Heterogeneity in the Responses of Adjacent Neurons to Natural Stimuli in Cat Striate Cortex

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Abstract
When presented with simple stimuli like bars and gratings, adjacent neurons in striate cortex exhibit shared selectivity for multiple stimulus dimensions, such as orientation, direction, and spatial frequency. This has led to the idea that local averaging of neuronal responses provides a more reliable representation of stimulus properties. However, when stimulated with complex, time-varying natural scenes (i.e., movies), striate neurons exhibit highly sparse responses. This raises the question of how much response heterogeneity the local population exhibits when stimulated with movies, and how it varies with separation distance between cells. We investigated this question by simultaneously recording the responses of groups of neurons in cat striate cortex to the repeated presentation of movies using silicon probes in a multi-tetrode configuration. We found, first, that the responses of striate neurons to movies are brief (tens of milliseconds), decorrelated, and exhibit high population sparseness. Second, we found that adjacent neurons differed significantly in their peak firing rates even when they responded to the same frames of a movie. Third, pairs of adjacent neurons recorded on the same tetrodes exhibited as much heterogeneity in their responses as pairs recorded by different tetrodes. These findings demonstrate that complex natural scenes evoke highly heterogeneous responses within local populations, suggesting that response redundancy in a cortical column is substantially lower than previously thought.