Photon capture and signalling by melanopsin retinal ganglion cells

Do, Michael Tri H; Kang, Shin H.; Xue, Tian; Zhong, Haining; Liao, Hsi-Wen Rock; Bergles, Dwight E.; Yau, King-Wai

doi:10.1038/nature07682

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Photon capture and signalling by melanopsin retinal ganglion cells

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Author(s): Michael Tri H. Do ¹ ^, ³ , Shin H. Kang ¹ , Tian Xue ¹ ^, ³ , Haining Zhong ¹ , Hsi-Wen Liao ¹ , Dwight E. Bergles ¹ , King-Wai Yau ¹ ^, ² ^, ³

Publication date (Electronic): 31 December 2008

Journal: Nature

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Abstract

A subset of retinal ganglion cells has recently been discovered to be intrinsically photosensitive, with melanopsin as the pigment. These cells project primarily to brain centers for non-image-forming visual functions such as the pupillary light reflex and circadian photoentrainment. How well they signal intrinsic light absorption to drive behavior remains unclear. Here we report fundamental parameters governing their intrinsic light responses and associated spike generation. The membrane density of melanopsin is 10 ⁴-fold lower than that of rod and cone pigments, resulting in a very low photon-catch and a phototransducing role only in relatively bright light. Nonetheless, each captured photon elicits a large and extraordinarily prolonged response, with a unique shape among known photoreceptors. Remarkably, like rods, these cells are capable of signalling single-photon absorption. A flash causing a few hundred isomerized melanopsin molecules in a retina is sufficient for reaching threshold for the pupillary light reflex.

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Most cited references 47

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

Dennis M Dacey, Hsi-Wen Liao, Beth B Peterson … (2005)

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.

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Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice.

S. Hattar, R. J. Lucas, N Mrosovsky … (2003)

In the mammalian retina, besides the conventional rod-cone system, a melanopsin-associated photoreceptive system exists that conveys photic information for accessory visual functions such as pupillary light reflex and circadian photo-entrainment. On ablation of the melanopsin gene, retinal ganglion cells that normally express melanopsin are no longer intrinsically photosensitive. Furthermore, pupil reflex, light-induced phase delays of the circadian clock and period lengthening of the circadian rhythm in constant light are all partially impaired. Here, we investigated whether additional photoreceptive systems participate in these responses. Using mice lacking rods and cones, we measured the action spectrum for phase-shifting the circadian rhythm of locomotor behaviour. This spectrum matches that for the pupillary light reflex in mice of the same genotype, and that for the intrinsic photosensitivity of the melanopsin-expressing retinal ganglion cells. We have also generated mice lacking melanopsin coupled with disabled rod and cone phototransduction mechanisms. These animals have an intact retina but fail to show any significant pupil reflex, to entrain to light/dark cycles, and to show any masking response to light. Thus, the rod-cone and melanopsin systems together seem to provide all of the photic input for these accessory visual functions.

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Diminished pupillary light reflex at high irradiances in melanopsin-knockout mice.

R. J. Lucas, S. Hattar, M Takao … (2003)

In the mammalian retina, a small subset of retinal ganglion cells (RGCs) are intrinsically photosensitive, express the opsin-like protein melanopsin, and project to brain nuclei involved in non-image-forming visual functions such as pupillary light reflex and circadian photoentrainment. We report that in mice with the melanopsin gene ablated, RGCs retrograde-labeled from the suprachiasmatic nuclei were no longer intrinsically photosensitive, although their number, morphology, and projections were unchanged. These animals showed a pupillary light reflex indistinguishable from that of the wild type at low irradiances, but at high irradiances the reflex was incomplete, a pattern that suggests that the melanopsin-associated system and the classical rod/cone system are complementary in function.

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Author and article information

Journal

Journal ID (nlm-journal-id): 0410462

Journal ID (pubmed-jr-id): 6011

Journal ID (nlm-ta): Nature

Title: Nature

ISSN (Print): 0028-0836

ISSN (Electronic): 1476-4687

Publication date Nihms-submitted: 27 March 2009

Publication date (Electronic): 31 December 2008

Publication date (Print): 15 January 2009

Publication date PMC-release: 15 December 2009

Volume: 457

Issue: 7227

Pages: 281-287

Affiliations

[1 ] Solomon H. Snyder Department of Neuroscience, The Johns Hopkins University School of Medicine, Baltimore, Maryland 21205, USA

[2 ] Department of Ophthalmology, The Johns Hopkins University School of Medicine, Baltimore, Maryland 21205, USA

[3 ] Center for Sensory Biology, The Johns Hopkins University School of Medicine, Baltimore, Maryland 21205, USA

Author notes

Correspondence and requests for materials should be addressed to Michael Tri H. Do ( mdo@ 123456jhmi.edu ) or King-Wai Yau ( kwyau@ 123456mail.jhmi.edu )

[4]

Present address: Janelia Farm Research Campus, HHMI, Ashburn, VA 20147, USA

[5]

Present address: Department of Neurobiology, Children’s Hospital Boston, Harvard Medical School, Boston, MA 02115, USA

Article

Manuscript ID: nihpa102688

DOI: 10.1038/nature07682

PMC ID: 2794210

PubMed ID: 19118382

SO-VID: f52147a7-0dde-4165-be99-20d9a2ebb8ea