Visual exposure enhances stimulus encoding and persistence in primary cortex

Abstract

Significance Experience shapes sensory responses, already at the earliest stages of cortical processing. We provide evidence that, in the primary visual cortex of anesthetized cats, brief repetitive exposure to a set of simple, abstract stimuli expands the range and decreases the variability of neuronal responses that persist after stimulus offset. These refinements increase the stimulus-specific clustering of neuronal population responses and result in a more efficient encoding of both stimulus identity and stimulus structure, thus potentially benefiting simple readouts in higher cortical areas. Similar results can be achieved via local plasticity mechanisms in recurrent networks, through self-organized refinements of internal dynamics that do not require changes in firing amplitudes. The brain adapts to the sensory environment. For example, simple sensory exposure can modify the response properties of early sensory neurons. How these changes affect the overall encoding and maintenance of stimulus information across neuronal populations remains unclear. We perform parallel recordings in the primary visual cortex of anesthetized cats and find that brief, repetitive exposure to structured visual stimuli enhances stimulus encoding by decreasing the selectivity and increasing the range of the neuronal responses that persist after stimulus presentation. Low-dimensional projection methods and simple classifiers demonstrate that visual exposure increases the segregation of persistent neuronal population responses into stimulus-specific clusters. These observed refinements preserve the representational details required for stimulus reconstruction and are detectable in postexposure spontaneous activity. Assuming response facilitation and recurrent network interactions as the core mechanisms underlying stimulus persistence, we show that the exposure-driven segregation of stimulus responses can arise through strictly local plasticity mechanisms, also in the absence of firing rate changes. Our findings provide evidence for the existence of an automatic, unguided 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.