Ultraviolet Light Provides a Major Input to Non-Image-Forming Light Detection in Mice

Abstract

The change in irradiance at dawn and dusk provides the primary cue for the entrainment of the mammalian circadian pacemaker. Irradiance detection has been ascribed largely to melanopsin-based phototransduction [1Berson D.M. Dunn F.A. Takao M. Phototransduction by retinal ganglion cells that set the circadian clock.Science. 2002; 295: 1070-1073Crossref PubMed Scopus (2542) Google Scholar, 2Brown T.M. Wynne J. Piggins H.D. Lucas R.J. Multiple hypothalamic cell populations encoding distinct visual information.J. Physiol. 2011; 589: 1173-1194Crossref PubMed Scopus (77) Google Scholar, 3Drouyer E. Rieux C. Hut R.A. Cooper H.M. Responses of suprachiasmatic nucleus neurons to light and dark adaptation: relative contributions of melanopsin and rod-cone inputs.J. Neurosci. 2007; 27: 9623-9631Crossref PubMed Scopus (62) Google Scholar, 4Gooley J.J. Rajaratnam S.M. Brainard G.C. Kronauer R.E. Czeisler C.A. Lockley S.W. Spectral responses of the human circadian system depend on the irradiance and duration of exposure to light.Sci. Transl. Med. 2010; 2: 31ra33Crossref PubMed Scopus (289) Google Scholar, 5Mure L.S. Rieux C. Hattar S. Cooper H.M. Melanopsin-dependent nonvisual responses: evidence for photopigment bistability in vivo.J. Biol. Rhythms. 2007; 22: 411-424Crossref PubMed Scopus (131) Google Scholar]. Here we examine the role of ultraviolet-sensitive (UVS) cones in the modulation of circadian behavior, sleep, and suprachiasmatic nucleus (SCN) electrical activity. UV light exposure leads to phase-shifting responses comparable to those of white light. Moreover, UV light exposure induces sleep in wild-type and melanopsin-deficient (Opn4−/−) mice with equal efficacy. Electrical recordings from the SCN of wild-type mice show that UV light elicits irradiance-dependent sustained responses that are similar to those induced by white light, with characteristic fast transient components occurring at the light transitions. These responses are retained in Opn4−/− mice and preserved under saturating photopic conditions. The sensitivity of phase-shifting responses to UV light is unaffected by the loss of rods but is severely attenuated by the additional loss of cones. Our data show that UVS cones play an important role in circadian and sleep regulation in mice.