Melanopsin-expressing ganglion cells in primate retina project to the LGN and signal both color and irradiance

Abstract

Human vision starts with the activation of rod photoreceptors in dim light and of short (S)-, medium (M)-, and long (L)- wavelength-sensitive cone photoreceptors in daylight. Recently, unique photoreceptive ganglion cells were discovered in the retina of nocturnal rodents(1). These cells express the putative photopigment melanopsin and serve subconscious, ‘non-image forming’ functions such as circadian photoentrainment and pupil constriction(1–7). A comparable photodetection pathway in the diurnal human has been hypothesized (8–12). We show here a population of ‘giant’, melanopsin-expressing retinal ganglion cells in primates with unexpected anatomical and functional properties. The giant cells attain a peak density in the parafovea and are retrogradely labelled from tracer injections into the lateral geniculate nucleus (LGN). Physiologically, these cells are strongly activated by rods and all three cone types, and display a rare, S-OFF type of color-opponent receptive field. Together, the intrinsic photoresponse and the rod-cone inputs provide an irradiance signal that spans the full dynamic range of vision and that could reach neocortex via the geniculocortical pathway and contribute to conscious visual perception. Moreover, cone-opponency implies that, in the trichromatic primate, wavelength information is available to the pupillomotor and circadian systems.