Functional Architecture of the Photoreceptive Ganglion Cell in Primate Retina: Intrinsic Photosensitivity, S-cone Spectral Opponency and Irradiance Coding

Abstract

Abstract: : Purpose: We sought to determine physiological response properties of melanopsin-immunoreactive ganglion cells in macaque retina (Peterson et al, ARVO 2003) and to test the hypothesis that these cells correspond to irradiance-coding pupillomotor ganglion cells (Gamlin, ARVO 2001) and are intrinsically photosensitive (Berson et al, Science 2002). Methods: Rhodamine-dextran was injected into the Lateral Geniculate Nucleus (LGN) and Pretectal Olivary Nucleus (PON). After appropriate survival, retinas were dissected and maintained in vitro. Retrogradely labeled cells were observed microscopically (Dacey et al, Neuron 2003), and ganglion cells with the morphology of the melanopsin-immunoreactive population were targeted for intracellular recording. L-, M- and S-cone isolating stimuli or sustained luminance steps were used to characterize the light response. To assess intrinsic photosensitivity, L-AP4 and CNQX were bath applied to remove excitatory input to inner retina. After retinal fixation anti-melanopsin immunolabeling further confirmed the identity of recorded cells. Results: Melanopsin-containing ganglion cells showed a sustained ON response to luminance modulation with overall sensitivity and temporal response characteristics of the cone signal pathway. This cell type was irradiance coding with maintained firing rate proportional to light level over a 3-log-unit range. Cone-isolating stimuli also revealed S-cone opponency with ON input from L- and M-cones and OFF input from S-cones. After L-AP4/CNQX blockade of cone input, long duration light steps (10 sec ON, at mid and high photopic levels) elicited a distinctive depolarizing light response with an extremely slow rise time that long outlasted the stimulus. Conclusions: In primate, melanopsin-containing ganglion cells retrogradely labeled from PON and LGN receive a robust sustained cone input, show tonic encoding of irradiance, S-OFF color opponency and intrinsic photosensitivity. The cone and intrinsic response are integrated over much of the photopic range and cone opponency may provide an important chromatic signal to the circadian system.

Keywords: retina: proximal(bipolar, amacrine, and gangli • ganglion cells • retinal connections, networks, circuitry