Retinal ganglion cell projections to the hamster suprachiasmatic nucleus, intergeniculate leaflet, and visual midbrain: Bifurcation and melanopsin immunoreactivity

Journal of Comparative Neurology

Volumn 465, Issue 3, 2003, Pages 401-416

  Morin, Lawrence P ^a   Blanchard, Jane H ^a   Provencio, Ignacio ^b  

^a STONY BROOK UNIVERSITY   (United States)

^b UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

Author keywords

Circadian rhythm; Olivary pretectal nucleus; Retinohypothalamic tract; Superior colliculus

Indexed keywords

MELANOPSIN; UNCLASSIFIED DRUG; VISUAL PIGMENT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; GENICULATE BODY; HAMSTER; HYPOTHALAMUS; IMMUNOREACTIVITY; LIGHT; MALE; MESENCEPHALON; NONHUMAN; OLIVARY NUCLEUS; PHOTOREACTIVITY; PRIORITY JOURNAL; RETINA; RETINA GANGLION CELL; SUPERIOR COLLICULUS; SUPRACHIASMATIC NUCLEUS;

NASA DISCIPLINE NEUROSCIENCE; NASA PROGRAM BIOMEDICAL RESEARCH AND COUNTERMEASURES; NON-NASA CENTER;

ANIMALS; CRICETINAE; GENICULATE GANGLION; IMMUNOCHEMISTRY; MALE; MESENCEPHALON; MESOCRICETUS; NEURAL PATHWAYS; OPSIN; RETINAL GANGLION CELLS; SUPRACHIASMATIC NUCLEUS;

EID: 0141433232     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10881     Document Type: Article

References (73)

1. Aggelopoulos NC, Meissl H. 2000. Responses of neurones of the rat suprachiasmatic nucleus to retinal illumination under photopic and scotopic conditions. J Physiol 523:211-222.
2. Balkema GW, Drager UC. 1990. Origins of uncrossed retinofugal projections in normal and hypopigmented mice. Vis Neurosci 4:595-604.
3. Berson DM, Dunn FA, Takao M. 2002. Phototransduction by retinal ganglion cells that set the circadian clock. Science 295:1070-1073.
4. Card JP, Moore RY. 1989. Organization of lateral geniculate-hypothalamic connections in the rat. J Comp Neurol 284:135-147.
5. Chen S, Aston-Jones G. 1995. Evidence that cholera toxin B subunit (CTb) can be avidly taken up and transported by fibers of passage. Brain Res 674:107-111.
6. Dong K, Ahmed AK, Setsu T, Sugioka K, Yamadori T. 1995. Bifurcated projections of retinal ganglion cells bilaterally innervate the lateral geniculate nuclei in the cat. Brain Res 703:231-236.
7. Dreher, B., Sefton AJ, Ni SYK, Nisbett G. 1985. The morphology, number, distribution and central projections of class I retinal ganglion cells in albino and hooded rats. Brain Behav Evol 26:10-48.
8. Dunn FA, Berson DM. 2002. Are intrinsically photosensitive retinal ganglion cells influenced by rods or cones?. Invest Ophthal Vis Sci 43: abstract 2982.
9. Eichler VB, Moore RY. 1974. The primary and accessory optic systems in the golden hamster, Mesocricetus auratus. Acta Anat 89:359-371.
10. Finlay BL, Schneps SE, Wilson KG, Schneider GE. 1978. Topography of visual and somatosensory projections to the superior colliculus of the golden hamster. Brain Res 142:223-235.
11. Finlay BL, Sengelaub DR, Berg AT, Cairns SJ. 1980. A neuroethological approach to hamster vision. Behav Brain Res 1:479-496.
12. Freedman MS, Lucas RJ, Soni B, Von Schantz M, Muñoz M, David-Gray Z, Foster R. 1999. Regulation of mammalian circadian behavior by non-rod, non-cone, ocular photoreceptors. Science 284:502-504.
13. Gooley JJ, Saper CB. 2002. A broad role for melanopsin in non-visual photoreception based on neuroanatomical evidence in rats. Soc Res Biol Rhythms 8:117.
14. Gooley JJ, Lu J, Chou TC, Scammell TE, Saper CB. 2001. Melanopsin in cells of origin of the retinohypothalamic tract. Nat Neurosci 4:1165.
15. Hannibal J, Ding JM, Chen D, Fahrenkrug J, Larsen PJ, Gillette MU, Mikkelsen JD. 1997. Pituitary adenylate cyclase-activating peptide (PACAP) in the retinohypothalamic tract: a potential daytime regulator of the biological clock. J Neurosci 17:2637-2644.
16. Hannibal J, Hindersson P, Knudsen SM, Georg B, Fahrenkrug J. 2002. The photopigment melanopsin is exclusively present in pituitary adenylated cyclase-activating polypeptide-containing retinal ganglion cells of the retinohypothalamic tract. J Neurosci 22:RC191 (1-7).
17. Harrington ME, Rusak B. 1986. Lesions of the thalamic intergeniculate leaflet alter hamster circadian rhythms. J Biol Rhythms 1:309-325.
18. 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.
19. Hsiao K, Sachs GM, Schneider GE. 1984. A minute fraction of Syrian golden hamster retinal ganglion cells project bilaterally. J Neurosci 4:359-367.
20. Illing R-B. 1980. Axonal bifurcation of cat retinal ganglion cells as demonstrated by retrograde double labelling with fluorescent dyes. Neurosci Lett 19:125-130.
21. Janik D, Mrosovsky N. 1994. Intergeniculate leaflet lesions and behaviorally-induced shifts of circadian rhythms. Brain Res 651:174-182.
22. Jeffery G, Cowey A, Kuypers HG. 1981. Bifurcating retinal ganglion cell axons in the rat, demonstrated by retrograde double labelling. Exp Brain Res 44:34-40.
23. Johnson RF, Moore RY, Morin LP. 1988a. Loss of entrainment and anatomical plasticity after lesions of the hamster retinohypothalamic tract. Brain Res 460:297-313.
24. Johnson RF, Morin LP, Moore RY. 1988b. Retinohypothalamic projections in the hamster and rat demonstrated using cholera toxin. Brain Res 462:301-312.
25. Johnson RF, Smale L, Moore RY, Morin LP. 1988c. Lateral geniculate lesions block circadian phase shift responses to a benzodiazepine. Proc Natl Acad Sci U S A 85:5301-5304.
26. Koontz MA, Rodieck RW, Farmer SG. 1985. The retinal projection to the cat pretectum. J Comp Neurol 236:42-59.
27. Ling C, Schneider GE, Jhaveri S. 1998. Target-specific morphology of retinal axon arbors in the adult hamster. Vis Neurosci 15:559-579.
28. Lucas RJ, Douglas RH, Foster RG. 2001a. Characterization of an ocular photopigment capable of driving pupillary constriction in mice. Nat Neurosci 4:621-626.
29. Lucas RJ, Freedman MS, Lupi D, Munoz M, David-Gray ZK, Foster RG. 2001b. Identifying the photoreceptive inputs to the mammalian circadian system using transgenic and retinally degenerate mice. Behav Brain Res 125:97-102.
30. Lucas RJ, Hattar S, Takao M, Berson DM, Foster RG, Yau KW. 2003. Diminished pupillary light reflex at high irradiances in melanopsin-knockout mice. Science 299:245-247.
31. Marchant EG, Morin LP. 1999. The hamster circadian rhythm system includes nuclei of the subcortical visual shell. J Neurosci 19:10482-10493.
32. McLean IW, Nakane PK. 1974. Periodate-lysine-paraformaldehyde fixative: a new fixative for immunoelectron microscopy. J Histochem Cytochem 22:1077-1083.
33. Millhouse OE. 1977. Optic chiasm collaterals afferent to the suprachiasmatic nucleus. Brain Res 137:351-355.
34. Moore RY, Lenn NJ. 1972. A retinohypothalamic projection in the rat. J Comp Neurol 146:1-14.
35. Moore RY, Weis R, Moga MM. 2000. Efferent projections of the intergeniculate leaflet and the ventral lateral geniculate nucleus in the rat. J Comp Neurol 420:398-418.
36. Morin LP. 1994. The circadian visual system. Brain Res Rev 67:102-127.
37. Morin LP, Blanchard JH. 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.
38. Morin LP, Blanchard JH. 1997. Nouropeptide Y and enkephalin immunoreactivity in retinorecipient nuclei of the hamster pretectum and thalamus. Vis Neurosci 14:765-777.
39. Morin LP, Blanchard JH. 1998a. 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.
40. Morin LP, Blanchard JH. 1998b. Interconnections of the IGL and VLG with hamster forebrain. Soc Neurosci Abstr 24:1919.
41. 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.
42. Morin LP, Blanchard JH. 2001. Neuromodulator content of hamster intergeniculate leaflet neurons and their projection to the suprachiasmatic nucleus or visual midbrain. J Comp Neurol 437:79-90.
43. Morin LP, Pace L. 2002. The intergeniculate leaflet, but not the visual midbrain, mediates hamster circadian rhythm response to constant light. J Biol Rhythms 17:217-226.
44. Morin LP, Wood RI. 2001. A stereotaxic atlas of the hamster brain. New York: Academic.
45. Morin LP, Blanchard JH, Moore RY. 1992. Intergeniculate leaflet and suprachiasmatic nucleus organization and connections in the hamster. Vis Neurosci 8:219-230.
46. 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.
47. Peterson BB, Liao HW, Dacey DM, Yau K-W, Gamlin PDR, Robinson FR, Marshak DW. 2003. Functional architecture of the photoreceptive ganglion cell in primate retina: morphology, mosaic organization and central targets of melanopsin immunostained cells. Invest Ophthal Vis Sci 44:5182.
48. Pickard GE. 1982. The afferent connections of the suprachiasmatic nucleus of the golden hamster with emphasis on the retinohypothalamic projection. J Comp Neurol 211:65-83.
49. Pickard GE. 1985. Bifurcating axons of retinal ganglion cells terminate in the hypothalamic suprachiasmatic nucleus and the intergeniculate leaflet of the thalamus. Neurosci Lett 55:211-217.
50. Pickard GE, Ralph MR, Menaker M. 1987. The intergeniculate leaflet partially mediates effects oflight on circadian rhythms. J Biol Rhythms 2:35-56.
51. Provencio I, Cooper HM, Foster RG. 1998a. Retinal projections in mice with inherited retinal degeneration: implications for circadian photoentraininent. J Comp Neurol 395:417-439.
52. Provencio I, Jiang G, De Grip WJ, Hayes WP, Rollag MD. 1998b. Melanopsin: an opsin in melanophores, brain, and eye. Proc Natl Acad Sci U S A 95:340-345.
53. 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.
54. Provencio I, Rollag MD, Castrucci AM. 2002. Photoreceptive net in the mammalian retina. This mesh of cells may explain how some blind mice can still tell day from night. Nature 415:493.
55. Redlin U, Mrosovsky N. 1999a. Masking by light in hamsters with SCN lesions. J Comp Physiol A 184:439-448.
56. Redlin U, Mrosovsky N. 1999b. Masking of locomotor activity in hamsters. J Comp Physiol A 184:429-437.
57. Redlin U, Vrang N, Mrosovsky N. 1999. Enhanced masking response to light in hamsters with IGL lesions. J Comp Physiol A 184:449-456.
58. Rhoades RW, Hsu L, Parfett G. 1979. An electronmicroscopic analysis of the optic nerve in the golden hamster. J Comp Neurol 186:491-504.
59. 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.
60. Rusak B. 1977. The role of the suprachiasmatic nuclei in the generation of circadian rhythms in the golden hamster, Mesocricetas auratus. J Comp Physiol 118:145-164.
61. Selby CP, Thompson C, Schmitz TM, Van Gelder RN, Sancar A. 2000. Functional redundancy of cryptochromes and classical photoreceptors for nonvisual ocular photoreception in mice. Proc Natl Acad Sci USA 97:14697-14702.
62. Simpson JI, Giolli RA, Blanks RHI. 1988. The pretectal nuclear complex and the accessory optic system. Rev Oculomot Res 2:335-364.
63. Sollars PJ, Smeraski CA, Kaufman JD, Ogilvie MD, Provencio I, Morin LP, Pickard GE. 2002. Melanopsin and non-melanopsin expressing retinal ganglion cells innervate the suprachiasmatic nucleus. Soc Neurosci Abstr 371:21.
64. Stein BE. 1984. Multimodal representation in the superior colliculus and optic tectum. In: Vanegas H, editor. Comparative neurology of the optic tectum. New York: Plenum. p 819-841.
65. Stephan FK, Zucker I. 1972. Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc Natl Acad Sci U S A 69:1583-1586.
66. Tiao Y-C, Blakemore C. 1976a. Functional organization in the visual cortex of the golden hamster. J Comp Neurol 168:459-482.
67. Tiao Y-C, Blakemore C. 1976b. Regional specialization in the golden hamster's retina. J Comp Neurol 168:439-458.
68. 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.
69. Wang G, Achim CL, Hamilton RL, Wiley CA, Soontornniyomkij V. 1999. Tyramide signal amplification method in multiple-label immunofluorescence confocal microscopy. Methods 18:459-464.
70. Wickland C, Turek FW. 1994. Lesions of the thalamic intergeniculate leaflet block activity-induced phase shifts in the circadian activity rhythm of the golden hamster. Brain Res 660:293-300.
71. Young MJ, Lund RD. 1997. The anatomical substrates subserving the pupillary light reflex in rats: origin of the consensual pupillary response. Neurosci 62:481-486.
72. Young MJ, Lund RD. 1998. The retinal ganglion cells that drive the pupilloconstrictor response in rats. Brain Res 787:191-202.
73. Zhang DX, Rusak B. 1989. Photic sensitivity of geniculate neurons that project to the suprachiasmatic nuclei or the contralateral geniculate. Brain Res 504:161-164.