Central projections of melanopsin-expressing retinal ganglion cells in the mouse

Journal of Comparative Neurology

Volumn 497, Issue 3, 2006, Pages 326-349

  Hattar, Samer ^a,c   Kumar, Monica ^b   Park, Alexander ^a   Tong, Patrick ^a   Tung, Jonathan ^b   Yau, King Wai ^a   Berson, David M ^b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BROWN UNIVERSITY   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Circadian; Melanopsin; Pretectum; Pupil; Retinal ganglion cell; Retinofugal; Retinohypothalamic tract; Superior colliculus; Suprachiasmatic nucleus

Indexed keywords

BETA GALACTOSIDASE; CHOLERA TOXIN B SUBUNIT; MELANOPSIN;

ADOLESCENT; AMYGDALOID NUCLEUS; ANIMAL TISSUE; ARTICLE; BRAIN NUCLEUS; BRAIN REGION; CELL SYNCHRONIZATION; CENTRAL NERVOUS SYSTEM; CIRCADIAN RHYTHM; ENUCLEATION; FEMALE; GENE; GENE LOCUS; GENE TARGETING; GENICULATE BODY; HABENULA; HISTOCHEMISTRY; HYPOTHALAMUS; IMMUNOFLUORESCENCE; INTERGENICULATE LEAFLET; LACZ GENE; LATERAL GENICULATE BODY; LATERAL GENICULATE NUCLEUS; LIGHT; MALE; MOUSE; NERVE PROJECTION; NERVE TRACT; NONHUMAN; OLIVARY NUCLEUS; OPTIC NERVE; PERIAQUEDUCTAL GRAY MATTER; PERISUPRAOPTIC NUCLEUS; PHOTIC SYNCHRONIZATION; PHOTORECEPTOR; POSTERIOR LIMITANS NUCLEUS; PREOPTIC AREA; PRETECTUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUPIL REFLEX; RETINA GANGLION CELL; RETINOFUGAL TRACT; RETINOHYPOTHALAMIC TRACT; SUBPARAVENTRICULAR ZONE; SUPERIOR COLLICULUS; SUPRACHIASMATIC NUCLEUS; SUPRAOPTIC NUCLEUS; TAU GENE; THALAMUS LATERAL NUCLEUS;

ANIMALS; BETA-GALACTOSIDASE; BIOLOGICAL MARKERS; EYE ENUCLEATION; FEMALE; FUNCTIONAL LATERALITY; MALE; MICE; MICE, KNOCKOUT; OPSIN; PHOTORECEPTORS; PHOTOTRANSDUCTION; RETINAL GANGLION CELLS; STAINING AND LABELING; VISUAL PATHWAYS;

EID: 31144447212     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.20970     Document Type: Article

References (110)

1. Abrahamson EE, Moore RY. 2001. Suprachiasmatic nucleus in the mouse: retinal innervation, intrinsic organization and efferent projections. Brain Res 916:172-191.
2. Aggelopoulos NC, Meissl H. 2000. Responses of neurones of the rat suprachiasmatic nucleus to retinal illumination under photopic and scotopic conditions. J Physiol (Lond) 523:211-222.
3. Alvarez-Lopez C, Cernuda-Cernuda R, Paniagua MA, Alvarez-Viejo M, Fernandez-Lopez A, Garcia-Fernandez JM. 2004. The transcription factor CREB is phosphorylated in neurons of the piriform cortex of blind mice in response to illumination of the retina. Neurosci Lett 357:223-226.
4. Barash S, Melikyan A, Sivakov A, Tauber M. 1998. Shift of visual fixation dependent on background illumination. J Neurophysiol 79:2766-2781.
5. Belenky MA, Smeraski CA, Provencio I, Sollars PJ, Pickard GE. 2003. Melanopsin retinal ganglion cells receive bipolar and amacrine cell synapses. J Comp Neurol 460:380-393.
6. Berson DM. 2003. Strange vision: ganglion cells as circadian photoreceptors. Trends Neurosci 26:314-320.
7. Berson DM, Dunn FA, Takao M. 2002. Phototransduction by retinal ganglion cells that set the circadian clock. Science 295:1070-1073.
8. Cassone VM, Speh JC, Card JP, Moore RY. 1988. Comparative anatomy of the mammalian hypothalamic suprachiasmatic nucleus. J Biol Rhythms 3:71-91.
9. Castel M, Belenky M, Cohen S, Ottersen OP, Storm-Mathisen J. 1993. Glutamate-like immunoreactivity in retinal terminals of the mouse suprachiasmatic nucleus. Eur J Neurosci 5:368-381.
10. Chaurasia SS, Rollag MD, Jiang G, Hayes WP, Haque R, Natesan A, Zatz M, Tosini G, Liu C, Korf HW, Iuvone PM, Provencio I. 2005. Molecular cloning, localization and circadian expression of chicken melanopsin (Opn4): differential regulation of expression in pineal and retinal cell types. J Neurochem 92:158-170.
11. Clarke RJ, Ikeda H. 1985. Luminance and darkness detectors in the olivary and posterior pretectal nuclei and their relationship to the pupillary light reflex in the rat. I. Studies with steady luminance levels. Exp Brain Res 57:224-232.
12. Cooper HM, Herbin M, Nevo E. 1993. Visual system of a naturally microphthalmic mammal: the blind mole rat, Spalax ehrenbergi. J Comp Neurol 328:313-350.
13. Cooper HM, Parvopassu F, Herbin M, Magnin M. 1994. Neuroanatomical pathways linking vision and olfaction in mammals. Psychoneuroendocrinology 19:623-639.
14. Cui LN, Jolley CJ, Dyball RE. 1997a. Electrophysiological evidence for retinal projections to the hypothalamic supraoptic nucleus and its perinuclear zone. J Neuroendocrinol 9:347-353.
15. Cui LN, Saeb-Parsy K, Dyball RE. 1997b. Neurones in the supraoptic nucleus of the rat are regulated by a projection from the suprachiasmatic nucleus. J Physiol 502:149-159.
16. Czeisler CA, Shanahan TL, Herman EB, Martens H, Brotman DJ, Emens JS, Klein T, Rizzo JFd. 1995. Suppression of melatonin secretion in some blind patients by exposure to bright light [see comments]. N Engl J Med 332:6-11.
17. Dacey DM, Liao HW, Peterson BB, Robinson FR, Smith VC, Pokorny J, Yau KW, Gamlin PD. 2005. Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. Nature 433:749-754.
18. Drager UC, Hubel DH. 1976. Topography of visual and somatosensory projections to mouse superior colliculus. J Neurophysiol 39:91-101.
19. Drager UC, Olsen JF. 1980. Origins of crossed and uncrossed retinal projections in pigmented and albino mice. J Comp Neurol 191:383-412.
20. Drivenes O, Soviknes AM, Ebbesson LO, Fjose A, Seo HC, Helvik JV. 2003. Isolation and characterization of two teleost melanopsin genes and their differential expression within the inner retina and brain. J Comp Neurol 456:84-93.
21. Dunn FA, Berson DM. 2002. Are intrinsically photosensitive retinal ganglion cells influenced by rods or cones? Abstract #2982, Association for Research in Vision and Ophthalmology, Ft. Lauderdale, FL; May 8, 2002.
22. Elliott AS, Weiss ML, Nunez AA. 1995. Direct retinal communication with the peri-amygdaloid area. Neuroreport 6:806-808.
23. Fite KV, Janusonis S, Foote W, Bengston L. 1999. Retinal afferents to the dorsal raphe nucleus in rats and Mongolian gerbils. J Comp Neurol 414:469-484.
24. Frost DO, Edwards MA, Sachs GM, Caviness VS, Jr. 1986. Retinotectal projection in reeler mutant mice: relationships among axon trajectories, arborization patterns and cytoarchitecture. Brain Res 393:109-120.
25. Fu Y, Zhong H, Wang MH, Luo D-G, Liao H-W, Maeda H, Hattar S, Frishman LJ, Yau K-W. 2005. Intrinsically photosensitive retinal ganglion cells detect light with a vitamin A-based photopigment, melanopsin. Proc Natl Acad Sci U S A 102:10339-10344.
26. Godement P, Salaun J, Imbert M. 1984. Prenatal and postnatal development of retinogeniculate and retinocollicular projections in the mouse. J Comp Neurol 230:552-575.
27. Gooley JJ, Lu J, Chou TC, Scammell TE, Saper CB. 2001. Melanopsin in cells of origin of the retinohypothalamic tract. Nat Neurosci 4:1165.
28. Gooley JJ, Lu J, Fischer D, Saper CB. 2003. A broad role for melanopsin in nonvisual photoreception. J Neurosci 23:7093-7106.
29. Hannibal J, Fahrenkrug J. 2004. Target areas innervated by PACAP-immunoreactive retinal ganglion cells. Cell Tissue Res 316:99-113.
30. Hannibal J, Hindersson P, Knudsen SM, Georg B, Fahrenkrug J. 2002. The photopigment melanopsin is exclusively present in pituitary adenylate cyclase-activating polypeptide-containing retinal ganglion cells of the retinohypothalamic tract. J Neurosci 22:RC191.
31. Hannibal J, Hindersson P, Ostergaard J, Georg B, Heegaard S, Larsen PJ, Fahrenkrug J. 2004. Melanopsin is expressed in PACAP-containing retinal ganglion cells of the human retinohypothalamic tract. Invest Ophthalmol Vis Sci 45:4202-4209.
32. Harrington ME. 1997. The ventral lateral geniculate nucleus and the intergeniculate leaflet: interrelated structures in the visual and circadian systems. Neurosci Biobehav Rev 21:705-727.
33. Harrington ME, Rusak B. 1989. Photic responses of geniculo-hypothalamic tract neurons in the Syrian hamster. Vis Neurosci 2:367-375.
34. Hattar S, Liao HW, Takao M, Berson DM, Yau KW. 2002. Melanopsin- containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science 295:1065-1070.
35. Hattar S, Lucas RJ, Mrosovsky N, Thompson S, Douglas RH, Hankins MW, Lem J, Biel M, Hofmann F, Foster RG, Yau KW. 2003. Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature 424:76-81.
36. Herkenham M, Nauta WJ. 1979. Efferent connections of the habenular nuclei in the rat. J Comp Neurol 187:19-47.
37. Hirota T, Fukada Y. 2004. Resetting mechanism of central and peripheral circadian clocks in mammals. Zool Sci 21:359-368.
38. Isa T. 2002. Intrinsic processing in the mammalian superior colliculus. Curr Opin Neurobiol 12:668-677.
39. Itaya SK, Van Hoesen GW, Benevento LA. 1986. Direct retinal pathways to the limbic thalamus of the monkey. Exp Brain Res 61:607-613.
40. Johnson RF, Morin LP, Moore RY. 1988. Retinohypothalamic projections in the hamster and rat demonstrated using cholera toxin. Brain Res 462:301-312.
41. Kim U, Chang SY. 2005. Dendritic morphology, local circuitry, and intrinsic electrophysiology of neurons in the rat medial and lateral habenular nuclei of the epithalamus. J Comp Neurol 483:236-250.
42. Klerman EB, Shanahan TL, Brotman DJ, Rimmer DW, Emens JS, Rizzo JF 3rd, Czeisler CA. 2002. Photic resetting of the human circadian pacemaker in the absence of conscious vision. J Biol Rhythms 17:548-555.
43. Klooster J, Vrensen GF. 1998. New indirect pathways subserving the pupillary light reflex: projections of the accessory oculomotor nuclei and the periaqueductal gray to the Edinger-Westphal nucleus and the thoracic spinal cord in rats. Anat Embryol (Berl) 198:123-132.
44. Klooster J, Vrensen GF, Muller LJ, van der Want JJ. 1995. Efferent projections of the olivary pretectal nucleus in the albino rat subserving the pupillary light reflex and related reflexes. A light microscopic tracing study. Brain Res 688:34-46.
45. Kostoglou-Athanassiou I, Treacher DF, Wheeler MJ, Forsling ML. 1998. Bright light exposure and pituitary hormone secretion. Clin Endocrinol (Oxf) 48:73-79.
46. Kramer A, Yang FC, Snodgrass P, Li X, Scammell TE, Davis FC, Weitz CJ. 2001. Regulation of daily locomotor activity and sleep by hypothalamic EGF receptor signaling. Science 294:2511-2515.
47. Kriegsfeld LJ, Leak RK, Yackulic CB, LeSauter J, Silver R. 2004. Organization of suprachiasmatic nucleus projections in Syrian hamsters (Mesocricetus auratus): an anterograde and retrograde analysis. J Comp Neurol 468:361-379.
48. Leak RK, Moore RY. 1997. Identification of retinal ganglion cells projecting to the lateral hypothalamic area of the rat. Brain Res 770:105-114.
49. Levine JD, Weiss ML, Rosenwasser AM, Miselis RR. 1991. Retinohypothalamic tract in the female albino rat: a study using horseradish peroxidase conjugated to cholera toxin. J Comp Neurol 306:344-360.
50. Levine JD, Zhao XS, Miselis RR. 1994. Direct and indirect retinohypothalamic projections to the supraoptic nucleus in the female albino rat. J Comp Neurol 341:214-224.
51. Ling C, Schneider GE, Northmore D, Jhaveri S. 1997. Afferents from the colliculus, cortex, and retina have distinct terminal morphologies in the lateral posterior thalamic nucleus. J Comp Neurol 388:467-483.
52. Ling C, Schneider GE, Jhaveri S. 1998. Target-specific morphology of retinal axon arbors in the adult hamster. Vis Neurosci 15:559-579.
53. Lu J, Zhang YH, Chou TC, Gaus SE, Elmquist JK, Shiromani P, Saper CB. 2001. Contrasting effects of ibotenate lesions of the paraventricular nucleus and subparaventricular zone on sleep-wake cycle and temperature regulation. J Neurosci 21:4864-4874.
54. Lucas RJ, Douglas RH, Foster RG. 2001. Characterization of an ocular photopigment capable of driving pupillary constriction in mice. Nat Neurosci 4:621-626.
55. Lucas RJ, Hattar S, Takao M, Berson DM, Foster RG, Yau K-W. 2003. Diminished pupillary light reflex at high irradiances in melanopsin-knockout mice. Science 299:245-247.
56. Matteau I, Boire D, Ptito M. 2003. Retinal projections in the cat: a cholera toxin B subunit study. Vis Neurosci 20:481-493.
57. Melyan Z, Tarttelin EE, Bellingham J, Lucas RJ, Hankins MW. 2005. Addition of human melanopsin renders mammalian cells photoresponsive. Nature 433:741-745.
58. Mick G, Cooper H, Magnin M. 1993. Retinal projection to the olfactory tubercle and basal telencephalon in primates. J Comp Neurol 327:205-219.
59. Mikkelsen JD. 1992. Visualization of efferent retinal projections by immunohistochemical identification of cholera toxin subunit B. Brain Res Bull 28:619-623.
60. Mikkelsen JD, Serviere J. 1992. Demonstration of a direct projection from the retina to the hypothalamic supraoptic nucleus of the hamster. Neurosci Lett 139:149-152.
61. Mikkelsen JD, Vrang N. 1994. A direct pretectosuprachiasmatic projection in the rat. Neuroscience 62:497-505.
62. Miura M, Dong K, Ahmed FA, Okamura H, Yamadori T. 1997. The termination of optic nerve fibers in the albino mouse. Kobe J Med Sci 43:99-108.
63. Moga MM, Moore RY. 1997. Organization of neural inputs to the suprachiasmatic nucleus in the rat. J Comp Neurol 389:508-534.
64. Moller M, Baeres FM. 2002. The anatomy and innervation of the mammalian pineal gland. Cell Tissue Res 309:139-150.
65. Mombaerts P, Wang F, Dulac C, Chao SK, Nemes A, Mendelsohn M, Edmondson J, Axel R. 1996. Visualizing an olfactory sensory map. Cell 87:675-686.
66. Moore RY, Card JP. 1994. Intergeniculate leaflet: an anatomically and functionally distinct subdivision of the lateral geniculate complex. J Comp Neurol 344:403-430.
67. Moore RY, Danchenko RL. 2002. Paraventricular-subparaventricular hypothalamic lesions selectively affect circadian function. Chronobiol Int 19:345-360.
68. Moore RY, Speh JC, Leak RK. 2002. Suprachiasmatic nucleus organization. Cell Tissue Res 309:89-98.
69. Morin LP, Blanchard J. 1995. Organization of the hamster intergeniculate leaflet: NPY and ENK projections to the suprachiasmatic nucleus, intergeniculate leaflet and posterior limitans nucleus. Vis Neurosci 12:57-67.
70. Morin LP, Blanchard JH. 1997. Neuropeptide Y and enkephalin immunoreactivity in retinorecipient nuclei of the hamster pretectum and thalamus. Vis Neurosci 14:765-777.
71. Morin LP, Blanchard JH. 1998. Interconnections among nuclei of the subcortical visual shell: the intergeniculate leaflet is a major constituent of the hamster subcortical visual system. J Comp Neurol 396:288-309.
72. Morin LP, Blanchard JH. 1999. Forebrain connections of the hamster intergeniculate leaflet: comparison with those of ventral lateral geniculate nucleus and retina. Vis Neurosci 16:1037-1054.
73. Morin LP, Blanchard J, Moore RY. 1992. Intergeniculate leaflet and suprachiasmatic nucleus organization and connections in the golden hamster. Vis Neurosci 8:219-230.
74. Morin LP, Blanchard JH, Provencio I. 2003. Retinal ganglion cell projections to the hamster suprachiasmatic nucleus, intergeniculate leaflet, and visual midbrain: bifurcation and melanopsin immunoreactivity. J Comp Neurol 465:401-416.
75. Mrosovsky N, Hattar S. 2003. Impaired masking responses to light in melanopsin-knockout mice. Chronobiol Int 20:989-999.
76. Muscat L, Huberman AD, Jordan CL, Morin LP. 2003. Crossed and uncrossed retinal projections to the hamster circadian system. J Comp Neurol 466:513-524.
77. Nakagawa S, Tamai Y, Yasui M, Konishi N. 1982. Termination of retinal fibers in lateral preoptic and hypothalamic areas of the crab-eating monkey, Macaca irus. Arch Histol Jpn 45:207-212.
78. Newman LA, Walker MT, Brown RL, Cronin TW, Robinson PR. 2003. Melanopsin forms a functional short-wavelength photopigment. Biochemistry 42:12734-12738.
79. Okoyama S, Moriizumi T. 2001. Onset of calbindin-D 28K and parvalbumin expression in the lateral geniculate complex and olivary pretectal nucleus during postnatal development of the rat. Int J Dev Neurosci 19:655-661.
80. Pak MW, Giolli RA, Pinto LH, Mangini NJ, Gregory KM, Vanable JW Jr. 1987. Retinopretectal and accessory optic projections of normal mice and the OKN-defective mutant mice beige, beige-J, and pearl. J Comp Neurol 258:435-446.
81. Panda S, Sato TK, Castrucci AM, Rollag MD, DeGrip WJ, Hogenesch JB, Provencio I, Kay SA. 2002. Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science 298:2213-2216.
82. Panda S, Provencio I, Tu DC, Pires SS, Rollag MD, Castrucci AM, Pletcher MT, Sato TK, Wiltshire T, Andahazy M, Kay SA, Van Gelder RN, Hogenesch JB. 2003. Melanopsin is required for non-image-forming photic responses in blind mice. Science 301:525-527.
83. Panda S, Nayak SK, Campo B, Walker JR, Hogenesch JB, Jegla T. 2005. Illumination of the melanopsin signaling pathway. Science 307:600-604.
84. Paxinos G, Franklin KBJ. 2001. The mouse brain in stereotaxic coordinates. San Diego: Academic Press.
85. Pickard GE, Silverman AJ. 1981. Direct retinal projections to the hypothalamus, piriform cortex, and accessory optic nuclei in the golden hamster as demonstrated by a sensitive anterograde horseradish peroxidase technique. J Comp Neurol 196:155-172.
86. Prichard JR, Stoffel RT, Quimby DL, Obermeyer WH, Benca RM, Behan M. 2002. Fos immunoreactivity in rat subcortical visual shell in response to illuminance changes. Neuroscience 114:781-793.
87. Provencio I, Jiang G, De Grip WJ, Hayes WP, Rollag MD. 1998. Melanopsin: an opsin in melanophores, brain, and eye. Proc Natl Acad Sci U S A 95:340-345.
88. Provencio I, Rodriguez IR, Jiang G, Hayes WP, Moreira EF, Rollag MD. 2000. A novel human opsin in the inner retina. J Neurosci 20:600-605.
89. Provencio I, Rollag MD, Castrucci AM. 2002. Photoreceptive net in the mammalian retina. Nature 415:493.
90. Qiu X, Kumbalasiri T, Carlson SM, Wong KY, Krishna V, Provencio I, Berson DM. 2005. Induction of photosensitivity by heterologous expression of melanopsin. Nature 433:745-749.
91. Qu T, Dong K, Sugioka K, Yamadori T. 1996. Demonstration of direct input from the retina to the lateral habenular nucleus in the albino rat. Brain Res 709:251-258.
92. Reuss S, Decker K. 1997. Anterograde tracing of retinohypothalamic afferents with Fluoro-Gold. Brain Res 745:197-204.
93. Ronnekleiv OK, Kelly MJ. 1984. Distribution of substance P neurons in the epithalamus of the rat: an immunohistochemical investigation. J Pineal Res 1:355-370.
94. Ronnekleiv OK, Kelly MJ, Wuttke W. 1980. Single unit recordings in the rat pineal gland: evidence for habenulo-pineal neural connections. Exp Brain Res 39:187-192.
95. Ruby NF, Brennan TJ, Xie X, Cao V, Franken P, Heller HC, O'Hara BF. 2002. Role of melanopsin in circadian responses to light. Science 298:2211-2213.
96. Scalia F. 1972. The termination of retinal axons in the pretectal region of mammals. J Comp Neurol 145:223-257.
97. Scalia F, Arango V. 1979. Topographic organization of the projections of the retina to the pretectal region in the rat. J Comp Neurol 186:271-292.
98. Sherin JE, Shiromani PJ, McCarley RW, Saper CB. 1996. Activation of ventrolateral preoptic neurons during sleep. Science 271:216-219.
99. Sollars PJ, Smeraski CA, Kaufman JD, Ogilvie MD, Provencio I, Pickard GE. 2003. Melanopsin and non-melanopsin expressing retinal ganglion cells innervate the hypothalamic suprachiasmatic nucleus. Vis Neurosci 20:601-610.
100. Tang IH, Murakami DM, Fuller CA. 2002. Unilateral optic nerve transection alters light response of suprachiasmatic nucleus and intergeniculate leaflet. Am J Physiol Regul Integr Comp Physiol 282:R569-577.
101. Trejo LJ, Cicerone CM. 1984. Cells in the pretectal olivary nucleus are in the pathway for the direct light reflex of the pupil in the rat. Brain Res 300:49-62.
102. Warren EJ, Allen CN, Brown RL, Robinson DW. 2003. Intrinsic light responses of retinal ganglion cells projecting to the circadian system. Eur J Neurosci 17:1727-1735.
103. Weber JT, Chen IL, Hutchins B. 1986. The pretectal complex of the cat: cells of origin of projections to the pulvinar nucleus. Brain Res 397:389-394.
104. Windle RJ, Forsling ML, Guzek JW. 1992. Daily rhythms in the hormone content of the neurohypophysial system and release of oxytocin and vasopressin in the male rat: effect of constant light. J Endocrinol 133:283-290.
105. Yan L, Silver R. 2002. Differential induction and localization of mPer1 and mPer2 during advancing and delaying phase shifts. Eur J Neurosci 16:1531-1540.
106. Yoshimura T, Ebihara S. 1996. Spectral sensitivity of photoreceptors mediating phase-shifts of circadian rhythms in retinally degenerate CBA/J (rd/rd) and normal CBA/N (+/+)mice. J Comp Physiol [A] 178:797-802.
107. Young MJ, Lund RD. 1994. The anatomical substrates subserving the pupillary light reflex in rats: origin of the consensual pupillary response. Neuroscience 62:481-496.
108. Youngstrom TG, Nunez AA. 1986. Comparative anatomy of the retinohypothalamic tract in photoperiodic and non-photoperiodic rodents. Brain Res Bull 17:485-492.
109. Youngstrom TG, Weiss ML, Nunez AA. 1991. Retinofugal projections to the hypothalamus, anterior thalamus and basal forebrain in hamsters. Brain Res Bull 26:403-411.
110. Zhao H, Rusak B. 2005. Circadian firing-rate rhythms and light responses of rat habenular nucleus neurons in vivo and in vitro. Neuroscience 132:519-528.