To understand a neural circuit requires knowing its connectivity. This paper reports measurements of functional connectivity between the input and ouput layers of the retina at single cell resolution and its implications for color vision. Multi-electrode technology was employed to record simultaneously from complete populations of the retinal ganglion cell types (midget, parasol, 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 exhibited 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.Color vision requires neural circuitry to compare signals from spectrally distinct cone types. For example, the signature of primate color vision -red-green and blue-yellow color opponency -implies that neural circuits pit signals from different cone types against one another. However, the pattern of connectivity between the (L)ong, (M)iddle, and (S)hort Users may view, print, copy, download and text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use: http://www.nature.com/authors/editorial_policies/license.html#terms Contact: E.J. Chichilnisky, Systems Neurobiology, The Salk Institute, 10010 North Torrey Pines Road, La Jolla, CA 92037, USA. ej@salk.edu, phone: (858) 453-4100 x1286. * Equal contributionsAuthor Contributions: 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., and E.J.C. performed the electrophysiological experiments. G.D.F, J.L.G., A.S., M.G., T.A.M., and L.P., analyzed the data. A.S., D.E.G., K.M., W.D., A.M.L. provided and supported the large-scale multielectrode array system. G.D.F. and E.J.C. wrote the manuscript. To resolve the fine structure of RFs, stimuli with 10-fold smaller pixels (5×5 μm) were used. At this resolution, RFs did not conform to the smooth Gaussian approximation used in Fig. 1a (center) and in previous studies 18 . Instead, each RF was composed of punctate islands of light sensitivity (Fig. 1a, flanking). The separation between islands was roughly equal to the spacing of the cone lattice, consistent with the idea that each island reflected the contribution of a single cone 10 , 19 . To test this hypothesis, locations of islands were compared to photographs of cone outer segments labeled with peanut agglutinin; a close alignment was observed (Fig. 1b, see Supplementary Methods). HHS Public AccessTh...

Electrical stimulation of retinal neurons with an advanced retinal prosthesis may eventually provide high-resolution artificial vision to the blind. However, the success of future prostheses depends on the ability to activate the major parallel visual pathways of the human visual system. Electrical stimulation of the five numerically dominant retinal ganglion cell types was investigated by simultaneous stimulation and recording in isolated peripheral primate (Macaca sp.) retina using multi-electrode arrays. ON and OFF midget, ON and OFF parasol, and small bistratified ganglion cells could all be activated directly to fire a single spike with submillisecond latency using brief pulses of current within established safety limits. Thresholds for electrical stimulation were similar in all five cell types. In many cases, a single cell could be specifically activated without activating neighboring cells of the same type or other types. These findings support the feasibility of direct electrical stimulation of the major visual pathways at or near their native spatial and temporal resolution.

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.

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