Visual exposure enhances stimulus encoding and persistence in primary cortex

Abstract

Sensory exposure alters the response properties of individual neurons in primary sensory cortices. However, it remains unclear how these changes affect stimulus encoding by populations of sensory cells. Here, recording from populations of neurons in cat primary visual cortex, we demonstrate that visual exposure enhances stimulus encoding and discrimination. We find that repeated presentation of brief, high-contrast shapes results in a stereotyped, biphasic population response consisting of a short-latency transient, followed by a late and extended period of reverberatory activity. Visual exposure selectively improves the stimulus specificity of the reverberatory activity, by increasing the magnitude and decreasing the trialto-trial variability of the neuronal response. Critically, this improved stimulus encoding is distributed across the population and depends on precise temporal coordination. Our findings provide evidence for the existence of an exposure-driven optimization process that enhances the encoding power of neuronal populations in early visual cortex, thus potentially benefiting simple readouts at higher stages of visual processing.

Recurrent dynamics in the cerebral cortex: Integration of sensory evidence with stored knowledge

“…The prediction that priors stored in the network contribute to the stimulus specificity of substates is also supported by the finding that classifiers trained to identify stimuli often perform better on the delayed, reverberating part of the responses than on the initial transients that are dominated by direct sensory input (175). Principal component analysis (PCA) of the rate vectors showed that the segregation of the vectors induced by different stimuli can increase over a few hundred milliseconds even after stimulus offset (175).…”

“…This interpretation is supported by simulations of self-organizing recurrent networks. If the recurrent connections are endowed with Hebbian synapses, they reproduce this improved classification of familiar stimuli (121,175,178). Direct evidence for unsupervised modifications of recurrent connections by repeated stimulation is also available from the cat visual cortex of anesthetized cats (166).…”

“…After frequent exposure to the same set of stimuli, performance of classifiers trained to discriminate between stimuli improved, suggesting enhanced orthogonalization of stimulus-specific substates. Accordingly, PCA analysis of the activity vectors revealed increased segregation of representations in the high-dimensional space for stimuli that had been presented particularly frequently ( 175 ). Also in agreement with this prediction is the evidence that stimulus-specific response vectors evoked by frequently repeated stimuli are replayed in the primary visual cortex during resting state.…”

“…Also in agreement with this prediction is the evidence that stimulus-specific response vectors evoked by frequently repeated stimuli are replayed in the primary visual cortex during resting state. Classifiers trained to reconstruct stimuli from spontaneously occurring response vectors achieved much better reconstructions for stimuli that had been presented frequently than for less familiar stimuli ( 175 ); see also ref. 177 .…”

Stimulus-specific plasticity of macaque V1 spike rates and gamma

“…This limits inferences on the cellular origins of increased synchronization. Since different neurons may show different repetition effects, these could average out, potentially masking repetition-related increases or stability in firing rate for subsets of neurons (Homann et al, 2017; Lazar et al, 2018; Patterson et al, 2013; Solomon and Kohn, 2014; Wissig and Kohn, 2012). Notably, Brunet et al (2014) showed that putative interneurons increasingly synchronized with repetition, whereas poorly driven putative excitatory cells dropped out of the gamma-rhythm.…”