Efficient coding of spatial information in the primate retina

Eizaburo Doi, Jeffrey L. Gauthier, Greg D. Field, Jonathon Shlens, Alexander Sher, Martin Greschner, Timothy A. Machado, Lauren H. Jepson, Keith Mathieson, Deborah E. Gunning, Alan M. Litke, Liam Paninski, E. J. Chichilnisky, Eero Simoncelli

Research output: Contribution to journalArticle

Abstract

Sensory neurons have been hypothesized to efficiently encode signals from the natural environment subject to resource constraints. The predictions of this efficient coding hypothesis regarding the spatial filtering properties of the visual system have been found consistent with human perception, but they have not been compared directly with neural responses. Here, we analyze the information that retinal ganglion cells transmit to the brain about the spatial information in natural images subject to three resource constraints: the number of retinal ganglion cells, their total response variances, and their total synaptic strengths. We derive a model that optimizes the transmitted information and compare it directly with measurements of complete functional connectivity between cone photoreceptors and the four major types of ganglion cells in the primate retina, obtained at single-cell resolution. We find that the ganglion cell population exhibited 80% efficiency in transmitting spatial information relative to the model. Both the retina and the model exhibited high redundancy (~30%) among ganglion cells of the same cell type. A novel and unique prediction of efficient coding, the relationships between projection patterns of individual cones to all ganglion cells, was consistent with the observed projection patterns in the retina. These results indicate a high level of efficiency with near-optimal redundancy in visual signaling by the retina.

Original languageEnglish (US)
Pages (from-to)16256-16264
Number of pages9
JournalJournal of Neuroscience
Volume32
Issue number46
DOIs
StatePublished - Nov 14 2012

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Primates
Retina
Ganglia
Retinal Ganglion Cells
Retinal Cone Photoreceptor Cells
Sensory Receptor Cells
Brain
Population

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Doi, E., Gauthier, J. L., Field, G. D., Shlens, J., Sher, A., Greschner, M., ... Simoncelli, E. (2012). Efficient coding of spatial information in the primate retina. Journal of Neuroscience, 32(46), 16256-16264. https://doi.org/10.1523/JNEUROSCI.4036-12.2012

Efficient coding of spatial information in the primate retina. / Doi, Eizaburo; Gauthier, Jeffrey L.; Field, Greg D.; Shlens, Jonathon; Sher, Alexander; Greschner, Martin; Machado, Timothy A.; Jepson, Lauren H.; Mathieson, Keith; Gunning, Deborah E.; Litke, Alan M.; Paninski, Liam; Chichilnisky, E. J.; Simoncelli, Eero.

In: Journal of Neuroscience, Vol. 32, No. 46, 14.11.2012, p. 16256-16264.

Research output: Contribution to journalArticle

Doi, E, Gauthier, JL, Field, GD, Shlens, J, Sher, A, Greschner, M, Machado, TA, Jepson, LH, Mathieson, K, Gunning, DE, Litke, AM, Paninski, L, Chichilnisky, EJ & Simoncelli, E 2012, 'Efficient coding of spatial information in the primate retina', Journal of Neuroscience, vol. 32, no. 46, pp. 16256-16264. https://doi.org/10.1523/JNEUROSCI.4036-12.2012
Doi E, Gauthier JL, Field GD, Shlens J, Sher A, Greschner M et al. Efficient coding of spatial information in the primate retina. Journal of Neuroscience. 2012 Nov 14;32(46):16256-16264. https://doi.org/10.1523/JNEUROSCI.4036-12.2012
Doi, Eizaburo ; Gauthier, Jeffrey L. ; Field, Greg D. ; Shlens, Jonathon ; Sher, Alexander ; Greschner, Martin ; Machado, Timothy A. ; Jepson, Lauren H. ; Mathieson, Keith ; Gunning, Deborah E. ; Litke, Alan M. ; Paninski, Liam ; Chichilnisky, E. J. ; Simoncelli, Eero. / Efficient coding of spatial information in the primate retina. In: Journal of Neuroscience. 2012 ; Vol. 32, No. 46. pp. 16256-16264.
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