Functional Connectivity in the Retina at the Resolution of Photoreceptors

To understand a neural circuit requires knowing the pattern of connectivity between its inputs and outputs. In the retina, this is the pattern of signal flow between the lattice of cone photoreceptors and multiple types of retinal ganglion cells that communicate visual information to the brain. This kind of functional circuitry information has generally been out of reach in the vertebrate nervous system. Here we report measurements of functional connectivity between input and output layers of the retina at single-cell resolution. We employed large-scale multi-electrode recordings to record simultaneously from complete populations of the four major ganglion cell types which collectively mediate high-resolution vision in primates. We then used fine-grained visual stimulation to separately identify the location and spectral type ([L]ong, [M]iddle or [S]hort-wavelength sensitive) of each cone photoreceptor providing input to each ganglion cell. Each of the major ganglion cell populations sampled essentially the complete population of L and M cones, with low redundancy. However, only OFF midget cells strongly sampled from S cones, an unexpected specificity. Using this technique, we have begun to study nonlinear interactions between cone signals in the retinal circuitry.