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High-sensitivity rod photoreceptor input to the blue-yellow color opponent pathway in macaque retina

Abstract

Small bistratified cells (SBCs) in the primate retina carry a major blue-yellow opponent signal to the brain. We found that SBCs also carry signals from rod photoreceptors, with the same sign as S cone input. SBCs exhibited robust responses under low scotopic conditions. Physiological and anatomical experiments indicated that this rod input arose from the AII amacrine cell–mediated rod pathway. Rod and cone signals were both present in SBCs at mesopic light levels. These findings have three implications. First, more retinal circuits may multiplex rod and cone signals than were previously thought to, efficiently exploiting the limited number of optic nerve fibers. Second, signals from AII amacrine cells may diverge to most or all of the 20 retinal ganglion cell types in the peripheral primate retina. Third, rod input to SBCs may be the substrate for behavioral biases toward perception of blue at mesopic light levels.

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Figure 1: SBC identification at photopic and scotopic light levels.
Figure 2: Change in SBC receptive field size between scotopic and photopic light levels.
Figure 3: Responses of SBCs and ON parasol cells to dim light steps.
Figure 4: L-APB nearly eliminated the light response in OFF parasol cells at low scotopic light levels.
Figure 5: Gap junctions are present at appositions between AII amacrine and S cone bipolar cells.
Figure 6: Spectral tuning and dynamics of SBC responses depended on light level.

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Acknowledgements

We thank C.K. Hulse for technical assistance; M.I. Grivich, D. Petrusca, W. Dabrowski, A. Grillo, P. Grybos, P. Hottowy and S. Kachiguine for technical development; H. Fox, M. Taffe, E. Callaway and K. Osborn for providing access to retinas; H. Wässle and J. O'Brien for providing antibodies; and S. Barry for machining. We thank the San Diego Supercomputer Center and the National Science Foundation (Cooperative Agreements 05253071 and 0438741) for large-scale data storage. This work was supported by the Helen Hay Whitney Foundation (G.D.F.), Deutsche Forschungsgemeinschaft (M.G.), a US National Institutes of Health National Research Service Award (NS054519-01), the Chapman Foundation (J.L.G.), the Miller Institute for Basic Research in Science, the University of California at Berkeley (J.S.), a Burroughs Wellcome Fund Career Award at Scientific Interface (A.S.), the McKnight Foundation (A.M.L. and E.J.C.), National Science Foundation grant PHY-0750525 (A.M.L.), a Sloan Research Fellowship and US National Institutes of Health grants EY13150 (E.J.C.), EY06472 (D.W.M.) and EY10608 (D.W.M.).

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G.D.F., D.W.M. and E.J.C. conceived the experiments and wrote the manuscript. G.D.F., M.G., J.L.G., J.S., A.S. and E.J.C. performed the electrophysiological experiments. C.R. and D.W.M. carried out the immunolabeling experiments. A.S. and A.L.M. provided and supported the large-scale multi-electrode array system.

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Correspondence to Greg D Field.

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Field, G., Greschner, M., Gauthier, J. et al. High-sensitivity rod photoreceptor input to the blue-yellow color opponent pathway in macaque retina. Nat Neurosci 12, 1159–1164 (2009). https://doi.org/10.1038/nn.2353

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