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Tiffany Schmidt, Nazia Alam, Shan Chen, Paulo Kofuji, Wei Li, Glen Prusky, Samer Hattar; Role for melanopsin in alpha retinal ganglion cell physiology and contrast detection. Invest. Ophthalmol. Vis. Sci. 2013;54(15):307.
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© ARVO (1962-2015); The Authors (2016-present)
Distinct populations of retinal ganglion cells (RGCs) drive image forming and non-image forming vision. Intrinsically photosensitive (ip)RGCs express the photopigment melanopsin and drive non-image forming functions such as circadian photoentrainment and the pupillary light reflex. Ablation of ipRGCs results in loss of non-image forming behaviors, but intact rod/cone dependent image forming vision. These findings have led to the conclusion that ipRGCs mediate non-image forming vision, while conventional RGCs mediate image formation via the relay of rod/cone signals.
We performed immunohistochemistry, electrophysiology, and spatial frequency and contrast measures of optokinetic tracking behavior in various mouse models lacking melanopsin or specific ipRGC subtypes.
Despite the prevailing view that rod/cone signals through conventional RGCs mediate image forming vision and rod/cone/melanopsin signals through ipRGCs mediate non-image-forming vision, we found that a conventional RGC type, the ON alpha RGC, is intrinsically photosensitive and that melanopsin phototransduction underlies this response. We also find that melanopsin plays a physiological role in the light-evoked signaling of ON alpha RGCs, allowing these cells to signal both prior lighting history and changes in environmental luminance over long periods. These properties are dependent upon melanopsin phototransduction because in the absence of the melanopsin protein ON alpha RGCs lose their ability to encode lighting history and environmental luminance. Consistent with the high contrast sensitivity of alpha RGCs, mice lacking melanopsin have a clear deficit in visual contrast sensitivity, demonstrating that melanopsin plays an unexpected role in contrast detection. Furthermore, animals lacking non-M1 ipRGCs, including ON alpha cells, show further reduction in contrast sensitivity. These phenomena may be a general property of the mammalian visual system, because the ON alpha-like RGCs of the cone-dominated retina of the ground squirrel are also intrinsically photosensitive.
These surprising findings indicate that ON alpha RGCs use melanopsin phototransduction and rod/cone signaling to mediate aspects of visual processing. Furthermore, these results identify the first behavioral function for non-M1 ipRGCs, and show that these cells play an important role in contrast detection in the image-forming visual system.
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