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

Abstract

Human vision starts with the activation of rod photoreceptors in dim light and short (S)-, medium (M)-, and long (L)- wavelength-sensitive cone photoreceptors in daylight. Recently a parallel, non-rod, non-cone photoreceptive pathway, arising from a population of retinal ganglion cells, was discovered in nocturnal rodents. These ganglion cells express the putative photopigment melanopsin and by signalling gross changes in light intensity serve the subconscious, 'non-image-forming' functions of circadian photoentrainment and pupil constriction. Here we show an anatomically distinct population of 'giant', melanopsin-expressing ganglion cells in the primate retina that, in addition to being intrinsically photosensitive, are strongly activated by rods and cones, and display a rare, S-Off, (L + M)-On type of colour-opponent receptive field. The intrinsic, rod and (L + M) cone-derived light responses combine in these giant cells to signal irradiance over the full dynamic range of human vision. In accordance with cone-based colour opponency, the giant cells project to the lateral geniculate nucleus, the thalamic relay to primary visual cortex. Thus, in the diurnal trichromatic primate, 'non-image-forming' and conventional 'image-forming' retinal pathways are merged, and the melanopsin-based signal might contribute to conscious visual perception.

Circadian regulation of lipid metabolism

“…Photic entrainment of circadian rhythms is mediated by a direct retinohypothalamic projection to the SCN that originates from intrinsically photosensitive retinal ganglion cells. The intrinsically photosensitive retinal ganglion cells contain the photopigment melanopsin (7)(8)(9) , which is most sensitive to short-wavelength blue light, but also receive input from rods and cones (7,10) . Hence, both visual photoreceptors and melanopsin cells likely contribute to photic circadian entrainment of rest-activity and feeding cycles.…”

Identification and Characterization of a Y-Like Primate Retinal Ganglion Cell Type

“…Because of recent observations indicating that some large-field ganglion cells possess selective connectivity to S-cones (Dacey and Packer, 2003;Dacey et al, , 2005Dacey, 2004), we investigated the S-cone input to the upsilon cells by using the cone-isolating S/(L ϩ M) stimulus (see Materials and Methods). The response of the upsilon cells to this stimulus was dominated by the (L ϩ M)-cone OFF component, as shown in Figure 4.…”

“…Although decades of work have been devoted to the study of primate retinal architecture, fewer than one-half of the 22 or more anatomically identified types of retinal ganglion cells (RGCs) (Rodieck and Watanabe, 1993;Dacey et al, , 2005Dacey, 2004;Yamada et al, 2005) have been characterized physiologically, namely the ON and OFF midget and parasol cells (Dacey, 1999;Chichilnisky and Kalmar, 2002), the small bistratified cells (Dacey and Lee, 1994;Chichilnisky and Baylor, 1999), the recently discovered giant sparse (melanopsin-expressing) cells (Dacey et al, , 2005Dacey, 2004), and, to some extent, the large bistratified cells and the cells of type "sparse" Dacey, 2004). One of the possible reasons for this discrepancy is that the morphological RGC types awaiting physiological characterization constitute only a small fraction of all the primate ganglion cells (1-4%) [see Dacey (2004), their table 20.1].…”

Stratification of alpha ganglion cells and ON/OFF directionally selective ganglion cells in the rabbit retina

“…This may boost the total number of types to between 15 and 20. For example, the melanopsin ganglion cell is a distinct type which only accounts for a small fraction, 0.2%, of primate ganglion cells (Dacey et al, 2005). If an assumption is made that each ganglion cell type represents an independent channel in the visual system, this may reflect the total number of layers in the IPL.…”