Rods-cones and melanopsin detect light and dark to modulate sleep independent of image formation

被引:211
作者
Altimus, C. M. [1 ]
Guler, A. D. [1 ]
Villa, K. L. [1 ]
McNeill, D. S. [1 ]
LeGates, T. A. [1 ]
Hattar, S. [1 ]
机构
[1] Johns Hopkins Univ, Dept Biol, Baltimore, MD 21218 USA
关键词
circadian photo-entrainment; intrinsically photosensitive retinal ganglion cell; masking; photoreceptor and opsin;
D O I
10.1073/pnas.0808312105
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Light detected in the retina modulates several physiological processes including circadian photo-entrainment and pupillary light reflex. Intrinsically photosensitive retinal ganglion cells (ipRGCs) convey rod-cone and melanopsin-driven light input to the brain. Using EEGs and electromyograms, we show that acute light induces sleep in mice during their nocturnal active phase whereas acute dark awakens mice during their diurnal sleep phase. We used retinal mutant mouse lines that lack (i) the ipRGCs, (ii) the phototransduction pathways of rods and cones, or (iii) the melanopsin protein and showed that the influence of light and dark on sleep requires both rod-cone and melanopsin signaling through ipRGCs and is independent of image formation. We further show that, although acute light pulses overcome circadian and homeostatic drives for sleep, upon repeated light exposures using a 3.5 h/3.5 h light/dark cycle, the circadian and homeostatic drives override the light input. Thus, in addition to their known role in aligning circadian physiology with day and night, ipRGCs also relay light and dark information from both rod-cone and melanopsin-based pathways to modulate sleep and wakefulness.
引用
收藏
页码:19998 / 20003
页数:6
相关论文
共 27 条
[1]   Melanopsin retinal ganglion cells receive bipolar and amacrine cell synapses [J].
Belenky, MA ;
Smeraski, CA ;
Provencio, I ;
Sollars, PJ ;
Pickard, GE .
JOURNAL OF COMPARATIVE NEUROLOGY, 2003, 460 (03) :380-393
[2]   Effects of lighting conditions on sleep and wakefulness in albino Lewis and pigmented brown Norway rats [J].
Benca, RM ;
Gilliland, MA ;
Obermeyer, WH .
SLEEP, 1998, 21 (05) :451-460
[3]  
Borbely A A, 1982, Hum Neurobiol, V1, P195
[4]   BRIGHT LIGHT INDUCTION OF STRONG (TYPE-0) RESETTING OF THE HUMAN CIRCADIAN PACEMAKER [J].
CZEISLER, CA ;
KRONAUER, RE ;
ALLAN, JS ;
DUFFY, JF ;
JEWETT, ME ;
BROWN, EN ;
RONDA, JM .
SCIENCE, 1989, 244 (4910) :1328-1333
[5]   PARADOXICAL TIMING OF THE CIRCADIAN-RHYTHM OF SLEEP PROPENSITY SERVES TO CONSOLIDATE SLEEP AND WAKEFULNESS IN HUMANS [J].
DIJK, DJ ;
CZEISLER, CA .
NEUROSCIENCE LETTERS, 1994, 166 (01) :63-68
[6]   Modeling the role of mid-wavelength cones in circadian responses to light [J].
Dkhissi-Benyahya, Ouria ;
Gronfier, Claude ;
De Vanssay, Wena ;
Flamant, Frederic ;
Cooper, Howard M. .
NEURON, 2007, 53 (05) :677-687
[7]   Retinal pathways influence temporal niche [J].
Doyle, Susan E. ;
Yoshikawa, Tolmoko ;
Hillson, Holly ;
Menaker, Michael .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2008, 105 (35) :13133-13138
[8]  
Franken P, 1999, SLEEP, V22, P155
[9]   Regulation of mammalian circadian behavior by non-rod, non-cone, ocular photoreceptors [J].
Freedman, MS ;
Lucas, RJ ;
Soni, B ;
von Schantz, M ;
Muñoz, M ;
David-Gray, Z ;
Foster, R .
SCIENCE, 1999, 284 (5413) :502-504
[10]   Broad role for melanopsin in nonvisual photoreception [J].
Gooley, JJ ;
Lu, J ;
Fischer, D ;
Saper, CB .
JOURNAL OF NEUROSCIENCE, 2003, 23 (18) :7093-7106