EyeLink Eye Trackers in Non-Human Primate Publications

@article{Yao2023a,

title = {High-dimensional topographic organization of visual features in the primate temporal lobe},

author = {Mengna Yao and Bincheng Wen and Mingpo Yang and Jiebin Guo and Haozhou Jiang and Chao Feng and Yilei Cao and Huiguang He and Le Chang},

doi = {10.1038/s41467-023-41584-0},

year  = {2023},

date = {2023-01-01},

journal = {Nature Communications},

volume = {14},

number = {1},

pages = {1–23},

publisher = {Springer US},

abstract = {The inferotemporal cortex supports our supreme object recognition ability. Numerous studies have been conducted to elucidate the functional organization of this brain area, but there are still important questions that remain unanswered, including how this organization differs between humans and non-human primates. Here, we use deep neural networks trained on object categorization to construct a 25-dimensional space of visual features, and systematically measure the spatial organization of feature preference in both male monkey brains and human brains using fMRI. These feature maps allow us to predict the selectivity of a previously unknown region in monkey brains, which is corroborated by additional fMRI and electrophysiology experiments. These maps also enable quantitative analyses of the topographic organization of the temporal lobe, demonstrating the existence of a pair of orthogonal gradients that differ in spatial scale and revealing significant differences in the functional organization of high-level visual areas between monkey and human brains.},

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pubstate = {published},

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}

@article{Yates2023,

title = {Detailed characterization of neural selectivity in free viewing primates},

author = {Jacob L. Yates and Shanna H. Coop and Gabriel H. Sarch and Ruei Jr Wu and Daniel A. Butts and Michele Rucci and Jude F. Mitchell},

doi = {10.1038/s41467-023-38564-9},

year  = {2023},

date = {2023-01-01},

journal = {Nature Communications},

volume = {14},

number = {1},

pages = {1–11},

publisher = {Springer US},

abstract = {Fixation constraints in visual tasks are ubiquitous in visual and cognitive neuroscience. Despite its widespread use, fixation requires trained subjects, is limited by the accuracy of fixational eye movements, and ignores the role of eye movements in shaping visual input. To overcome these limitations, we developed a suite of hardware and software tools to study vision during natural behavior in untrained subjects. We measured visual receptive fields and tuning properties from multiple cortical areas of marmoset monkeys who freely viewed full-field noise stimuli. The resulting receptive fields and tuning curves from primary visual cortex (V1) and area MT match reported selectivity from the literature which was measured using conventional approaches. We then combined free viewing with high-resolution eye tracking to make the first detailed 2D spatiotemporal measurements of foveal receptive fields in V1. These findings demonstrate the power of free viewing to characterize neural responses in untrained animals while simultaneously studying the dynamics of natural behavior.},

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pubstate = {published},

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}

@article{Yiling2023,

title = {Robust encoding of natural stimuli by neuronal response sequences in monkey visual cortex},

author = {Yang Yiling and Katharine Shapcott and Alina Peter and Johanna Klon-Lipok and Huang Xuhui and Andreea Lazar and Wolf Singer},

doi = {10.1038/s41467-023-38587-2},

year  = {2023},

date = {2023-01-01},

journal = {Nature Communications},

volume = {14},

number = {1},

pages = {1–18},

publisher = {Springer US},

abstract = {Parallel multisite recordings in the visual cortex of trained monkeys revealed that the responses of spatially distributed neurons to natural scenes are ordered in sequences. The rank order of these sequences is stimulus-specific and maintained even if the absolute timing of the responses is modified by manipulating stimulus parameters. The stimulus specificity of these sequences was highest when they were evoked by natural stimuli and deteriorated for stimulus versions in which certain statistical regularities were removed. This suggests that the response sequences result from a matching operation between sensory evidence and priors stored in the cortical network. Decoders trained on sequence order performed as well as decoders trained on rate vectors but the former could decode stimulus identity from considerably shorter response intervals than the latter. A simulated recurrent network reproduced similarly structured stimulus-specific response sequences, particularly once it was familiarized with the stimuli through non-supervised Hebbian learning. We propose that recurrent processing transforms signals from stationary visual scenes into sequential responses whose rank order is the result of a Bayesian matching operation. If this temporal code were used by the visual system it would allow for ultrafast processing of visual scenes.},

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pubstate = {published},

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}

@article{Yun2023,

title = {Distinct roles of the orbitofrontal cortex, ventral striatum, and dopamine neurons in counterfactual thinking of decision outcomes},

author = {Mengxi Yun and Masafumi Nejime and Takashi Kawai and Jun Kunimatsu and Hiroshi Yamada and Hyung Goo R. Kim and Masayuki Matsumoto},

doi = {10.1126/sciadv.adh2831},

year  = {2023},

date = {2023-01-01},

journal = {Science Advances},

volume = {9},

number = {32},

pages = {1–14},

abstract = {Individuals often assess past decisions by comparing what was gained with what would have been gained had they acted differently. Thoughts of past alternatives that counter what actually happened are called “counterfactuals.” Recent theories emphasize the role of the prefrontal cortex in processing counterfactual outcomes in decision-making, although how subcortical regions contribute to this process remains to be elucidated. Here we report a clear distinction among the roles of the orbitofrontal cortex, ventral striatum and midbrain dopamine neurons in processing counterfactual outcomes in monkeys. Our findings suggest that actually gained and counterfactual outcome signals are both processed in the cortico-subcortical network constituted by these regions but in distinct manners and integrated only in the orbitofrontal cortex in a way to compare these outcomes. This study extends the prefrontal theory of counterfactual thinking and provides key insights regarding how the prefrontal cortex cooperates with subcortical regions to make decisions using counterfactual information.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Zanini2023,

title = {Ultra-high field fMRI identifies an action-observation network in the common marmoset},

author = {Alessandro Zanini and Audrey Dureux and Janahan Selvanayagam and Stefan Everling},

doi = {10.1038/s42003-023-04942-8},

year  = {2023},

date = {2023-01-01},

journal = {Communications Biology},

volume = {6},

number = {1},

pages = {1–11},

abstract = {The observation of others' actions activates a network of temporal, parietal and premotor/prefrontal areas in macaque monkeys and humans. This action-observation network (AON) has been shown to play important roles in social action monitoring, learning by imitation, and social cognition in both species. It is unclear whether a similar network exists in New-World primates, which separated from Old-Word primates ~35 million years ago. Here we used ultra-high field fMRI at 9.4 T in awake common marmosets (Callithrix jacchus) while they watched videos depicting goal-directed (grasping food) or non-goal-directed actions. The observation of goal-directed actions activates a temporo-parieto-frontal network, including areas 6 and 45 in premotor/prefrontal cortices, areas PGa-IPa, FST and TE in occipito-temporal region and areas V6A, MIP, LIP and PG in the occipito-parietal cortex. These results show overlap with the humans and macaques' AON, demonstrating the existence of an evolutionarily conserved network that likely predates the separation of Old and New-World primates.},

keywords = {},

pubstate = {published},

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}

@article{Zhou2023c,

title = {Posterior parietal cortex plays a causal role in abstract memory-based visual categorical decisions},

author = {Yang Zhou and Ou Zhu and David J. Freedman},

doi = {10.1523/JNEUROSCI.2241-22.2023},

year  = {2023},

date = {2023-01-01},

journal = {Journal of Neuroscience},

volume = {43},

number = {23},

pages = {4315–4328},

abstract = {Neural activity in the lateral intraparietal cortex (LIP) correlates with both sensory evaluation and motor planning underlying visuomotor decisions. We previously showed that LIP plays a causal role in visually-based perceptual and categorical decisions, and preferentially contributes to evaluating sensory stimuli over motor planning. In that study, however, monkeys reported their decisions with a saccade to a colored target associated with the correct motion category or direction. Since LIP is known to play a role in saccade planning, it remains unclear whether LIP's causal role in such decisions extend to decision-making tasks which do not involve saccades. Here, we employed reversible pharmacological inactivation of LIP neural activity while two male monkeys performed delayed match to category (DMC) and delayed match to sample (DMS) tasks. In both tasks, monkeys needed to maintain gaze fixation throughout the trial and report whether a test stimulus was a categorical match or nonmatch to the previous sample stimulus by releasing a touch bar. LIP inactivation impaired monkeys' behavioral performance in both tasks, with deficits in both accuracy and reaction time (RT). Furthermore, we recorded LIP neural activity in the DMC task targeting the same cortical locations as in the inactivation experiments. We found significant neural encoding of the sample category, which was correlated with monkeys' categorical decisions in the DMC task. Taken together, our results demonstrate that LIP plays a generalized role in visual categorical decisions independent of the task-structure and motor response modality.},

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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.},

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pubstate = {published},

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}

@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.},

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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.},

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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{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.},

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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{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{Russ2023,

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}

}

@article{Tian2023,

title = {An ultraflexible electrode array for large-scale chronic recording in the nonhuman primate brain},

author = {Yixin Tian and Jiapeng Yin and Chengyao Wang and Zhenliang He and Jingyi Xie and Xiaoshan Feng and Yang Zhou and Tianyu Ma and Yang Xie and Xue Li and Tianming Yang and Chi Ren and Chengyu Li and Zhengtuo Zhao},

doi = {10.1002/advs.202302333},

year  = {2023},

date = {2023-01-01},

journal = {Advanced Science},

volume = {10},

number = {33},

pages = {1–15},

abstract = {Single-unit (SU) recording in nonhuman primates (NHPs) is indispensible in the quest of how the brain works, yet electrodes currently used for the NHP brain are limited in signal longevity, stability, and spatial coverage. Using new structural materials, microfabrication, and penetration techniques, we develop a mechanically robust ultraflexible, 1 µm thin electrode array (MERF) that enables pial penetration and high-density, large-scale, and chronic recording of neurons along both vertical and horizontal cortical axes in the nonhuman primate brain. Recording from three monkeys yields 2,913 SUs from 1,065 functional recording channels (up to 240 days), with some SUs tracked for up to 2 months. Recording from the primary visual cortex (V1) reveals that neurons with similar orientation preferences for visual stimuli exhibited higher spike correlation. Furthermore, simultaneously recorded neurons in different cortical layers of the primary motor cortex (M1) show preferential firing for hand movements of different directions. Finally, it is shown that a linear decoder trained with neuronal spiking activity across M1 layers during monkey's hand movements can be used to achieve on-line control of cursor movement. Thus, the MERF electrode array offers a new tool for basic neuroscience studies and brain–machine interface (BMI) applications in the primate brain.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Tremblay2023,

title = {Neural cognitive signals during spontaneous movements in the macaque},

author = {Sébastien Tremblay and Camille Testard and Ron W. Ditullio and Jeanne Inchauspé and Michael Petrides},

doi = {10.1038/s41593-022-01220-4},

year  = {2023},

date = {2023-01-01},

journal = {Nature Neuroscience},

volume = {26},

number = {2},

pages = {295–305},

publisher = {Springer US},

abstract = {The single-neuron basis of cognitive processing in primates has mostly been studied in laboratory settings where movements are severely restricted. It is unclear, therefore, how natural movements might affect neural signatures of cognition in the brain. Moreover, studies in mice indicate that body movements, when measured, account for most of the neural dynamics in the cortex. To examine these issues, we recorded from single-neuron ensembles in the prefrontal cortex in moving monkeys performing a cognitive task and characterized eye, head and body movements using video tracking. Despite considerable trial-to-trial movement variability, single-neuron tuning could be precisely measured and decision signals accurately decoded on a single-trial basis. Creating or abolishing spontaneous movements through head restraint and task manipulations had no measurable impact on neural responses. However, encoding models showed that uninstructed movements explained as much neural variance as task variables, with most movements aligned to task events. These results demonstrate that cognitive signals in the cortex are robust to natural movements, but also that unmeasured movements are potential confounds in cognitive neurophysiology experiments.},

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{Merken2022,

title = {Thin flexible arrays for long-term multi-electrode recordings in macaque primary visual cortex},

author = {Lara Merken and Maarten Schelles and Frederik Ceyssens and Michael Kraft and Peter Janssen},

doi = {10.1088/1741-2552/ac98e2},

year  = {2022},

date = {2022-12-01},

journal = {Journal of Neural Engineering},

pages = {1–14},

publisher = {IOP Publishing},

abstract = {Objective. Basic, translational and clinical neuroscience are increasingly focusing on large-scale invasive recordings of neuronal activity. However, in large animals such as nonhuman primates and humans – in which the larger brain size with sulci and gyri imposes additional challenges compared to rodents, there is a huge unmet need to record from hundreds of neurons simultaneously anywhere in the brain for long periods of time. Here, we tested the electrical and mechanical properties of thin, flexible multi-electrode arrays inserted into the primary visual cortex of two macaque monkeys, and assessed their Magnetic Resonance Imaging (MRI) compatibility and their capacity to record extracellular activity over a period of 1 year. Approach. To allow insertion of the floating arrays into the visual cortex, the 20 by 100 µm2 shafts were temporarily strengthened by means of a resorbable poly(lactic-co-glycolic acid) (PLGA) coating. Main results. After manual insertion of the arrays, the ex vivo and in vivo MRI compatibility of the arrays proved to be excellent. We recorded clear single-unit activity (SUA) from up to 50% of the electrodes, and multi-unit activity (MUA) on 60-100% of the electrodes, which allowed detailed measurements of the receptive fields and the orientation selectivity of the neurons. Even 1 year after insertion, we obtained significant MUA responses on 70-100% of the electrodes, while the receptive fields remained remarkably stable over the entire recording period. Significance. Thus, the thin and flexible multielectrode arrays we tested offer several crucial advantages compared to existing arrays, most notably in terms of brain tissue compliance, scalability, and brain coverage. Future brain-machine interface applications in humans may strongly benefit from this new generation of chronically implanted multi-electrode arrays.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Zhou2022g,

title = {Abstract encoding of categorical decisions in medial superior temporal and lateral intraparietal cortices},

author = {Yang Zhou and Krithika Mohan and David J. Freedman},

doi = {10.1523/jneurosci.0017-22.2022},

year  = {2022},

date = {2022-10-01},

journal = {Journal of Neuroscience},

volume = {42},

number = {48},

pages = {9069–9081},

publisher = {Society for Neuroscience},

abstract = {Categorization is an essential cognitive and perceptual process for decision making and recognition. The posterior parietal cortex (PPC), particularly the lateral intraparietal (LIP) area has been suggested to transform visual feature encoding into abstract categorical representations. By contrast, areas closer to sensory input, such as the middle temporal (MT) area, encode stimulus features but not more abstract categorical information during categorization tasks. Here, we compare the contributions of the medial superior temporal (MST) and LIP areas in category computation by recording neuronal activity in both areas from two male rhesus macaques trained to perform a visual motion categorization task. MST is a core motion processing area interconnected with MT, and often considered an intermediate processing stage between MT and LIP. Here we show that MST exhibits robust decision-correlated motion category encoding and working memory encoding similar to LIP, suggesting that MST plays a substantial role in cognitive computation, extending beyond its widely recognized role in visual motion processing. SIGNIFICANCE STATEMENT: Categorization requires assigning incoming sensory stimuli into behaviorally relevant groups. Previous work found that parietal area LIP shows a strong encoding of the learned category membership of visual motion stimuli, while visual area MT shows strong direction tuning but not category tuning during a motion direction categorization task. Here we show that area MST, a visual motion processing area interconnected with both LIP and MT, shows strong visual category encoding similar to that observed in LIP. This suggests that MST plays a greater role in abstract cognitive functions, extending beyond it well known role in visual motion processing.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Waidmann2022,

title = {Local features drive identity responses in macaque anterior face patches},

author = {Elena N. Waidmann and Kenji W. Koyano and Julie J. Hong and Brian E. Russ and David A. Leopold},

doi = {10.1038/s41467-022-33240-w},

year  = {2022},

date = {2022-01-01},

journal = {Nature Communications},

volume = {13},

number = {1},

pages = {1–13},

publisher = {Springer US},

abstract = {Humans and other primates recognize one another in part based on unique structural details of the face, including both local features and their spatial configuration within the head and body. Visual analysis of the face is supported by specialized regions of the primate cerebral cortex, which in macaques are commonly known as face patches. Here we ask whether the responses of neurons in anterior face patches, thought to encode face identity, are more strongly driven by local or holistic facial structure. We created stimuli consisting of recombinant photorealistic images of macaques, where we interchanged the eyes, mouth, head, and body between individuals. Unexpectedly, neurons in the anterior medial (AM) and anterior fundus (AF) face patches were predominantly tuned to local facial features, with minimal neural selectivity for feature combinations. These findings indicate that the high-level structural encoding of face identity rests upon populations of neurons specialized for local features.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Wang2022b,

title = {Pupil-linked arousal signals in the midbrain superior colliculus},

author = {Chin-an Wang and Brian White and Douglas P. Munoz},

year  = {2022},

date = {2022-01-01},

journal = {Journal of Cognitive Neuroscience},

volume = {34},

number = {8},

pages = {1340–1354},

abstract = {The orienting response evoked by the appearance of a salient stimulus is modulated by arousal; however, neural under- pinnings for the interplay between orienting and arousal are not well understood. The superior colliculus (SC), causally involved in multiple components of the orienting response including gaze and attention shifts, receives not only multisensory and cognitive inputs but also arousal-regulated inputs from various cortical and subcortical structures. To investigate the impact of moment-by-moment fluctuations in arousal on orienting saccade responses, we used microstimulation of the monkey SC to trigger saccade responses, and we used pupil size and velocity to index the level ofarousal at stimulation onset because these measures correlate with changes in brain states and locus coeruleus activity. Saccades induced by SC microstimulation correlated with prestimulation pupil velocity, with higher pupil velocities on trials without evoked saccades than with evoked saccades. In contrast, prestimulation absolute pupil size did not correlate with saccade behavior. Moreover, pupil velocity correlated with evoked saccade latency and metrics. Together, our results demonstrated that small fluctuations in arousal, indexed by pupil velocity, can modulate the saccade response evoked by SC microstimulation in awake behaving monkeys.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Wang2022f,

title = {A structural and functional subdivision in central orbitofrontal cortex},

author = {Maya Zhe Wang and Benjamin Y. Hayden and Sarah R. Heilbronner},

doi = {10.1038/s41467-022-31273-9},

year  = {2022},

date = {2022-01-01},

journal = {Nature Communications},

volume = {13},

number = {1},

pages = {1–12},

publisher = {Springer US},

abstract = {Economic choice requires many cognitive subprocesses, including stimulus detection, valuation, motor output, and outcome monitoring; many of these subprocesses are associated with the central orbitofrontal cortex (cOFC). Prior work has largely assumed that the cOFC is a single region with a single function. Here, we challenge that unified view with convergent anatomical and physiological results from rhesus macaques. Anatomically, we show that the cOFC can be subdivided according to its much stronger (medial) or weaker (lateral) bidirectional anatomical connectivity with the posterior cingulate cortex (PCC). We call these subregions cOFCm and cOFCl, respectively. These two subregions have notable functional differences. Specifically, cOFCm shows enhanced functional connectivity with PCC, as indicated by both spike-field coherence and mutual information. The cOFCm-PCC circuit, but not the cOFCl-PCC circuit, shows signatures of relaying choice signals from a non-spatial comparison framework to a spatially framed organization and shows a putative bidirectional mutually excitatory pattern.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Webb2022a,

title = {Remus: System for remote deep brain interventions},

author = {Taylor D. Webb and Matthew G. Wilson and Henrik Odéen and Jan Kubanek},

doi = {10.1016/j.isci.2022.105251},

year  = {2022},

date = {2022-01-01},

journal = {iScience},

volume = {25},

number = {11},

pages = {1–13},

abstract = {Transcranial-focused ultrasound brings personalized medicine to the human brain. Ultrasound can modulate neural activity or release drugs in specific neural circuits but this personalized approach requires a system that delivers ultrasound into specified targets flexibly and on command. We developed a remote ultrasound system (Remus) that programmatically targets deep brain regions with high spatiotemporal precision and in a multi-focal manner. We validated these functions by modulating two deep brain nuclei—the left and right lateral geniculate nucleus—in a task-performing nonhuman primate. This flexible system will enable researchers and clinicians to diagnose and treat specific deep brain circuits in a noninvasive yet targeted manner, thus embodying the promise of personalized treatments of brain disorders.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{WeinbergWolf2022,

title = {Increasing central serotonin with 5-hydroxytryptophan disrupts the inhibition of social gaze in nonhuman primates},

author = {Hannah B. Weinberg-Wolf and Nick Fagan and Olga Dal Monte and Steve W. C. Chang},

doi = {10.1523/JNEUROSCI.0413-21.2021},

year  = {2022},

date = {2022-01-01},

journal = {Journal of Neuroscience},

volume = {42},

number = {4},

pages = {670–681},

abstract = {To competently navigate the world, individuals must flexibly balance distinct aspects of social gaze, orienting toward others and inhibiting orienting responses, depending on the context. These behaviors are often disrupted amongst patient populations treated with serotonergic drugs. However, those in the field lack a clear understanding of how the serotonergic system mediates social orienting and inhibiting behaviors. Here, we tested how increasing central concentrations of serotonin with the direct precursor 5-hydroxytryptophan (5-HTP) would modulate the ability of rhesus macaques (both sexes) to use eye movements to flexibly orient to, or inhibit orienting to, faces. Systemic administrations of 5-HTP effectively increased central serotonin levels and impaired flexible orientation and inhibition. Critically, 5-HTP selectively impaired the ability of monkeys to inhibit orienting to face images, whereas it similarly impaired orienting to face and control images. 5-HTP also caused monkeys to perseverate on their gaze responses, making them worse at flexibly switching between orienting and inhibiting behaviors. Furthermore, the effects of 5-HTP on performance correlated with a constriction of the pupil, an increased time to initiate trials, and an increased reaction time, suggesting that the disruptive effects of 5-HTP on social gaze behaviors are likely driven by a downregulation of arousal and motivational states. Together, these findings provide causal evidence for a modulatory relationship between 5-HTP and social gaze behaviors in nonhuman primates and offer translational insights for the role of the serotonergic system in social gaze.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Westerberg2022,

title = {Laminar microcircuitry of visual cortex producing attention-associated electric fields},

author = {Jacob A. Westerberg and Michelle S. Schall and Alexander Maier and Geoffrey F. Woodman and Jeffrey D. Schall},

doi = {10.7554/eLife.72139},

year  = {2022},

date = {2022-01-01},

journal = {eLife},

volume = {11},

pages = {1–23},

abstract = {Cognitive operations are widely studied by measuring electric fields through EEG and ECoG. However, despite their widespread use, the neural circuitry giving rise to these signals remains unknown because the functional architecture of cortical columns producing attention-associated electric fields has not been explored. Here we detail the laminar cortical circuitry underlying an attention-associated electric field measured over posterior regions of the brain in humans and monkeys. First, we identified visual cortical area V4 as one plausible contributor to this attention-associated electric field through inverse modeling of cranial EEG in macaque monkeys performing a visual attention task. Next, we performed laminar neurophysiological recordings on the prelunate gyrus and identified the electric-field-producing dipoles as synaptic activity in distinct cortical layers of area V4. Specifically, activation in the extragranular layers of cortex resulted in the generation of the attention-associated dipole. Feature selectivity of a given cortical column determined the overall contribution to this electric field. Columns selective for the attended feature contributed more to the electric field than columns selective for a different feature. Lastly, the laminar profile of synaptic activity generated by V4 was sufficient to produce an attention-associated signal measurable outside of the column. These findings suggest that the top-down recipient cortical layers produce an attention-associated electric field that can be measured extracortically with the relative contribution of each column depending upon the underlying functional architecture.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Wild2022,

title = {Electrophysiological dataset from macaque visual cortical area MST in response to a novel motion stimulus},

author = {Benedict Wild and Amr Maamoun and Yifan Mayr and Ralf Brockhausen and Stefan Treue},

doi = {10.1038/s41597-022-01239-z},

year  = {2022},

date = {2022-01-01},

journal = {Scientific Data},

volume = {9},

pages = {1–10},

publisher = {Springer US},

abstract = {Establishing the cortical neural representation of visual stimuli is a central challenge of systems neuroscience. Publicly available data would allow a broad range of scientific analyses and hypothesis testing, but are rare and largely focused on the early visual system. To address the shortage of open data from higher visual areas, we provide a comprehensive dataset from a neurophysiology study in macaque monkey visual cortex that includes a complete record of extracellular action potential recordings from the extrastriate medial superior temporal (MST) area, behavioral data, and detailed stimulus records. It includes spiking activity of 172 single neurons recorded in 139 sessions from 4 hemispheres of 3 rhesus macaque monkeys. The data was collected across 3 experiments, designed to characterize the response properties of MST neurons to complex motion stimuli. This data can be used to elucidate visual information processing at the level of single neurons in a high-level area of primate visual cortex. Providing open access to this dataset also promotes the 3R-principle of responsible animal research.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Woo2022,

title = {The PRO model accounts for the anterior cingulate cortex role in risky decision-making and monitoring},

author = {Jae Hyung Woo and Habiba Azab and Andrew Jahn and Benjamin Hayden and Joshua W. Brown},

doi = {10.3758/s13415-022-00992-3},

year  = {2022},

date = {2022-01-01},

journal = {Cognitive, Affective, & Behavioral Neuroscience},

volume = {22},

number = {5},

pages = {952–968},

publisher = {Springer US},

abstract = {The anterior cingulate cortex (ACC) has been implicated in a number of functions, including performance monitoring and decision-making involving effort. The prediction of responses and outcomes (PRO) model has provided a unified account of much human and monkey ACC data involving anatomy, neurophysiology, EEG, fMRI, and behavior. We explored the computational nature of ACC with the PRO model, extending it to account specifically for both human and macaque monkey decision-making under risk, including both behavioral and neural data. We show that the PRO model can account for a number of additional effects related to outcome prediction, decision-making under risk, gambling behavior. In particular, we show that the ACC represents the variance of uncertain outcomes, suggesting a link between ACC function and mean-variance theories of decision making. The PRO model provides a unified account of a large set of data regarding the ACC.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Wu2022,

title = {Macaques preferentially attend to intermediately surprising information},

author = {Shengyi Wu and Tommy Blanchard and Emily Meschke and Richard N. Aslin and Benjamin Y. Hayden and Celeste Kidd},

doi = {10.1098/rsbl.2022.0144},

year  = {2022},

date = {2022-01-01},

journal = {Biology Letters},

volume = {18},

pages = {1–5},

abstract = {Normative learning theories dictate that we should preferentially attend to informative sources, but only up to the point that our limited learning systems can process their content. Humans, including infants, show this predicted strategic deployment of attention. Here, we demonstrate that rhesus monkeys, much like humans, attend to events of moderate surprisingness over both more and less surprising events. They do this in the absence of any specific goal or contingent reward, indicating that the behavioural pattern is spontaneous. We suggest this U-shaped attentional preference represents an evolutionarily preserved strategy for guiding intelligent organisms toward material that is maximally useful for learning.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Xie2022,

title = {Modulation of neuronal activity and saccades at theta rhythm during visual search in non-human primates},

author = {Jin Xie and Ting Yan and Jie Zhang and Zhengyu Ma and Huihui Zhou},

doi = {10.1007/s12264-022-00884-z},

year  = {2022},

date = {2022-01-01},

journal = {Neuroscience Bulletin},

volume = {38},

number = {10},

pages = {1183–1198},

publisher = {Springer Nature Singapore},

abstract = {Active exploratory behaviors have often been associated with theta oscillations in rodents, while theta oscillations during active exploration in non-human primates are still not well understood. We recorded neural activities in the frontal eye field (FEF) and V4 simultaneously when monkeys performed a free-gaze visual search task. Saccades were strongly phase-locked to theta oscillations of V4 and FEF local field potentials, and the phase-locking was dependent on saccade direction. The spiking probability of V4 and FEF units was significantly modulated by the theta phase in addition to the time-locked modulation associated with the evoked response. V4 and FEF units showed significantly stronger responses following saccades initiated at their preferred phases. Granger causality and ridge regression analysis showed modulatory effects of theta oscillations on saccade timing. Together, our study suggests phase-locking of saccades to the theta modulation of neural activity in visual and oculomotor cortical areas, in addition to the theta phase locking caused by saccade-triggered responses.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Xue2022,

title = {Dynamic task-belief is an integral part of decision-making},

author = {Cheng Xue and Lily E. Kramer and Marlene R. Cohen},

doi = {10.1016/j.neuron.2022.05.010},

year  = {2022},

date = {2022-01-01},

journal = {Neuron},

volume = {110},

number = {15},

pages = {2503–2511},

publisher = {Elsevier Inc.},

abstract = {Natural decisions involve two seemingly separable processes: inferring the relevant task (task-belief) and performing the believed-relevant task. The assumed separability has led to the traditional practice of studying task-switching and perceptual decision-making individually. Here, we used a novel paradigm to manipulate and measure macaque monkeys' task-belief and demonstrated inextricable neuronal links between flexible task-belief and perceptual decision-making. We showed that in animals, but not in artificial networks that performed as well or better than the animals, stronger task-belief is associated with better perception. Correspondingly, recordings from neuronal populations in cortical areas 7a and V1 revealed that stronger task-belief is associated with better discriminability of the believed-relevant, but not the believed-irrelevant, feature. Perception also impacts belief updating; noise fluctuations in V1 help explain how task-belief is updated. Our results demonstrate that complex tasks and multi-area recordings can reveal fundamentally new principles of how biology affects behavior in health and disease.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Yang2022a,

title = {Monkey plays Pac-Man with compositional strategies and hierarchical decision-making},

author = {Qianli Yang and Zhongqiao Lin and Wenyi Zhang and Jianshu Li and Xiyuan Chen and Jiaqi Zhang and Tianming Yang},

doi = {10.7554/eLife.74500},

year  = {2022},

date = {2022-01-01},

journal = {eLife},

volume = {11},

pages = {1–39},

abstract = {Humans can often handle daunting tasks with ease by developing a set of strategies to reduce decision-making into simpler problems. The ability to use heuristic strategies demands an advanced level of intelligence and has not been demonstrated in animals. Here, we trained macaque monkeys to play the classic video game Pac-Man. The monkeys' decision-making may be described with a strategy-based hierarchical decision-making model with over 90% accuracy. The model reveals that the monkeys adopted the take-the-best heuristic by using one dominating strategy for their decision-making at a time and formed compound strategies by assembling the basis strategies to handle particular game situations. With the model, the computationally complex but fully quan-tifiable Pac-Man behavior paradigm provides a new approach to understanding animals' advanced cognition.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Yoo2022a,

title = {Attention to visual motion suppresses neuronal and behavioral sensitivity in nearby feature space},

author = {Sang-Ah Yoo and Julio C. Martinez-Trujillo and Stefan Treue and John K. Tsotsos and Mazyar Fallah},

doi = {10.1186/s12915-022-01428-7},

year  = {2022},

date = {2022-01-01},

journal = {BMC Biology},

volume = {20},

number = {1},

pages = {1–19},

publisher = {BioMed Central},

abstract = {Background: Feature-based attention prioritizes the processing of the attended feature while strongly suppressing the processing of nearby ones. This creates a non-linearity or “attentional suppressive surround” predicted by the Selective Tuning model of visual attention. However, previously reported effects of feature-based attention on neuronal responses are linear, e.g., feature-similarity gain. Here, we investigated this apparent contradiction by neurophysiological and psychophysical approaches. Results: Responses of motion direction-selective neurons in area MT/MST of monkeys were recorded during a motion task. When attention was allocated to a stimulus moving in the neurons' preferred direction, response tuning curves showed its minimum for directions 60–90° away from the preferred direction, an attentional suppressive surround. This effect was modeled via the interaction of two Gaussian fields representing excitatory narrowly tuned and inhibitory widely tuned inputs into a neuron, with feature-based attention predominantly increasing the gain of inhibitory inputs. We further showed using a motion repulsion paradigm in humans that feature-based attention produces a similar non-linearity on motion discrimination performance. Conclusions: Our results link the gain modulation of neuronal inputs and tuning curves examined through the feature-similarity gain lens to the attentional impact on neural population responses predicted by the Selective Tuning model, providing a unified framework for the documented effects of feature-based attention on neuronal responses and behavior.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Zhang2022h,

title = {Surprise and recency in novelty detection in the primate brain},

author = {Kaining Zhang and Ethan S. Bromberg-Martin and Fatih Sogukpinar and Kim Kocher and Ilya E. Monosov},

doi = {10.1016/j.cub.2022.03.064},

year  = {2022},

date = {2022-01-01},

journal = {Current Biology},

volume = {32},

number = {10},

pages = {2160–2173},

publisher = {The Author(s)},

abstract = {Primates and other animals must detect novel objects. However, the neuronal mechanisms of novelty detection remain unclear. Prominent theories propose that visual object novelty is either derived from the computation of recency (how long ago a stimulus was experienced) or is a form of sensory surprise (stimulus unpredictability). Here, we use high-channel electrophysiology in primates to show that in many primate prefrontal, temporal, and subcortical brain areas, object novelty detection is intertwined with the computations of recency and sensory surprise. Also, distinct circuits could be engaged by expected versus unexpected sensory surprise. Finally, we studied neuronal novelty-to-familiarity transformations during learning across many days. We found a diversity of timescales in neurons' learning rates and between-session forgetting rates, both within and across brain areas, that are well suited to support flexible behavior and learning in response to novelty. Our findings show that novelty sensitivity arises on multiple timescales across single neurons due to diverse but related computations of sensory surprise and recency and shed light on the computational underpinnings of novelty detection in the primate brain.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Zhang2022i,

title = {Look twice: A generalist computational model predicts return fixations across tasks and species},

author = {Mengmi Zhang and Marcelo Armendariz and Will Xiao and Olivia Rose and Katarina Bendtz and Margaret Livingstone and Carlos Ponce and Gabriel Kreiman},

doi = {10.1371/journal.pcbi.1010654},

year  = {2022},

date = {2022-01-01},

journal = {PLoS Computational Biology},

volume = {18},

number = {11},

pages = {1–38},

abstract = {Primates constantly explore their surroundings via saccadic eye movements that bring different parts of an image into high resolution. In addition to exploring new regions in the visual field, primates also make frequent return fixations, revisiting previously foveated locations. We systematically studied a total of 44,328 return fixations out of 217,440 fixations. Return fixations were ubiquitous across different behavioral tasks, in monkeys and humans, both when subjects viewed static images and when subjects performed natural behaviors. Return fixations locations were consistent across subjects, tended to occur within short temporal offsets, and typically followed a 180-degree turn in saccadic direction. To understand the origin of return fixations, we propose a proof-of-principle, biologically-inspired and image-computable neural network model. The model combines five key modules: an image feature extractor, bottom-up saliency cues, task-relevant visual features, finite inhibition-of-return, and saccade size constraints. Even though there are no free parameters that are fine-tuned for each specific task, species, or condition, the model produces fixation sequences resembling the universal properties of return fixations. These results provide initial steps towards a mechanistic understanding of the trade-off between rapid foveal recognition and the need to scrutinize previous fixation locations.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Zhang2022k,

title = {Reward salience but not spatial attention dominates the value representation in the orbitofrontal cortex},

author = {Wenyi Zhang and Yang Xie and Tianming Yang},

doi = {10.1038/s41467-022-34084-0},

year  = {2022},

date = {2022-01-01},

journal = {Nature Communications},

volume = {13},

number = {1},

pages = {1–12},

publisher = {Springer US},

abstract = {The orbitofrontal cortex (OFC) encodes value and plays a key role in value-based decision-making. However, the attentional modulation of the OFC's value encoding is poorly understood. We trained two monkeys to detect a luminance change at a cued location between a pair of visual stimuli, which were over-trained pictures associated with different amounts of juice reward and, thus, different reward salience. Both the monkeys' behavior and the dorsolateral prefrontal cortex neuronal activities indicated that the monkeys actively directed their spatial attention toward the cued stimulus during the task. However, the OFC's neuronal responses were dominated by the stimulus with higher reward salience and encoded its value. The value of the less salient stimulus was only weakly represented regardless of spatial attention. The results demonstrate that reward and spatial attention are distinctly represented in the prefrontal cortex and the OFC maintains a stable representation of reward salience minimally affected by attention.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Zhang2022p,

title = {Evidence accumulation occurs locally in the parietal cortex},

author = {Zhewei Zhang and Chaoqun Yin and Tianming Yang},

doi = {10.1038/s41467-022-32210-6},

year  = {2022},

date = {2022-01-01},

journal = {Nature Communications},

volume = {13},

number = {1},

pages = {1–11},

publisher = {Springer US},

abstract = {Decision making often entails evidence accumulation, a process that is represented by neural activities in a network of multiple brain areas. Yet, it has not been identified where exactly the accumulation originates. We reason that a candidate brain area should both represent evidence accumulation and information that is used to compute evidence. Therefore, we designed a two-stage probabilistic reasoning task in which the evidence for accumulation had to be first determined from sensory signals orthogonal to decisions. With a linear encoding model, we decomposed the responses of posterior parietal neurons to each stimulus into an early and a late component that represented two dissociable stages of decision making. The former reflected the transformation from sensory inputs to accumulable evidence, and the latter reflected the accumulation of evidence and the formation of decisions. The presence of both computational stages indicates that evidence accumulation signal in the parietal cortex is computed locally.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Mitchell2022,

title = {Stimulating both eyes with matching stimuli enhances V1 responses},

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

doi = {10.1016/j.isci.2022.104182},

year  = {2022},

date = {2022-01-01},

journal = {iScience},

volume = {25},

pages = {1–20},

abstract = {Neurons in the primary visual cortex (V1) of primates play a key role in combining monocular inputs to form a binocular response. Although much has been gleaned from studying how V1 responds to discrepant (dichoptic) images, equally important is to understand how V1 responds to concordant (dioptic) images in the two eyes. Here, we investigated the extent to which concordant, balanced, zero-disparity binocular stimulation modifies V1 responses to varying stimulus contrast using intracranial multielectrode arrays. On average, binocular stimuli evoked stronger V1 activity than their monocular counterparts. This binocular facilitation scaled most proportionately with contrast during the initial transient. As V1 responses evolved, additional contrast-mediated dynamics emerged. Specifically, responses exhibited longer maintenance of facilitation for lower contrast and binocular suppression at high contrast. These results suggest that V1 processes concordant stimulation of both eyes in at least two sequential steps: initial response enhancement followed by contrast-dependent control of excitation.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Ni2022,

title = {Methylphenidate as a causal test of translational and basic neural coding hypotheses},

author = {Amy M. Ni and Brittany S. Bowes and Douglas A. Ruff and Marlene R. Cohen},

doi = {10.1073/pnas.2120529119},

year  = {2022},

date = {2022-01-01},

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

volume = {119},

number = {17},

pages = {1–7},

abstract = {Most systems neuroscience studies fall into one of two categories: basic science work aimed at understanding the relationship between neurons and behavior, or translational work aimed at developing treatments for neuropsychiatric disorders. Here we use these two approaches to inform and enhance each other. Our study both tests hypotheses about basic science neural coding principles and elucidates the neuronal mechanisms underlying clinically relevant behavioral effects of systemically administered methylphenidate (Ritalin). We discovered that orally administered methylphenidate, used clinically to treat attention deficit hyperactivity disorder (ADHD) and generally to enhance cognition, increases spatially selective visual attention, enhancing visual performance at only the attended location. Further, we found that this causal manipulation enhances vision in rhesus macaques specifically when it decreases the mean correlated variability of neurons in visual area V4. Our findings demonstrate that the visual system is a platform for understanding the neural underpinnings of both complex cognitive processes (basic science) and neuropsychiatric disorders (translation). Addressing basic science hypotheses, our results are consistent with a scenario in which methylphenidate has cognitively specific effects by working through naturally selective cognitive mechanisms. Clinically, our findings suggest that the often staggeringly specific symptoms of neuropsychiatric disorders may be caused and treated by leveraging general mechanisms.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Niemeyer2022,

title = {Perceptual enhancement and suppression correlate with V1 neural activity during active sensing},

author = {James E. Niemeyer and Seth Akers-Campbell and Aaron Gregoire and Michael A. Paradiso},

doi = {10.1016/j.cub.2022.04.067},

year  = {2022},

date = {2022-01-01},

journal = {Current Biology},

volume = {32},

pages = {2654–2667},

publisher = {Elsevier Inc.},

abstract = {Perception in multiple sensory modalities is an active process that involves exploratory behaviors. In humans and other primates, vision results from sensory sampling guided by saccadic eye movements. Saccades are known to modulate visual perception, and a corollary discharge signal associated with saccades appears to establish a sense of visual stability. Neural recordings have shown that saccades also modulate activity widely across the brain. To investigate the neural basis of saccadic effects on perception, simultaneous recordings from multiple neurons in area V1 were made as animals performed a contrast detection task. Perceptual and neural measures were compared when the animal made real saccades that brought a stimulus into V1 receptive fields and when simulated saccades were made (identical retinal stimulation but no eye movement). When real saccades were made and low spatial frequency stimuli were presented, we observed a reduction in both perceptual sensitivity and neural activity compared with simulated saccades; conversely, with higher spatial frequency stimuli, saccades increased visual sensitivity and neural activity. The performance of neural decoders, which used the activity of the population of simultaneously recorded neurons, showed saccade effects on sensitivity that mirrored the frequency-dependent perceptual changes, suggesting that the V1 population activity could support the perceptual effects. A minority of V1 neurons had significant choice probabilities, and the saccades decreased both average choice probability and pairwise noise correlations. Taken together, the findings suggest that a signal related to saccadic eye movements alters V1 spiking to increase the independence of spiking neurons and bias the system toward processing higher spatial frequencies, presumably to enhance object recognition. The effects of saccades on visual perception and noise correlations appear to parallel effects observed in other sensory modalities, suggesting a general principle of active sensory processing.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Pai2022,

title = {Laser stimulation of the skin for quantitative study of decision-making and motivation},

author = {Julia Pai and Takaya Ogasawara and Ethan S. Bromberg-Martin and Kei Ogasawara and Robert W. Gereau and Ilya E. Monosov},

doi = {10.1016/j.crmeth.2022.100296},

year  = {2022},

date = {2022-01-01},

journal = {Cell Reports Methods},

volume = {2},

number = {9},

pages = {1–18},

publisher = {The Authors},

abstract = {Neuroeconomics studies how decision-making is guided by the value of rewards and punishments. But to date, little is known about how noxious experiences impact decisions. A challenge is the lack of an aversive stimulus that is dynamically adjustable in intensity and location, readily usable over many trials in a single experimental session, and compatible with multiple ways to measure neuronal activity. We show that skin laser stimulation used in human studies of aversion can be used for this purpose in several key animal models. We then use laser stimulation to study how neurons in the orbitofrontal cortex (OFC), an area whose many roles include guiding decisions among different rewards, encode the value of rewards and punishments. We show that some OFC neurons integrated the positive value of rewards with the negative value of aversive laser stimulation, suggesting that the OFC can play a role in more complex choices than previously appreciated.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Pakravan2022,

title = {Coordinated multivoxel coding beyond univariate effects is not likely to be observable in fMRI data},

author = {Mansooreh Pakravan and Mojtaba Abbaszadeh and Ali Ghazizadeh},

doi = {10.1016/j.neuroimage.2021.118825},

year  = {2022},

date = {2022-01-01},

journal = {NeuroImage},

volume = {247},

pages = {1–14},

publisher = {Elsevier Inc.},

abstract = {Simultaneous recording of activity across brain regions can contain additional information compared to regional recordings done in isolation. In particular, multivariate pattern analysis (MVPA) across voxels has been interpreted as evidence for distributed coding of cognitive or sensorimotor processes beyond what can be gleaned from a collection of univariate effects (UVE) using functional magnetic resonance imaging (fMRI). Here, we argue that regardless of patterns revealed, conventional MVPA is merely a decoding tool with increased sensitivity arising from considering a large number of ‘weak classifiers' (i.e., single voxels) in higher dimensions. We propose instead that ‘real' multivoxel coding should result in changes in higher-order statistics across voxels between conditions such as second-order multivariate effects (sMVE). Surprisingly, analysis of conditions with robust multivariate effects (MVE) revealed by MVPA failed to show significant sMVE in two species (humans and macaques). Further analysis showed that while both MVE and sMVE can be readily observed in the spiking activity of neuronal populations, the slow and nonlinear hemodynamic coupling and low spatial resolution of fMRI activations make the observation of higher-order statistics between voxels highly unlikely. These results reveal inherent limitations of fMRI signals for studying coordinated coding across voxels. Together, these findings suggest that care should be taken in interpreting significant MVPA results as representing anything beyond a collection of univariate effects.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Park2022,

title = {Parallel functional subnetworks embedded in the macaque face patch system},

author = {Soo Hyun Park and Kenji W. Koyano and Brian E. Russ and Elena N. Waidmann and David B. T. McMahon and David A. Leopold},

doi = {10.1126/sciadv.abm2054},

year  = {2022},

date = {2022-01-01},

journal = {Science Advances},

volume = {8},

pages = {1–8},

abstract = {During normal vision, our eyes provide the brain with a continuous stream of useful information about the world. How visually specialized areas of the cortex, such as face-selective patches, operate under natural modes of behavior is poorly understood. Here we report that, during the free viewing of movies, cohorts of face-selective neurons in the macaque cortex fractionate into distributed and parallel subnetworks that carry distinct information. We classified neurons into functional groups on the basis of their movie-driven coupling with functional magnetic resonance imaging time courses across the brain. Neurons from each group were distributed across multiple face patches but intermixed locally with other groups at each recording site. These findings challenge prevailing views about functional segregation in the cortex and underscore the importance of naturalistic paradigms for cognitive neuroscience.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Popovkina2022,

title = {Task context modulates feature-selective responses in area v4},

author = {Dina V. Popovkina and Anitha Pasupathy},

doi = {10.1523/JNEUROSCI.1386-21.2022},

year  = {2022},

date = {2022-01-01},

journal = {Journal of Neuroscience},

volume = {42},

number = {33},

pages = {6408–6423},

abstract = {Feature selectivity of visual cortical responses measured during passive fixation provides only a partial view of selectivity because it does not account for the influence of cognitive factors. Here we focus on primate area V4 and ask how neuronal tuning is modulated by task engagement. We investigated whether responses to colored shapes during active shape discrimination are simple, stimulus-agnostic, scaled versions of responses during passive fixation, akin to results from attentional studies. Alternatively, responses could be subject to stimulus-specific scaling, that is, responses to different stimuli are modulated differently, resulting in changes in underlying shape/color selectivity. Among 83 well-isolated V4 neurons in two male macaques, only a minority (16 of 83), which were weakly tuned to both shape and color, displayed responses during fixation and discrimination tasks that could be related by stimulus-agnostic scaling. The majority (67 of 83), which were strongly tuned to shape, color, or both, displayed stimulus-dependent response changes during discrimination. For some of these neurons (39 of 83), the shape or color of the stimulus dictated the magnitude of the change, and for others (28 of 83) it was the combination of stimulus shape and color. Importantly, for neurons with one strong and one weak tuning dimension, stimulus-dependent response changes during discrimination were associated with a relative increase in selectivity along the stronger tuning dimension, without changes in tuning peak. These results reveal that more strongly tuned V4 neurons may also be more flexible in their selectivity, and imbalances in selectivity are amplified during active task contexts.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Qi2022,

title = {Neural dynamics of causal inference in the macaque frontoparietal circuit},

author = {Guangyao Qi and Wen Fang and Shenghao Li and Junru Li and Liping Wang},

doi = {10.7554/elife.76145},

year  = {2022},

date = {2022-01-01},

journal = {eLife},

volume = {11},

pages = {1–30},

abstract = {Natural perception relies inherently on inferring causal structure in the environment. However, the neural mechanisms and functional circuits essential for representing and updating the hidden causal structure and corresponding sensory representations during multisensory processing are unknown. To address this, monkeys were trained to infer the probability of a potential common source from visual and proprioceptive signals based on their spatial disparity in a virtual reality system. The proprioceptive drift reported by monkeys demonstrated that they combined previous experience and current multisensory signals to estimate the hidden common source and subsequently updated the causal structure and sensory representation. Single-unit recordings in premotor and parietal cortices revealed that neural activity in the premotor cortex represents the core computation of causal inference, characterizing the estimation and update of the likelihood of integrating multiple sensory inputs at a trial-by-trial level. In response to signals from the premotor cortex, neural activity in the parietal cortex also represents the causal structure and further dynamically updates the sensory representation to maintain consistency with the causal inference structure. Thus, our results indicate how the premotor cortex integrates previous experience and sensory inputs to infer hidden variables and selectively updates sensory representations in the parietal cortex to support behavior. This dynamic loop of frontal-parietal interactions in the causal inference framework may provide the neural mechanism to answer long-standing questions regarding how neural circuits represent hidden structures for body awareness and agency.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Rajalingham2022,

title = {Recurrent neural networks with explicit representation of dynamic latent variables can mimic behavioral patterns in a physical inference task},

author = {Rishi Rajalingham and Aída Piccato and Mehrdad Jazayeri},

doi = {10.1038/s41467-022-33581-6},

year  = {2022},

date = {2022-01-01},

journal = {Nature Communications},

volume = {13},

number = {1},

pages = {1–15},

publisher = {Springer US},

abstract = {Primates can richly parse sensory inputs to infer latent information. This ability is hypothesized to rely on establishing mental models of the external world and running mental simulations of those models. However, evidence supporting this hypothesis is limited to behavioral models that do not emulate neural computations. Here, we test this hypothesis by directly comparing the behavior of primates (humans and monkeys) in a ball interception task to that of a large set of recurrent neural network (RNN) models with or without the capacity to dynamically track the underlying latent variables. Humans and monkeys exhibit similar behavioral patterns. This primate behavioral pattern is best captured by RNNs endowed with dynamic inference, consistent with the hypothesis that the primate brain uses dynamic inferences to support flexible physical predictions. Moreover, our work highlights a general strategy for using model neural systems to test computational hypotheses of higher brain function.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Jeurissen2022,

title = {Deficits in decision-making induced by parietal cortex inactivation are compensated at two timescales},

author = {Danique Jeurissen and S. Shushruth and Yasmine El-Shamayleh and Gregory D. Horwitz and Michael N. Shadlen},

doi = {10.1016/j.neuron.2022.03.022},

year  = {2022},

date = {2022-01-01},

journal = {Neuron},

volume = {110},

pages = {1924–1931},

publisher = {The Author(s)},

abstract = {Perceptual decisions arise through the transformation of samples of evidence into a commitment to a proposition or plan of action. Such transformation is thought to involve cortical circuits capable of computation over timescales associated with working memory, attention, and planning. Neurons in the lateral intraparietal area (LIP) play a role in these functions, and much of what is known about the neurobiology of decision-making has been influenced by studies of LIP and its network of connections. However, the causal role of LIP remains controversial. In this study, we used pharmacological and chemogenetic methods to inactivate LIP in one brain hemisphere of four rhesus monkeys. This inactivation produced biases in decisions, but the effects dissipated despite persistent neural inactivation, implying compensation by unaffected areas. Compensation occurred rapidly within an experimental session and more gradually across sessions. These findings resolve disparate studies and inform the interpretation of focal perturbations of brain function.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Jiang2022b,

title = {Oxytocin and testosterone administration amplify viewing preferences for sexual images in male rhesus macaques},

author = {Yaoguang Jiang and Feng Sheng and Naz Belkaya and Michael L. Platt},

doi = {10.1098/rstb.2021.0133},

year  = {2022},

date = {2022-01-01},

journal = {Philosophical Transactions of the Royal Society B: Biological Sciences},

volume = {377},

pages = {1–12},

abstract = {Social stimuli, like faces, and sexual stimuli, like genitalia, spontaneously attract visual attention in both human and non-human primates. Social orienting behaviour is thought to be modulated by neuropeptides as well as sex hormones. Using a free viewing task in which paired images of monkey faces and anogenital regions were presented simultaneously, we found that male rhesus macaques overwhelmingly preferred to view images of anogenital regions over faces. They were more likely to make an initial gaze shift towards, and spent more time viewing, anogenital regions compared with faces, and this preference was accompanied by relatively constricted pupils. On face images, monkeys mostly fixated on the forehead and eyes. These viewing preferences were found for images of both males and females. Both oxytocin (OT), a neuropeptide linked to social bonding and affiliation, and testosterone (TE), a sex hormone implicated in mating and aggression, amplified the pre-existing orienting bias for female genitalia over female faces; neither treatment altered the viewing preference for male anogenital regions over male faces. Testosterone but not OT increased the probability of monkeys making the first gaze shift towards female anogenital rather than face pictures, with the strongest effects on anogenital images of young and unfamiliar females. Finally, both OT and TE promoted viewing of the forehead region of both female and male faces, which display sexual skins, but decreased the relative salience of the eyes of older males. Together, these results invite the hypothesis that both OT and TE regulate reproductive behaviours by acting as a gain control on the visual orienting network to increase attention to mating-relevant signals in the environment. This article is part of the theme issue 'Interplays between oxytocin and other neuromodulators in shaping complex social behaviours'.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Johnston2022a,

title = {EEG signals index a global signature of arousal embedded in neuronal population recordings},

author = {Richard Johnston and Adam C. Snyder and Rachel S. Schibler and Matthew A. Smith},

year  = {2022},

date = {2022-01-01},

journal = {eNeuro},

volume = {9},

number = {3},

pages = {1–16},

abstract = {Electroencephalography (EEG) has long been used to index brain states, from early studies describing activity in the presence and absence of visual stimulation to modern work employing complex perceptual tasks. These studies have shed light on brain-wide signals but often lack explanatory power at the single neuron level. Similarly, single neuron recordings can suffer from an inability to measure brain-wide signals accessible using EEG. Here, we combined these techniques while monkeys performed a change detection task and discovered a novel link between spontaneous EEG activity and a neural signal embedded in the spiking responses of neuronal populations. This “slow drift” was associated with fluctuations in the subjects' arousal levels over time: decreases in prestimulus a power were accompanied by increases in pupil size and decreases in microsaccade rate. These re- sults show that brain-wide EEG signals can be used to index modes of activity present in single neuron recordings, that in turn reflect global changes in brain state that influence perception and behavior.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Kharas2022,

title = {Brain state limits propagation of neural signals in laminar cortical circuits},

author = {Natasha Kharas and Ariana Andrei and Samantha R. Debes and Valentin Dragoi},

doi = {10.1073/pnas.2104192119},

year  = {2022},

date = {2022-01-01},

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

volume = {119},

number = {30},

pages = {1–10},

abstract = {Our perception of the environment relies on the efficient propagation of neural signals across cortical networks. During the time course of a day, neural responses fluctuate dramatically as the state of the brain changes to possibly influence how electrical signals propagate across neural circuits. Despite the importance of this issue, how patterns of spiking activity propagate within neuronal circuits in different brain states remains unknown. Here, we used multielectrode laminar arrays to reveal that brain state strongly modulates the propagation of neural activity across the layers of early visual cortex (V1). We optogenetically induced synchronized state transitions within a group of neurons and examined how far electrical signals travel during wakefulness and rest. Although optogenetic stimulation elicits stronger neural responses during wakefulness relative to rest, signals propagate only weakly across the cortical column during wakefulness, and the extent of spread is inversely related to arousal level. In contrast, the lightinduced population activity vigorously propagates throughout the entire cortical column during rest, even when neurons are in a desynchronized wake-like state prior to light stimulation. Mechanistically, the influence of global brain state on the propagation of spiking activity across laminar circuits can be explained by state-dependent changes in the coupling between neurons. Our results impose constraints on the conclusions of causal manipulation studies attempting to influence neural function and behavior, as well as on previous computational models of perception assuming robust signal propagation across cortical layers and areas.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Kienitz2022,

title = {Microstimulation of visual area V4 improves visual stimulus detection},

author = {Ricardo Kienitz and Kleopatra Kouroupaki and Michael C. Schmid},

doi = {10.1016/j.celrep.2022.111392},

year  = {2022},

date = {2022-01-01},

journal = {Cell Reports},

volume = {40},

number = {12},

pages = {1–11},

publisher = {The Authors},

abstract = {Neuronal activity in visual area V4 is well known to be modulated by selective attention, and there are reports on V4 lesions leading to attentional deficits. However, it remains unclear whether V4 microstimulation can elicit attentional benefits. To test this hypothesis, we performed local microstimulation in area V4 and explored its spatial and time dynamics in two macaque monkeys performing a visual detection task. Microstimulation was delivered via chronically implanted multi-electrode arrays. We found that microstimulation increases average performance by 35% and reduces luminance detection thresholds by −30%. This benefit critically depends on the onset of microstimulation relative to the stimulus, consistent with known dynamics of endogenous attention. These results show that local microstimulation of V4 can improve behavior and highlight the critical role of V4 for attention.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Krause2022,

title = {Brain stimulation competes with ongoing oscillations for control of spike timing in the primate brain},

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

doi = {10.1371/journal.pbio.3001650},

year  = {2022},

date = {2022-01-01},

journal = {PLoS Biology},

volume = {20},

number = {5},

pages = {1–27},

abstract = {Transcranial alternating current stimulation (tACS) is a popular method for modulating brain activity noninvasively. In particular, tACS is often used as a targeted intervention that enhances a neural oscillation at a specific frequency to affect a particular behavior. However, these interventions often yield highly variable results. Here, we provide a potential explanation for this variability: tACS competes with the brain's ongoing oscillations. Using neural recordings from alert nonhuman primates, we find that when neural firing is independent of ongoing brain oscillations, tACS readily entrains spiking activity, but when neurons are strongly entrained to ongoing oscillations, tACS often causes a decrease in entrainment instead. Consequently, tACS can yield categorically different results on neural activity, even when the stimulation protocol is fixed. Mathematical analysis suggests that this competition is likely to occur under many experimental conditions. Attempting to impose an external rhythm on the brain may therefore often yield precisely the opposite effect.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Kumar2022,

title = {It is not just the category: Behavioral effects of fMRI-guided electrical microstimulation result from a complex interplay of factors},

author = {Satwant Kumar and Eline Mergan and Rufin Vogels},

doi = {10.1093/texcom/tgac010},

year  = {2022},

date = {2022-01-01},

journal = {Cerebral Cortex Communications},

volume = {3},

pages = {1–16},

abstract = {Functional imaging and electrophysiological studies in primates revealed the existence of patches selective for visual categories in the inferior temporal cortex. Understanding the contribution of these patches to perception requires causal techniques that assess the effect of neural activity manipulations on perception. We used electrical microstimulation (EM) to determine the role of body patch activity in visual categorization in macaques. We tested the hypothesis that EM in a body patch would affect the categorization of bodies versus objects but not of other visual categories. We employed low-current EM of an anterior body patch (ASB) in the superior temporal sulcus, which was defined by functional magnetic resonance imaging and verified with electrophysiological recordings in each session. EM of ASB affected body categorization, but the EM effects were more complex than the expected increase of body-related choices: EM affected the categorization of both body and inanimate images and showed interaction with the choice target location, but its effect was location-specific (tested in 1 subject) on a millimeter scale. Our findings suggest that the behavioral effects of EM in a category-selective patch are not merely a manifestation of the category selectivity of the underlying neuronal population but reflect a complex interplay of multiple factors.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Kuraoka2022,

title = {Facial temperature and pupil size as indicators of internal state in primates},

author = {Koji Kuraoka and Kae Nakamura},

doi = {10.1016/j.neures.2022.01.002},

year  = {2022},

date = {2022-01-01},

journal = {Neuroscience Research},

publisher = {Elsevier Ireland Ltd and Japan Neuroscience Society},

abstract = {Studies in human subjects have revealed that autonomic responses provide objective and biologically relevant information about cognitive and affective states. Measures of autonomic responses can also be applied to studies of non-human primates, which are neuro-anatomically and physically similar to humans. Facial temperature and pupil size are measured remotely and can be applied to physiological experiments in primates, preferably in a head-fixed condition. However, detailed guidelines for the use of these measures in non-human primates is lacking. Here, we review the neuronal circuits and methodological considerations necessary for measuring and analyzing facial temperature and pupil size in non-human primates. Previous studies have shown that the modulation of these measures primarily reflects sympathetic reactions to cognitive and emotional processes, including alertness, attention, and mental effort, over different time scales. Integrated analyses of autonomic, behavioral, and neurophysiological data in primates are promising methods that reflect multiple dimensions of emotion and could potentially provide tools for understanding the mechanisms underlying neuropsychiatric disorders and vulnerabilities characterized by cognitive and affective disturbances.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Lee2022a,

title = {Lateral habenula neurons signal step-by-step changes of reward prediction},

author = {Hyunchan Lee and Okihide Hikosaka},

doi = {10.1016/j.isci.2022.105440},

year  = {2022},

date = {2022-01-01},

journal = {iScience},

volume = {25},

pages = {1–23},

publisher = {The Author(s)},

abstract = {In real life, multiple objects of different values are mixed in a variety of environments. To survive, animals need to find rewarding objects that may be located but hidden in particular contexts (e.g., environments) with bad objects that are unassociated with reward. Then, animals and humans pay attention to the enriched environment so that they can find the rewarding object vigorously. How can the brain initiate such behavior based on the context? We thus created a behavioral task for monkeys in which multiple contextual events (environment, action cue) sequentially occurred before objects appeared. We then studied the lateral habenula (LHb), which inhibit dopamine neurons (Matsumoto and Hikosaka, 2007). LHb neurons showed phasic responses in each event step-by-step across the sequential events, whose direction (excitation or inhibition) corresponded to the immediate change of the predicted value. Moreover, LHb neurons sequentially compared detailed prediction errors based on their significance in multiple contexts.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Lee2022,

title = {Lateral habenula responses during eye contact in a reward conditioning task},

author = {Hyunchan Lee and Okihide Hikosaka},

doi = {10.3389/fnbeh.2022.815461},

year  = {2022},

date = {2022-01-01},

journal = {Frontiers in Behavioral Neuroscience},

volume = {16},

pages = {1–9},

abstract = {For many animals, social interaction may have intrinsic reward value over and above its utility as a means to the desired end. Eye contact is the starting point of interactions in many social animals, including primates, and abnormal patterns of eye contact are present in many mental disorders. Whereas abundant previous studies have shown that negative emotions such as fear strongly affect eye contact behavior, modulation of eye contact by reward has received scant attention. Here we recorded eye movement patterns and neural activity in lateral habenula while monkeys viewed faces in the context of Pavlovian and instrumental conditioning tasks. Faces associated with larger rewards spontaneously elicited longer periods of eye contact from the monkeys, even though this behavior was not required or advantaged in the task. Concurrently, lateral habenula neurons were suppressed by faces signaling high value and excited by faces signaling low value. These results suggest that the reward signaling of lateral habenula may contribute to social behavior and disorders, presumably through its connections with the basal ganglia.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Lowe2022,

title = {Frontal eye fields in macaque monkeys: Prefrontal and premotor contributions to visually guided saccades},

author = {Kaleb A. Lowe and Wolf Zinke and Joshua D. Cosman and Jeffrey D. Schall},

doi = {10.1093/cercor/bhab533},

year  = {2022},

date = {2022-01-01},

journal = {Cerebral Cortex},

volume = {32},

pages = {5083–5107},

abstract = {Neuronal spiking was sampled from the frontal eye field (FEF) and from the rostral part of area 6 that reaches to the superior limb of the arcuate sulcus, dorsal to the arcuate spur when present (F2vr) in macaque monkeys performing memory-guided saccades and visually guided saccades for visual search. Neuronal spiking modulation in F2vr resembled that in FEF in many but not all respects. A new consensus clustering algorithm of neuronal modulation patterns revealed that F2vr and FEF contain a greater variety of modulation patterns than previously reported. The areas differ in the proportions of visuomotor neuron types, the proportions of neurons discriminating a target from distractors during visual search, and the consistency of modulation patterns across tasks. However, between F2vr and FEF we found no difference in the magnitude of delay period activity, the timing of the peak discharge rate relative to saccades, or the time of search target selection. The observed similarities and differences between the 2 cortical regions contribute to other work establishing the organization of eye fields in the frontal lobe and may help explain why FEF in monkeys is identified within granular prefrontal area 8 but in humans is identified within agranular premotor area 6.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Ma2022a,

title = {Multiple step saccades in simply reactive saccades could serve as a complementary biomarker for the early diagnosis of Parkinson's disease},

author = {Wenbo Ma and Min Li and Junru Wu and Zhihao Zhang and Fangfang Jia and Mingsha Zhang and Hagai Bergman and Xuemei Li and Zhipei Ling and Xin Xu},

doi = {10.3389/fnagi.2022.912967},

year  = {2022},

date = {2022-01-01},

journal = {Frontiers in Aging Neuroscience},

volume = {14},

pages = {1–14},

abstract = {Objective: It has been argued that the incidence of multiple step saccades (MSS) in voluntary saccades could serve as a complementary biomarker for diagnosing Parkinson's disease (PD). However, voluntary saccadic tasks are usually difficult for elderly subjects to complete. Therefore, task difficulties restrict the application of MSS measurements for the diagnosis of PD. The primary objective of the present study is to assess whether the incidence of MSS in simply reactive saccades could serve as a complementary biomarker for the early diagnosis of PD. Materials and methods: There were four groups of human subjects: PD patients, mild cognitive impairment (MCI) patients, elderly healthy controls (EHCs), and young healthy controls (YHCs). There were four monkeys with subclinical hemi-PD induced by injection of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) through the unilateral internal carotid artery and three healthy control monkeys. The behavioral task was a visually guided reactive saccade. Results: In a human study, the incidence of MSS was significantly higher in PD than in YHC, EHC, and MCI groups. In addition, receiver operating characteristic (ROC) analysis could discriminate PD from the EHC and MCI groups, with areas under the ROC curve (AUCs) of 0.76 and 0.69, respectively. In a monkey study, while typical PD symptoms were absent, subclinical hemi-PD monkeys showed a significantly higher incidence of MSS than control monkeys when the dose of MPTP was greater than 0.4 mg/kg. Conclusion: The incidence of MSS in simply reactive saccades could be a complementary biomarker for the early diagnosis of PD.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Malevich2022,

title = {Faster detection of “darks” than “brights” by monkey superior colliculus neurons},

author = {Tatiana Malevich and Tong Zhang and Matthias P. Baumann and Amarender R. Bogadhi and Ziad M. Hafed},

doi = {10.1523/jneurosci.1489-22.2022},

year  = {2022},

date = {2022-01-01},

journal = {Journal of Neuroscience},

volume = {45},

number = {2},

pages = {9356–9371},

abstract = {Visual processing is segregated into ON and OFF channels as early as in the retina, and the 48 superficial (output) layers of the primary visual cortex are dominated by neurons preferring 49 dark stimuli. However, it is not clear how the timing of neural processing differs between “darks” and “brights” in general, especially in light of psychophysical evidence; it is also equally not clear how subcortical visual pathways that are critical for active orienting represent stimuli of positive (luminance increments) and negative (luminance decrements) contrast polarity. Here, we recorded from all visually-responsive neuron types in the 54 superior colliculus (SC) of two male rhesus macaque monkeys. We presented a disc (0.51 deg 55 radius) within the response fields (RF's) of neurons, and we varied, across trials, stimulus 56 Weber contrast relative to a gray background. We also varied contrast polarity. There was a large diversity of preferences for darks and brights across the population. However, regardless of individual neural sensitivity, most neurons responded significantly earlier to dark than bright stimuli. This resulted in a dissociation between neural preference and visual response onset latency: a neuron could exhibit a weaker response to a dark stimulus than to a bright stimulus of the same contrast, but it would still have an earlier response to the dark stimulus. Our results highlight an additional candidate visual neural pathway for explaining behavioral differences between the processing of darks and brights, and they demonstrate the importance of temporal aspects in the visual neural code for orienting eye movements.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Csorba2022,

title = {Long-range cortical synchronization supports abrupt visual learning},

author = {Bennett A. Csorba and Matthew R. Krause and Theodoros P. Zanos and Christopher C. Pack},

doi = {10.1016/j.cub.2022.04.029},

year  = {2022},

date = {2022-01-01},

journal = {Current Biology},

volume = {32},

number = {11},

pages = {2467–2479},

publisher = {Elsevier Inc.},

abstract = {Visual plasticity declines sharply after the critical period, yet we easily learn to recognize new faces and places, even as adults. Such learning is often characterized by a “moment of insight,” an abrupt and dramatic improvement in recognition. The mechanisms that support abrupt learning are unknown, but one hypothesis is that they involve changes in synchronization between brain regions. To test this hypothesis, we used a behavioral task in which non-human primates rapidly learned to recognize novel images and to associate them with specific responses. Simultaneous recordings from inferotemporal and prefrontal cortices revealed a transient synchronization of neural activity between these areas that peaked around the moment of insight. Synchronization was strongest between inferotemporal sites that encoded images and reward-sensitive prefrontal sites. Moreover, its magnitude intensified gradually over image exposures, suggesting that abrupt learning is the culmination of a search for informative signals within a circuit linking sensory information to task demands.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{DalMonte2022,

title = {Widespread implementations of interactive social gaze neurons in the primate prefrontal-amygdala networks},

author = {Olga Dal Monte and Siqi Fan and Nicholas A. Fagan and Cheng Chi J. Chu and Michael B. Zhou and Philip T. Putnam and Amrita R. Nair and Steve W. C. Chang},

doi = {10.1016/j.neuron.2022.04.013},

year  = {2022},

date = {2022-01-01},

journal = {Neuron},

volume = {110},

pages = {2183–2197},

publisher = {The Author(s)},

abstract = {Social gaze interaction powerfully shapes interpersonal communication. However, compared with social perception, very little is known about the neuronal underpinnings of real-life social gaze interaction. Here, we studied a large number of neurons spanning four regions in primate prefrontal-amygdala networks and demonstrate robust single-cell foundations of interactive social gaze in the orbitofrontal, dorsomedial prefrontal, and anterior cingulate cortices, in addition to the amygdala. Many neurons in these areas exhibited high temporal heterogeneity for social discriminability, with a selectivity bias for looking at a conspecific compared with an object. Notably, a large proportion of neurons in each brain region parametrically tracked the gaze of self or other, providing substrates for social gaze monitoring. Furthermore, several neurons displayed selective encoding of mutual eye contact in an agent-specific manner. These findings provide evidence of widespread implementations of interactive social gaze neurons in the primate prefrontal-amygdala networks during social gaze interaction.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Froesel2022,

title = {Socially meaningful visual context either enhances or inhibits vocalisation processing in the macaque brain},

author = {Mathilda Froesel and Maëva Gacoin and Simon Clavagnier and Marc Hauser and Quentin Goudard and Suliann Ben Hamed},

doi = {10.1038/s41467-022-32512-9},

year  = {2022},

date = {2022-01-01},

journal = {Nature Communications},

volume = {13},

number = {1},

pages = {1–17},

publisher = {Springer US},

abstract = {Social interactions rely on the interpretation of semantic and emotional information, often from multiple sensory modalities. Nonhuman primates send and receive auditory and visual communicative signals. However, the neural mechanisms underlying the association of visual and auditory information based on their common social meaning are unknown. Using heart rate estimates and functional neuroimaging, we show that in the lateral and superior temporal sulcus of the macaque monkey, neural responses are enhanced in response to species-specific vocalisations paired with a matching visual context, or when vocalisations follow, in time, visual information, but inhibited when vocalisation are incongruent with the visual context. For example, responses to affiliative vocalisations are enhanced when paired with affiliative contexts but inhibited when paired with aggressive or escape contexts. Overall, we propose that the identified neural network represents social meaning irrespective of sensory modality.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Ghosh2022,

title = {Neuronal correlates of selective attention and effort in visual area V4 are invariant of motivational context},

author = {Supriya Ghosh and John H. R. Maunsell},

doi = {10.1126/sciadv.abc8812},

year  = {2022},

date = {2022-01-01},

journal = {Science Advances},

volume = {8},

number = {23},

pages = {1–16},

abstract = {Task demands can differentially engage two fundamental attention components: selectivity (spatial bias) and effort (total nonselective attentional intensity). The relative contributions and interactions of these components in modulating neuronal signals remain unknown. We recorded V4 neurons while monkeys' spatially selective attention and effort were independently controlled by adjusting either task difficulty or reward size at two locations. Neurons were robustly modulated by either selective attention or effort. Notably, increasing overall effort to improve performance at a distant site reduced neuronal responses even when performance was unchanged for receptive field stimuli. This interaction between attentional selectivity and effort was evident in single-trial spiking and can be explained by divisive normalization of spatially distributed behavioral performance at the single-neuron level. Changing motivation using task difficulty or reward produced indistinguishable effects. These results provide a cellular-level mechanism of how attention components integrate to modulate sensory processing in different motivational contexts.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Giacometti2022,

title = {Frontal cortical functional connectivity is impacted by anaesthesia in macaques},

author = {Camille Giacometti and Audrey Dureux and Delphine Autran-Clavagnier and Charles R. E. Wilson and Jérôme Sallet and Manon Dirheimer and Emmanuel Procyk and Fadila Hadj-Bouziane and Céline Amiez},

doi = {10.1093/cercor/bhab465},

year  = {2022},

date = {2022-01-01},

journal = {Cerebral Cortex},

volume = {32},

pages = {4050–4067},

abstract = {A critical aspect of neuroscience is to establish whether and how brain networks evolved across primates. To date, most comparative studies have used resting-state functional magnetic resonance imaging (rs-fMRI) in anaesthetized nonhuman primates and in awake humans. However, anaesthesia strongly affects rs-fMRI signals. The present study investigated the impact of the awareness state (anaesthesia vs. awake) within the same group of macaque monkeys on the rs-fMRI functional connectivity organization of a well-characterized network in the human brain, the cingulo-frontal lateral network. Results in awake macaques show that rostral seeds in the cingulate sulcus exhibited stronger correlation strength with rostral compared to caudal lateral frontal cortical areas, while more caudal seeds displayed stronger correlation strength with caudal compared to anterior lateral frontal cortical areas. Critically, this inverse rostro-caudal functional gradient was abolished under anaesthesia. This study demonstrated a similar functional connectivity (FC) organization of the cingulo-frontal cortical network in awake macaque to that previously uncovered in the human brain pointing toward a preserved FC organization from macaque to human. However, it can only be observed in awake state suggesting that this network is sensitive to anaesthesia and warranting significant caution when comparing FC patterns across species under different states.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Henry2022,

title = {Feature representation under crowding in macaque V1 and V4 neuronal populations},

author = {Christopher A. Henry and Adam Kohn},

doi = {10.1016/j.cub.2022.10.049},

year  = {2022},

date = {2022-01-01},

journal = {Current Biology},

volume = {32},

number = {23},

pages = {5126–5137},

publisher = {Elsevier Inc.},

abstract = {Visual perception depends strongly on spatial context. A profound example is visual crowding, whereby the presence of nearby stimuli impairs the discriminability of object features. Despite extensive work on perceptual crowding and the spatial integrative properties of visual cortical neurons, the link between these two aspects of visual processing remains unclear. To understand better the neural basis of crowding, we recorded activity simultaneously from neuronal populations in V1 and V4 of fixating macaque monkeys. We assessed the information available from the measured responses about the orientation of a visual target both for tar- gets presented in isolation and amid distractors. Both single neuron and population responses had less information about target orientation when distractors were present. Information loss was moderate in V1 and more substantial in V4. Information loss could be traced to systematic divisive and additive changes in neuronal tuning. Additive and multiplicative changes in tuning were more severe in V4; in addition, tuning ex- hibited other, non-affine transformations that were greater in V4, further restricting the ability of a fixed sen- sory readout strategy to extract accurate feature information across displays. Our results provide a direct test of crowding effects at different stages of the visual hierarchy. They reveal how crowded visual environments alter the spiking activity of cortical populations by which sensory stimuli are encoded and connect these changes to established mechanisms of neuronal spatial integration.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Herpers2022,

title = {Limited pairings of electrical micro-stimulation of the ventral tegmental area and a visual stimulus enhance visual cortical responses},

author = {Jerome Herpers and Wim Vanduffel and Rufin Vogels},

year  = {2022},

date = {2022-01-01},

journal = {Journal of Cognitive Neuroscience},

volume = {34},

pages = {1259–1273},

abstract = {Previous studies demonstrated that pairing a visual stimulus and electrical micro-stimulation of the ventral tegmental area (VTA-EM) for multiple days is sufficient to induce visual cortical plasticity and changes perception. However, a brief epoch of VTA-EM–stimulus pairing within a single day has been shown to result in a behavioral preference for the paired stimulus. Here, we investigated whether a brief single-day session of VTA-EM–stimulus pairings is sufficient to induce changes in visual cortical responses. We examined macaque posterior infe- rior temporal (PIT) cortex because previous studies demon- strated response changes after VTA-EM stimulus pairing in that area. Multi-unit recordings in PIT were interleaved with VTA- EM–stimulus pairing epochs. During the short VTA-EM–stimulus pairing epochs (60 pairings), one image (fractal) was paired with VTA-EM (STIM) whereas another, unpaired fractal was pre- sented as control. Two other fractals (dummies) were presented only during the recordings. The difference in response between the STIM and control fractals already increased after the first VTA-EM–stimulus pairing epoch, reflecting a relative increase of the response to the STIM fractal. However, the response to the STIM fractal did not increase further with more VTA-EM– stimulus pairing epochs. The relative increase in firing rate for the paired fractal was present early in the response, in line with a local/ bottom–up origin. These effects were absent when com- paring the responses to the dummies pre- and post-VTA-EM. This study shows that pairing a visual image and VTA-EM in a brief single-day session is sufficient to increase the response for the paired image in macaque PIT.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Herrera2022,

title = {Resolving the mesoscopic missing link: Biophysical modeling of EEG from cortical columns in primates},

author = {Beatriz Herrera and Jacob A. Westerberg and Michelle S. Schall and Alexander Maier and Geoffrey F. Woodman and Jeffrey D. Schall and Jorge J. Riera},

doi = {10.1016/j.neuroimage.2022.119593},

year  = {2022},

date = {2022-01-01},

journal = {NeuroImage},

volume = {263},

pages = {1–14},

publisher = {Elsevier Inc.},

abstract = {Event-related potentials (ERP) are among the most widely measured indices for studying human cognition. While their timing and magnitude provide valuable insights, their usefulness is limited by our understanding of their neural generators at the circuit level. Inverse source localization offers insights into such generators, but their solutions are not unique. To address this problem, scientists have assumed the source space generating such signals comprises a set of discrete equivalent current dipoles, representing the activity of small cortical regions. Based on this notion, theoretical studies have employed forward modeling of scalp potentials to understand how changes in circuit-level dynamics translate into macroscopic ERPs. However, experimental validation is lacking because it requires in vivo measurements of intracranial brain sources. Laminar local field potentials (LFP) offer a mechanism for estimating intracranial current sources. Yet, a theoretical link between LFPs and intracranial brain sources is missing. Here, we present a forward modeling approach for estimating mesoscopic intracranial brain sources from LFPs and predict their contribution to macroscopic ERPs. We evaluate the accuracy of this LFP-based representation of brain sources utilizing synthetic laminar neurophysiological measurements and then demonstrate the power of the approach in vivo to clarify the source of a representative cognitive ERP component. To that end, LFP was measured across the cortical layers of visual area V4 in macaque monkeys performing an attention demanding task. We show that area V4 generates dipoles through layer-specific transsynaptic currents that biophysically recapitulate the ERP component through the detailed forward modeling. The constraints imposed on EEG production by this method also revealed an important dissociation between computational and biophysical contributors. As such, this approach represents an important bridge between laminar microcircuitry, through the mesoscopic activity of cortical columns to the patterns of EEG we measure at the scalp.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Heusser2022,

title = {Decoding the time course of spatial information from spiking and local field potential activities in the superior colliculus.},

author = {Michelle R. Heusser and Clara Bourrelly and Neeraj J. Gandhi},

doi = {10.1523/ENEURO.0347-22.2022},

year  = {2022},

date = {2022-01-01},

journal = {eNeuro},

volume = {9},

number = {6},

pages = {1–13},

abstract = {Place code representation is ubiquitous in circuits that encode spatial parameters. For visually guided eye movements, neurons in many brain regions emit spikes when a stimulus is presented in their receptive fields and/or when a movement is directed into their movement fields. Crucially, individual neurons respond for a broad range of directions or eccentricities away from the optimal vector, making it difficult to decode the stimulus location or the saccade vector from each cell's activity. We investigated whether it is possible to decode the spatial parameter with a population-level analysis, even when the optimal vectors are similar across neurons. Spiking activity and local field potentials (LFP) in the superior colliculus were recorded with a laminar probe as monkeys performed a delayed saccade task to one of eight targets radially equidistant in direction. A classifier was applied offline to decode the spatial configuration as the trial progresses from sensation to action. For spiking activity, decoding performance across all eight directions was highest during the visual and motor epochs and lower but well above chance during the delay period. Classification performance followed a similar pattern for LFP activity too, except the performance during the delay period was limited mostly to the preferred direction. Increasing the number of neurons in the population consistently increased classifier performance for both modalities. Overall, this study demonstrates the power of population activity for decoding spatial information not possible from individual neurons.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}

@article{Jagadisan2022,

title = {Population temporal structure supplements the rate code during sensorimotor transformations},

author = {Uday K. Jagadisan and Neeraj J. Gandhi},

doi = {10.1016/j.cub.2022.01.015},

year  = {2022},

date = {2022-01-01},

journal = {Current Biology},

volume = {32},

pages = {1010–1025},

publisher = {Elsevier Inc.},

abstract = {Sensorimotor transformations are mediated by premotor brain networks where individual neurons represent sensory, cognitive, and movement-related information. Such multiplexing poses a conundrum—how does a decoder know precisely when to initiate a movement if its inputs are active at times when a movement is not desired (e.g., in response to sensory stimulation)? Here, we propose a novel hypothesis: movement is triggered not only by an increase in firing rate but, critically, also by a reliable temporal pattern in the population response. Laminar recordings in the macaque superior colliculus (SC), a midbrain hub of orienting control, and pseudo-population analyses in SC and cortical frontal eye fields (FEFs) corroborated this hypothesis. Specifically, using a measure that captures the fidelity of the population code—here called temporal stability—we show that the temporal structure fluctuates during the visual response but becomes increasingly stable during the movement command. Importantly, we used spatiotemporally patterned microstimulation to causally test the contribution of population temporal stability in gating movement initiation and found that stable stimulation patterns were more likely to evoke a movement. Finally, a spiking neuron model was able to discriminate between stable and unstable input patterns, providing a putative biophysical mechanism for decoding temporal structure. These findings offer new insights into the long-standing debate on motor preparation and generation by situating the movement gating signal in temporal features of activity in shared neural substrates, and they highlight the importance of short-term population history in neuronal communication and behavior.},

keywords = {},

pubstate = {published},

tppubtype = {article}

}