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Cohen, M. R.

Publications and source records attributed to Cohen, M. R..

24 records · Page 2Linked to original sources

A general decoding strategy explains the relationship between behavior and correlated variability

Improvements in perception are frequently accompanied by decreases in correlated variability in sensory cortex. This relationship is puzzling because overall changes in correlated variability should minimally affect optimal information coding. We hypothesize that this relationship arises because instead of using optimal strategies for decoding the specific stimuli at hand, observers prioritize generality: a single set of neuronal weights to decode any stimuli. We tested this using a combination of multineuron recordings in the visual cortex of behaving rhesus monkeys and a cortical circuit model. We found that general decoders optimized for broad rather than narrow sets of visual stimuli better matched the animals decoding strategy, and that their performance was more related to the magnitude of correlated variability. In conclusion, the inverse relationship between perceptual performance and correlated variability can be explained by observers using a general decoding strategy, capable of decoding neuronal responses to the variety of stimuli encountered in natural vision. IMPACT STATEMENTThe frequently observed relationship between perceptual performance and correlated variability in sensory cortex can be explained by observers using a decoding strategy that prioritizes generality for many stimuli over precision.

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Patterns of neural correlations in V1 vary with the number of objects

Sensory receptive fields are large enough that they can contain more than one perceptible stimulus. How, then, can the brain encode information about each of the stimuli that may be present at a given moment? We recently showed that when more than one stimulus is present, single neurons can fluctuate between coding one vs. the other(s) across some time period, suggesting a form of neural multiplexing of different stimuli (Caruso et al., 2018). Here we investigate (a) whether such coding fluctuations occur in early visual cortical areas; (b) how coding fluctuations are coordinated across the neural population; and (c) how coordinated coding fluctuations depend on the parsing of stimuli into separate vs. fused objects. We found coding fluctuations do occur in macaque V1 but only when the two stimuli form separate objects. Such separate objects evoked a novel pattern of V1 spike count ("noise") correlations involving distinct distributions of positive and negative values. This bimodal correlation pattern was most pronounced among pairs of neurons showing the strongest evidence for coding fluctuations or multiplexing. Whether a given pair of neurons exhibited positive or negative correlations depended on whether the two neurons both responded better to the same object or had different object preferences. Distinct distributions of spike count correlations based on stimulus preferences were also seen in V4 for separate objects but not when two stimuli fused to form one object. These findings suggest multiple objects evoke different response dynamics than those evoked by single stimuli, lending support to the multiplexing hypothesis and suggesting a means by which information about multiple objects can be preserved despite the apparent coarseness of sensory coding. Significance StatementHow the brain separates information about multiple objects despite overlap in the neurons responsive to each item is not well understood. Here we show that some neurons in V1 exhibit coding fluctuations in response to two objects, and that these coding fluctuations are coordinated at the population level in ways that are not observed for single objects. Broadly similar results were obtained in V4. These response dynamics lend support to the hypothesis that information about individual objects may be multiplexed across the neural population, preserving information about each item despite the coarseness of sensory coding.

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Low rank mechanisms underlying flexible visual representations

Neuronal population responses to sensory stimuli are remarkably flexible. The responses of neurons in visual cortex depend on stimulus properties (e.g. contrast), processes that affect all stages of visual processing (e.g. adaptation), and cognitive processes (e.g attention or task switching). The effects of all of these processes on trial-averaged responses of individual neurons are well-described by divisive normalization, in which responses are scaled by the total stimulus drive. Normalization describes how a staggering variety of sensory, cognitive, and motor processes affect individual neurons (1), but whether different normalization processes could be mediated by the same mechanism remains poorly understood. We and others recently showed that attention has low rank effects on the covariability of populations of neurons in visual area V4 (2-4), which strongly constrains mechanistic models mechanism (2). We hypothesized that measuring changes in population covariability associated with other normalization processes could clarify whether they might share a mechanism. Our experimental design included measurements in multiple visual areas using four normalization processes. We found that contrast, adaptation, attention, and task switching affect the responses of populations of neurons in primate visual cortex in a similarly low rank way. These results suggest that a given circuit uses a common mechanism to perform many forms of normalization and likely reflect a general principle that applies to a wide range of brain areas and sensory, cognitive, or motor processes.

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Simultaneous multi-area recordings suggest a novel hypothesis about how attention improves performance

Visual attention dramatically improves subjects ability to see and also modulates the responses of neurons in every known visual and oculomotor area, but whether those modulations can account for perceptual improvements remains unclear. We measured the relationship between populations of visual neurons, oculomotor neurons, and behavior during detection and discrimination tasks. We found that neither of the two prominent hypothesized neuronal mechanisms underlying attention (which concern changes in information coding and the way sensory information is read out) provide a satisfying account of the observed behavioral improvements. Instead, our results are more consistent with the novel hypothesis that attention reshapes the representation of attended stimuli to more effectively influence behavior. Our results suggest a path toward understanding the neural underpinnings of perception and cognition in health and disease by analyzing neuronal responses in ways that are constrained by behavior and interactions between brain areas.

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Neuronal population mechanisms of lightness perception

The way that humans and animals perceive the lightness of an object depends on its physical luminance as well as its surrounding context. While neuronal responses throughout the visual pathway are modulated by context, the relationship between neuronal responses and lightness perception is poorly understood. We searched for a neuronal mechanism of lightness by recording responses of neuronal populations in monkey primary visual cortex (V1) and area V4 to stimuli that produce a lightness illusion in humans, in which the lightness of a disk depends on the context in which it is embedded. We found that the way individual units encode the luminance (or equivalently for our stimuli, contrast) of the disk and its context is extremely heterogeneous. This motivated us to ask whether the population representation in either V1 or V4 satisfies three criteria: 1) disk luminance is represented with high fidelity, 2) the context surrounding the disk is also represented, and 3) the representations of disk luminance and context interact to create a representation of lightness that depends on these factors in a manner consistent with human psychophysical judgments of disk lightness. We found that populations of units in both V1 and V4 fulfill the first two criteria, but that we cannot conclude that the two types of information in either area interact in a manner that clearly predicts human psychophysical measurements: the interpretation of our population measurements depends on how subsequent areas read out lightness from the population responses.\n\nNew & NoteworthyA core question in visual neuroscience is how the brain extracts stable representations of object properties from the retinal image. We searched for a neuronal mechanism of lightness perception by determining whether the responses of neuronal populations in primary visual cortex and area V4 could account for a lightness illusion measured using human psychophysics. Our results suggest that comparing psychophysics with population recordings will yield insight into neuronal mechanisms underlying a variety of perceptual phenomena.

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Learning And Attention Reveal A General Relationship Between Neuronal Variability And Perception

The trial-to-trial response variability that is shared between pairs of neurons (termed spike count correlations1 or rSC) has been the subject of many recent studies largely because it might limit the amount of information that can be encoded by neuronal populations. Spike count correlations are flexible and change depending on task demands2-7. However, the relationship between correlated variability and information coding is a matter of current debate2-14. This debate has been difficult to resolve because testing the theoretical predictions would require simultaneous recordings from an experimentally unfeasible number of neurons. We hypothesized that if correlated variability limits population coding, then spike count correlations in visual cortex should a) covary with subjects performance on visually guided tasks and b) lie along the dimensions in neuronal population space that contain information that is used to guide behavior. We focused on two processes that are known to improve visual performance: visual attention, which allows observers to focus on important parts of a visual scene15-17, and perceptual learning, which slowly improves observers ability to discriminate specific, well-practiced stimuli18-20. Both attention and learning improve performance on visually guided tasks, but the two processes operate on very different timescales and are typically studied using different perceptual tasks. Here, by manipulating attention and learning in the same task, subjects, trials, and neuronal populations, we show that there is a single, robust relationship between correlated variability in populations of visual neurons and performance on a change-detection task. We also propose an explanation for the mystery of how correlated variability might affect performance: it is oriented along the dimensions of population space used by the animal to make perceptual decisions. Our results suggest that attention and learning affect the same aspects of the neuronal population activity in visual cortex, which may be responsible for learning- and attention-related improvements in behavioral performance. More generally, our study provides a framework for leveraging the activity of simultaneously recorded populations of neurons, cognitive factors, and perceptual decisions to understand the neuronal underpinnings of behavior.

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