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.

Footnotes

 We'd like to thank Dr. Christine Curcio and the Age-Related Maculopathy Histopathology Laboratory (supported by the International Retinal Research Foundation, the National Eye Institute (EY06109)), and the Vision Science Research Center (P30EY03039), University of Alabama at Birmingham for the human retinae used in the immunohistochemical studies. Macaque retinae were provided by the Tissue Distribution program of the National Primate Research Center at the University of Washington (Core RR00166). We thank Orin Packer and Toni Haun for technical assistance. Supported by U.S. National Eye Institute grants EY06678 and EY09625 (DMD), EY00901 (JP), EY06837 and EY14596 (K-WY, H-WL), EY10578 (FRR) and Vision Core EY01730 (DMD), EY09380 (PDG) and the Retina Research Foundation Paul Kayser Award (DMD).