Functional Identification of Individual Cones in the Receptive Fields of Primate Retinal Ganglion Cells

Abstract

Purpose: : Characterize the spatial sampling of individual photoreceptor inputs by complete populations of parasol and midget ganglion cells in peripheral primate retina.

Methods: : We used a combination of (1) large scale recording of retinal ganglion cell (RGC) activity in the peripheral macaque retina in vitro (5-8 mm eccentricity), using 512-electrode arrays with 60 and 30 micron inter-electrode spacing; (2) a fine-grained white noise visual stimulus in which each stimulus pixel usually stimulated only one cone; (3) fluorescence imaging of cone photoreceptor outer segments after recording.

Results: : Reverse correlation of the stimulus with the RGC spike train produced a spatiotemporal map of light sensitivity within the receptive field of each recorded RGC. Receptive fields exhibited punctate islands of light sensitivity separated by regions of little or no light sensitivity. Alignment of anatomical images of cone outer segments with receptive fields revealed that the punctate sensitivity represented the inputs of individual cones to the RGC receptive field. Full mosaics of cone photoreceptors over the area of the microelectrode array were identified by combining information from the hundreds of midget and parasol cells detected simultaneously in each recording. This allowed us to measure connectivity of individual cones to receptive field center and surround of both midget and parasol cells. Each RGC sampled approximately all of the cones within the spatial extent of its receptive field. Midget RGCs received signals from ~6 times fewer cones than parasol RGCs. For both midget and parasol populations, neighboring cells in the mosaic shared a small number of inputs from the same cones. Individual S cones, easily identified by their maximal sensitivity to modulation of the blue display primary, provided clear input to OFF-midget cells but were rarely sampled by ON-midget and ON- and OFF-parasol cells.

Conclusions: : The mosaic of cones is sampled nearly completely and with minimal overlap by mosaics of midget and parasol RGCs.[A.S., J.L.G., G.D.F. contributed equally]

Keywords: ganglion cells • receptive fields • color vision