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Functional connectivity in the retina at the resolution of photoreceptors

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Abstract

To understand a neural circuit requires knowledge of its connectivity. Here we report measurements of functional connectivity between the input and ouput layers of the macaque retina at single-cell resolution and the implications of these for colour vision. Multi-electrode technology was used to record simultaneously from complete populations of the retinal ganglion cell types (midget, parasol and small bistratified) that transmit high-resolution visual signals to the brain. Fine-grained visual stimulation was used to identify the location, type and strength of the functional input of each cone photoreceptor to each ganglion cell. The populations of ON and OFF midget and parasol cells each sampled the complete population of long- and middle-wavelength-sensitive cones. However, only OFF midget cells frequently received strong input from short-wavelength-sensitive cones. ON and OFF midget cells showed a small non-random tendency to selectively sample from either long- or middle-wavelength-sensitive cones to a degree not explained by clumping in the cone mosaic. These measurements reveal computations in a neural circuit at the elementary resolution of individual neurons.

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Figure 1: Cell-type classification and receptive fields at single-cone resolution.
Figure 2: Cone-type identification and inputs to RGCs.
Figure 3: Full functional sampling of cone lattice by four RGC types.
Figure 4: Cone-type specificity.

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Acknowledgements

This work was supported by the Helen Hay Whitney Foundation (G.D.F.), German Research Foundation (M.G.), National Institutes of Health (NIH) National Research Service Award (NS054519-01) and Chapman Foundation (J.L.G.), Miller Institute for Basic Research in Science (J.S.), Polish Ministry of Science and Higher Education (W.D.), Burroughs Wellcome Fund Career Award at Scientific Interface (A.S.), Engineering and Physical Sciences Research Council (D.E.G.), Royal Society of Edinburgh (K.M.), McKnight Foundation (A.M.L. and E.J.C.), NSF Grant PHY-0750525 (A.M.L.), a Sloan Research Fellowship and NIH Grant EY13150 (E.J.C). We thank C. K. Hulse for technical assistance; M. I. Grivich, D. Petrusca, 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; S. Barry for machining; F. Rieke and T. Sejnowski for providing comments on the manuscript. We thank the San Diego Supercomputer Center and the National Science Foundation (Cooperative Agreements 05253071 and 0438741) for large-scale data storage.

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G.D.F., J.L.G., A.S. and E.J.C. conceived the experiments. G.D.F., J.L.G., A.S., M.G., J.S., L.H.J. and E.J.C. performed the electrophysiological experiments. G.D.F., J.L.G., A.S., M.G., T.A.M., E.J.C. and L.P. analysed the data. A.S., D.E.G., K.M., W.D. and A.M.L. provided and supported the large-scale multielectrode array system. G.D.F. and E.J.C. wrote the manuscript.

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Correspondence to E. J. Chichilnisky.

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Field, G., Gauthier, J., Sher, A. et al. Functional connectivity in the retina at the resolution of photoreceptors. Nature 467, 673–677 (2010). https://doi.org/10.1038/nature09424

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