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Pasupathy, A.

Publications and source records attributed to Pasupathy, A..

7 recordsLinked to original sources

Functional clusters for shape, texture, and motion encoding in macaque V2

Macaque primary visual cortex (V1) exhibits exquisite columnar organization, while midlevel area V4 does not. Here we investigated the functional organization and representational bases of intervening area V2 with high-density Neuropixels recordings and a variety of visual stimuli--shape, texture, drifting grating, and translational motion patches. We observed dense clusters of similarly tuned neurons often spanning [~]500 {micro}m for shape and motion stimuli, and larger for texture stimuli, consistent with a columnar structure. In terms of representational bases, V2 responses were largely explained by stimulus features based on local image statistics: shape tuning is well-modeled by a linear combination of orientation filters, and direction selectivity is stronger with surface compared to object motion, in striking contrast to V4. Overall, our results support the progression from columns to sparse clusters as neuronal representations transform from encoding local features and feature conjunctions in V1/V2 to a high-dimensional object-based code in V4. Significance StatementBy recording hundreds of neurons simultaneously across layers of macaque visual area V2, we show the first evidence of exquisite fine-scale functional clusters that encode higher-order shape, texture, and motion features, extending well beyond the classic orientation-selective columns seen in area V1. Comparative analyses with V4 further reveal distinct representational bases and organization patterns between adjacent cortical areas, offering insights into how columnar organization is preserved in early visual areas (V1 and V2) but markedly attenuated in higher-order cortex such as V4.

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Recycling of prefrontal subspaces dynamically multiplexes information

Cortical spiking activity in areas like prefrontal cortex (PFC) encodes information only along a small number of dimensions, a subspace of the full space of population activity patterns. PFC often uses distinct subspaces to represent incoming sensory information and to maintain it in working memory. However, its generally assumed that a subspace carries specific information within a specific time frame. Here, in two datasets, we show that neither assumption is correct. The same subspace used during initial encoding was later reactivated during the behavioral response. We also found that subspaces ostensibly dedicated to processing sensory information were recycled to represent behavioral response information later in a trial. We further found a consistent spatial mapping between the original subspace usage and its later recycling. These results demonstrate previously unknown flexibility of PFC subspace coding, both in the deployment of subspaces across time and in their multiplexing of information. This flexibility suggests that PFC subspaces function more like "workspaces" into which different types of information can be written.

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High-density recording reveals sparse clusters (but not columns) for shape and texture encoding in macaque V4

Macaque area V4 includes neurons that exhibit exquisite selectivity for visual form and surface texture, but their functional organization across laminae is unknown. We used high-density Neuropixels probes in two awake monkeys to characterize shape and texture tuning of dozens of neurons simultaneously across layers. We found sporadic clusters of neurons that exhibit similar tuning for shape and texture: [~]20% exhibited similar tuning with their neighbors. Importantly, these clusters were confined to a few layers, seldom columnar in structure. This was the case even when neurons were strongly driven, and exhibited robust contrast invariance for shape and texture tuning. We conclude that functional organization in area V4 is not columnar for shape and texture stimulus features and in general organization maybe at a coarse scale (e.g. encoding of 2D vs 3D shape) rather than at a fine scale in terms of similarity in tuning for specific features (as in the orientation columns in V1). We speculate that this may be a direct consequence of the great diversity of inputs integrated by V4 neurons to build variegated tuning manifolds in a high-dimensional space. Significance StatementIn primary visual cortex of the macaque monkey, studies have demonstrated columnar functional organization, i.e. shared tuning across layers for stimulus orientation, spatial frequency, ocular dominance, etc. In mid and higher level visual form processing stages, where neurons exhibit high-dimensional tuning, functional organization has been harder to evaluate. Here, leveraging the use of the high-density Neuropixels probes to record simultaneously from dozens of neurons across cortical layers, we demonstrate that functional organization is not columnar for shape and texture tuning in area V4, a midlevel stage critical for form processing. Our results contribute to the debate about the functional significance of cortical columns providing support to the idea that they emerge due to one-to-many representational expansion.

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Neural correlates of crowding in macaque area V4

Visual crowding refers to the phenomenon where a target object that is easily identifiable in isolation becomes difficult to recognize when surrounded by other stimuli (distractors). Extensive psychophysical studies support two alternative possibilities for the underlying mechanisms. One hypothesis suggests that crowding results from the loss of visual information due to pooled encoding of multiple nearby stimuli in the mid-level processing stages along the ventral visual pathway. Alternatively, crowding may arise from limited resolution in decoding object information during recognition and the encoded information may remain inaccessible unless it is salient. To rigorously test these alternatives, we studied the responses of single neurons in macaque area V4, an intermediate stage of the ventral, object-processing pathway, to parametrically designed crowded displays and their texture-statistics matched metameric counterparts. Our investigations reveal striking parallels between how crowding parameters, e.g., number, distance, and position of distractors, influence human psychophysical performance and V4 shape selectivity. Importantly, we found that enhancing the salience of a target stimulus could reverse crowding effects even in highly cluttered scenes and such reversals could be protracted reflecting a dynamical process. Overall, we conclude that a pooled encoding of nearby stimuli cannot explain the observed responses and we propose an alternative model where V4 neurons preferentially encode salient stimuli in crowded displays. Significance StatementPsychophysicists have long studied the phenomena of visual crowding, but the underlying neural mechanisms are unknown. Our results reveal striking correlations between the responses of neurons in mid-level visual cortical area V4 and psychophysical demonstrations, revealing that crowding is influenced not only by the number and spatial arrangement of distractors but also by the similarity of features between target and distractors, as well as among the distractors themselves. Overall, our studies provide strong evidence that the visual system uses strategies to preferentially encode salient features in a visual scene presumably to process visual information efficiently. When multiple nearby stimuli are equally salient, the phenomenon of crowding ensues.

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Ultra-high density electrodes improve detection, yield, and cell type specificity of brain recordings

To understand the neural basis of behavior, it is essential to sensitively and accurately measure neural activity at single neuron and single spike resolution. Extracellular electrophysiology delivers this, but it has biases in the neurons it detects and it imperfectly resolves their action potentials. To minimize these limitations, we developed a silicon probe with much smaller and denser recording sites than previous designs, called Neuropixels Ultra (NP Ultra). This device samples neuronal activity at ultra-high spatial density ([~]10 times higher than previous probes) with low noise levels, while trading off recording span. NP Ultra is effectively an implantable voltage-sensing camera that captures a planar image of a neurons electrical field. We use a spike sorting algorithm optimized for these probes to demonstrate that the yield of visually-responsive neurons in recordings from mouse visual cortex improves up to [~]3-fold. We show that NP Ultra can record from small neuronal structures including axons and dendrites. Recordings across multiple brain regions and four species revealed a subset of extracellular action potentials with unexpectedly small spatial spread and axon-like features. We share a large-scale dataset of these brain-wide recordings in mice as a resource for studies of neuronal biophysics. Finally, using ground-truth identification of three major inhibitory cortical cell types, we found that these cell types were discriminable with approximately 75% success, a significant improvement over lower-resolution recordings. NP Ultra improves spike sorting performance, detection of subcellular compartments, and cell type classification to enable more powerful dissection of neural circuit activity during behavior.

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Inserting a Neuropixels probe into awake monkey cortex: two probes, two methods

Neuropixels probes have revolutionized neurophysiological studies in the rodent, but inserting these probes through the much thicker primate dura remains a challenge. Here we describe two methods we have developed for the insertion of two types of Neuropixels probes acutely into the awake monkey cortex. For the fine rodent probe, which is unable to pierce native primate dura, we developed a duraleyelet method to insert the probe repeatedly without breakage. For the thicker NHP probe, we developed an artificial dura system to insert the probe. We have now conducted successful experiments in 3 animals across 7 recording chambers with the procedures described here and have achieved stable recordings over several months in each case. Here we describe our hardware, surgical preparation, methods for insertion and methods for removal of broken probe parts. We hope that our methods are of value to primate physiologists everywhere.

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Task context modulates feature-selective responses in area V4

Feature selectivity of neuronal responses in primate visual cortex is typically measured while animals fixate a small dot on the screen and a stimulus is presented in the near-periphery. This paradigm allows the efficient exploration of feature space, but it provides only a partial view of selectivity by failing to characterize how cognitive factors influence neuronal tuning. Here we focus on primate area V4, known to be influenced by cognitive processes, and ask how neuronal tuning is modulated by task engagement. We compared the tuning for shape and color in 83 well-isolated V4 neurons measured during passive fixation and during active engagement in a shape discrimination task. In both tasks, animals saw the same set of objects--shape x color combinations--but while neither stimulus feature was relevant during the fixation task, shape identity was relevant for behavior during the discrimination task. Consistent with attentional studies, V4 responses during the discrimination task showed a stimulus-independent gain scaling relative to passive fixation, but this was only in a minority of neurons (21/83). For the rest (62/83), response modulations during discrimination depended on stimulus identity: on stimulus shape in neurons more strongly tuned to shape, and on color in neurons more strongly tuned to color. Overall, this resulted in broader tuning for stimulus color, but not shape, during active task engagement. These results suggest that task context can influence the shape and color selectivity of V4 neurons, and in some neurons this effect is consistent with a change in the width of feature tuning.

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