {10.1093/cercor/bhad411},

year  = {2024},

date = {2024-01-01},

journal = {Cerebral Cortex},

volume = {34},

number = {1},

pages = {1–12},

abstract = {Sensory stimulation triggers synchronized bioelectrical activity in the brain across various frequencies. This study delves into network-level activities, specifically focusing on local field potentials as a neural signature of visual category representation. Specifically, we studied the role of different local field potential frequency oscillation bands in visual stimulus category representation by presenting images of faces and objects to three monkeys while recording local field potential from inferior temporal cortex. We found category selective local field potential responses mainly for animate, but not inanimate, objects. Notably, face-selective local field potential responses were evident across all tested frequency bands, manifesting in both enhanced (above mean baseline activity) and suppressed (below mean baseline activity) local field potential powers. We observed four different local field potential response profiles based on frequency bands and face selective excitatory and suppressive responses. Low-frequency local field potential bands (1–30 Hz) were more prodominstaly suppressed by face stimulation than the high-frequency (30–170 Hz) local field potential bands. Furthermore, the low-frequency local field potentials conveyed less face category informtion than the high-frequency local field potential in both enhansive and suppressive conditions. Furthermore, we observed a negative correlation between face/object d-prime values in all the tested local field potential frequency bands and the anterior–posterior position of the recording sites. In addition, the power of low-frequency local field potential systematically declined across inferior temporal anterior–posterior positions, whereas high-frequency local field potential did not exhibit such a pattern. In general, for most of the above-mentioned findings somewhat similar results were observed for body, but not, other stimulus categories. The observed findings suggest that a balance of face selective excitation and inhibition across time and cortical space shape face category selectivity in inferior temporal cortex.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Samonds2024,

title = {Mammals achieve common neural coverage of visual scenes using distinct sampling behaviors},

author = {Jason M. Samonds and Martin Szinte and Carrie Barr and Anna Montagnini and Guillaume S. Masson and Nicholas J. Priebe},

doi = {10.1523/ENEURO.0287-23.2023},

year  = {2024},

date = {2024-01-01},

journal = {eNeuro},

volume = {11},

number = {2},

pages = {1–13},

abstract = {Most vertebrates use head and eye movements to quickly change gaze orientation and sample different portions of the environment with periods of stable fixation. Visual information must be integrated across fixations to construct a complete perspective of the visual environment. In concert with this sampling strategy, neurons adapt to unchanging input to conserve energy and ensure that only novel information from each fixation is processed. We demonstrate how adaptation recovery times and saccade properties interact and thus shape spatiotemporal tradeoffs observed in the motor and visual systems of mice, cats, marmosets, macaques, and humans. These tradeoffs predict that in order to achieve similar visual coverage over time, animals with smaller receptive field sizes require faster saccade rates. Indeed, we find comparable sampling of the visual environment by neuronal populations across mammals when integrating measurements of saccadic behavior with receptive field sizes and V1 neuronal den-sity. We propose that these mammals share a common statistically driven strategy of maintaining coverage of their visual environment over time calibrated to their respective visual system characteristics.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Selvanayagam2024,

title = {Laminar dynamics of target selection in the posterior parietal cortex of the common marmoset},

author = {Janahan Selvanayagam and Kevin D. Johnston and Stefan Everling},

doi = {10.1523/JNEUROSCI.1583-23.2024},

year  = {2024},

date = {2024-01-01},

journal = {The Journal of Neuroscience},

volume = {44},

number = {21},

pages = {1–16},

abstract = {The lateral intraparietal area (LIP) plays a crucial role in target selection and attention in primates, but the laminar microcircuitry of this region is largely unknown. To address this, we used ultra-high density laminar electrophysiology with Neuropixels probes to record neural activity in the posterior parietal cortex (PPC) of two adult marmosets while they performed a simple visual target selection task. Our results reveal neural correlates of visual target selection in the marmoset, similar to those observed in macaques and humans, with distinct timing and profiles of activity across cell types and cortical layers. Notably, a greater proportion of neurons exhibited stimulus-related activity in superficial layers whereas a greater proportion of infragranular neurons exhibited significant postsaccadic activity. Stimulus-related activity was first observed in granular layer putative interneurons, whereas target discrimination activity emerged first in supragranular layers putative pyramidal neurons, supporting a canonical laminar circuit underlying visual target selection in marmoset PPC. These findings provide novel insights into the neural basis of visual attention and target selection in primates.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Shahbazi2024,

title = {Perceptography unveils the causal contribution of inferior temporal cortex to visual perception},

author = {Elia Shahbazi and Timothy Ma and Martin Pernuš and Walter Scheirer and Arash Afraz},

doi = {10.1038/s41467-024-47356-8},

year  = {2024},

date = {2024-01-01},

journal = {Nature Communications},

volume = {15},

number = {1},

pages = {1–11},

abstract = {Neurons in the inferotemporal (IT) cortex respond selectively to complex visual features, implying their role in object perception. However, perception is subjective and cannot be read out from neural responses; thus, bridging the causal gap between neural activity and perception demands independent characterization of perception. Historically, though, the complexity of the perceptual alterations induced by artificial stimulation of IT cortex has rendered them impossible to quantify. To address this old problem, we tasked male macaque monkeys to detect and report optical impulses delivered to their IT cortex. Combining machine learning with high-throughput behavioral optogenetics, we generated complex and highly specific images that were hard for the animal to distinguish from the state of being cortically stimulated. These images, named “perceptograms” for the first time, reveal and depict the contents of the complex hallucinatory percepts induced by local neural perturbation in IT cortex. Furthermore, we found that the nature and magnitude of these hallucinations highly depend on concurrent visual input, stimulation location, and intensity. Objective characterization of stimulation-induced perceptual events opens the door to developing a mechanistic theory of visual perception. Further, it enables us to make better visual prosthetic devices and gain a greater understanding of visual hallucinations in mental disorders.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Stan2024,

title = {Recent visual experience reshapes V4 neuronal activity and improves perceptual performance},

author = {Patricia L. Stan and Matthew A. Smith},

doi = {10.1523/jneurosci.1764-23.2024},

year  = {2024},

date = {2024-01-01},

journal = {The Journal of Neuroscience},

volume = {44},

number = {41},

pages = {1–17},

abstract = {Recent visual experience heavily influences our visual perception, but how this is mediated by the reshaping of neuronal activity to alter and improve perceptual discrimination remains unknown. We recorded from populations of neurons in visual cortical area V4 while two male rhesus macaque monkeys performed a natural image change detection task under different experience conditions. We found that maximizing the recent experience with a particular image led to an improvement in the ability to detect a change in that image. This improvement was associated with decreased neural responses to the image, consistent with neuronal changes previously seen in studies of adaptation and expectation. We found that the magnitude of behavioral improvement was correlated with the magnitude of response suppression. Furthermore, this suppression of activity led to an increase in signal separation, providing evidence that a reduction in activity can improve stimulus encoding. Within populations of neurons, greater recent experience was associated with decreased trial-to-trial shared variability, indicating that a reduction in variability is a key means by which experience influences perception. Taken together, the results of our study contribute to an understanding of how recent visual experience can shape our perception and behavior through modulating activity patterns in mid-level visual cortex. Significance Statement Our visual experience shapes our perception and behavior. This work identifies neural signatures of visual experience that directly link to behavioral performance, an area that has been elusive in past work. Our study represents a demonstration of how the activity of populations of neurons in the visual cortex, shaped by experience, can reflect an altered neural code that underlies behavior.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Steinemann2024,

title = {Direct observation of the neural computations underlying a single decision},

author = {Natalie A Steinemann and Gabriel M Stine and Eric M Trautmann and Ariel Zylberberg and Daniel M Wolpert and Michael N Shadlen},

year  = {2024},

date = {2024-01-01},

journal = {eLife},

volume = {12},

pages = {1–29},

abstract = {Neurobiological investigations of perceptual decision-making have furnished the first glimpse of a flexible cognitive process at the level of single neurons (Shadlen & Newsome, 1996; Shadlen & Kiani 2013). Neurons in the parietal and prefrontal cortex (Kim & Shadlen, 1999; Romo, Hernandez & Zainos, 2004; Hernandez, Zainos & Romo, 2002; Ding & Gold, 2012) are thought to represent the accumulation of noisy evidence, acquired over time, leading to a decision. Neural recordings averaged over many decisions have provided support for the deterministic rise in activity to a termination bound (Roitman & Shadlen, 2002). Critically, it is the unobserved stochastic component that is thought to confer variability in both choice and decision time (Gold & Shadlen, 2007). Here, we elucidate this stochastic, diffusion-like signal on individual decisions by recording simultaneously from hundreds of neurons in the lateral intraparietal cortex (LIP). We show that a small subset of these neurons, previously studied singly, represent a combination of deterministic drift and stochastic diffusion—the integral of noisy evidence—during perceptual decision making, and we provide direct support for the hypothesis that this diffusion signal is the quantity responsible for the variability in choice and reaction times. Neuronal state space and decoding analyses, applied to the whole population, also identify the drift diffusion signal. However, we show that the signal relies on the subset of neurons with response fields that overlap the choice targets. This parsimonious observation would escape detection by these powerful methods, absent a clear hypothesis. ### Competing Interest Statement The authors have declared no competing interest.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Tanaka2024,

title = {An easy-to-implement, non-invasive head restraint method for monkey fMRI},

author = {Reiji Tanaka and Kei Watanabe and Takafumi Suzuki and Kae Nakamura and Masaharu Yasuda and Hiroshi Ban and Ken Okada and Shigeru Kitazawa},

doi = {10.1016/j.neuroimage.2023.120479},

year  = {2024},

date = {2024-01-01},

journal = {NeuroImage},

volume = {285},

pages = {1–12},

publisher = {Elsevier Inc.},

abstract = {Functional magnetic resonance imaging (fMRI) in behaving monkeys has a strong potential to bridge the gap between human neuroimaging and primate neurophysiology. In monkey fMRI, to restrain head movements, researchers usually surgically implant a plastic head-post on the skull. Although time-proven to be effective, this technique could create burdens for animals, including a risk of infection and discomfort. Furthermore, the presence of extraneous objects on the skull, such as bone screws and dental cement, adversely affects signals near the cortical surface. These side effects are undesirable in terms of both the practical aspect of efficient data collection and the spirit of “refinement” from the 3R's. Here, we demonstrate that a completely non-invasive fMRI scan in awake monkeys is possible by using a plastic head mask made to fit the skull of individual animals. In all of the three monkeys tested, longitudinal, quantitative assessment of head movements showed that the plastic mask has effectively suppressed head movements, and we were able to obtain reliable retinotopic BOLD signals in a standard retinotopic mapping task. The present, easy-to-make plastic mask has a strong potential to simplify fMRI experiments in awake monkeys, while giving data that is as good as or even better quality than that obtained with the conventional head-post method.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Tauber2024,

title = {Propofol-mediated unconsciousness disrupts progression of sensory signals through the cortical hierarchy},

author = {John M. Tauber and Scott L. Brincat and Emily P. Stephen and Jacob A. Donoghue and Leo Kozachkov and Emery N. Brown and Earl K. Miller},

doi = {10.1162/jocn_a_02081},

year  = {2024},

date = {2024-01-01},

journal = {Journal of Cognitive Neuroscience},

volume = {36},

number = {2},

pages = {394–413},

abstract = {A critical component of anesthesia is the loss of sensory perception. Propofol is the most widely used drug for general anesthesia, but the neural mechanisms of how and when it disrupts sensory processing are not fully understood. We analyzed local field potential and spiking recorded from Utah arrays in auditory cortex, associative cortex, and cognitive cortex of nonhuman primates before and during propofol-mediated unconsciousness. Sensory stimuli elicited robust and decodable stimulus responses and triggered periods of stimulus-related synchronization between brain areas in the local field potential of Awake animals. By contrast, propofol-mediated unconsciousness eliminated stimulus-related synchrony and drastically weakened stimulus responses and information in all brain areas except for auditory cortex, where responses and information persisted. However, we found stimuli occurring during spiking Up states triggered weaker spiking responses than in Awake animals in auditory cortex, and little or no spiking responses in higher order areas. These results suggest that propofol's effect on sensory processing is not just because of asynchronous Down states. Rather, both Down states and Up states reflect disrupted dynamics.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Tian2024,

title = {Mental programming of spatial sequences in working memory in the macaque frontal cortex},

author = {Zhenghe Tian and Jingwen Chen and Cong Zhang and Bin Min and Bo Xu and Liping Wang},

doi = {10.1126/science.adp6091},

year  = {2024},

date = {2024-01-01},

journal = {Science},

volume = {385},

number = {1437},

pages = {1–1},

abstract = {WM refers to our ability to temporarily maintain and manipulate information, which is foundational to the organization of goal-directed behavior. Although the nature of WM maintenance has been the focus of WM research in the past decades, WM manipulation or volitional control is more complex and has received less attention. The control process is what makes WM distinct and sets it apart from short-term memory. Previous human imaging studies have shown that the frontal cortex was highly involved inWM control. However, the neural dynamics and computational mechanisms supporting the control are not understood. We aimed to characterize these neural computations in the frontal cortex of nonhuman primates.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Uchimura2024,

title = {Neural transformation from retinotopic to background-centric coordinates in the macaque precuneus},

author = {Motoaki Uchimura and Hironori Kumano and Shigeru Kitazawa},

doi = {10.1523/JNEUROSCI.0892-24.2024},

year  = {2024},

date = {2024-01-01},

journal = {The Journal of Neuroscience},

volume = {44},

number = {48},

pages = {1–19},

abstract = {Visual information is initially represented in retinotopic coordinates and later in craniotopic coordinates. Psychophysical evidence suggests that visual information is further represented in more general coordinates related to the external world; however, the neural basis of nonegocentric coordinates remains elusive. This study investigates the automatic transformation from egocentric to nonegocentric coordinates in the macaque precuneus (two males, one female), identified by a functional imaging study as a key area for nonegocentric representation. We found that 6.2% of neurons in the precuneus have receptive fields (RFs) anchored to the background rather than to the retina or the head, while 16% had traditional retinotopic RFs. Notably, these two types were not exclusive: many background-centric neurons initially encode a stimulus' position in retinotopic coordinates (up to ∼90 ms from the stimulus onset) but later shift to background coordinates, peaking at ∼150 ms. Regarding retinotopic information, the stimulus dominated the initial period, whereas the background dominated the later period. In the absence of a background, there is a dramatic surge in retinotopic information about the stimulus during the later phase, clearly delineating two distinct periods of retinotopic encoding: one focusing on the figure to be attended and another on the background. These findings suggest that the initial retinotopic information of the stimulus is combined with the background retinotopic information in a subsequent stage, yielding a more stable representation of the stimulus relative to the background through time-division multiplexing.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Vieira2024,

title = {Temporal interference stimulation disrupts spike timing in the primate brain},

author = {Pedro G. Vieira and Matthew R. Krause and Christopher C. Pack},

doi = {10.1038/s41467-024-48962-2},

year  = {2024},

date = {2024-01-01},

journal = {Nature Communications},

volume = {15},

number = {1},

pages = {11–17},

publisher = {Springer US},

abstract = {Electrical stimulation can regulate brain activity, producing clear clinical benefits, but focal and effective neuromodulation often requires surgically implanted electrodes. Recent studies argue that temporal interference (TI) stimulation may provide similar outcomes non-invasively. During TI, scalp electrodes generate multiple electrical fields in the brain, modulating neural activity only at their intersection. Despite considerable enthusiasm for this approach, little empirical evidence demonstrates its effectiveness, especially under conditions suitable for human use. Here, using single-neuron recordings in non-human primates, we establish that TI reliably alters the timing, but not the rate, of spiking activity. However, we show that TI requires strategies—high carrier frequencies, multiple electrodes, and amplitude-modulated waveforms—that also limit its effectiveness. Combined, these factors make TI 80 % weaker than other forms of non-invasive brain stimulation. Although unlikely to cause widespread neuronal entrainment, TI may be ideal for disrupting pathological oscillatory activity, a hallmark of many neurological disorders.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Wang2024,

title = {Mixed coding of content-temporal detail by dorsomedial posterior parietal neurons},

author = {Lei Wang and Xufeng Zhou and Jie Yang and Fu Zeng and Shuzhen Zuo and Makoto Kusunoki and Huimin Wang and Yong-di Zhou and Aihua Chen and Sze Chai Kwok},

doi = {10.2139/ssrn.4216244},

year  = {2024},

date = {2024-01-01},

journal = {Journal of Neuroscience},

volume = {44},

number = {3},

pages = {1–16},

abstract = {The dorsomedial posterior parietal cortex (dmPPC) is part of a higher-cognition network implicated in elaborate processes under- pinning memory formation, recollection, episode reconstruction, and temporal information processing. Neural coding for complex episodic processing is however under-documented. Here, we recorded extracellular neural activities from three male rhesus macaques (Macaca mulatta) and revealed a set of neural codes of “neuroethogram” in the primate parietal cortex. Analyzing neural responses in macaque dmPPC to naturalistic videos, we discovered several groups of neurons that are sensitive to different categories of ethogram items, low-level sensory features, and saccadic eye movement. We also discovered that the processing of category and feature information by these neurons is sustained by the accumulation of temporal information over a long timescale of up to 30 s, corroborating its reported long temporal receptive windows. We performed an additional behavioral experiment with additional two male rhesus macaques and found that saccade-related activities could not account for the mixed neuronal responses elicited by the video stimuli. We further observed monkeys' scan paths and gaze consistency are modulated by video content. Taken altogether, these neural findings explain how dmPPC weaves fabrics of ongoing experiences together in real time. The high dimensionality of neural representations should motivate us to shift the focus of attention from pure selectivity neurons to mixed selectivity neurons, especially in increasingly complex naturalistic task designs.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Wong2024,

title = {Functional specialization and distributed processing across marmoset lateral prefrontal subregions},

author = {Raymond Ka Wong and Janahan Selvanayagam and Kevin Johnston and Stefan Everling},

doi = {10.1093/cercor/bhae407},

year  = {2024},

date = {2024-01-01},

journal = {Cerebral Cortex},

volume = {34},

number = {10},

pages = {1–15},

abstract = {A prominent aspect of primate lateral prefrontal cortex organization is its division into several cytoarchitecturally distinct subregions. Neurophysiological investigations in macaques have provided evidence for the functional specialization of these subregions, but an understanding of the relative representational topography of sensory, social, and cognitive processes within them remains elusive. One explanatory factor is that evidence for functional specialization has been compiled largely from a patchwork of findings across studies, in many animals, and with considerable variation in stimulus sets and tasks. Here, we addressed this by leveraging the common marmoset (Callithrix jacchus) to carry out large-scale neurophysiological mapping of the lateral prefrontal cortex using high-density microelectrode arrays, and a diverse suite of test stimuli including faces, marmoset calls, and spatial working memory task. Task-modulated units and units responsive to visual and auditory stimuli were distributed throughout the lateral prefrontal cortex, while those with saccade-related activity or face-selective responses were restricted to 8aV, 8aD, 10, 46 V, and 47. Neurons with contralateral visual receptive fields were limited to areas 8aV and 8aD. These data reveal a mixed pattern of functional specialization in the lateral prefrontal cortex, in which responses to some stimuli and tasks are distributed broadly across lateral prefrontal cortex subregions, while others are more limited in their representation.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Wu2024b,

title = {Mesoscopic calcium imaging in a head-unrestrained male non-human primate using a lensless microscope},

author = {Jimin Wu and Yuzhi Chen and Ashok Veeraraghavan and Eyal Seidemann and Jacob T. Robinson},

doi = {10.1038/s41467-024-45417-6},

year  = {2024},

date = {2024-01-01},

journal = {Nature Communications},

volume = {15},

number = {1},

pages = {1–14},

publisher = {Springer US},

abstract = {Mesoscopic calcium imaging enables studies of cell-type specific neural activity over large areas. A growing body of literature suggests that neural activity can be different when animals are free to move compared to when they are restrained. Unfortunately, existing systems for imaging calcium dynamics over large areas in non-human primates (NHPs) are table-top devices that require restraint of the animal's head. Here, we demonstrate an imaging device capable of imaging mesoscale calcium activity in a head-unrestrained male non-human primate. We successfully miniaturize our system by replacing lenses with an optical mask and computational algorithms. The resulting lensless microscope can fit comfortably on an NHP, allowing its head to move freely while imaging. We are able to measure orientation columns maps over a 20 mm2 field-of-view in a head-unrestrained macaque. Our work establishes mesoscopic imaging using a lensless microscope as a powerful approach for studying neural activity under more naturalistic conditions.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Xiao2024a,

title = {Feature-selective responses in macaque visual cortex follow eye movements during natural vision},

author = {Will Xiao and Saloni Sharma and Gabriel Kreiman and Margaret S. Livingstone},

doi = {10.1038/s41593-024-01631-5},

year  = {2024},

date = {2024-01-01},

journal = {Nature Neuroscience},

volume = {27},

number = {6},

pages = {1157–1166},

publisher = {Springer US},

abstract = {In natural vision, primates actively move their eyes several times per second via saccades. It remains unclear whether, during this active looking, visual neurons exhibit classical retinotopic properties, anticipate gaze shifts or mirror the stable quality of perception, especially in complex natural scenes. Here, we let 13 monkeys freely view thousands of natural images across 4.6 million fixations, recorded 883 h of neuronal responses in six areas spanning primary visual to anterior inferior temporal cortex and analyzed spatial, temporal and featural selectivity in these responses. Face neurons tracked their receptive field contents, indicated by category-selective responses. Self-consistency analysis showed that general feature-selective responses also followed eye movements and remained gaze-dependent over seconds of viewing the same image. Computational models of feature-selective responses located retinotopic receptive fields during free viewing. We found limited evidence for feature-selective predictive remapping and no viewing-history integration. Thus, ventral visual neurons represent the world in a predominantly eye-centered reference frame during natural vision.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Yang2024e,

title = {Assessment of visual function in blind mice and monkeys with subretinally implanted nanowire arrays as artificial photoreceptors},

author = {Ruyi Yang and Peng Zhao and Liyang Wang and Chenli Feng and Chen Peng and Zhexuan Wang and Yingying Zhang and Minqian Shen and Kaiwen Shi and Shijun Weng and Chunqiong Dong and Fu Zeng and Tianyun Zhang and Xingdong Chen and Shuiyuan Wang and Yiheng Wang and Yuanyuan Luo and Qingyuan Chen and Yuqing Chen and Chunhui Chengyong Jiang and Shanshan Jia and Zhaofei Yu and Jian Liu and Fei Wang and Su Jiang and Wendong Xu and Liang Li and Gang Wang and Xiaofen Mo and Gengfeng Zheng and Aihua Chen and Xingtao Zhou and Chunhui Chengyong Jiang and Yuanzhi Yuan and Biao Yan and Jiayi Zhang},

doi = {10.1038/s41551-023-01137-8},

year  = {2024},

date = {2024-01-01},

journal = {Nature Biomedical Engineering},

volume = {8},

number = {8},

pages = {1018–1039},

publisher = {Springer US},

abstract = {Retinal prostheses could restore image-forming vision in conditions of photoreceptor degeneration. However, contrast sensitivity and visual acuity are often insufficient. Here we report the performance, in mice and monkeys with induced photoreceptor degeneration, of subretinally implanted gold-nanoparticle-coated titania nanowire arrays providing a spatial resolution of 77.5 μm and a temporal resolution of 3.92 Hz in ex vivo retinas (as determined by patch-clamp recording of retinal ganglion cells). In blind mice, the arrays allowed for the detection of drifting gratings and flashing objects at light-intensity thresholds of 15.70–18.09 μW mm–2, and offered visual acuities of 0.3–0.4 cycles per degree, as determined by recordings of visually evoked potentials and optomotor-response tests. In monkeys, the arrays were stable for 54 weeks, allowed for the detection of a 10-μW mm–2 beam of light (0.5° in beam angle) in visually guided saccade experiments, and induced plastic changes in the primary visual cortex, as indicated by long-term in vivo calcium imaging. Nanomaterials as artificial photoreceptors may ameliorate visual deficits in patients with photoreceptor degeneration.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Yiling2024a,

title = {Joint encoding of stimulus and decision in monkey primary visual cortex},

author = {Yang Yiling and Johanna Klon-Lipok and Wolf Singer},

doi = {10.1093/cercor/bhad420},

year  = {2024},

date = {2024-01-01},

journal = {Cerebral Cortex},

volume = {34},

number = {1},

pages = {1–6},

abstract = {We investigated whether neurons in monkey primary visual cortex (V1) exhibit mixed selectivity for sensory input and behavioral choice. Parallel multisite spiking activity was recorded from area V1 of awake monkeys performing a delayed match-to-sample task. The monkeys had to make a forced choice decision of whether the test stimulus matched the preceding sample stimulus. The population responses evoked by the test stimulus contained information about both the identity of the stimulus and with some delay but before the onset of the motor response the forthcoming choice. The results of subspace identification analysis indicate that stimulus-specific and decision-related information coexists in separate subspaces of the high-dimensional population activity, and latency considerations suggest that the decision-related information is conveyed by top-down projections.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Yiling2024,

title = {Dynamic fading memory and expectancy effects in the monkey primary visual cortex},

author = {Yang Yiling and Johanna Klon Lipok and Katharine Shapcott and Andreea Lazar and Wolf Singer},

year  = {2024},

date = {2024-01-01},

journal = {Proceedings of the National Academy of Sciences},

volume = {121},

number = {8},

pages = {2024},

abstract = {In order to investigate the involvement of the primary visual cortex (V1) in working memory (WM), parallel, multisite recordings of multi-unit activity were obtained from monkey V1 while the animals performed a delayed match-to-sample (DMS) task. During the delay period, V1 population firing rate vectors maintained a lingering trace of the sample stimulus that could be reactivated by intervening impulse stimuli that enhanced neuronal firing. This fading trace of the sample did not require active engagement of the monkeys in the DMS task and likely reflects the intrinsic dynamics of recurrent cortical networks in lower visual areas. This renders an active, attention-dependent involvement of V1 in the maintenance of WM contents unlikely. By contrast, population responses to the test stimulus depended on the probabilistic contingencies between sample and test stimuli. Responses to tests that matched expectations were reduced which agrees with concepts of predictive coding.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Yoshida2024,

title = {Involvement of neurons in the nonhuman primate anterior striatum in proactive inhibition},

author = {Atsushi Yoshida and Okihide Hikosaka},

doi = {10.1523/JNEUROSCI.0866-24.2024},

year  = {2024},

date = {2024-01-01},

journal = {The Journal of Neuroscience},

volume = {44},

number = {49},

pages = {1–20},

abstract = {Behaving as desired requires selecting the appropriate behavior and inhibiting the selection of inappropriate behavior. This inhibitory function involves multiple processes, such as reactive and proactive inhibition, instead of a single process. In this study, two male macaque monkeys were required to perform a task in which they had to sequentially select (accept) or refuse (reject) a choice. Neural activity was recorded from the anterior striatum, which is considered to be involved in behavioral inhibition, focusing on the distinction between proactive and reactive inhibitions. We identified neurons with significant activity changes during the rejection of bad objects. Cluster analysis revealed three distinct groups, of which only one showed increased activity during object rejection, suggesting its involvement in proactive inhibition. This activity pattern was consistent irrespective of the rejection method, indicating a role beyond saccadic suppression. Furthermore, minimal activity changes during the fixation task indicated that these neurons were not primarily involved in reactive inhibition. In conclusion, these findings suggest that the anterior striatum plays a crucial role in cognitive control and orchestrates goal-directed behavior through proactive inhibition, which may be critical in understanding the mechanisms of behavioral inhibition dysfunction that occur in patients with basal ganglia disease.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Yu2024,

title = {Short-latency preference for faces in primate superior colliculus depends on visual cortex},

author = {Gongchen Yu and Leor N. Katz and Christian Quaia and Adam Messinger and Richard J. Krauzlis},

doi = {10.1016/j.neuron.2024.06.005},

year  = {2024},

date = {2024-01-01},

journal = {Neuron},

volume = {112},

number = {16},

pages = {2814–2822},

publisher = {Elsevier Inc.},

abstract = {Face processing is fundamental to primates and has been extensively studied in higher-order visual cortex. Here, we report that visual neurons in the midbrain superior colliculus (SC) of macaque monkeys display a preference for images of faces. This preference emerges within 40 ms of stimulus onset—well before “face patches” in visual cortex—and, at the population level, can be used to distinguish faces from other visual objects with accuracies of ∼80%. This short-latency face preference in SC depends on signals routed through early visual cortex because inactivating the lateral geniculate nucleus, the key relay from retina to cortex, virtually eliminates visual responses in SC, including face-related activity. These results reveal an unexpected circuit in the primate visual system for rapidly detecting faces in the periphery, complementing the higher-order areas needed for recognizing individual faces.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{YusifRodriguez2024,

title = {Different subregions of monkey lateral prefrontal cortex respond to abstract sequences and their components},

author = {Nadira Yusif Rodriguez and Aarit Ahuja and Debaleena Basu and Theresa H. McKim and Theresa M. Desrochers},

doi = {10.1523/JNEUROSCI.1353-24.2024},

year  = {2024},

date = {2024-01-01},

journal = {The Journal of Neuroscience},

volume = {44},

number = {47},

pages = {1–13},

abstract = {Sequential information permeates daily activities, such as when watching for the correct series of buildings to determine when to get off the bus or train. These sequences include periodicity (the spacing of the buildings), the identity of the stimuli (the kind of house), and higher-order more abstract rules that may not depend on the exact stimulus (e.g., house, house, house, business). Previously, we found that the posterior fundus of area 46 in the monkey lateral prefrontal cortex (LPFC) responds to rule changes in such abstract visual sequences. However, it is unknown if this region responds to other components of the sequence, i.e., image periodicity and identity, in isolation. Further, it is unknown if this region dissociates from other, more ventral LPFC subregions that have been associated with sequences and their components. To address these questions, we used awake functional magnetic resonance imaging in three male macaque monkeys during two no-report visual tasks. One task contained abstract visual sequences, and the other contained no visual sequences but maintained the same image periodicity and identities. We found the fundus of area 46 responded only to abstract sequence rule violations. In contrast, the ventral bank of area 46 responded to changes in image periodicity and identity, but not changes in the abstract sequence. These results suggest a functional specialization within anatomical substructures of LPFC to signal different kinds of stimulus regularities. This specialization may provide key scaffolding to identify abstract patterns and construct complex models of the world for daily living.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Zafirova2024,

title = {Configuration-sensitive face-body interactions in primate visual cortex},

author = {Yordanka Zafirova and Anna Bognár and Rufin Vogels},

doi = {10.1016/j.pneurobio.2023.102545},

year  = {2024},

date = {2024-01-01},

journal = {Progress in Neurobiology},

volume = {232},

pages = {1–16},

abstract = {Traditionally, the neural processing of faces and bodies is studied separately, although they are encountered together, as parts of an agent. Despite its social importance, it is poorly understood how faces and bodies interact, particularly at the single-neuron level. Here, we examined the interaction between faces and bodies in the macaque inferior temporal (IT) cortex, targeting an fMRI-defined patch. We recorded responses of neurons to monkey images in which the face was in its natural location (natural face-body configuration), or in which the face was mislocated with respect to the upper body (unnatural face-body configuration). On average, the neurons did not respond stronger to the natural face-body configurations compared to the summed responses to their faces and bodies, presented in isolation. However, the neurons responded stronger to the natural compared to the unnatural face-body configurations. This configuration effect was present for face- and monkey-centered images, did not depend on local feature differences between configurations, and was present when the face was replaced by a small object. The face-body interaction rules differed between natural and unnatural configurations. In sum, we show for the first time that single IT neurons process faces and bodies in a configuration-specific manner, preferring natural face-body configurations.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Zhang2024h,

title = {Testing Hubel and Wiesel's "ice-cube" model of functional maps at cellular resolution in macaque V1},

author = {Sheng Hui Zhang and Shi Ming Tang and Cong Yu},

doi = {10.1093/cercor/bhae471},

year  = {2024},

date = {2024-01-01},

journal = {Cerebral Cortex},

volume = {34},

number = {12},

pages = {1–11},

abstract = {Hubel and Wiesel's ice-cube model proposed that V1 orientation and ocular dominance functional maps intersect orthogonally to optimize wiring efficiency. Here, we revisited this model and additional arrangements at both cellular and pixel levels in awake macaques using two-photon calcium imaging. The recorded response fields of view were similar in size to hypercolumns, each containing up to 2,000 identified neurons and representing full periods of orientation preferences and ocular dominance. We estimated each neuron/pixel's orientation, ocular dominance, and spatial frequency preferences, constructed respective functional maps, computed geometric gradients of feature preferences, and calculated intersection angles among these gradients. At the cellular level, the intersection angles among functional maps were nearly evenly distributed. Nonetheless, pixel-based maps after Gaussian smoothing displayed orientation-ocular dominance and orientation-spatial frequency orthogonality, as well as ocular dominance-spatial frequency parallelism, in alignment with previous results, even though the trends were weak and highly variable. However, these Gaussian smoothing effects were not observed in cellular maps, indicating that the pixel-based trends may not accurately represent the relationships among feature-tuning properties of V1 neurons. We suggest that the widely distributed intersections among cellular maps can ensure that multiple stimulus features are represented within a hypercolumn, and no pair of features is represented with the least economical wiring (e.g. parallel intersections).},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Zhang2024i,

title = {Ocular dominance-dependent binocular combination of monocular neuronal responses in macaque V1},

author = {Sheng Hui Zhang and Xing Nan Zhao and Dan Qing Jiang and Shi Ming Tang and Cong Yu},

doi = {10.7554/eLife.92839},

year  = {2024},

date = {2024-01-01},

journal = {eLife},

volume = {13},

pages = {1–15},

abstract = {Primates rely on two eyes to perceive depth, while maintaining stable vision when either one eye or both eyes are open. Although psychophysical and modeling studies have investigated how monocular signals are combined to form binocular vision, the underlying neuronal mechanisms, particularly in V1 where most neurons exhibit binocularity with varying eye preferences, remain poorly understood. Here, we used two-photon calcium imaging to compare the monocular and binocular responses of thousands of simultaneously recorded V1 superficial-layer neurons in three awake macaques. During monocular stimulation, neurons preferring the stimulated eye exhibited significantly stronger responses compared to those preferring both eyes. However, during binocular stimulation, the responses of neurons preferring either eye were suppressed on the average, while those preferring both eyes were enhanced, resulting in similar neuronal responses irrespective of their eye preferences, and an overall response level similar to that with monocular viewing. A neuronally realistic model of binocular combination, which incorporates ocular dominance-dependent divisive interocular inhibition and binocular summation, is proposed to account for these findings.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Zhao2024c,

title = {Population coding for figure-ground texture segregation in macaque V1 and V4},

author = {Xing-Nan Zhao and Xing-Si Dong and Dan-Qing Jiang and Si Wu and Shi-Ming Tang and Cong Yu},

doi = {10.1016/j.pneurobio.2024.102655},

year  = {2024},

date = {2024-01-01},

journal = {Progress in Neurobiology},

volume = {240},

pages = {1–11},

abstract = {Object recognition often involves the brain segregating objects from their surroundings. Neurophysiological studies of figure-ground texture segregation have yielded inconsistent results, particularly on whether V1 neurons can perform figure-ground texture segregation or just detect texture borders. To address this issue from a population perspective, we utilized two-photon calcium imaging to simultaneously record the responses of large samples of V1 and V4 neurons to figure-ground texture stimuli in awake, fixating macaques. The average response changes indicate that V1 neurons mainly detect texture borders, while V4 neurons are involved in figure-ground segregation. However, population analysis (SVM decoding of PCA-transformed neuronal responses) reveal that V1 neurons not only detect figure-ground borders, but also contribute to figure-ground texture segregation, although requiring substantially more principal components than V4 neurons to reach a 75 % decoding accuracy. Individually, V1/V4 neurons showing larger (negative/positive) figure-ground response differences contribute more to figure-ground segregation. But for V1 neurons, the contribution becomes significant only when many principal components are considered. We conclude that V1 neurons participate in figure-ground segregation primarily by defining the figure borders, and the poorly structured figure-ground information V1 neurons carry could be further utilized by V4 neurons to accomplish figure-ground segregation.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Zhu2024f,

title = {Differential clustering of visual and choice- and saccade-related activity in macaque V3A and CIP},

author = {Zikang Zhu and Byounghoon Kim and Raymond Doudlah and Ting Yu Chang and Ari Rosenberg},

doi = {10.1152/jn.00285.2023},

year  = {2024},

date = {2024-01-01},

journal = {Journal of Neurophysiology},

volume = {131},

number = {4},

pages = {709–722},

abstract = {Neurons in sensory and motor cortices tend to aggregate in clusters with similar functional properties. Within the primate dorsal ("where") pathway, an important interface between three-dimensional (3-D) visual processing and motor-related functions consists of two hierarchically organized areas: V3A and the caudal intraparietal (CIP) area. In these areas, 3-D visual information, choice-related activity, and saccade-related activity converge, often at the single-neuron level. Characterizing the clustering of functional properties in areas with mixed selectivity, such as these, may help reveal organizational principles that support sensorimotor transformations. Here we quantified the clustering of visual feature selectivity, choice-related activity, and saccaderelated activity by performing correlational and parametric comparisons of the responses of well-isolated, simultaneously recorded neurons in macaque monkeys. Each functional domain showed statistically significant clustering in both areas. However, there were also domain-specific differences in the strength of clustering across the areas. Visual feature selectivity and saccade-related activity were more strongly clustered in V3A than in CIP. In contrast, choice-related activity was more strongly clustered in CIP than in V3A. These differences in clustering may reflect the areas' roles in sensorimotor processing. Stronger clustering of visual and saccade-related activity in V3A may reflect a greater role in within-domain processing, as opposed to cross-domain synthesis. In contrast, stronger clustering of choice-related activity in CIP may reflect a greater role in synthesizing information across functional domains to bridge perception and action.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Ziemba2024,

title = {Neuronal and behavioral responses to naturalistic texture im­ages in macaque monkeys},

author = {Corey M. Ziemba and Robbe L. T. Goris and Gabriel M. Stine and Richard K. Perez and Eero P. Simoncelli and J. Anthony Movshon},

doi = {10.1523/jneurosci.0349-24.2024},

year  = {2024},

date = {2024-01-01},

journal = {The Journal of Neuroscience},

volume = {44},

number = {42},

pages = {1–14},

abstract = {The visual world is richly adorned with texture, which can serve to delineate important elements of natural scenes. In anes­thetized macaque monkeys, selectivity for the statistical features of natural texture is weak in V1, but substantial in V2, sug­gesting that neuronal activity in V2 might directly support texture perception. To test this, we investigated the relation between single cell activity in macaque V1 and V2 and simultaneously measured behavioral judgments of texture. We generated stim­uli along a continuum between naturalistic texture and phase-randomized noise and trained two macaque monkeys to judge whether a sample texture more closely resembled one or the other extreme. Analysis of responses revealed that individual V1 and V2 neurons carried much less information about texture naturalness than behavioral reports. However, the sensitivity of V2 neurons, especially those preferring naturalistic textures, was significantly closer to that of behavior compared with V1. The firing of both V1 and V2 neurons predicted perceptual choices in response to repeated presentations of the same ambiguous stimulus in one monkey, despite low individual neural sensitivity. However, neither population predicted choice in the second monkey. We conclude that neural responses supporting texture perception likely continue to develop downstream of V2. Fur­ther, combined with neural data recorded while the same two monkeys performed an orientation discrimination task, our results demonstrate that choice-correlated neural activity in early sensory cortex is unstable across observers and tasks, untethered from neuronal sensitivity, and thus unlikely to reflect a critical aspect of the formation of perceptual decisions. Significance statement As visual signals propagate along the cortical hierarchy, they encode increasingly complex aspects of the sensory environment and likely have a more direct relationship with perceptual experience. We replicate and extend previous results from anes­thetized monkeys differentiating the selectivity of neurons along the first step in cortical vision from area V1 to V2. However, our results further complicate efforts to establish neural signatures that reveal the relationship between perception and the neu­ronal activity of sensory populations. We find that choice-correlated activity in V1 and V2 is unstable across different observers and tasks, and also untethered from neuronal sensitivity and other features of nonsensory response modulation.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Abbaszadeh2023,

title = {Prefrontal cortex encodes value pop-out in visual search},

author = {Mojtaba Abbaszadeh and Armin Panjehpour and Seyyed Mohammad Amin Alemohammad and Ali Ghavampour and Ali Ghazizadeh},

doi = {10.1016/j.isci.2023.107521},

year  = {2023},

date = {2023-01-01},

journal = {iScience},

volume = {26},

number = {9},

pages = {1–15},

publisher = {The Author(s)},

abstract = {Recent evidence demonstrates that long-term object value association can enhance visual search efficiency, a phenomenon known as value pop-out. However, the neural mechanism underlying this effect is not fully understood. Given the known role of the ventrolateral prefrontal cortex (vlPFC) in visual search and value memory, we recorded its single-unit activity (n = 526) in two macaque monkeys while they engaged in the value-driven search. Monkeys had to determine whether a high-value target was present within a variable number of low-value objects. Differential neural firing, as well as gamma-band power, indicated the presence of a target within ∼150ms of display onset. Notably, this differential activity was negatively correlated with search time and had reduced set-size dependence during efficient search. On the other hand, neural firing and its variability were higher in inefficient search. These findings implicate vlPFC in rapid detection of valuable targets which would be a crucial skill in competitive environments.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Andrei2023,

title = {Rapid compensatory plasticity revealed by dynamic correlated activity in monkeys in vivo},

author = {Ariana R. Andrei and Alan E. Akil and Natasha Kharas and Robert Rosenbaum and Krešimir Josić and Valentin Dragoi},

doi = {10.1038/s41593-023-01446-w},

year  = {2023},

date = {2023-01-01},

journal = {Nature Neuroscience},

volume = {26},

number = {11},

pages = {1960–1969},

publisher = {Springer US},

abstract = {To produce adaptive behavior, neural networks must balance between plasticity and stability. Computational work has demonstrated that network stability requires plasticity mechanisms to be counterbalanced by rapid compensatory processes. However, such processes have yet to be experimentally observed. Here we demonstrate that repeated optogenetic activation of excitatory neurons in monkey visual cortex (area V1) induces a population-wide dynamic reduction in the strength of neuronal interactions over the timescale of minutes during the awake state, but not during rest. This new form of rapid plasticity was observed only in the correlation structure, with firing rates remaining stable across trials. A computational network model operating in the balanced regime confirmed experimental findings and revealed that inhibitory plasticity is responsible for the decrease in correlated activity in response to repeated light stimulation. These results provide the first experimental evidence for rapid homeostatic plasticity that primarily operates during wakefulness, which stabilizes neuronal interactions during strong network co-activation.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Bigelow2023,

title = {Dissociation in neuronal encoding of object versus surface motion in the primate brain},

author = {Anthony Bigelow and Taekjun Kim and Tomoyuki Namima and Wyeth Bair and Anitha Pasupathy},

doi = {10.1016/j.cub.2023.01.016},

year  = {2023},

date = {2023-01-01},

journal = {Current Biology},

volume = {33},

number = {4},

pages = {711–719},

publisher = {Elsevier Inc.},

abstract = {A paradox exists in our understanding of motion processing in the primate visual system: neurons in the dorsal motion processing stream often strikingly fail to encode long-range and perceptually salient jumps of a moving stimulus. Psychophysical studies suggest that such long-range motion, which requires integration over more distant parts of the visual field, may be based on higher-order motion processing mechanisms that rely on feature or object tracking. Here, we demonstrate that ventral visual area V4, long recognized as critical for processing static scenes, includes neurons that maintain direction selectivity for long-range motion, even when conflicting local motion is present. These V4 neurons exhibit specific selectivity for the motion of objects, i.e., targets with defined boundaries, rather than the motion of surfaces behind apertures, and are selective for direction of motion over a broad range of spatial displacements and defined by a variety of features. Motion direction at a range of speeds can be accurately decoded on single trials from the activity of just a few V4 neurons. Thus, our results identify a novel motion computation in the ventral stream that is strikingly different from, and complementary to, the well-established system in the dorsal stream, and they support the hypothesis that the ventral stream system interacts with the dorsal stream to achieve the higher level of abstraction critical for tracking dynamic objects.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Boch2023,

title = {Functionally analogous body- and animacy-responsive areas are present in the dog (Canis familiaris) and human occipito-temporal lobe},

author = {Magdalena Boch and Isabella C. Wagner and Sabrina Karl and Ludwig Huber and Claus Lamm},

doi = {10.1038/s42003-023-05014-7},

year  = {2023},

date = {2023-01-01},

journal = {Communications Biology},

volume = {6},

number = {1},

pages = {1–15},

publisher = {Springer US},

abstract = {Comparing the neural correlates of socio-cognitive skills across species provides insights into the evolution of the social brain and has revealed face- and body-sensitive regions in the primate temporal lobe. Although from a different lineage, dogs share convergent visuo-cognitive skills with humans and a temporal lobe which evolved independently in carnivorans. We investigated the neural correlates of face and body perception in dogs (N = 15) and humans (N = 40) using functional MRI. Combining univariate and multivariate analysis approaches, we found functionally analogous occipito-temporal regions involved in the perception of animate entities and bodies in both species and face-sensitive regions in humans. Though unpredicted, we also observed neural representations of faces compared to inanimate objects, and dog compared to human bodies in dog olfactory regions. These findings shed light on the evolutionary foundations of human and dog social cognition and the predominant role of the temporal lobe.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Bourrelly2023,

title = {Rapid input-output transformation between local field potential and spiking activity during sensation but not action in the superior colliculus},

author = {Clara Bourrelly and Corentin Massot and Neeraj J. Gandhi},

doi = {10.1523/JNEUROSCI.2318-22.2023},

year  = {2023},

date = {2023-01-01},

journal = {Journal of Neuroscience},

volume = {43},

number = {22},

pages = {4047–4061},

abstract = {Sensorimotor transformation is the sequential process of registering a sensory signal in the environment and then responding with the relevant movement at an appropriate time. For visually guided eye movements, neural signatures in the form of spiking activity of neurons have been extensively studied along the dorsoventral axis of the superior colliculus (SC). In contrast, the local field potential (LFP), which represents the putative input to a region, remains largely unexplored in the SC. We therefore compared amplitude levels and onset times of both spike bursts and LFP modulations recorded simultaneously with a laminar probe along the dorsoventral axis of SC in 3 male monkeys performing the visually guided delayed saccade task. Both signals displayed a gradual transition from sensory activity in the superficial layers to a predominantly motor response in the deeper layers, although the transition from principally sensory to mostly motor response occurred;500 lm deeper for the LFP. For the sensory response, LFP modulation preceded spike burst onset by,5 ms in the superficial and intermediate layers and only when data were analyzed on a trial-by-trial basis. The motor burst in the spiking activity led LFP modulation by.25 ms in the deeper layers. The results reveal a fast and efficient input-output transformation between LFP modulation and spike burst in the visually responsive layers activity during sensation but not during action. The spiking pattern observed during the movement phase is likely dominated by intracollicular processing that is not captured in the LFP.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Brunamonti2023,

title = {Neuronal activity in posterior parietal cortex area LIP is not sufficient for saccadic eye movement production},

author = {Emiliano Brunamonti and Martin Paré},

doi = {10.3389/fnint.2023.1251431},

year  = {2023},

date = {2023-01-01},

journal = {Frontiers in Integrative Neuroscience},

pages = {1–14},

abstract = {It is widely recognized that the posterior parietal cortex (PPC) plays a role in active exploration with eye movements, arm reaching, and hand grasping. Whether this role is causal in nature is largely unresolved. One region of the PPC appears dedicated to the control of saccadic eye movement—lateral intraparietal (LIP) area. This area LIP possesses direct projections to well-established oculomotor centers and contains neurons with movement-related activity. In this study, we tested whether these neurons are implicated in saccade initiation and production. The movement-related activity of LIP neurons was tested by recording these neurons while monkeys performed a countermanding task. We found that LIP neuronal activity is not different before the execution or the cancelation of commanded saccades and thereby is not sufficient for the initiation and production of saccades. Consistent with the evolutionarily late emergence of the PPC, this finding relegates the role of this PPC area to processes that can regulate but not trigger eye movements.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Carlson2023,

title = {Does V1 response suppression initiate binocular rivalry?},

author = {Brock M. Carlson and Blake A. Mitchell and Kacie Dougherty and Jacob A. Westerberg and Michele A. Cox and Alexander Maier},

doi = {10.1016/j.isci.2023.107359},

year  = {2023},

date = {2023-01-01},

journal = {iScience},

volume = {26},

number = {8},

pages = {1–23},

publisher = {The Authors},

abstract = {During binocular rivalry (BR) only one eye's view is perceived. Neural underpinnings of BR are debated. Recent studies suggest that primary visual cortex (V1) initiates BR. One trigger might be response suppression across most V1 neurons at the onset of BR. Here, we utilize a variant of BR called binocular rivalry flash suppression (BRFS) to test this hypothesis. BRFS is identical to BR, except stimuli are shown with a ∼1s delay. If V1 response suppression was required to initiate BR, it should occur during BRFS as well. To test this, we compared V1 spiking in two macaques observing BRFS. We found that BRFS resulted in response facilitation rather than response suppression across V1 neurons. However, BRFS still reduces responses in a subset of V1 neurons due to the adaptive effects of asynchronous stimulus presentation. We argue that this selective response suppression could serve as an alternate initiator of BR.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Chakravarty2023,

title = {Closed-loop control of anesthetic state in nonhuman primates},

author = {Sourish Chakravarty and Jacob Donoghue and Ayan S. Waite and Meredith Mahnke and Indie C. Garwood and Sebastian Gallo and Earl K. Miller and Emery N. Brown},

doi = {10.1093/pnasnexus/pgad293},

year  = {2023},

date = {2023-01-01},

journal = {PNAS Nexus},

volume = {2},

number = {10},

pages = {1–14},

publisher = {Oxford University Press},

abstract = {Research in human volunteers and surgical patients has shown that unconsciousness under general anesthesia can be reliably tracked using real-time electroencephalogram processing. Hence, a closed-loop anesthesia delivery (CLAD) system that maintains precisely specified levels of unconsciousness is feasible and would greatly aid intraoperative patient management. The US Federal Drug Administration has approved no CLAD system for human use due partly to a lack of testing in appropriate animal models. To address this key roadblock, we implement a nonhuman primate (NHP) CLAD system that controls the level of unconsciousness using the anesthetic propofol. The key system components are a local field potential (LFP) recording system; propofol pharmacokinetics and pharmacodynamic models; the control variable (LFP power between 20 and 30 Hz), a programmable infusion system and a linear quadratic integral controller. Our CLAD system accurately controlled the level of unconsciousness along two different 125-min dynamic target trajectories for 18 h and 45 min in nine experiments in two NHPs. System performance measures were comparable or superior to those in previous CLAD reports. We demonstrate that an NHP CLAD system can reliably and accurately control in real-time unconsciousness maintained by anesthesia. Our findings establish critical steps for CLAD systems' design and testing prior to human testing.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Chen2023c,

title = {Stable neural population dynamics in the regression subspace for continuous and categorical task parameters in monkeys},

author = {He Chen and Jun Kunimatsu and Tomomichi Oya and Yuri Imaizumi and Yukiko Hori and Masayuki Matsumoto and Takafumi Minamimoto and Yuji Naya and Hiroshi Yamada},

doi = {10.1523/ENEURO.0016-23.2023},

year  = {2023},

date = {2023-01-01},

journal = {eNeuro},

volume = {10},

number = {7},

pages = {1–20},

abstract = {Neural population dynamics provide a key computational framework for understanding information processing in the sensory, cognitive, and motor functions of the brain. They systematically depict complex neural population activity, dominated by strong temporal dynamics as trajectory geometry in a low-dimensional neural space. However, neural population dynamics are poorly related to the conventional analytical framework of single-neuron activity, the rate-coding regime that analyzes firing rate modulations using task parameters. To link the rate-coding and dynamic models, we developed a variant of state-space analysis in the regression subspace, which describes the temporal structures of neural modulations using continuous and categorical task parameters. In macaque monkeys, using two neural population datasets containing either of two standard task parameters, continuous and categorical, we revealed that neural modulation structures are reliably captured by these task parameters in the regression subspace as trajectory geometry in a lower dimension. Furthermore, we combined the classical optimal-stimulus response analysis (usually used in rate-coding analysis) with the dynamic model and found that the most prominent modulation dynamics in the lower dimension were derived from these optimal responses. Using those analyses, we successfully extracted geometries for both task parameters that formed a straight geometry, suggesting that their functional relevance is characterized as a unidimensional feature in their neural modulation dynamics. Collectively, our approach bridges neural modulation in the rate-coding model and the dynamic system, and provides researchers with a significant advantage in exploring the temporal structure of neural modulations for pre-existing datasets.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Claron2023,

title = {Co-variations of cerebral blood volume and single neurons discharge during resting state and visual cognitive tasks in non-human primates},

author = {Julien Claron and Matthieu Provansal and Quentin Salardaine and Pierre Tissier and Alexandre Dizeux and Thomas Deffieux and Serge Picaud and Mickael Tanter and Fabrice Arcizet and Pierre Pouget},

doi = {10.1016/j.celrep.2023.112369},

year  = {2023},

date = {2023-01-01},

journal = {Cell Reports},

volume = {42},

number = {4},

pages = {1–16},

publisher = {The Author(s)},

abstract = {To better understand how the brain allows primates to perform various sets of tasks, the ability to simultaneously record neural activity at multiple spatiotemporal scales is challenging but necessary. However, the contribution of single-unit activities (SUAs) to neurovascular activity remains to be fully understood. Here, we combine functional ultrasound imaging of cerebral blood volume (CBV) and SUA recordings in visual and fronto-medial cortices of behaving macaques. We show that SUA provides a significant estimate of the neurovascular response below the typical fMRI spatial resolution of 2mm3. Furthermore, our results also show that SUAs and CBV activities are statistically uncorrelated during the resting state but correlate during tasks. These results have important implications for interpreting functional imaging findings while one constructs inferences of SUA during resting state or tasks.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Conroy2023,

title = {Inhibitory tagging in the superior colliculus during visual search},

author = {Christopher Conroy and Rakesh Nanjappa and Robert M. McPeek},

doi = {10.1152/jn.00095.2023},

year  = {2023},

date = {2023-01-01},

journal = {Journal of Neurophysiology},

volume = {130},

number = {4},

pages = {824–837},

abstract = {Inhibitory tagging is an important feature of many models of saccade target selection, in particular those that are based on the notion of a neural priority map. The superior colliculus (SC) has been suggested as a potential site of such a map, yet it is unknown whether inhibitory tagging is represented in the SC during visual search. In this study, we tested the hypothesis that SC neurons represent inhibitory tagging during search, as might be expected if they contribute to a priority map. To do so, we recorded the activity of SC neurons in a multisaccade visual-search task. On each trial, a single reward-bearing target was embedded in an array of physically identical, potentially reward-bearing targets and physically distinct, non-reward-bearing distractors. The task was to fixate the reward-bearing target. We found that, in the context of this task, the activity of many SC neurons was greater when their response field stimulus was a target than when it was a distractor and was reduced when it had been previously fixated relative to when it had not. Moreover, we found that the previous-fixation-related reduction of activity was larger for targets than for distractors and decreased with increasing time (or number of saccades) since fixation. Taken together, the results suggest that fixated stimuli are transiently inhibited in the SC during search, consistent with the notion that inhibitory tagging plays an important role in visual search and that SC neurons represent this inhibition as part of a priority map used for saccade target selection.NEW & NOTEWORTHY Searching a cluttered scene for an object of interest is a ubiquitous task in everyday life, which we often perform relatively quickly and efficiently. It has been suggested that to achieve such speed and efficiency an inhibitory-tagging mechanism inhibits saccades to objects in the scene once they have been searched and rejected. Here, we demonstrate that the superior colliculus represents this type of inhibition during search, consistent with its role in saccade target selection.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Corrigan2023,

title = {View cells in the hippocampus and prefrontal cortex of macaques during virtual navigation},

author = {Benjamin W. Corrigan and Roberto A. Gulli and Guillaume Doucet and Borna Mahmoudian and Mohamad Abbass and Megan Roussy and Rogelio Luna and Adam J. Sachs and Julio C. Martinez-Trujillo},

doi = {10.1002/hipo.23534},

year  = {2023},

date = {2023-01-01},

journal = {Hippocampus},

volume = {33},

number = {5},

pages = {573–585},

abstract = {Cells selectively activated by a particular view of an environment have been found in the primate hippocampus (HPC). Whether view cells are present in other brain areas, and how view selectivity interacts with other variables such as object features and place remain unclear. Here, we explore these issues by recording the responses of neurons in the HPC and the lateral prefrontal cortex (LPFC) of rhesus macaques performing a task in which they learn new context-object associations while navigating a virtual environment using a joystick. We measured neuronal responses at different locations in a virtual maze where animals freely directed gaze to different regions of the visual scenes. We show that specific views containing task relevant objects selectively activated a proportion of HPC units, and an even higher proportion of LPFC units. Place selectivity was scarce and generally dependent on view. Many view cells were not affected by changing the object color or the context cue, two task relevant features. However, a small proportion of view cells showed selectivity for these two features. Our results show that during navigation in a virtual environment with complex and dynamic visual stimuli, view cells are found in both the HPC and the LPFC. View cells may have developed as a multiarea specialization in diurnal primates to encode the complexities and layouts of the environment through gaze exploration which ultimately enables building cognitive maps of space that guide navigation.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Daumail2023,

title = {Rapid adaptation of primate LGN neurons to drifting grating stimulation},

author = {Loïc Daumail and Brock M. Carlson and Blake A. Mitchell and Michele A. Cox and Jacob A. Westerberg and Cortez Johnson and Paul R. Martin and Frank Tong and Alexander Maier and Kacie Dougherty},

doi = {10.1152/jn.00058.2022},

year  = {2023},

date = {2023-01-01},

journal = {Journal of Neurophysiology},

volume = {129},

number = {6},

pages = {1447–1467},

abstract = {The visual system needs to dynamically adapt to changing environments. Much is known about the adaptive effects of constant stimulation over prolonged periods. However, there are open questions regarding adaptation to stimuli that are changing over time, interrupted, or repeated. Feature-specific adaptation to repeating stimuli has been shown to occur as early as primary visual cortex (V1), but there is also evidence for more generalized, fatigue-like adaptation that might occur at an earlier stage of processing. Here, we show adaptation in the lateral geniculate nucleus (LGN) of awake, fixating monkeys following brief (1 s) exposure to repeated cycles of a 4-Hz drifting grating. We examined the relative change of each neuron's response across successive (repeated) grating cycles. We found that neurons from all cell classes (parvocellular, magnocellular, and koniocellular) showed significant adaptation. However, only magnocellular neurons showed adaptation when responses were averaged to a population response. In contrast to firing rates, response variability was largely unaffected. Finally, adaptation was comparable between monocular and binocular stimulation, suggesting that rapid LGN adaptation is monocular in nature.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Emonds2023,

title = {Object representation in a gravitational reference frame},

author = {Alexandriya M. X. Emonds and Ramanujan Srinath and Kristina J. Nielsen and Charles E. Connor},

doi = {10.7554/eLife.81701},

year  = {2023},

date = {2023-01-01},

journal = {eLife},

volume = {12},

pages = {1–14},

abstract = {When your head tilts laterally, as in sports, reaching, and resting, your eyes counterrotate less than 20%, and thus eye images rotate, over a total range of about 180°. Yet, the world appears stable and vision remains normal. We discovered a neural strategy for rotational stability in anterior inferotemporal cortex (IT), the final stage of object vision in primates. We measured object orientation tuning of IT neurons in macaque monkeys tilted +25 and –25° laterally, producing ~40° difference in retinal image orientation. Among IT neurons with consistent object orientation tuning, 63% remained stable with respect to gravity across tilts. Gravitational tuning depended on vestibular/somatosensory but also visual cues, consistent with previous evidence that IT processes scene cues for gravity's orientation. In addition to stability across image rotations, an internal gravitational reference frame is important for physical understanding of a world where object position, posture, structure, shape, movement, and behavior interact critically with gravity.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Fine2023,

title = {Abstract value encoding in neural populations but not single neurons},

author = {Justin M. Fine and David J. N. Maisson and Seng Bum Michael Yoo and Tyler V. Cash-Padgett and Maya Zhe Wang and Jan Zimmermann and Benjamin Y. Hayden},

doi = {10.1523/JNEUROSCI.1954-22.2023},

year  = {2023},

date = {2023-01-01},

journal = {Journal of Neuroscience},

volume = {43},

number = {25},

pages = {4650–4663},

abstract = {An important open question in neuroeconomics is how the brain represents the value of offers in a way that is both abstract (allowing for comparison) and concrete (preserving the details of the factors that influence value). Here, we examine neuronal responses to risky and safe options in five brain regions that putatively encode value in male macaques. Surprisingly, we find no detectable overlap in the neural codes used for risky and safe options, even when the options have identical subjective values (as revealed by preference) in any of the regions. Indeed, responses are weakly correlated and occupy distinct (semi-orthogonal) encoding subspaces. Notably, however, these subspaces are linked through a linear transform of their constituent encodings, a property that allows for comparison of dissimilar option types. This encoding scheme allows these regions to multiplex decision related processes: they can encode the detailed factors that influence offer value (here, risky and safety) but also directly compare dissimilar offer types. Together these results suggest a neuronal basis for the qualitatively different psychological properties of risky and safe options and highlight the power of population geometry to resolve outstanding problems in neural coding.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Fracasso2023,

title = {Peri-saccadic orientation identification performance and visual neural sensitivity are higher in the upper visual field},

author = {Alessio Fracasso and Antimo Buonocore and Ziad M. Hafed},

doi = {10.1523/JNEUROSCI.1740-22.2023},

year  = {2023},

date = {2023-01-01},

journal = {Journal of Neuroscience},

volume = {43},

number = {41},

pages = {6884–6897},

abstract = {Visual neural processing is distributed among a multitude of sensory and sensory-motor brain areas exhibiting varying degrees of functional specializations and spatial representational anisotropies. Such diversity raises the question of how perceptual performance is determined, at any one moment in time, during natural active visual behavior. Here, exploiting a known dichotomy between the primary visual cortex and superior colliculus in representing either the upper or lower visual fields, we asked whether peri-saccadic orientation identification performance is dominated by one or the other spatial anisotropy. Humans (48 participants, 29 females) reported the orientation of peri-saccadic upper visual field stimuli significantly better than lower visual field stimuli, unlike their performance during steady-state gaze fixation, and contrary to expected perceptual superiority in the lower visual field in the absence of saccades. Consistent with this, peri-saccadic superior colliculus visual neural responses in two male rhesus macaque monkeys were also significantly stronger in the upper visual field than in the lower visual field. Thus, peri-saccadic orientation identification performance is more in line with oculomotor, rather than visual, map spatial anisotropies.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Griggs2023,

title = {Decoding motor plans using a closed-loop ultrasonic brain–machine interface},

author = {Whitney S. Griggs and Sumner L. Norman and Thomas Deffieux and Florian Segura and Bruno Félix Osmanski and Geeling Chau and Vasileios Christopoulos and Charles Liu and Mickael Tanter and Mikhail G. Shapiro and Richard A. Andersen},

doi = {10.1038/s41593-023-01500-7},

year  = {2023},

date = {2023-01-01},

journal = {Nature Neuroscience},

volume = {27},

pages = {1–23},

publisher = {Springer US},

abstract = {Brain–machine interfaces (BMIs) enable people living with chronic paralysis to control computers, robots and more with nothing but thought. Existing BMIs have trade-offs across invasiveness, performance, spatial coverage and spatiotemporal resolution. Functional ultrasound (fUS) neuroimaging is an emerging technology that balances these attributes and may complement existing BMI recording technologies. In this study, we use fUS to demonstrate a successful implementation of a closed-loop ultrasonic BMI. We streamed fUS data from the posterior parietal cortex of two rhesus macaque monkeys while they performed eye and hand movements. After training, the monkeys controlled up to eight movement directions using the BMI. We also developed a method for pretraining the BMI using data from previous sessions. This enabled immediate control on subsequent days, even those that occurred months apart, without requiring extensive recalibration. These findings establish the feasibility of ultrasonic BMIs, paving the way for a new class of less-invasive (epidural) interfaces that generalize across extended time periods and promise to restore function to people with neurological impairments.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Herrera2023,

title = {Cortical origin of theta error signals},

author = {Beatriz Herrera and Amirsaman Sajad and Steven P. Errington and Jeffrey D. Schall and Jorge J. Riera},

doi = {10.1093/cercor/bhad367},

year  = {2023},

date = {2023-01-01},

journal = {Cerebral Cortex},

volume = {33},

number = {23},

pages = {11300–11319},

abstract = {A multi-scale approach elucidated the origin of the error-related-negativity (ERN), with its associated theta-rhythm, and the post-error-positivity (Pe) in macaque supplementary eye field (SEF). Using biophysical modeling, synaptic inputs to a subpopulation of layer-3 (L3) and layer-5 (L5) pyramidal cells (PCs) were optimized to reproduce error-related spiking modulation and inter-spike intervals. The intrinsic dynamics of dendrites in L5 but not L3 error PCs generate theta rhythmicity with random phases. Saccades synchronized the phases of the theta-rhythm, which was magnified on errors. Contributions from error PCs to the laminar current source density (CSD) observed in SEF were negligible and could not explain the observed association between error-related spiking modulation in L3 PCs and scalp-EEG. CSD from recorded laminar field potentials in SEF was comprised of multipolar components, with monopoles indicating strong electro-diffusion, dendritic/axonal electrotonic current leakage outside SEF, or violations of the model assumptions. Our results also demonstrate the involvement of secondary cortical regions, in addition to SEF, particularly for the later Pe component. The dipolar component from the observed CSD paralleled the ERN dynamics, while the quadrupolar component paralleled the Pe. These results provide the most advanced explanation to date of the cellular mechanisms generating the ERN.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Jendritza2023,

title = {Multi-area recordings and optogenetics in the awake, behaving marmoset},

author = {Patrick Jendritza and Frederike J. Klein and Pascal Fries},

doi = {10.1038/s41467-023-36217-5},

year  = {2023},

date = {2023-01-01},

journal = {Nature Communications},

volume = {14},

number = {1},

pages = {1–16},

publisher = {Springer US},

abstract = {The common marmoset has emerged as a key model in neuroscience. Marmosets are small in size, show great potential for genetic modification and exhibit complex behaviors. Thus, it is necessary to develop technology that enables monitoring and manipulation of the underlying neural circuits. Here, we describe a novel approach to record and optogenetically manipulate neural activity in awake, behaving marmosets. Our design utilizes a light-weight, 3D printed titanium chamber that can house several high-density silicon probes for semi-chronic recordings, while enabling simultaneous optogenetic stimulation. We demonstrate the application of our method in male marmosets by recording multi- and single-unit data from areas V1 and V6 with 192 channels simultaneously, and show that optogenetic activation of excitatory neurons in area V6 can influence behavior in a detection task. This method may enable future studies to investigate the neural basis of perception and behavior in the marmoset.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Katz2023,

title = {Correlated variability in primate superior colliculus depends on functional class},

author = {Leor N. Katz and Gongchen Yu and James P. Herman and Richard J. Krauzlis},

doi = {10.1038/s42003-023-04912-0},

year  = {2023},

date = {2023-01-01},

journal = {Communications Biology},

volume = {6},

number = {1},

pages = {1–13},

publisher = {Springer US},

abstract = {Correlated variability in neuronal activity (spike count correlations, rSC) can constrain how information is read out from populations of neurons. Traditionally, rSC is reported as a single value summarizing a brain area. However, single values, like summary statistics, stand to obscure underlying features of the constituent elements. We predict that in brain areas containing distinct neuronal subpopulations, different subpopulations will exhibit distinct levels of rSC that are not captured by the population rSC. We tested this idea in macaque superior colliculus (SC), a structure containing several functional classes (i.e., subpopulations) of neurons. We found that during saccade tasks, different functional classes exhibited differing degrees of rSC. “Delay class” neurons displayed the highest rSC, especially during saccades that relied on working memory. Such dependence of rSC on functional class and cognitive demand underscores the importance of taking functional subpopulations into account when attempting to model or infer population coding principles.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Koyano2023,

title = {Progressive neuronal plasticity in primate visual cortex during stimulus familiarization},

author = {Kenji W. Koyano and Elena M. Esch and Julie J. Hong and Elena N. Waidmann and Haitao Wu and David A. Leopold},

doi = {10.1126/sciadv.ade4648},

year  = {2023},

date = {2023-01-01},

journal = {Science Advances},

volume = {9},

number = {12},

pages = {1–12},

abstract = {The primate brain is equipped to learn and remember newly encountered visual stimuli such as faces and objects. In the macaque inferior temporal (IT) cortex, neurons mark the familiarity of a visual stimulus through response modification, often involving a decrease in spiking rate. Here, we investigate the emergence of this neural plasticity by longitudinally tracking IT neurons during several weeks of familiarization with face images. We found that most neurons in the anterior medial (AM) face patch exhibited a gradual decline in their late-phase visual responses to multiple stimuli. Individual neurons varied from days to weeks in their rates of plasticity, with time constants determined by the number of days of exposure rather than the cumulative number of presentations. We postulate that the sequential recruitment of neurons with experience-modified responses may provide an internal and graded measure of familiarity strength, which is a key mnemonic component of visual recognition.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{LaferSousa2023,

title = {Behavioral detectability of optogenetic stimulation of inferior temporal cortex varies with the size of concurrently viewed objects},

author = {Rosa Lafer-Sousa and Karen Wang and Reza Azadi and Emily Lopez and Simon Bohn and Arash Afraz},

doi = {10.1016/j.crneur.2022.100063},

year  = {2023},

date = {2023-01-01},

journal = {Current Research in Neurobiology},

volume = {4},

pages = {1–7},

publisher = {Elsevier B.V.},

abstract = {We have previously demonstrated that macaque monkeys can behaviorally detect a subtle optogenetic impulse delivered to their inferior temporal (IT) cortex. We have also shown that the ability to detect the cortical stimulation impulse varies depending on some characteristics of the visual images viewed at the time of brain stimulation, revealing the visual nature of the perceptual events induced by stimulation of the IT cortex. Here we systematically studied the effect of the size of viewed objects on behavioral detectability of optogenetic stimulation of the central IT cortex. Surprisingly, we found that behavioral detection of the same optogenetic impulse highly varies with the size of the viewed object images. Reduction of the object size in four steps from 8 to 1 degree of visual angle significantly decreased detection performance. These results show that identical stimulation impulses delivered to the same neural population induce variable perceptual events depending on the mere size of the objects viewed at the time of brain stimulation.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Levi2023,

title = {Sensory and choice responses in MT distinct from motion encoding},

author = {Aaron J. Levi and Yuan Zhao and Il Memming Park and Alexander C. Huk},

doi = {10.1523/JNEUROSCI.0267-22.2023},

year  = {2023},

date = {2023-01-01},

journal = {Journal of Neuroscience},

volume = {43},

number = {12},

pages = {2090–2103},

abstract = {The macaque middle temporal (MT) area is well known for its visual motion selectivity and relevance to motion perception, but the possibility of it also reflecting higher-level cognitive functions has largely been ignored. We tested for effects of task performance distinct from sensory encoding by manipulating subjects' temporal evidence-weighting strategy during a direction discrimination task while performing electrophysiological recordings from groups of MT neurons in rhesus macaques (one male, one female). This revealed multiple components of MT responses that were, surprisingly, not interpretable as behaviorally relevant modulations of motion encoding, or as bottom-up consequences of the readout of motion direction from MT. The time-varying motion-driven responses of MT were strongly affected by our strategic manipulation—but with time courses opposite the subjects' temporal weighting strategies. Furthermore, large choice-correlated signals were represented in population activity distinct from its motion responses, with multiple phases that lagged psychophysical readout and even continued after the stimulus (but which preceded motor responses). In summary, a novel experimental manipulation of strategy allowed us to control the time course of readout to challenge the correlation between sensory responses and choices, and population-level analyses of simultaneously recorded ensembles allowed us to identify strong signals that were so distinct from direction encoding that conventional, single-neuron-centric analyses could not have revealed or properly characterized them. Together, these approaches revealed multiple cognitive contributions to MT responses that are task related but not functionally relevant to encoding or decoding of motion for psychophysical direction discrimination, providing a new perspective on the assumed status of MT as a simple sensory area.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Liska2023,

title = {Running modulates primate and rodent visual cortex differently},

author = {John P. Liska and Declan P. Rowley and Trevor T. K. Nguyen and Jens-Oliver Muthmann and Daniel A. Butts and Jacob L. Yates and Alexander C. Huk and Liska John P. and Rowley Declan P. and Nguyen Trevor T. K. and Muthmann Jens-Oliver and Butts Daniel A. and Yates Jacob L. and Huk Alexander C.},

year  = {2023},

date = {2023-01-01},

journal = {eLife},

volume = {12},

number = {415},

pages = {1–30},

abstract = {When mice run, activity in their primary visual cortex (V1) is strongly modulated. This observation has altered conception of a brain region assumed to be a passive image processor. Extensive work has followed to dissect the circuits and functions of running-correlated modulation. However, it remains unclear whether visual processing in primates might similarly change during locomotion. We measured V1 activity in marmosets while they viewed stimuli on a treadmill. In contrast to mouse V1, marmoset V1 was slightly but reliably suppressed during running. Population-level analyses revealed trial-to-trial fluctuations of shared gain across V1 in both species, but these gain modulations were smaller and more often negatively correlated with running in marmosets. Thus, population-scale gain fluctuations of V1 reflect a common feature of mammalian visual cortical function, but important quantitative differences yield distinct consequences for the relation between vision and action in primates versus rodents.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Liu2023e,

title = {Probing the processing of facial expressions in monkeys via time perception and eye tracking},

author = {Xin He Liu and Lu Gan and Zhi Ting Zhang and Pan Ke Yu and Ji Dai},

doi = {10.24272/j.WEBBLE.2095-8137.2023.003},

year  = {2023},

date = {2023-01-01},

journal = {Zoological Research},

volume = {44},

number = {5},

pages = {882–893},

abstract = {Accurately recognizing facial expressions is essential for effective social interactions. Non-human primates (NHPs) are widely used in the study of the neural mechanisms underpinning facial expression processing, yet it remains unclear how well monkeys can recognize the facial expressions of other species such as humans. In this study, we systematically investigated how monkeys process the facial expressions of conspecifics and humans using eye-tracking technology and sophisticated behavioral tasks, namely the temporal discrimination task (TDT) and face scan task (FST). We found that monkeys showed prolonged subjective time perception in response to Negative facial expressions in monkeys while showing longer reaction time to Negative facial expressions in humans. Monkey faces also reliably induced divergent pupil contraction in response to different expressions, while human faces and scrambled monkey faces did not. Furthermore, viewing patterns in the FST indicated that monkeys only showed bias toward emotional expressions upon observing monkey faces. Finally, masking the eye region marginally decreased the viewing duration for monkey faces but not for human faces. By probing facial expression processing in monkeys, our study demonstrates that monkeys are more sensitive to the facial expressions of conspecifics than those of humans, thus shedding new light on inter-species communication through facial expressions between NHPs and humans.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Lupkin2023,

title = {Monkeys exhibit human-like gaze biases in economic decisions},

author = {Shira M. Lupkin and Vincent B. McGinty},

doi = {10.7554/eLife.78205},

year  = {2023},

date = {2023-01-01},

journal = {eLife},

volume = {12},

pages = {1–27},

abstract = {In economic decision-making individuals choose between items based on their perceived value. For both humans and nonhuman primates, these decisions are often carried out while shifting gaze between the available options. Recent studies in humans suggest that these shifts in gaze actively influence choice, manifesting as a bias in favor of the items that are viewed first, viewed last, or viewed for the overall longest duration in a given trial. This suggests a mechanism that links gaze behavior to the neural computations underlying value-based choices. In order to identify this mechanism, it is first necessary to develop and validate a suitable animal model of this behavior. To this end, we have created a novel value-based choice task for macaque monkeys that captures the essential features of the human paradigms in which gaze biases have been observed. Using this task, we identified gaze biases in the monkeys that were both qualitatively and quantita-tively similar to those in humans. In addition, the monkeys' gaze biases were well-explained using a sequential sampling model framework previously used to describe gaze biases in humans—the first time this framework has been used to assess value-based decision mechanisms in nonhuman primates. Together, these findings suggest a common mechanism that can explain gaze-related choice biases across species, and open the way for mechanistic studies to identify the neural origins of this behavior.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Madariaga2023,

title = {SaFiDe: Detection of saccade and fixation periods based on eye-movement attributes from video-oculography, scleral coil or electrooculography data},

author = {Samuel Madariaga and Cecilia Babul and José Ignacio Egaña and Iván Rubio-Venegas and Gamze Güney and Miguel Concha-Miranda and Pedro E. Maldonado and Christ Devia},

doi = {10.1016/j.mex.2023.102041},

year  = {2023},

date = {2023-01-01},

journal = {MethodsX},

volume = {10},

pages = {1–10},

publisher = {Elsevier B.V.},

abstract = {In this work we present SaFiDe, a deterministic method to detect eye movements (saccades and fixations) from eye-trace data. We developed this method for human and nonhuman primate data from video- and coil-recorded eye traces and further applied the algorithm to eye traces computed from electrooculograms. All the data analyzed were from free-exploration paradigms, where the main challenge was to detect periods of saccades and fixations that were uncued by the task. The method uses velocity and acceleration thresholds, calculated from the eye trace, to detect saccade and fixation periods. We show that our fully deterministic method detects saccades and fixations from eye traces during free visual exploration. The algorithm was implemented in MATLAB, and the code is publicly available on a GitHub repository. • The algorithm presented is entirely deterministic, simplifying the comparison between subjects and tasks. • Thus far, the algorithm presented can operate over video-based eye tracker data, human electrooculogram records, or monkey scleral eye coil data.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Maeda2023,

title = {Environmental context-dependent activation of dopamine neurons via putative amygdala-nigra pathway in macaques},

author = {Kazutaka Maeda and Ken Inoue and Masahiko Takada and Okihide Hikosaka},

doi = {10.1038/s41467-023-37584-9},

year  = {2023},

date = {2023-01-01},

journal = {Nature Communications},

volume = {14},

number = {1},

pages = {1–12},

publisher = {Springer US},

abstract = {Seeking out good and avoiding bad objects is critical for survival. In practice, objects are rarely good every time or everywhere, but only at the right time or place. Whereas the basal ganglia (BG) are known to mediate goal-directed behavior, for example, saccades to rewarding objects, it remains unclear how such simple behaviors are rendered contingent on higher-order factors, including environmental context. Here we show that amygdala neurons are sensitive to environments and may regulate putative dopamine (DA) neurons via an inhibitory projection to the substantia nigra (SN). In male macaques, we combined optogenetics with multi-channel recording to demonstrate that rewarding environments induce tonic firing changes in DA neurons as well as phasic responses to rewarding events. These responses may be mediated by disinhibition via a GABAergic projection onto DA neurons, which in turn is suppressed by an inhibitory projection from the amygdala. Thus, the amygdala may provide an additional source of learning to BG circuits, namely contingencies imposed by the environment.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{McGinty2023,

title = {Behavioral read-out from population value signals in primate orbitofrontal cortex},

author = {Vincent B. McGinty and Shira M. Lupkin},

doi = {10.1038/s41593-023-01473-7},

year  = {2023},

date = {2023-01-01},

journal = {Nature Neuroscience},

volume = {26},

number = {12},

pages = {2203–2212},

publisher = {Springer US},

abstract = {The primate orbitofrontal cortex (OFC) has long been recognized for its role in value-based decisions; however, the exact mechanism linking value representations in the OFC to decision outcomes has remained elusive. Here, to address this question, we show, in non-human primates, that trial-wise variability in choices can be explained by variability in value signals decoded from many simultaneously recorded OFC neurons. Mechanistically, this relationship is consistent with the projection of activity within a low-dimensional value-encoding subspace onto a potentially higher-dimensional, behaviorally potent output subspace. Identifying this neural–behavioral link answers longstanding questions about the role of the OFC in economic decision-making and suggests population-level read-out mechanisms for the OFC similar to those recently identified in sensory and motor cortex.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Mitchell2023,

title = {A role for ocular dominance in binocular integration},

author = {Blake A. Mitchell and Brock M. Carlson and Jacob A. Westerberg and Michele A. Cox and Alexander Maier},

doi = {10.1016/j.cub.2023.08.019},

year  = {2023},

date = {2023-01-01},

journal = {Current Biology},

volume = {33},

number = {18},

pages = {3884–3895},

publisher = {Elsevier Inc.},

abstract = {Neurons in the primate primary visual cortex (V1) combine left- and right-eye information to form a binocular output. Controversy surrounds whether ocular dominance, the preference of these neurons for one eye over the other, is functionally relevant. Here, we demonstrate that ocular dominance impacts gain control during binocular combination. We recorded V1 spiking activity while monkeys passively viewed grating stimuli. Gratings were either presented to one eye (monocular), both eyes with the same contrasts (binocular balanced), or both eyes with different contrasts (binocular imbalanced). We found that contrast placed in a neuron's dominant eye was weighted more strongly than contrast placed in a neuron's non-dominant eye. This asymmetry covaried with neurons' ocular dominance. We then tested whether accounting for ocular dominance within divisive normalization improves the fit to neural data. We found that ocular dominance significantly improved model performance, with interocular normalization providing the best fits. These findings suggest that V1 ocular dominance is relevant for response normalization during binocular stimulation.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Odean2023,

title = {Transient oscillations of neural firing rate associated with routing of evidence in a perceptual decision},

author = {Naomi N. Odean and Mehdi Sanayei and Michael N. Shadlen},

doi = {10.1523/JNEUROSCI.2200-22.2023},

year  = {2023},

date = {2023-01-01},

journal = {Journal of Neuroscience},

volume = {43},

number = {37},

pages = {6369–6383},

abstract = {To form a perceptual decision, the brain must acquire samples of evidence from the environment and incorporate them in computations that mediate choice behavior. While much is known about the neural circuits that process sensory information and those that form decisions, less is known about the mechanisms that establish the functional linkage between them. We trained monkeys of both sexes to make difficult decisions about the net direction of visual motion under conditions that required trial-by-trial control of functional connectivity. In one condition, the motion appeared at different locations on different trials. In the other, two motion patches appeared, only one of which was informative. Neurons in the parietal cortex produced brief oscillations in their firing rate at the time routing was established: upon onset of the motion display when its location was unpredictable across trials, and upon onset of an attention cue that indicated in which of two locations an informative patch of dots would appear. The oscillation was absent when the stimulus location was fixed across trials. We interpret the oscillation as a manifestation of the mechanism that establishes the source and destination of flexibly routed information, but not the transmission of the information per se.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Oor2023,

title = {Stimulus salience conflicts and colludes with endogenous goals during urgent choices},

author = {Emily E. Oor and Terrence R. Stanford and Emilio Salinas},

doi = {10.1016/j.isci.2023.106253},

year  = {2023},

date = {2023-01-01},

journal = {iScience},

volume = {26},

number = {3},

pages = {1–17},

publisher = {The Authors},

abstract = {Selecting where to look next depends on both the salience of objects and current goals (what we are looking for), but discerning their relative contributions over the time frame of typical visuomotor decisions (200–250 ms) has been difficult. Here we investigate this problem using an urgent choice task with which the two contributions can be dissociated and tracked moment by moment. Behavioral data from three monkeys corresponded with model-based predictions: when salience favored the target, perceptual performance evolved rapidly and steadily toward an asymptotic level; when salience favored the distracter, many rapid errors were produced and the rise in performance took more time—effects analogous to oculomotor and attentional capture. The results show that salience has a brief (∼50 ms) but inexorable impact that leads to exogenous, involuntary capture, and this can either help or hinder performance, depending on the alignment between salience and ongoing internal goals.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Orczyk2023,

title = {Saccadic inhibition during free viewing in macaque monkeys},

author = {John J. Orczyk and Annamaria Barczak and Monica N. O'Connell and Yoshinao Kajikawa},

doi = {10.1152/jn.00225.2022},

year  = {2023},

date = {2023-01-01},

journal = {Journal of Neurophysiology},

volume = {129},

number = {2},

pages = {356–367},

abstract = {We investigated the time courses of saccade rate following visual stimuli during three conditions of free viewing in macaque monkeys. Under all conditions, saccade rate decreased transiently after the onset of visual stimuli. These results suggest that saccadic inhibition occurs during free viewing.Through the process of saccadic inhibition, visual events briefly suppress eye movements including microsaccades. In humans, saccadic inhibition has been shown to occur in response to the presentation of parafoveal or peripheral visual distractors during fixation and target-directed saccades and to physical changes of behaviorally relevant visual objects. In monkeys performing tasks that controlled eye movements, saccadic inhibition of microsaccades and target-directed saccades has been shown. Using eye data from three previously published studies, we investigated how saccade rate changed while monkeys were presented with visual stimuli under conditions with loose or no viewing demands. In two conditions, animals passively sat while an LED lamp flashed or screen-wide images appeared in front of them. In the third condition, images were repeated semiperiodically while animals had to maintain their gaze within a wide rectangular area and detect oddballs. Despite animals not being required to maintain fixation or make saccades to particular targets, the onset of visual events led to a temporary reduction of saccade rate across all conditions. Interestingly, saccadic inhibition was found at image offsets as well. These results show that saccadic inhibition occurs in monkeys during free viewing.NEW & NOTEWORTHY We investigated the time courses of saccade rate following visual stimuli during three conditions of free viewing in macaque monkeys. Under all conditions, saccade rate decreased transiently after the onset of visual stimuli. These results suggest that saccadic inhibition occurs during free viewing.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{OrlandoDessaints2023,

title = {Tracking a moving visual target in the rhesus monkey: Influence of the occurrence frequency of the target path},

author = {Nicolas Orlando Dessaints and Laurent Goffart},

doi = {10.1152/jn.00280.2023},

year  = {2023},

date = {2023-01-01},

journal = {Journal of Neurophysiology},

volume = {130},

number = {6},

pages = {1425–1443},

abstract = {Following previous studies documenting the ability to generate anticipatory responses, we tested whether the repeated motion of a visual target along the same path affected its oculomotor tracking. In six rhesus monkeys, we evaluated how the frequency of a target path influenced the onset, accuracy, and velocity of eye movements. Three hundred milliseconds after its extinction, a central target reappeared and immediately moved toward the periphery in four possible (oblique) directions and at a constant speed (20°/s or 40°/s). During each daily session, the frequency of one motion direction was either uncertain (25% of trials) or certain (100% of trials). Our results show no reduction of saccade latency between the two sessions. No express saccades were observed in either session. A slow eye movement started after target onset (presaccadic glissade) and its velocity was larger during the "certain" sessions only with the 40°/s target. No anticipatory eye movement was observed. Longer intersaccadic intervals were found during the "certain" sessions but the postsaccadic pursuit velocity exhibited no change. No correlation was found between the accuracy and precision of saccades (interceptive or catch-up) and the postsaccadic pursuit velocity. Repeatedly tracking a target that moves always along the same path does not favor the generation of anticipatory eye movements, saccadic or slow. Their occurrence is not spontaneous but seems to require preliminary training. Finally, for both sessions, the lack of correlation between the saccade-related and pursuit-related kinematic parameters is consistent with separate control of saccadic and slow eye movements.NEW & NOTEWORTHY Following previous studies documenting anticipatory movements, we investigated how the frequency of occurrence of a target path influenced the generation of tracking eye movements. When present, the effects were small. The limited performance that we found suggests that anticipatory responses require preliminary training, in which case, they should not be considered as a behavioral marker of the primates' ability to extrapolate but the outcome of learning and remembering past experience.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{OrtizRios2023,

title = {Optogenetic stimulation of the primary visual cortex drives activity in the visual association cortex},

author = {Michael Ortiz-Rios and Beshoy Agayby and Fabien Balezeau and Marcus Haag and Samy Rima and Jaime Cadena-Valencia and Michael C. Schmid},

doi = {10.1016/j.crneur.2023.100087},

year  = {2023},

date = {2023-01-01},

journal = {Current Research in Neurobiology},

volume = {4},

pages = {1–13},

publisher = {Elsevier B.V.},

abstract = {Developing optogenetic methods for research in non-human primates (NHP) is important for translational neuroscience and for delineating brain function with unprecedented specificity. Here we assess, in macaque monkeys, the selectivity by which optogenetic stimulation of the primary visual cortex (V1) drives the local laminar and widespread cortical connectivity related to visual perception. Towards this end, we transfected neurons with light-sensitive channelrhodopsin in dorsal V1. fMRI revealed that optogenetic stimulation of V1 using blue light at 40 Hz increased functional activity in the visual association cortex, including areas V2/V3, V4, motion-sensitive area MT and frontal eye fields, although nonspecific heating and eye movement contributions to this effect could not be ruled out. Neurophysiology and immunohistochemistry analyses confirmed optogenetic modulation of spiking activity and opsin expression with the strongest expression in layer 4-B in V1. Stimulating this pathway during a perceptual decision task effectively elicited a phosphene percept in the receptive field of the stimulated neurons in one monkey. Taken together, our findings demonstrate the great potential of optogenetic methods to drive the large-scale cortical circuits of the primate brain with high functional and spatial specificity.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Park2023,

title = {Prior expectation enhances sensorimotor behavior by modulating population tuning and subspace activity in sensory cortex},

author = {JeongJun Park and Seolmin Kim and Hyung Goo R. Kim and Joonyeol Lee},

doi = {10.1126/sciadv.adg4156},

year  = {2023},

date = {2023-01-01},

journal = {Science Advances},

volume = {9},

number = {27},

pages = {1–20},

abstract = {Prior knowledge facilitates our perception and goal-directed behaviors, particularly when sensory input is lacking or noisy. However, the neural mechanisms underlying the improvement in sensorimotor behavior by prior expectations remain unknown. In this study, we examine the neural activity in the middle temporal (MT) area of visual cortex while monkeys perform a smooth pursuit eye movement task with prior expectation of the visual target's motion direction. Prior expectations discriminately reduce the MT neural responses depending on their preferred directions, when the sensory evidence is weak. This response reduction effectively sharpens neural population direction tuning. Simulations with a realistic MT population demonstrate that sharpening the tuning can explain the biases and variabilities in smooth pursuit, suggesting that neural computations in the sensory area alone can underpin the integration of prior knowledge and sensory evidence. State-space analysis further supports this by revealing neural signals of prior expectations in the MT population activity that correlate with behavioral changes.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Patel2023,

title = {Serotonergic modulation of local network processing in V1 mirrors previously reported signatures of local network modulation by spatial attention},

author = {Aashay M. Patel and Katsuhisa Kawaguchi and Lenka Seillier and Hendrikje Nienborg},

doi = {10.1111/ejn.15953},

year  = {2023},

date = {2023-01-01},

journal = {European Journal of Neuroscience},

volume = {57},

number = {8},

pages = {1368–1382},

abstract = {Sensory processing is influenced by neuromodulators such as serotonin, thought to relay behavioural state. Recent work has shown that the modulatory effect of serotonin itself differs with the animal's behavioural state. In primates, including humans, the serotonin system is anatomically important in the primary visual cortex (V1). We previously reported that in awake fixating macaques, serotonin reduces the spiking activity by decreasing response gain in V1. But the effect of serotonin on the local network is unknown. Here, we simultaneously recorded single-unit activity and local field potentials (LFPs) while iontophoretically applying serotonin in V1 of alert monkeys fixating on a video screen for juice rewards. The reduction in spiking response we observed previously is the opposite of the known increase of spiking activity with spatial attention. Conversely, in the local network (LFP), the application of serotonin resulted in changes mirroring the local network effects of previous reports in macaques directing spatial attention to the receptive field. It reduced the LFP power and the spike–field coherence, and the LFP became less predictive of spiking activity, consistent with reduced functional connectivity. We speculate that together, these effects may reflect the sensory side of a serotonergic contribution to quiet vigilance: The lower gain reduces the salience of stimuli to suppress an orienting reflex to novel stimuli, whereas at the network level, visual processing is in a state comparable to that of spatial attention.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Pattadkal2023,

title = {Ocular following eye movements in marmosets follow complex motion trajectories},

author = {Jagruti J. Pattadkal and Carrie Barr and Nicholas J. Priebe},

doi = {10.1523/ENEURO.0072-23.2023},

year  = {2023},

date = {2023-01-01},

journal = {eNeuro},

volume = {10},

number = {6},

pages = {1–9},

abstract = {Ocular following eye movements help stabilize images on the retina and offer a window to study motion inter-pretation by visual circuits. We use these ocular following eye movements to study motion integration behavior in the marmosets. We characterize ocular following responses in the marmosets using different moving stimuli such as dot patterns, gratings, and plaids. Marmosets track motion along different directions and exhibit spatial frequency and speed sensitivity, which closely matches the sensitivity reported in neurons from their mo-tion-selective area MT. Marmosets are also able to track the integrated motion of plaids, with tracking direction consistent with an intersection of constraints model of motion integration. Marmoset ocular following responses are similar to responses in macaques and humans with certain species-specific differences in peak sensitivities. Such motion-sensitive eye movement behavior in combination with direct access to cortical circuitry makes the marmoset model well suited to study the neural basis of motion integration.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Putnam2023,

title = {Dissociation of vicarious and experienced rewards by coupling frequency within the same neural pathway},

author = {Philip T. Putnam and Cheng Chi J. Chu and Nicholas A. Fagan and Olga Dal Monte and Steve W. C. Chang},

doi = {10.1016/j.neuron.2023.05.020},

year  = {2023},

date = {2023-01-01},

journal = {Neuron},

volume = {111},

number = {16},

pages = {2513–2522},

publisher = {Elsevier Inc.},

abstract = {Vicarious reward, essential to social learning and decision making, is theorized to engage select brain regions similarly to experienced reward to generate a shared experience. However, it is just as important for neural systems to also differentiate vicarious from experienced rewards for social interaction. Here, we investigated the neuronal interaction between the primate anterior cingulate cortex gyrus (ACCg) and the basolateral amygdala (BLA) when social choices made by monkeys led to either vicarious or experienced reward. Coherence between ACCg spikes and BLA local field potential (LFP) selectively increased in gamma frequencies for vicarious reward, whereas it selectively increased in alpha/beta frequencies for experienced reward. These respectively enhanced couplings for vicarious and experienced rewards were uniquely observed following voluntary choices. Moreover, reward outcomes had consistently strong directional influences from ACCg to BLA. Our findings support a mechanism of vicarious reward where social agency is tagged by interareal coordination frequency within the same shared pathway.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Raman2023,

title = {Bodies in motion: Unraveling the distinct roles of motion and shape in dynamic body responses in the temporal cortex},

author = {Rajani Raman and Anna Bognár and Ghazaleh Ghamkhari Nejad and Nick Taubert and Martin Giese and Rufin Vogels},

doi = {10.1016/j.celrep.2023.113438},

year  = {2023},

date = {2023-01-01},

journal = {Cell Reports},

volume = {42},

number = {12},

pages = {1–20},

abstract = {The temporal cortex represents social stimuli, including bodies. We examine and compare the contributions of dynamic and static features to the single-unit responses to moving monkey bodies in and between a patch in the anterior dorsal bank of the superior temporal sulcus (dorsal patch [DP]) and patches in the anterior inferotemporal cortex (ventral patch [VP]), using fMRI guidance in macaques. The response to dynamics varies within both regions, being higher in DP. The dynamic body selectivity of VP neurons correlates with static features derived from convolutional neural networks and motion. DP neurons' dynamic body selectivity is not predicted by static features but is dominated by motion. Whereas these data support the dominance of motion in the newly proposed “dynamic social perception” stream, they challenge the traditional view that distinguishes DP and VP processing in terms of motion versus static features, underscoring the role of inferotemporal neurons in representing body dynamics.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Reppert2023,

title = {Neural mechanisms for executive control of speed-accuracy trade-off},

author = {Thomas R. Reppert and Richard P. Heitz and Jeffrey D. Schall},

doi = {10.1016/j.celrep.2023.113422},

year  = {2023},

date = {2023-01-01},

journal = {Cell Reports},

volume = {42},

number = {11},

pages = {1–18},

publisher = {The Authors},

abstract = {The medial frontal cortex (MFC) plays an important but disputed role in speed-accuracy trade-off (SAT). In samples of neural spiking in the supplementary eye field (SEF) in the MFC simultaneous with the visuomotor frontal eye field and superior colliculus in macaques performing a visual search with instructed SAT, during accuracy emphasis, most SEF neurons discharge less from before stimulus presentation until response generation. Discharge rates adjust immediately and simultaneously across structures upon SAT cue changes. SEF neurons signal choice errors with stronger and earlier activity during accuracy emphasis. Other neurons signal timing errors, covarying with adjusting response time. Spike correlations between neurons in the SEF and visuomotor areas did not appear, disappear, or change sign across SAT conditions or trial outcomes. These results clarify findings with noninvasive measures, complement previous neurophysiological findings, and endorse the role of the MFC as a critic for the actor instantiated in visuomotor structures.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Rodriguez2023,

title = {Monkey dorsolateral prefrontal cortex represents abstract visual sequences during a no-report task},

author = {Nadira Yusif Rodriguez and Theresa H. McKim and Debaleena Basu and Aarit Ahuja and Theresa M. Desrochers},

doi = {10.1523/JNEUROSCI.2058-22.2023},

year  = {2023},

date = {2023-01-01},

journal = {Journal of Neuroscience},

volume = {43},

number = {15},

pages = {2741–2755},

abstract = {Monitoring sequential information is an essential component of our daily lives. Many of these sequences are abstract, in that they do not depend on the individual stimuli, but do depend on an ordered set of rules (e.g., chop then stir when cooking). Despite the ubiquity and utility of abstract sequential monitoring, little is known about its neural mechanisms. Human rostrolateral prefrontal cortex (RLPFC) exhibits specific increases in neural activity (i.e., “ramping”) during abstract sequences. Monkey dorsolateral prefrontal cortex (DLPFC) has been shown to represent sequential information in motor (not abstract) sequence tasks, and contains a subregion, area 46, with homologous functional connectivity to human RLPFC. To test the prediction that area 46 may represent abstract sequence information, and do so with parallel dynamics to those found in humans, we conducted functional magnetic resonance imaging (fMRI) in three male monkeys. When monkeys performed no-report abstract sequence viewing, we found that left and right area 46 responded to abstract sequential changes. Interestingly, responses to rule and number changes overlapped in right area 46 and left area 46 exhibited responses to abstract sequence rules with changes in ramping activation, similar to that observed in humans. Together, these results indicate that monkey DLPFC monitors abstract visual sequential information, potentially with a preference for different dynamics in the two hemispheres. More generally, these results show that abstract sequences are represented in functionally homologous regions across monkeys and humans.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Rouse2023,

title = {Topological insights into the neural basis of flexible behavior},

author = {Tevin C. Rouse and Amy M. Ni and Chengcheng Huang and Marlene R. Cohen},

doi = {10.1073/pnas.2219557120},

year  = {2023},

date = {2023-01-01},

journal = {Proceedings of the National Academy of Sciences},

volume = {120},

number = {24},

pages = {1–11},

abstract = {It is widely accepted that there is an inextricable link between neural computations, biological mechanisms, and behavior, but it is challenging to simultaneously relate all three. Here, we show that topological data analysis (TDA) provides an important bridge between these approaches to studying how brains mediate behavior. We demonstrate that cognitive processes change the topological description of the shared activity of populations of visual neurons. These topological changes constrain and distinguish between competing mechanistic models, are connected to subjects performance on a visual change detection task, and, via a link with network control theory, reveal a tradeoff between improving sensitivity to subtle visual stimulus changes and increasing the chance that the subject will stray off task. These connections provide a blueprint for using TDA to uncover the biological and computational mechanisms by which cognition affects behavior in health and disease.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Rouzitalab2023,

title = {Ensembles code for associative learning in the primate lateral prefrontal cortex},

author = {Alireza Rouzitalab and Chadwick B. Boulay and Jeongwon Park and Julio C. Martinez-Trujillo and Adam J. Sachs},

doi = {10.1016/j.celrep.2023.112449},

year  = {2023},

date = {2023-01-01},

journal = {Cell Reports},

volume = {42},

number = {5},

pages = {1–16},

publisher = {The Author(s)},

abstract = {The lateral prefrontal cortex (LPFC) of primates is thought to play a role in associative learning. However, it remains unclear how LPFC neuronal ensembles dynamically encode and store memories for arbitrary stimulus-response associations. We recorded the activity of neurons in LPFC of two macaques during an associative learning task using multielectrode arrays. During task trials, the color of a symbolic cue indicated the location of one of two possible targets for a saccade. During a trial block, multiple randomly chosen associations were learned by the subjects. A state-space analysis indicated that LPFC neuronal ensembles rapidly learn new stimulus-response associations mirroring the animals' learning. Multiple associations acquired during training are stored in a neuronal subspace and can be retrieved hours after learning. Finally, knowledge of old associations facilitates learning new, similar associations. These results indicate that neuronal ensembles in the primate LPFC provide a flexible and dynamic substrate for associative learning.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Russ2022,

title = {Temporal continuity shapes visual responses of macaque face patch neurons},

author = {Brian E. Brain E. Russ and Kenji W. Koyano and Julian Day-Cooney and Neda Perwez and David A. Leopold},

doi = {10.1016/j.neuron.2022.12.021},

year  = {2023},

date = {2023-01-01},

journal = {Neuron},

volume = {111},

number = {6},

pages = {903–914},

publisher = {Elsevier Inc.},

abstract = {Macaque inferior temporal cortex neurons respond selectively to complex visual images, with recent work showing that they are also entrained reliably by the evolving content of natural movies. To what extent does visual continuity itself shape the responses of high-level visual neurons? We addressed this question by measuring how cells in face-selective regions of the macaque temporal cortex were affected by the manipulation of a movie's temporal structure. Sampling the movie at 1s intervals, we measured neural responses to randomized, brief stimuli of different lengths, ranging from 800 ms dynamic movie snippets to 100 ms static frames. We found that the disruption of temporal continuity strongly altered neural response profiles, particularly in the early onset response period of the randomized stimulus. The results suggest that models of visual system function based on discrete and randomized visual presentations may not translate well to the brain's natural modes of operation.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Sachse2023,

title = {Dynamic attention signalling in V4: Relation to fast-spiking/non-fast-spiking cell class and population coupling},

author = {Elizabeth M. Sachse and Adam C. Snyder},

doi = {10.1111/ejn.15928},

year  = {2023},

date = {2023-01-01},

journal = {European Journal of Neuroscience},

volume = {57},

number = {6},

pages = {918–939},

abstract = {The computational role of a neuron during attention depends on its firing properties, neurotransmitter expression and functional connectivity. Neurons in the visual cortical area V4 are reliably engaged by selective attention but exhibit diversity in the effect of attention on firing rates and correlated variability. It remains unclear what specific neuronal properties shape these attention effects. In this study, we quantitatively characterised the distribution of attention modulation of firing rates across populations of V4 neurons. Neurons exhibited a continuum of time-varying attention effects. At one end of the continuum, neurons' spontaneous firing rates were slightly depressed with attention (compared to when unattended), whereas their stimulus responses were enhanced with attention. The other end of the continuum showed the converse pattern: attention depressed stimulus responses but increased spontaneous activity. We tested whether the particular pattern of time-varying attention effects that a neuron exhibited was related to the shape of their actions potentials (so-called ‘fast-spiking' [FS] neurons have been linked to inhibition) and the strength of their coupling to the overall population. We found an interdependence among neural attention effects, neuron type and population coupling. In particular, we found neurons for which attention enhanced spontaneous activity but suppressed stimulus responses were less likely to be fast-spiking (more likely to be non-fast-spiking) and tended to have stronger population coupling, compared to neurons with other types of attention effects. These results add important information to our understanding of visual attention circuits at the cellular level.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Stine2023,

title = {A neural mechanism for terminating decisions},

author = {Gabriel M. Stine and Eric M. Trautmann and Danique Jeurissen and Michael N. Shadlen},

doi = {10.1016/j.neuron.2023.05.028},

year  = {2023},

date = {2023-01-01},

journal = {Neuron},

volume = {111},

number = {16},

pages = {2601–2613},

publisher = {The Authors},

abstract = {The brain makes decisions by accumulating evidence until there is enough to stop and choose. Neural mechanisms of evidence accumulation are established in association cortex, but the site and mechanism of termination are unknown. Here, we show that the superior colliculus (SC) plays a causal role in terminating decisions, and we provide evidence for a mechanism by which this occurs. We recorded simultaneously from neurons in the lateral intraparietal area (LIP) and SC while monkeys made perceptual decisions. Despite similar trial-averaged activity, we found distinct single-trial dynamics in the two areas: LIP displayed drift-diffusion dynamics and SC displayed bursting dynamics. We hypothesized that the bursts manifest a threshold mechanism applied to signals represented in LIP to terminate the decision. Consistent with this hypothesis, SC inactivation produced behavioral effects diagnostic of an impaired threshold sensor and prolonged the buildup of activity in LIP. The results reveal the transformation from deliberation to commitment.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Takakuwa2023,

title = {Protocol for making an animal model of “blindsight” in macaque monkeys},

author = {Norihiro Takakuwa and Kaoru Isa and Reona Yamaguchi and Hirotaka Onoe and Jun Takahashi and Masatoshi Yoshida and Tadashi Isa},

doi = {10.1016/j.xpro.2022.101960},

year  = {2023},

date = {2023-01-01},

journal = {STAR Protocols},

volume = {4},

number = {1},

pages = {1–22},

publisher = {The Authors},

abstract = {Patients with damage to the primary visual cortex (V1) can respond correctly to visual stimuli in their lesion-affected visual field above the chance level, an ability named blindsight. Here, we present a protocol for making an animal model of blindsight in macaque monkeys. We describe the steps to perform pre-lesion training of monkeys on a visual task, followed by lesion surgery, post-lesion training, and evaluation of blindsight. This animal model can be used to investigate the source of visual awareness. For complete details on the use and execution of this protocol, please refer to Yoshida et al. (2008)1 and Takakuwa et al. (2021).2},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Talluri2023,

title = {Activity in primate visual cortex is minimally driven by spontaneous movements},

author = {Bharath Chandra Talluri and Incheol Kang and Adam Lazere and Katrina R. Quinn and Nicholas Kaliss and Jacob L. Yates and Daniel A. Butts and Hendrikje Nienborg},

doi = {10.1038/s41593-023-01459-5},

year  = {2023},

date = {2023-01-01},

journal = {Nature Neuroscience},

volume = {26},

number = {11},

pages = {1953–1959},

publisher = {Springer US},

abstract = {Organisms process sensory information in the context of their own moving bodies, an idea referred to as embodiment. This idea is important for developmental neuroscience, robotics and systems neuroscience. The mechanisms supporting embodiment are unknown, but a manifestation could be the observation in mice of brain-wide neuromodulation, including in the primary visual cortex, driven by task-irrelevant spontaneous body movements. We tested this hypothesis in macaque monkeys (Macaca mulatta), a primate model for human vision, by simultaneously recording visual cortex activity and facial and body movements. We also sought a direct comparison using an analogous approach to those used in mouse studies. Here we found that activity in the primate visual cortex (V1, V2 and V3/V3A) was associated with the animals' own movements, but this modulation was largely explained by the impact of the movements on the retinal image, that is, by changes in visual input. These results indicate that visual cortex in primates is minimally driven by spontaneous movements and may reflect species-specific sensorimotor strategies.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Tan2023a,

title = {Distinct lateral prefrontal regions are organized in an anterior-posterior functional gradient},

author = {Pin Kwang Tan and Cheng Tang and Roger Herikstad and Arunika Pillay and Camilo Libedinsky},

doi = {10.1523/JNEUROSCI.0007-23.2023},

year  = {2023},

date = {2023-01-01},

journal = {Journal of Neuroscience},

volume = {43},

number = {38},

pages = {6564–6572},

abstract = {The dorsolateral prefrontal cortex (dlPFC) is composed of multiple anatomically-defined regions involved in higher-order cognitive processes, including working memory and selective attention. It is organized in an anterior-posterior global gradient where posterior regions track changes in the environment while anterior regions support abstract neural representations. However, it remains unknown if such a global gradient results from a smooth gradient that spans regions, or an emergent property arising from functionally distinct regions, i.e. an areal gradient. Here, we recorded single-neurons in the dlPFC of non-human primates trained to perform a memory-guided saccade task with an interfering distractor, and analyzed their physiological properties along the anterior-posterior axis. We found that these physiological properties were best described by an areal gradient. Further, population analyses revealed that there is a distributed representation of spatial information across the dlPFC. Our results validate the functional boundaries between anatomically-defined dlPFC regions and highlight the distributed nature of computations underlying working memory across the dlPFC. Significance Statement Activity of frontal lobe regions is known to possess an anterior-posterior functional gradient. However, it is not known whether this gradient is the result of individual brain regions organized in a gradient (like a staircase), or a smooth gradient that spans regions (like a slide). Analysis of physiological properties of individual neurons in the primate frontal regions suggest that individual regions are organized as a gradient, rather than a smooth gradient. At the population level, working memory was more prominent in posterior regions, even though it was also present in anterior regions. This is consistent with the functional segregation of brain regions that is also observed in other systems (i.e. the visual system).},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Thompson2023,

title = {Hierarchical computation of 3D motion across macaque areas MT and FST},

author = {Lowell W. Thompson and Byounghoon Kim and Bas Rokers and Ari Rosenberg},

doi = {10.1016/j.celrep.2023.113524},

year  = {2023},

date = {2023-01-01},

journal = {Cell Reports},

volume = {42},

number = {12},

pages = {1–18},

publisher = {The Author(s)},

abstract = {Computing behaviorally relevant representations of three-dimensional (3D) motion from two-dimensional (2D) retinal signals is critical for survival. To ascertain where and how the primate visual system performs this computation, we recorded from the macaque middle temporal (MT) area and its downstream target, the fundus of the superior temporal sulcus (area FST). Area MT is a key site of 2D motion processing, but its role in 3D motion processing is controversial. The functions of FST remain highly underexplored. To distinguish representations of 3D motion from those of 2D retinal motion, we contrast responses to multiple motion cues during a motion discrimination task. The results reveal a hierarchical transformation whereby many FST but not MT neurons are selective for 3D motion. Modeling results further show how generalized, cue-invariant representations of 3D motion in FST may be created by selectively integrating the output of 2D motion selective MT neurons.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}