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The Journal of Neuroscience, April 15, 2009, 29(15):5022-5031; doi:10.1523/JNEUROSCI.5187-08.2009

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Behavioral/Systems/Cognitive
The Structure of Large-Scale Synchronized Firing in Primate Retina

Jonathon Shlens,^1,3 Greg D. Field,¹ Jeffrey L. Gauthier,¹ Martin Greschner,¹ Alexander Sher,² Alan M. Litke,² and E. J. Chichilnisky¹

¹The Salk Institute, La Jolla, California 92037, ²Santa Cruz Institute for Particle Physics, University of California, Santa Cruz, California 95064, and ³University of California, Berkeley, California 94720

Correspondence should be addressed to Jonathon Shlens, Systems Neurobiology, The Salk Institute, 10010 North Torrey Pines Road, La Jolla, CA 92037. Email: shlens{at}salk.edu

Synchronized firing among neurons has been proposed to constitute an elementary aspect of the neural code in sensory and motor systems. However, it remains unclear how synchronized firing affects the large-scale patterns of activity and redundancy of visual signals in a complete population of neurons. We recorded simultaneously from hundreds of retinal ganglion cells in primate retina, and examined synchronized firing in completely sampled populations of 50–100 ON-parasol cells, which form a major projection to the magnocellular layers of the lateral geniculate nucleus. Synchronized firing in pairs of cells was a subset of a much larger pattern of activity that exhibited local, isotropic spatial properties. However, a simple model based solely on interactions between adjacent cells reproduced 99% of the spatial structure and scale of synchronized firing. No more than 20% of the variability in firing of an individual cell was predictable from the activity of its neighbors. These results held both for spontaneous firing and in the presence of independent visual modulation of the firing of each cell. In sum, large-scale synchronized firing in the entire population of ON-parasol cells appears to reflect simple neighbor interactions, rather than a unique visual signal or a highly redundant coding scheme.

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Received Oct. 27, 2008; revised Feb. 12, 2009; accepted Feb. 28, 2009.

Correspondence should be addressed to Jonathon Shlens, Systems Neurobiology, The Salk Institute, 10010 North Torrey Pines Road, La Jolla, CA 92037. Email: shlens{at}salk.edu

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