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Biological visual systems have evolved to process natural scenes. A full understanding of visual cortical functions requires a comprehensive characterization of how neuronal populations in each visual area encode natural scenes. Here, we utilized widefield calcium imaging to record V4 cortical response to tens of thousands of natural images in male macaques. Using this large dataset, we developed a deep-learning digital twin of V4 that allowed us to map the natural image preferences of the neural population at 100-µm scale. This detailed map revealed a diverse set of functional domains in V4, each encoding distinct natural image features. We validated these model predictions using additional widefield imaging and single-cell resolution two-photon imaging. Feature attribution analysis revealed that these domains lie along a continuum from preferring spatially localized shape features to preferring spatially dispersed surface features. These results provide insights into the organizing principles that govern natural scene encoding in V4. How natural scenes are represented by the neuronal populations of a specific visual area such as V4 remain not fully understood. The authors produced a dataset of widefield calcium imaging of macaque V4 responses to a large set of natural images, and used deep learning techniques to elucidate how natural image features are encoded and topologically organized in V4.

Abstract Background and Hypothesis Visual fixation is a dynamic process, with the spontaneous occurrence of microsaccades and macrosaccades. These fixational saccades are sensitive to the structural and functional alterations of the cortical-subcortical-cerebellar circuit. Given that dysfunctional cortical-subcortical-cerebellar circuit contributes to cognitive and behavioral impairments in schizophrenia, we hypothesized that patients with schizophrenia would exhibit abnormal fixational saccades and these abnormalities would be associated with the clinical manifestations. Study Design Saccades were recorded from 140 drug-naïve patients with first-episode schizophrenia and 160 age-matched healthy controls during ten separate trials of 6-second steady fixations. Positive and negative symptoms were assessed using the Positive and Negative Syndrome Scale (PANSS). Cognition was assessed using the Measurement and Treatment Research to Improve Cognition in Schizophrenia Consensus Cognitive Battery (MCCB). Study Results Patients with schizophrenia exhibited fixational saccades more vertically than controls, which was reflected in more vertical saccades with angles around 90° and a greater vertical shift of horizontal saccades with angles around 0° in patients. The fixational saccades, especially horizontal saccades, showed longer durations, faster peak velocities, and larger amplitudes in patients. Furthermore, the greater vertical shift of horizontal saccades was associated with higher PANSS total and positive symptom scores in patients, and the longer duration of horizontal saccades was associated with lower MCCB neurocognitive composite, attention/vigilance, and speed of processing scores. Finally, based solely on these fixational eye movements, a K-nearest neighbors model classified patients with an accuracy of 85%. Conclusions: Our results reveal spatial and temporal abnormalities of fixational saccades and suggest fixational saccades as a promising biomarker for cognitive and positive symptoms and for diagnosis of schizophrenia.

The ventral visual pathway is crucially involved in integrating low-level visual features into complex representations for objects and scenes. At an intermediate stage of the ventral visual pathway, V4 plays a crucial role in supporting this transformation. Many V4 neurons are selective for shape segments like curves and corners; however, it remains unclear whether these neurons are organized into clustered functional domains, a structural motif common across other visual cortices. Using two-photon calcium imaging in awake macaques, we confirmed and localized cortical domains selective for curves or corners in V4. Single-cell resolution imaging confirmed that curve- or corner-selective neurons were spatially clustered into such domains. When tested with hexagonal-segment stimuli, we find that stimulus smoothness is the cardinal difference between curve and corner selectivity in V4. Combining cortical population responses with single-neuron analysis, our results reveal that curves and corners are encoded by neurons clustered into functional domains in V4. This functionally specific population architecture bridges the gap between the early and late cortices of the ventral pathway and may serve to facilitate complex object recognition.

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

In a pattern of horizontal lines containing ± 45° zigzagging phase-shifted strips, vivid illusory motion is perceived when the pattern is translated up or down at a moderate speed. Two forms of illusory motion are seen: [i] a motion “racing” along the diagonal interface between the strips and [ii] lateral (sideways) motion of the strip sections. We found the relative salience of these two illusory motions to be strongly influenced by the vertical spacing and length of the line gratings, and the period length of the zigzag strips. Both illusory motions are abolished when the abutting strips are interleaved, separated by a gap or when a real line is superimposed at the interface. Illusory motion is also severely weakened when equiluminant colored grating lines are used. Illusory motion perception is fully restored at < 20% luminance contrast. Using adaptation, we find that line-ends alone are insufficient for illusory motion perception, and that both physical carrier motion and line orientation are required. We finally test a classical spatiotemporal energy model of V1 cells that exhibit direction tuning changes that are consistent with the direction of illusory motion. Taking this data together, we constructed a new visual illusion and surmise its origin to interactions of spatial and temporal energy of the lines and line-ends preferentially driving the magnocellular pathway.

Visual information is highly advantageous for the evolutionary success of almost all animals. This information is likewise critical for many computing tasks, and visual computing has achieved tremendous successes in numerous applications over the last 60 years or so. In that time, the development of visual computing has moved forwards with inspiration from biological mechanisms many times. In particular, deep neural networks were inspired by the hierarchical processing mechanisms that exist in the visual cortex of primate brains (including ours), and have achieved huge breakthroughs in many domainspecific visual tasks. In order to better understand biologically inspired visual computing, we will present a survey of the current work, and hope to offer some new avenues for rethinking visual computing and designing novel neural network architectures.

Sociality influences ethologically important decisions and demand a high level of cognitive sophistication We used a novel decision making task with 6 macaques where social hierarchy could be tested across social audience, coaction, envy, altruism, cooperation & competition contexts. Subject’s decision making performance was significantly modulated by context and social rank, reflected by their social eye gaze patterns. There were significant differences in fronto-parietal brain regions as the social context changed Social interactions shape many of our most ethologically relevant decisions and require considerable cognitive sophistication. Factors such as immediate needs, social bonds, hierarchical status, and reciprocity norms impact decision-making. Yet most laboratory paradigms examine individuals in isolation. We developed a face-to-face cognitive testing platform using a transparent touchscreen that allowed pairs of adult male Macaca fascicularis (n = 6) with established dominance relationships to perform a decision-making task across six social contexts: audience, co-action, envy, cooperation, competition, and altruism. We recorded eye movements simultaneously from both subjects (gaze position and pupil diameter), synchronised behavioural video, and task performance. Across social contexts, macaques performed better in the presence of a conspecific than when tested alone, but performance declined under altruistic and competitive conditions. Dominance substantially modulated motivation: dominant subjects were less willing to engage when rewards were shared (envy), when only the partner was rewarded (altruism), or when contingent action with a subordinate was required (cooperation). Eye-tracking revealed greater pre-choice arousal and social attention during social sessions, indexed by larger pupils, longer fixations on the partner’s face, and more saccades before—but not during or after—choices. Pupil dilation was larger in dyads where both individuals were dominant than in dyads where one was subordinate. Finally, noninvasive functional near-infrared spectroscopy (fNIRS) showed increased cortical engagement relative to baseline in audience, altruism, competition, and cooperation conditions. These findings demonstrate that social context and hierarchical dominance systematically shape choices, attentional allocation, autonomic arousal, and cortical engagement in macaques, and provide a tractable platform for further dissecting the neural bases of contextual social decisionmaking.

The visual system evolved to process natural scenes, yet most of our understanding of the topology and function of visual cortex derives from studies using artificial stimuli. To gain deeper insights into visual processing of natural scenes, we utilized widefield calcium-imaging of primate V4 in response to many natural images, generating a large dataset of columnar-scale responses. We used this dataset to build a digital twin of V4 via deep learning, generating a detailed topographical map of natural image preferences at each cortical position. The map revealed clustered functional domains for specific classes of natural image features. These ranged from surface-related attributes like color and texture to shape-related features such as edges, curvature, and facial features. We validated the model-predicted domains with additional widefield calcium-imaging and single-cell resolution two-photon imaging. Our study illuminates the detailed topological organization and neural codes in V4 that represent natural scenes.

Equiluminant stimuli help assess the integrity of colour perception and the relationship of colour to other visual features. As a result of individual variation, it is necessary to calibrate experimental visual stimuli to suit each individual's unique equiluminant ratio. Most traditional methods rely on training observers to report their subjective equiluminance point. Such paradigms cannot easily be implemented on pre-verbal or non-verbal observers. Here, we present a novel Pupil Frequency-Tagging Method (PFTM) for detecting a participant's unique equiluminance point without verbal instruction and with minimal training. PFTM analyses reflexive pupil oscillations induced by slow (< 2 Hz) temporal alternations between coloured stimuli. Two equiluminant stimuli will induce a similar pupil dilation response regardless of colour; therefore, an observer's equiluminant point can be identified as the luminance ratio between two colours for which the oscillatory amplitude of the pupil at the tagged frequency is minimal. We compared pupillometry-based equiluminance ratios to those obtained with two established techniques in humans: minimum flicker and minimum motion. In addition, we estimated the equiluminance point in non-human primates, demonstrating that this new technique can be successfully employed in non-verbal subjects.Competing Interest StatementThe authors have declared no competing interest.Footnotes* 1) Replot pupil data calibrated to millimeters. 2) Add Bland-Altman plots to Fig. 4.* https://github.com/iandol/equiluminance

in vivo rAAV applications, accelerating and augmenting gene transduction at doxorubicin concentrations paralleling medical practice. Highlights 1. Anti-cancer drug doxorubicin doubles the rate of rAAV-mediated transgene expression 2. Doxorubicin enhancement generalizes across rAAV serotypes and animal species 3. The effect is observed in both locally and retrogradely infected cortical neurons 4. The effective dosage is free from appreciable cytotoxicity and matches clinical settings Competing Interest Statement The authors have declared no competing interest. Footnotes * ↵5 Lead Contact * Rapid and efficient gene transduction via recombinant adeno-associated viruses (rAAVs) is highly desirable across many basic and clinical research domains. Here we report vector co-infusion with doxorubicin, a clinical anti-cancer drug, markedly enhanced rAAV-mediated gene expression in the cerebral cortex across mammalian species (cat, mouse, and macaque), acting throughout the time-period examined and detectable at just three days post-transfection. This enhancement showed serotype generality, being common to rAAV serotypes 2, 8, 9 and PHP.eB tested, and was observed both locally, and at remote locations consistent with doxorubicin undergoing retrograde axonal transport. All these effects were observed at doses matching human blood plasma levels in clinical therapy, and lacked detectable cytotoxicity as assessed by cell morphology, activity, apoptosis and behavioral testing. Altogether, this study identifies an effective means to improve the capability and scope of in vivo rAAV applications, accelerating and augmenting gene transduction at doxorubicin concentrations paralleling medical practice.