Biology subjects

Movshon, J. A.

Publications and source records attributed to Movshon, J. A..

18 recordsLinked to original sources

bioRxiv2026

Curvature tuning in areas V2 and V4 of the developing macaque

Visual areas V2 and V4 are critical for the perception of visual forms in primates. Neurons in area V4 of macaque monkeys are often sensitive to the curvature of specific boundary segments within shapes, but it is unknown how curvature tuning is represented in the developing brain. To address this, we recorded multiunit neural activity from areas V2 and V4 of two macaque monkeys, at both 30 and 58 weeks of age, in response to shape stimuli which primarily varied in curvature along a single segment. Observable curvature tuning was adult-like from 30 weeks of age in both V2 and V4. We compared the tuning of sites to shapes presented at multiple positions. We saw evidence of position-invariant tuning in V4, but not in V2. Position invariance in V4 was stable from 30 weeks of age. Finally, we fit two models - a stimulus-centric model of boundary curvature tuning, and a simple linear model based on the spike-triggered average response to all stimuli. We found many sites in both V2 and V4 whose responses could be captured by one or both models, but no evidence of age-related changes in curvature tuning within the space of either model. Our results suggest that the neural representation of curvature in both areas reaches maturity soon after birth, and that object-centric representations of curvature first emerge in V4, not V2.

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bioRxiv2025

Variations in neuronal selectivity create efficient representational geometries for perception

A complete understanding of population coding requires connecting multiple levels of neural processing: individual responses, population representations, and behavior. We link these by relating the distribution of neuronal tuning properties to a populations representational geometry and its efficiency for perceptual tasks. We use theory, analysis of recordings from macaque primary visual cortex (V1), and simulations to reveal how diversity of tuning amplitude and bandwidth enhances the population code for visual discrimination and identification. Both types of diversity drive different, but complementary changes to the representational geometry. Amplitude diversity increases the Euclidean distance between the responses to different stimuli, while bandwidth diversity creates a larger angular distance between them. The first utilizes the range of firing rates available to neurons, and the second exploits the high-dimensional nature of population responses. Population codes can be improved using these two different geometric changes, and amplitude and bandwidth diversity provide biological mechanisms for doing so. HighlightsO_LI- Perceptual performance is improved both by increased diversity of response amplitude and increased diversity of tuning bandwidth. C_LIO_LI- Both kinds of diversity improve visual discrimination and identification. C_LIO_LI- Amplitude diversity improves discrimination more, and bandwidth diversity improves identification more. C_LIO_LI- Representational geometry reveals the mechanisms of these effects. C_LI

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bioRxiv2025

Neural sensitivity to radial frequency patterns in the visual cortex of developing macaques

Visual resolution, contrast sensitivity and form perception improve gradually with age. In nonhuman primates, the sensitivity and resolution of cells in the retina, lateral geniculate nucleus and primary visual cortex (V1) also improve, but not enough to account for the perceptual changes. So, what aspects of visual system development limit visual sensitivity in infants? Improvements in behavioral sensitivity might arise from maturation of regions downstream of V1 such as V2, V4 and pIT, which are thought to support increasingly complex perceptual abilities. We recorded the responses of populations of neurons in areas V1, V2, V4, and pIT to radial frequency patterns - a type of global form stimulus. Subjects were three young monkeys between the ages of 19 and 54 weeks, and a single adult animal. We found that neurons and neural populations in V4 reliably encoded global form in radial frequency stimuli at the earliest ages we studied, while V1 neurons do not. V2 and pIT populations also showed some degree of selectivity for these patterns at early ages, especially at higher radial frequency values. We did not find significant, systematic changes in neural decoding performance that could account for the improvement in behavioral performance over the same age range in an overlapping group of animals (Rodriguez Deliz et al., 2024). Finally, consistent with our prior behavioral results, neural populations in V4 show highest sensitivity for the higher radial frequency values which contain the highest concentration of curvature and orientation cues. SIGNIFICANCE STATEMENTInfants have remarkably limited ability to discriminate shapes. These limitations cannot be fully explained by postnatal changes in their eyes, visual thalamus, or primary visual cortex. The perception of shape requires integration of local cues across space to create global form information. We therefore examined populations of neurons in extrastriate visual cortex to learn whether information represented in these regions might limit infants abilities to process global forms. We found instead that extrastriate areas involved in global form processing function maturely early in life, by the age of 4-6 months, suggesting that infants perceptual limits are set by other aspects of brain development.

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bioRxiv2025

Emergence of a contrast-invariant representation of naturalistic texture in macaque visual cortex

Sensory stimuli vary across a variety of dimensions, like contrast, orientation, or texture. The brain must rely on population representations to distinguish changes in one dimension from changes in another. To understand how the visual system might extract separable stimulus representations, we recorded multiunit neuronal responses to texture images varying along two dimensions: contrast, a property represented as early as the retina, and naturalistic statistical structure, a property that modulates neuronal responses in V2 and V4, but not in V1. We measured how sites in these 3 cortical areas responded to variation in both dimensions. Contrast modulated responses in all areas. In V2 and V4, the presence of naturalistic structure both modulated responses and increased contrast sensitivity. Tuning for naturalistic structure was both strongest and most dispersed in V4. We measured how well populations in each area could support the linear readout of both dimensions. Populations in V2 and V4 could support the linear readout of naturalistic structure, but in V4, this readout was more robust to variations in contrast. Significance StatementTo support flexible behavior, the brain must simultaneously represent different stimulus dimensions. Single neurons are typically modulated by multiple dimensions, and so cannot distinguish them - they must be extracted by decoding neural populations. We studied neuronal responses in three cortical visual areas - V1, V2, V4 - using texture images varying in both contrast and naturalistic image structure. We used population decoders to read out each dimension. In all areas, contrast was well decoded independently of image structure. On the other hand, V1 could not decode image structure independent of contrast, while V2 and V4 could. V4 decoding was greatly superior, because the selectivity of individual sites for texture was more diverse than in V1 or V2.

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bioRxiv2024

Responses to visual motion of neurons in the extrastriate visual cortex of macaque monkeys with experimental amblyopia

Amblyopia is a developmental disorder that results from abnormal visual experience in early life. Amblyopia typically reduces visual performance in one eye. We studied the representation of visual motion information in area MT and nearby extrastriate visual areas in two monkeys made amblyopic by creating an artificial strabismus in early life, and in a single age-matched control monkey. Tested monocularly, cortical responses to moving dot patterns, gratings, and plaids were qualitatively normal in awake, fixating amblyopic monkeys, with primarily subtle differences between the eyes. However, the number of binocularly driven neurons was substantially lower than normal; of the neurons driven predominantly by one eye, the great majority responded only to stimuli presented to the fellow eye. The small population driven by the amblyopic eye showed reduced coherence sensitivity and a preference for faster speeds in much the same way as behavioral deficits. We conclude that, while we do find important differences between neurons driven by the two eyes, amblyopia does not lead to a large scale reorganization of visual receptive fields in the dorsal stream when tested through the amblyopic eye, but rather creates a substantial shift in eye preference toward the fellow eye.

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bioRxiv2024

Foundations of visual form selectivity for neurons in macaque V1 and V2

Neurons early in the primate visual cortical pathway generate responses by combining signals from other neurons: some from downstream areas, some from within the same area, and others from areas upstream. Here we develop a model that selectively combines afferents derived from a population model of V1 cells. We use this model to account for responses we recorded of both V1 and V2 neurons in awake fixating macaque monkeys to stimuli composed of a sparse collection of locally oriented features ("droplets") designed to drive subsets of V1 neurons. The first stage computes the rectified responses of a fixed population of oriented filters at different scales that cover the visual field. The second stage computes a weighted combination of these first-stage responses, followed by a final nonlinearity, with parameters optimized to fit data from physiological recordings and constrained to encourage sparsity and locality. The fitted model accounts for the responses of both V1 and V2 neurons, capturing an average of 43% of the explainable variance for V1 and 38% for V2. The models fitted to droplet recordings predict responses to classical stimuli, such as gratings of different orientations and spatial frequencies, as well as to textures of different spectral content, which are known to be especially effective in driving V2. The models are less effective, however, at capturing the selectivity of responses to textures that include naturalistic image statistics. The pattern of afferents -- defined by their weights over the 4 dimensions of spatial position, orientation, and spatial frequency -- provides a common and interpretable characterization of the origin of many neuronal response properties in the early visual cortex.

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bioRxiv2024

Neuronal and behavioral responses to naturalistic texture images in macaque monkeys

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

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bioRxiv2024

Developmentally stable representations of naturalistic image structure in macaque visual cortex

We studied visual development in macaque monkeys using texture stimuli, matched in local spectral content but varying in "naturalistic" structure. In adult monkeys, naturalistic textures preferentially drive neurons in areas V2 and V4, but not V1. We paired behavioral measurements of naturalness sensitivity with separately-obtained neuronal population recordings from neurons in areas V1, V2, V4, and inferotemporal cortex (IT). We made behavioral measurements from 16 weeks of age and physiological measurements as early as 20 weeks, and continued through 56 weeks. Behavioral sensitivity reached half of maximum at roughly 25 weeks of age. Neural sensitivities remained stable from the earliest ages tested. As in adults, neural sensitivity to naturalistic structure increased from V1 to V2 to V4. While sensitivities in V2 and IT were similar, the dimensionality of the IT representation was more similar to V4s than to V2s.

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bioRxiv2024

Responses of neurons in macaque V4 to object and texture images

Humans and monkeys can rapidly recognize objects in everyday scenes. It is not fully understood where this computation arises, but previous work suggests selectivity for object shape first emerges in cortical area V4. To explore the mechanisms of this selectivity, we generated images on a continuum between "scrambled" textures and photographic images, preserving the local statistics of the original image while discarding structural information about scene and shape. We defined this continuum by the size of the region in which statistics were measured ("pooling region"). On average, neurons responded equally to photographic images and their scrambled counterparts. However, neurons exhibited a greater dynamic range of response to photographs. As a result, neuronal populations in V4 could more reliably discriminate between photographs than between scrambled images. Responses to partially scrambled images were more similar to responses to fully scrambled images than to photographs, even for perceptually subtle changes, and only began to resemble responses to photographs for pooling regions roughly half the size of typical V4 receptive fields. These same patterns emerged in an image similarity metric designed to predict human judgements of image degradation. Finally, V4 object selectivity showed dynamics that grew slowly and persisted following response offset, suggesting this signal may arise from recurrent mechanisms. Significance StatementObject recognition is a primary goal of visual processing, but is too complex to be computed by early visual areas. To evaluate where object-selective signals emerge, we recorded the responses of individual neurons in mid-level area V4 as macaque monkeys viewed images of objects ("things") and of matched textures ("stuff"). Object selective V4 responses emerged in two phases. Short-latency responses discriminate objects from one another, but the distinction between objects and textures arrived later. This late-emerging signal was sensitive even to small image degradations, as is human perception. Our results show how V4 initiates the brains representation of visual objects.

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bioRxiv2024

Development of radial frequency pattern perception in macaque monkeys

Infant primates see poorly, and most perceptual functions mature steadily beyond early infancy. Behavioral studies on human and macaque infants show that global form perception, as measured by the ability to integrate contour information into a coherent percept, improves dramatically throughout the first several years after birth. However, it is unknown when sensitivity to curvature and shape emerges in early life. We studied the development of shape sensitivity in eighteen macaques, aged 2 months to 10 years. Using radial frequency stimuli (RFS), circular targets whose radii are modulated sinusoidally, we tested monkeys ability to discriminate RFS from circles as a function of the depth and frequency of sinusoidal modulation. We implemented a new 4-choice oddity task and compared the resulting data with that from a traditional 2-alternative task. Behavioral performance at all radial frequencies improved with age. Performance was better for higher radial frequencies, suggesting the developing visual system prioritizes processing of fine visual details that are ecologically relevant. By utilizing two complementary methods, we were able to capture a comprehensive developmental trajectory for shape perception.

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bioRxiv2023

DREDge: robust motion correction for high-density extracellular recordings across species

High-density microelectrode arrays (MEAs) have opened new possibilities for systems neuroscience in human and non-human animals, but brain tissue motion relative to the array poses a challenge for downstream analyses, particularly in human recordings. We introduce DREDge (Decentralized Registration of Electrophysiology Data), a robust algorithm which is well suited for the registration of noisy, nonstationary extracellular electrophysiology recordings. In addition to estimating motion from spikes in the action potential (AP) frequency band, DREDge enables automated tracking of motion at high temporal resolution in the local field potential (LFP) frequency band. In human intraoperative recordings, which often feature fast (period <1s) motion, DREDge correction in the LFP band enabled reliable recovery of evoked potentials, and significantly reduced single-unit spike shape variability and spike sorting error. Applying DREDge to recordings made during deep probe insertions in nonhuman primates demonstrated the possibility of tracking probe motion of centimeters across several brain regions while simultaneously mapping single unit electrophysiological features. DREDge reliably delivered improved motion correction in acute mouse recordings, especially in those made with an recent ultra-high density probe. We also implemented a procedure for applying DREDge to recordings made across tens of days in chronic implantations in mice, reliably yielding stable motion tracking despite changes in neural activity across experimental sessions. Together, these advances enable automated, scalable registration of electrophysiological data across multiple species, probe types, and drift cases, providing a stable foundation for downstream scientific analyses of these rich datasets.

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bioRxiv2023

Shared mechanisms drive ocular following and motion perception

How features of complex visual patterns combine to drive perception and eye movements is not well understood. We simultaneously assessed human observers perceptual direction estimates and ocular following responses (OFR) evoked by moving plaids made from two summed gratings with varying contrast ratios. When the gratings were of equal contrast, observers eye movements and perceptual reports followed the motion of the plaid pattern. However, when the contrasts were unequal, eye movements and reports during early phases of the OFR were biased toward the direction of the high-contrast grating component; during later phases, both responses more closely followed the plaid pattern direction. The shift from component- to pattern-driven behavior resembles the shift in tuning seen under similar conditions in neuronal responses recorded from monkey MT. Moreover, for some conditions, pattern tracking and perceptual reports were correlated on a trial-by-trial basis. The OFR may therefore provide a precise behavioural read-out of the dynamics of neural motion integration for complex visual patterns.

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bioRxiv2022

Contrast and luminance gain control in the macaque'slateral geniculate nucleus

In natural scenes, there is substantial variation in the mean and fluctuation of light levels (luminance and contrast). Retinal ganglion cells maintain their sensitivity despite this variation and their limited signaling bandwidth using two adaptive mechanisms, which control luminance and contrast gain. However, the signature of each mechanism and their interactions further downstream of the retina are unknown. We recorded neurons in the magnocellular and parvocellular layers of the lateral geniculate nucleus (LGN) in anesthetized adult male macaques and characterized how they adapt to changes in contrast and luminance. As contrast increases, neurons in the magnocellular layers maintain sensitivity to high temporal frequency stimuli but attenuate sensitivity to low temporal-frequency stimuli. Neurons in the parvocellular layers do not adapt to changes in contrast. As luminance increases, magnocellular and parvocellular cells increase their sensitivity to high temporal frequency stimuli. Adaptation to luminance is independent of adaptation to contrast, as previously reported for LGN neurons in the cat. Our results are similar to those previously reported for macaque retinal ganglion cells, suggesting that adaptation to luminance and contrast result from two independent mechanisms that are retinal in origin.

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bioRxiv2022

Sensitivity to naturalistic texture relies primarily on high spatial frequencies

Natural images contain information at multiple spatial scales. Although we understand how early visual mechanisms split multi-scale images into distinct spatial frequency channels, we do not know how the outputs of these channels are processed further by mid-level visual mechanisms. We have recently developed a naturalness discrimination task that uses synthesized, multi-scale textures to isolate these mid-level mechanisms (Freeman et. al. 2013). Here, we use three experimental manipulations (image blur, image rescaling, and eccentric viewing) to show that naturalness sensitivity is strongly dependent on image features at high object spatial frequencies (measured in cycles/image). As a result, sensitivity depends on a texture acuity limit, a property of the visual system that sets the highest retinal spatial frequency (measured in cycles/degree) that can be used to solve the task. A model observer analysis shows that high object spatial frequencies carry more task-relevant information than low object spatial frequencies. Comparing the outcome of this analysis with human performance reveals that human observers efficiency is similar for all object spatial frequencies. We conclude that the mid-level mechanisms that underlie naturalness sensitivity effectively extract information from all image features below the texture acuity limit, regardless of their retinal and object spatial frequency.

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bioRxiv2022

Neural Basis of The Double Drift Illusion

In the "double-drift" illusion, local motion within a window moving in the periphery alters the windows perceived path. The illusion is strong even when the eyes track a target whose motion matches the window so that the stimulus remains stable on the retina. This implies that the illusion involves the integration of retinal signals with non-retinal eye-movement signals. To identify where in the brain this integration occurs, we measured BOLD fMRI responses in visual cortex while subjects experienced the double drift illusion. We identified a number of cortical areas that responded more strongly during the illusion, but only in area hMT+ was it possible to decode the illusory trajectory. Our results provide evidence for a perceptual representation in human visual cortex that is not linked to retinal position.

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bioRxiv2019

Laminar differences in responses to naturalistic texture in macaque V1 and V2

Most single units recorded from macaque V2 respond with higher firing rates to synthetic texture images containing \"naturalistic\" higher-order statistics than to spectrally matched \"noise\" images lacking these statistics. In contrast, few single units in V1 show this property. We explored how the strength and dynamics of response vary across the different layers of visual cortex by recording multiunit and gamma band activity evoked by brief presentations of naturalistic and noise images in V1 and V2 of anesthetized macaque monkeys. As previously reported, recordings in V2 showed consistently stronger responses to naturalistic texture than to spectrally matched noise. In contrast to single unit recordings, V1 multiunit activity showed some preference for images with naturalistic statistics, and in gamma band activity this preference was comparable across V1 and V2. Sensitivity to naturalistic image structure was strongest in the supragranular and infragranular layers of V1, but weak in granular layers, suggesting that it might reflect feedback from V2. Response timing was consistent with this idea. Visual responses appeared first in V1, followed by V2. Sensitivity to naturalistic texture emerged first in V2, followed by the supragranular and infragranular layers of V1, and finally in the granular layers of V1. Our results demonstrate laminar differences in the encoding of higher-order statistics of natural texture, and suggest that this sensitivity first arises in V2 and is fed back to modulate activity in V1.\n\nSignificance StatementThe circuit mechanisms responsible for visual representations of intermediate complexity are largely unknown. We used a well-validated set of synthetic texture stimuli to probe the temporal and laminar profile of sensitivity to the higher-order statistical structure of natural images. We found that this sensitivity emerges first and most strongly in V2 but soon after in V1. However, sensitivity in V1 is higher in the laminae (extragranular) and recording modalities (local field potential) most likely affected by V2 connections, suggesting a feedback origin. Our results show how sensitivity to naturalistic image structure emerges across time and circuitry in the early visual cortex.

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bioRxiv2019

Compound stimuli reveal the structure of visual motion selectivity in macaque MT neurons

Motion selectivity in primary visual cortex (V1) is approximately separable in orientation, spatial frequency, and temporal frequency (\"frequency-separable\"). Models for area MT neurons posit that their selectivity arises by combining direction-selective V1 afferents whose tuning is organized around a tilted plane in the frequency domain, specifying a particular direction and speed (\"velocity-separable\"). This construction explains \"pattern direction selective\" MT neurons, which are velocity-selective but relatively invariant to spatial structure, including spatial frequency, texture and shape. Surprisingly, when tested with single drifting gratings, most MT neurons responses are fit equally well by models with either form of separability. However, responses to plaids (sums of two moving gratings) tend to be better described as velocity-separable, especially for pattern neurons. We conclude that direction selectivity in MT is primarily computed by summing V1 afferents, but pattern-invariant velocity tuning for complex stimuli may arise from local, recurrent interactions.\n\nSignificance StatementHow do sensory systems build representations of complex features from simpler ones? Visual motion representation in cortex is a well-studied example: the direction and speed of moving objects, regardless of shape or texture, is computed from the local motion of oriented edges. Here we quantify tuning properties based on single-unit recordings in primate area MT, then fit a novel, generalized model of motion computation. The model reveals two core properties of MT neurons -- speed tuning and invariance to local edge orientation -- result from a single organizing principle: each MT neuron combines afferents that represent edge motions consistent with a common velocity, much as V1 simple cells combine thalamic inputs consistent with a common orientation.

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bioRxiv2019

Altered functional interactions between neurons in primary visual cortex of macaque monkeys with experimental amblyopia

Amblyopia, a disorder in which vision through one of the eyes is degraded, arises because of defective processing of information by the visual system. Amblyopia often develops in humans after early misalignment of the eyes (strabismus), and can be simulated in macaque monkeys by artificially inducing strabismus. In such amblyopic animals, single-unit responses in primary visual cortex (V1) are appreciably reduced when evoked by the amblyopic eye compared to the other (fellow) eye. However, this degradation in single V1 neuron responsivity is not commensurate with the marked losses in visual sensitivity and resolution measured behaviorally. Here we explored the idea that changes in patterns of coordinated activity across populations of V1 neurons may contribute to degraded visual representations in amblyopia, potentially making it more difficult to read out evoked activity to support perceptual decisions. We studied the visually-evoked activity of V1 neuronal populations in three macaques (M. nemestrina) with strabismic amblyopia and in one control. Activity driven through the amblyopic eye was diminished, and these responses also showed more interneuronal correlation at all stimulus contrasts than responses driven through the fellow eye or responses in the control. A decoding analysis showed that responses driven through the amblyopic eye carried less visual information than other responses. Our results suggest that part of the reduced visual capacity of amblyopes may be due to changes in the patterns of functional interaction among neurons in V1.\n\nNew and noteworthyAmblyopia is a developmental disorder of visual processing that reduces visual function and changes the visual responses of cortical neurons in macaque monkeys. The neuronal and behavioral changes are not always well correlated. We found that the interactions among neurons in the visual cortex of monkeys with amblyopia are also altered. These changes may contribute to amblyopic visual deficits by diminishing the amount of information relayed by neuronal populations driven by the amblyopic eye.

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