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The Journal of Neuroscience, November 28, 2007, 27(48):13261-13272; doi:10.1523/JNEUROSCI.3437-07.2007

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Behavioral/Systems/Cognitive
Spatial Properties and Functional Organization of Small Bistratified Ganglion Cells in Primate Retina

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

¹Salk Institute for Biological Studies, La Jolla, California 92037, and ²Santa Cruz Institute for Particle Physics, University of California, Santa Cruz, California 95064

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

The primate visual system consists of parallel pathways initiated by distinct cell types in the retina that encode different features of the visual scene. Small bistratified cells (SBCs), which form a major projection to the thalamus, exhibit blue-ON/yellow-OFF [S-ON/(L+M)-OFF] light responses thought to be important for high-acuity color vision. However, the spatial processing properties of individual SBCs and their spatial arrangement across the visual field are poorly understood. The present study of peripheral primate retina reveals that contrary to previous suggestions, SBCs exhibit center-surround spatial structure, with the (L+M)-OFF component of the receptive field 50% larger in diameter than the S-ON component. Analysis of response kinetics shows that the (L+M)-OFF response in SBCs is slower than the S-ON response and significantly less transient than that of simultaneously recorded OFF-parasol cells. The (L+M)-OFF response in SBCs was eliminated by bath application of the metabotropic glutamate receptor agonist L-APB. These observations indicate that the (L+M)-OFF response of SBCs is not formed by OFF-bipolar cell input as has been suspected and suggest that it arises from horizontal cell feedback. Finally, the receptive fields of SBCs form orderly mosaics, with overlap and regularity similar to those of ON-parasol cells. Thus, despite their distinctive morphology and chromatic properties, SBCs exhibit two features of other retinal ganglion cell types: center-surround antagonism and regular mosaic sampling of visual space.

Key words: receptive field; color; vision; APB; blue–yellow; opponent; nearest neighbor; center-surround; koniocellular; mosaic

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Received July 29, 2007; revised Oct. 19, 2007; accepted Oct. 20, 2007.

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

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