Photic induction of c-Fos in enkephalin neurons of the rat intergeniculate leaflet innervated by retinal PACAP fibres

Cell and Tissue Research

Volumn 329, Issue 3, 2007, Pages 491-502

  Juhl, Fie ^a   Hannibal, Jens ^a   Fahrenkrug, Jan ^a  

^a BISPEBJERG HOSPITAL   (Denmark)

Author keywords

Circadian rhythm; Entrainment; Immediate early gene; Photic response; Rat (Wistar, male)

Indexed keywords

ENKEPHALIN; NEUROPEPTIDE Y; PITUITARY ADENYLATE CYLASE ACTIVATING POLYPEPTIDE; POLYPEPTIDE; PROTEIN C FOS; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; ENUCLEATION; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; PHOTOSTIMULATION; PRIORITY JOURNAL; RAT; RETINA GANGLION CELL;

ANIMALS; BIOLOGICAL CLOCKS; ENKEPHALINS; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; NEURONS; NEUROPEPTIDE Y; PHOTIC STIMULATION; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, WISTAR; RETINAL GANGLION CELLS; SUPRACHIASMATIC NUCLEUS; THALAMUS;

RATTUS;

EID: 34547764770     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00441-007-0422-6     Document Type: Article

References (66)

1. Abe H, Rusak B (1994) Physiological mechanism regulating photic induction of Fos-like protein in hamster suprachiasmatic nucleus. Neurosci Biobehav Rev 18:531-536
2. Albers HE, Ferris CF (1984) Neuropeptide Y: role in light-dark cycle entrainment of hamster circadian rhythms. Neurosci Lett 50:163-168
3. Berson DM, Dunn FA, Takao M (2002) Phototransduction by retinal ganglion cells that set the circadian clock. Science 295:1070-1073
4. Biello SM, Mrosovsky N (1996) Phase response curves to neuropeptide Y in wildtype and tau mutant hamsters. J Biol Rhythms 11:27-34
5. Biello SM, Golombeck DA, Schak KM, Harrington ME (1997) Circadian phase shifts to neuropeptide Y in vitro: cellular communication and signal transaction. J Neurosci 17:8468-8475
6. Blasiak T, Lewandowski MH (2004) Identification of intergeniculate leaflet slow bursting cells projection target-an antidromic study in the rat. FENS Abstract 2:A024.03
7. Card JP, Moore RY (1989) Organization of lateral geniculate-hypothalamic connections in the rat. J Comp Neurol 284:135-147
8. Card JP, Brecha N, Karten HJ, Moore RY (1981) Immunocytochemical localization of vasoactive intestinal polypeptide-containing cells and processes in the suprachiasmatic nucleus of the rat: light and electron microscopic analysis. J Neurosci 1:1289-1303
9. Cheng H-YM, Obrietan K, Cain SW, Lee BY, Agostino PV, Joza NA, Harrington ME, Ralph MR, Penninger JM (2004) Dexras1 potentiates photic and suppresses nonphotic responses of the circadian clock. Neuron 43:715-728
10. Colwell CS, Foster RG (1992) Photic regulation of Fos-like immunoreactivity in the suprachiasmatic nucleus of the mouse. J Comp Neurol 324:135-142
11. 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 433:698-699
12. Edelstein K, Beaule C, D'Abramo R, Amir S (2000) Expression profiles of JunB and c-Fos proteins in the rat circadian system. Brain Res 870:54-65
13. Fetissov SO, Byrne LC, Hassani H, Ernfors P, Hökfelt T (2004) Characterization of neuropeptide Y Y2 and Y5 receptor expression in the mouse hypothalamus. J Comp Neurol 470:256-265
14. Gamble KL, Ehlen JC, Albers HE (2005) Circadian control during the day and night: role of neuropeptide Y Y5 receptors in the suprachiasmatic nucleus. Brain Res Bull 65:513-519
15. Hannibal J (2006) Roles of PACAP-containing retinal ganglion cells in circadian timing. Int Rev Cytol 251:1-39
16. Hannibal J, Fahrenkrug J (2004) Target areas innervated by PACAP-immunoreactive retinal ganglion cells. Cell Tissue Res 316:99-113
17. Hannibal J, Fahrenkrug J (2006) Neuronal input pathways to the brain's biological clock and their functional significance. Adv Embryol Cell Biol 182:1-71
18. Hannibal J, Mikkelsen JD, Clausen H, Holst JJ, Wulff BS, Fahrenkrug J (1995) Gene expression of pituitary adenylate cyclase activating polypeptide (PACAP) in the rat hypothalamus. Regul Pept 55:133-148
19. Hannibal J, Hindersson P, Knudsen SM, Georg B, Fahrenkrug J (2002) The photopigment melanopsin is exclusively present in PACAP containing retinal ganglion cells of the retinohypothalamic tract. J Neurosci 22 (RC191):1-7
20. 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
21. Harrington ME, Schak KM (2000) Neuropeptide Y phase advances the in vitro hamster circadian clock during the subjective day with no effect on phase during the subjective night. Can J Physiol Pharmacol 78:87-92
22. Harrington ME, Nance DM, Rusak B (1985) Neuropeptide Y immunoreactivity in the hamster geniculo-suprachiasmatic tract. Brain Res Bull 15:465-472
23. Hastings MH, Duffield GE, Smith EJ, Maywood ES, Ebling FJ (1998) Entrainment of the circadian system of mammals by nonphotic cues. Chronobiol Int 15:425-445
24. Hattar S, Liao HW, Takao M, Berson DM, Yau KW (2002) Melanopsin- containing retinal ganglion cells: architecture, projections, and intrinsic phosensitivity. Science 295:1065-1070
25. Hickey TL, Spear PD (1976) Retinogeniculate projections in hooded and albino rats: an autoradiographic study. Exp Brain Res 24:523-529
26. Laemle LK, Fugaro C, Bentley T (1993) The geniculohypothalamic pathway in a congenitally anopthalmic mouse. Brain Res 618:352-357
27. Lall GS, Biello SM (2003a) Attenuation of circadian light induced phase advances and delays by neuropeptide Y and a neuropeptide Y Y1/Y5 receptor agonist. Neuroscience 119:611-618
28. Lall GS, Biello SM (2003b) Neuropeptide Y (NPY) attenuates photic phase shifts via the NPY Y5 receptor subtype. Soc Neurosci 510:14
29. Larsen PJ, Kristensen P (1998) Distribution of neuropeptide Y receptor expression in the rat suprachiasmatic nucleus. Mol Brain Res 60:69-76
30. Lewandowski MH, Blasiak T, Domoslawski J, Wolkowska A (2000) Ultradian rhythmic neuronal oscillation in the intergeniculate leaflet. Neuroreport 11:317-321
31. Lewandowski MH, Blasiak T, Blasiak A (2002) Are ultra-slow isoperiodic oscillations in rat intergeniculate leaflet neurons dependent on reciprocal connection with its contralaterally located counterpart? Neurosci Lett 330:243-246
32. 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
33. Mantyh PW, Kemp JA (1983) The distribution of putative neurotransmitters in the lateral geniculate nucleus of the rat. Brain Res 288:344-348
34. Mikkelsen JD (1992) The organization of the crossed geniculogeniculate pathway of the rat: a Phaseolus vulgaris-leucoagglutinin study. Neuroscience 48:953-962
35. Mikkelsen JD (1994) Analysis of the efferent projections of the lateral geniculate nucleus with special reference to the innervation of the subcommissural organ and related areas. Cell Tissue Res 277:437-445
36. Mikkelsen JD, O'Hare MM (1991) An immunohistochemical and chromatographic analysis of the distribution and processing of proneuropeptide Y in the rat suprachiasmatic nucleus. Neurosci Lett 12:177-185
37. Moore RY, Card JP (1994) Intergeniculate leaflet: an anatomically and functionally distinct subdivision of the lateral geniculate complex. J Comp Neurol 344:403-430
38. Moore RY, Speh JC (1993) GABA is the principal neurotransmitter of the circadian system. Neurosci Lett 150:112-116
39. Moore RY, Gustafson EL, Card JP (1984) Identical immunoreactivity of afferents to the rat suprachiasmatic nucleus with antisera against avian pancreatic polypeptide, molluscan cardioexcitatory peptide and neuropeptide Y. Cell Tissue Res 236:41-46
40. Morin LP (1994) The circadian visual system. Brain Res Rev 19:102-107
41. Morin LP, Allen CN (2006) The circadian visual system, 2005. Brain Res Rev 51:1-60
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, Blanchard J, Moore RY (1992) Intergeniculate leaflet and suprachiasmatic nucleus organization and connections in the golden hamster. Vis Neurosci 8:219-230
44. 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
45. Ohara PT, Lieberman AR, Hunt SP, Wu JY (1983) Neural elements containing glutamic acid decarboxylase (GAD) in the dorsal lateral geniculate nucleus of the rat; immunohistochemical studies by light and electron microscopy. Neuroscience 8:189-211
46. Park HT, Baek SY, Kim BS, Kim JB, Kim JJ (1993) Profile of Fos-like immunoreactivity induction by light stimuli in the intergeniculate leaflet is different from that of the suprachiasmatic nucleus. Brain Res 610:334-339
47. Paxinos G, Watson C (1997) The rat brain in stereotaxic coordinates, 3rd ed. Academic Press, San Diego
48. 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
49. Reuss S, Decker K (1997) Anterograde tracing of retinohypothalamic afferents with fluoro-gold. Brain Res 745:197-204
50. Ribak CE, Peters A (1975) An autoradiographic study of the projections from the lateral geniculate body of the rat. Brain Res 92:341-368
51. Rusak B, Robertson HA, Wisden W, Hunt SP (1990) Light pulses that shift rhythms induce gene expression in the suprachiasmatic nucleus. Science 248:1237-1240
52. SAS Institute (1994) SAS/STAT user's guide, 4th version, 6th edn. SAS Institute, Cary, N.C., USA
53. Shindler KS, Roth KA (1996) Double immunofluorescent staining using two unconjugated primary antisera raised in the same species. J Histochem Cytochem 44:1331-1335
54. Soscia SJ, Harrington ME (2005) Neuropeptide Y does not reset the circadian clock in NPY Y2-/- mice. Neurosci Lett 373:175-178
55. Swanson LW, Cowan WM, Jones EG (1974) An autoradiographic study of the efferent connections of the ventral lateral geniculate nucleus in the albino rat and the cat. J Comp Neurol 156:143-163
56. Takatsuji K, Miguel-Hidalgo J-J, Tohyama M (1991) Retinal fibers make synaptic contact with neuropeptide Y and enkephalin immunoreactive neurons in the intergeniculate leaflet of the rat. Neurosci Lett 125:73-76
57. Thankachan S, Rusak B (2005) Juxtacellular recording/labeling analysis of physiological and anatomical characteristics of rat intergeniculate leaflet neurons. J Neurosci 25:9195-9204
58. Vrang N, Mrosovsky N, Mikkelsen JD (2003) Afferent projections to the hamster intergeniculate leaflet demonstrated by retrograde and anterograde tracing. Brain Res Bull 59:267-288
59. Wadhwa S, Rath S, Jotwani G, Bijlani V (1990) Development of substance P, Leu-enkephalin and serotonin profiles in the lateral geniculate nuclear complex of albino rat. Neurosci Lett 120:146-150
60. Warren EJ, Allen CN, Brown RL, Robinson D (2003) Intrinsic light responses of retinal ganglion cells projecting to the circadian system. Eur J Neurosci 17:1727-1735
61. Weber ET, Rea MA (1997) Neuropeptide Y blocks light-induced phase advances but not delays of the circadian activity rhythm in hamsters. Neurosci Lett 231:159-162
62. Wolak ML, deJoseph R, Cator AD, Mokashi AS, Brownfield MS, Urban JH (2003) Comparative distribution of neuropeptide Y Y1 and Y5 receptors in the rat brain by using immunohistochemistry. J Comp Neurol 464:285-311
63. Woldbye DP, Greisen MH, Bolwig TG, Larsen PJ, Mikkelsen JD (1997) Prolonged induction of c-fos in neuropeptide Y- and somatostatin-immunoreactive neurons of the rat dentate gyrus after electroconvulsive stimulation. J Neurosci 17:8468-8475
64. Yannielli PC, Harrington ME (2001) The neuropeptide Y Y5 receptor mediates the blockade of "photic-like" NMDA-induced phase shifts in the golden hamster. J Neurosci 14:5367-5373
65. Yannielli PC, Harrington ME (2004) Let there be "more" light: enhancement of light actions on the circadian system through non-photic pathways. Prog Neurobiol 74:59-76
66. 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