Separation of function for classical and ganglion cell photoreceptors with respect to circadian rhythm entrainment and induction of photosomnolence

Neuroscience

Volumn 199, Issue , 2011, Pages 213-224

  Morin, L P ^a,b   Studholme, K M ^a  

^a STONY BROOK UNIVERSITY MEDICAL CENTER   (United States)

^b STONY BROOK UNIVERSITY   (United States)

Author keywords

Circadian; Dark preference; Light aversion; Masking; Melanopsin; Sleep

Indexed keywords

MELANOPSIN;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; DARK ADAPTATION; LIGHT ADAPTATION; LIGHT DARK CYCLE; LOCOMOTION; MALE; MOUSE; NONHUMAN; PHOTOPERIODICITY; PHOTORECEPTOR; PHOTOSOMNOLENCE; PRIORITY JOURNAL; RETINA GANGLION CELL; SLEEP; STIMULUS RESPONSE;

ANIMALS; CIRCADIAN RHYTHM; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR ACTIVITY; PHOTOPERIOD; PHOTORECEPTOR CELLS, VERTEBRATE; RETINAL GANGLION CELLS; ROD OPSINS; SLEEP;

EID: 83055184370     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.09.057     Document Type: Article

References (39)

1. Altimus C.M., Güler A.D., Alam N.M., Arman A.C., Prusky G.T., Sampath A.P., Hattar S. Rod photoreceptors drive circadian photoentrainment across a wide range of light intensities. Nat Neurosci 2010, 13:1107-1112.
2. Altimus C.M., Güler A.D., Villa K.L., McNeill D.S., LeGates T.A., Hattar S. Rods-cones and melanopsin detect light and dark to modulate sleep independent of image formation. Proc Natl Acad Sci U S A 2008, 105:19998-20003.
3. Berson D.M., Dunn F.A., Takao M. Phototransduction by retinal ganglion cells that set the circadian clock. Science 2002, 295:1070-1073.
4. Borbély A.A. Circadian rhythm of vigilance in rats: modulation by short light-dark cycles. Neurosci Lett 1975, 1:67-71.
5. Borbély A.A., Huston J.P., Waser P.G. Control of sleep states in the rat by short light-dark cycles. Brain Res 1975, 95:89-101.
6. Carter-Dawson L.D., LaVail M.M., Sidman R.L. Differential effect of the rd mutation on rods and cones in the mouse retina. Invest Ophthalmol Vis Sci 1978, 17:489-498.
7. Deboer T., Ruijgrok G., Meijer J.H. Short light-dark cycles affect sleep in mice. Eur J Neurosci 2007, 26:3518-3523.
8. Evans J.A., Elliott J.A., Gorman M.R. Circadian effects of light no brighter than moonlight. J Biol Rhythms 2007, 22:356-367.
9. Evans J.A., Elliott J.A., Gorman M.R. Dim nighttime illumination accelerates adjustment to timezone travel in an animal model. Curr Biol 2009, 19:R156-R157.
10. Fisher SP, Godinho SI, Pothecary CA, Hankins MW, Foster RG, Peirson SN (in press) Rapid assessment of sleep/wake behaviour in mice. J Biol Rhythms, in press.
11. Gorman M.R., Kendall M., Elliott J.A. Scotopic illumination enhances entrainment of circadian rhythms to lengthening light:dark cycles. J Biol Rhythms 2005, 20:38-48.
12. Göz D., Studholme K., Lappi D.A., Rollag M.D., Provencio I., Morin L.P. Targeted destruction of photosensitive retinal ganglion cells with a saporin conjugate alters the effects of light on mouse circadian rhythms. PLoS ONE 2008, 3:e3153.
13. Güler A.D., Ecker J.L., Lall G.S., Haq S., Altimus C.M., Liao H.W., Barnard A.R., Cahill H., Badea T.C., Zhao H., Hankins M.W., Berson D.M., Lucas R.J., Yau K.W., Hattar S. Melanopsin cells are the principal conduits for rod-cone input to non-image-forming vision. Nature 2008, 453:102-105.
14. Hatori M., Le H., Vollmers C., Keding S.R., Tanaka N., Schmedt C., Jegla T., Panda S. Inducible ablation of melanopsin-expressing retinal ganglion cells reveals their central role in non-image forming visual responses. PLoS One 2008, 3:e2451.
15. Hattar S., Lucas R.J., Mrosovsky N., Thompson S., Douglas R.H., Hankins M.W., Lem J., Biel M., Hofmann F., Foster R.G., Yau K.W. Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature 2003, 424:76-81.
16. Johnson R.F., Moore R.Y., Morin L.P. Loss of entrainment and anatomical plasticity after lesions of the hamster retinohypothalamic tract. Brain Res 1988, 460:297-313.
17. Lall G.S., Revell V.L., Momiji H., Al Enezi J., Altimus C.M., Güler A.D., Aguilar C., Cameron M.A., Allender S., Hankins M.W., Lucas R.J. Distinct contributions of rod, cone, and melanopsin photoreceptors to encoding irradiance. Neuron 2010, 66:417-428.
18. Lisk R.D. Increased sexual behavior in the male rat following lesions in the mammillary region. J Exp Zool 1966, 161:129-136.
19. Lucas R.J., Hattar S., Takao M., Berson D.M., Foster R.G., Yau K.W. Diminished pupillary light reflex at high irradiances in melanopsin-knockout mice. Science 2003, 299:245-247.
20. Lupi D., Oster H., Thompson S., Foster R.G. The acute light-induction of sleep is mediated by OPN4-based photoreception. Nat Neurosci 2008, 11:1068-1073.
21. Morin L.P., Blanchard J.H., Provencio I. Retinal ganglion cell projections to the hamster suprachiasmatic nucleus, intergeniculate leaflet and visual midbrain: bifurcation and melanopsin immunoreactivity. J Comp Neurol 2003, 465:401-416.
22. Morin L.P., Lituma P.J., Studholme K.M. Two components of nocturnal locomotor suppression by light. J Biol Rhythms 2010, 25:197-207.
23. Morin L.P., Studholme K.M. Millisecond light pulses make mice stop running, then display prolonged sleep-like behavior in the absence of light. J Biol Rhythms 2009, 24:497-508.
24. Mrosovsky N., Foster R.G., Salmon P.A. Thresholds for masking responses to light in three strains of retinally degenerate mice. J Comp Physiol A: Sens Neural Behav Physiol 1999, 184:423-428.
25. Mrosovsky N., Hampton R.R. Spatial responses to light in mice with severe retinal degeneration. Neurosci Lett 1997, 222:204-206.
26. Mrosovsky N., Hattar S. Impaired masking responses to light in melanopsin-knockout mice. Chronobiol Int 2003, 20:989-999.
27. Naarendorp F., Esdaille T.M., Banden S.M., Andrews-Labenski J., Gross O.P., Pugh E.N. Dark light, rod saturation, and the absolute and incremental sensitivity of mouse cone vision. J Neurosci 2010, 30:12495-12507.
28. Pack A.I., Galante R.J., Maislin G., Cater J., Metaxas D., Lu S., Zhang L., Von Smith R., Kay T., Lian J., Svenson K., Peters L.L. Novel method for high-throughput phenotyping of sleep in mice. Physiol Genomics 2007, 28:232-238.
29. Panda S., Provencio I., Tu D.C., Pires S.S., Rollag M.D., Castrucci A.M., Pletcher M.T., Sato T.K., Wiltshire T., Andahazy M., Kay S.A., Van Gelder R.N., Hogenesch J.B. Melanopsin is required for non-image-forming photic responses in blind mice. Science 2003, 301:525-527.
30. Panda S., Sato T.K., Castrucci A.M., Rollag M.D., DeGrip W.J., Hogenesch J.B., Provencio I., Kay S.A. Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science 2002, 298:2213-2216.
31. Roberts M.R., Hendrickson A., McGuire C.R., Reh T.A. Retinoid X receptor (gamma) is necessary to establish the S-opsin gradient in cone photoreceptors of the developing mouse retina. Invest Ophthalmol Vis Sci 2005, 46:2897-2904.
32. Ruby N.F., Brennan T.J., Xie X., Cao V., Franken P., Heller H.C., O'Hara B.F. Role of melanopsin in circadian responses to light. Science 2002, 298:2211-2213.
33. Salam J.N., Fox J.H., Detroy E.M., Guignon M.H., Wohl D.F., Falls W.A. Voluntary exercise in C57 mice is anxiolytic across several measures of anxiety. Behav Brain Res 2009, 197:31-40.
34. Sherry D.M., Wang M.M., Bates J., Frishman L.J. Expression of vesicular glutamate transporter 1 in the mouse retina reveals temporal ordering in development of rod vs. cone and ON vs. OFF circuits. J Comp Neurol 2003, 465:480-498.
35. Thompson S., Foster R.G., Stone E.M., Sheffield V.C., Mrosovsky N. Classical and melanopsin photoreception in irradiance detection: negative masking of locomotor activity by light. Eur J Neurosci 2008, 27:1973-1979.
36. Thompson S., Recober A., Vogel T.W., Kuburas A., Owens J.A., Sheffield V.C., Russo A.F., Stone E.M. Light aversion in mice depends on nonimage-forming irradiance detection. Behav Neurosci 2010, 124:821-827.
37. Tsai J.W., Hannibal J., Hagiwara G., Colas D., Ruppert E., Ruby N.F., Heller H.C., Franken P., Bourgin P. Melanopsin as a sleep modulator: circadian gating of the direct effects of light on sleep and altered sleep homeostasis in Opn4(-/-) mice. PLoS Biol 2009, 7:e1000125.
38. Vidal L., Morin L.P. Absence of normal photic integration in the circadian visual system: response to millisecond light flashes. J Neurosci 2007, 27:3375-3382.
39. Warthen D.M., Wiltgen B.J., Provencio I. Light enhances learned fear. Proc Natl Acad Sci U S A 2011, 108:13788-13793.