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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 rodents1. 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 constriction1,2,3,4,5,6,7. 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.

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Figure 1: Morphology of melanopsin-immunoreactive cells.
Figure 2: Retrograde tracer labelling from LGN and pretectum colocalize with melanopsin immunostain.
Figure 3: Giant cells show rod and colour-opponent inputs and are inherently photoreceptive.
Figure 4: Spectral sensitivity of the giant cell's inherent light response.
Figure 5: Irradiance coding and visual sensitivity range for the giant cell.

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Acknowledgements

We woud like to thank C. Curcio and the Age-Related Maculopathy Histopathology Laboratory (supported by the International Retinal Research Foundation, the National Eye Institute and the Vision Science Research Center), 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. We thank O. Packer and T. Haun for technical assistance. Supported by US National Eye Institute grants to D.M.D., J.P., K.-W.Y., H.W.-L. and F.R.R., Vision Research Center Core grants to D.M.D. and P.D.G., an Alabama EyeSight Foundation award to P.D.G. and a Retina Research Foundation Paul Kayser Award to D.M.D.

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Correspondence to Dennis M. Dacey.

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Dacey, D., Liao, HW., Peterson, B. et al. Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. Nature 433, 749–754 (2005). https://doi.org/10.1038/nature03387

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