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B.B. Peterson, H. Liao, D.M. Dacey, K. Yau, P.D. Gamlin, F.R. Robinson, D.W. Marshak; Functional Architecture of the Photoreceptive Ganglion Cell in Primate Retina: Morphology, Mosaic Organization and Central Targets of Melanopsin Immunostained Cells . Invest. Ophthalmol. Vis. Sci. 2003;44(13):5182.
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© ARVO (1962-2015); The Authors (2016-present)
Purpose: Melanopsin is expressed in the human and macaque monkey inner retina (Provencio et al, J Neurosci 2000); in rat retina melanopsin-containing ganglion cells are intrinsically photoreceptive (Hattar et al, Science 2002) and may provide an irradiance signal used by hypothalamic circadian pacemaker (Berson et al, Science 2002). We tested the hypothesis that the human and macaque monkey retina contain an analogous population of melanopsin-containing ganglion cells. Methods: Polyclonal antibodies were generated against an N-terminal amino-acid sequence of human melanopsin and used to immunolabel flat mounts and vertical sections of paraformaldehyde-fixed retina; one macaque retina was further processed for electron microscopy. Central targets were assessed in macaque by colocalizing melanopsin immunoreactivity and retrograde label after central injections of rhodamine dextrans into the Lateral Geniculate Nucleus (LGN) or the Pretectal Olivary Nucleus (PON). Results: Immunostaining revealed the cell bodies and complete dendritic trees of a single population of ~3000 extremely large field, sparsely branching ganglion cells with regular spacing and a shallow density gradient ranging from a peak of 20-25 cells/mm2 around the fovea to 3-5 cells/mm2 in the far periphery; about 60% of the somas were displaced to the amacrine cell layer. A regularly arranged dendritic plexus was localized to two narrow bands that demarcated the extreme outer and inner borders of the inner plexiform layer (IPL), displaced cells stratified in outer IPL, cells in the ganglion-cell layer stratified principally in inner IPL. At the ultrastructural level, immunolabeled dendrites received synaptic input from cone bipolar and amacrine cells. Retrograde labeling from either the LGN or PON was consistently colocalized with melanopsin immunoreactivity in both cell bodies and dendritic trees. Conclusions: A single anatomically distinct population of melanopsin immunoreactive ganglion cells creates an unusual bistratified plexus within the IPL. We hypothesize that the axon of this ganglion cell type is highly collateralized contributing to non-image forming pathways that serve the circadian system and the pupillary light reflex as well as to the retinogeniculate pathway.
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