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J Neurophysiol (November 1, 2006). doi:10.1152/jn.00747.2006
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Submitted on July 20, 2006
Accepted on October 28, 2006

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

Shih-Cheng Yen1*, Jonathan Baker1, and Charles M Gray2

1 Center for Computational Biology, Montana State University, Bozeman, Montana, United States
2 Cell Biology and Neuroscience, Montana State University, Bozeman, Montana, United States

* To whom correspondence should be addressed. E-mail: shihcheng{at}alumni.upenn.edu.

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 (10s of ms), 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.




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