c-Fos expression in the brains of behaviorally "split" hamsters in constant light: Calling attention to a dorsolateral region of the suprachiasmatic nucleus and the medial division of the lateral habenula

Journal of Biological Rhythms

Volumn 20, Issue 5, 2005, Pages 419-429

  Tavakoli Nezhad, Mahboubeh ^a   Schwartz, William J ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

c Fos; Calbindin; Circadian; PER; Splitting; Suprachiasmatic nucleus

Indexed keywords

BIOLOGICAL MARKER; GLUTAMATE RECEPTOR ANTAGONIST; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN C FOS;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CELL LABELING; CIRCADIAN RHYTHM; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DARKNESS; HABENULA; ILLUMINATION; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; LIGHT DARK CYCLE; LIGHT EXPOSURE; MALE; NONHUMAN; OSCILLATION; PREOPTIC AREA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SUPRACHIASMATIC NUCLEUS; SYRIAN HAMSTER; TISSUE SECTION;

ANIMALS; CIRCADIAN RHYTHM; CRICETINAE; DARKNESS; HABENULA; LIGHT; MALE; MESOCRICETUS; MOTOR ACTIVITY; NUCLEAR PROTEINS; PHOTOPERIOD; PROTO-ONCOGENE PROTEINS C-FOS; SUPRACHIASMATIC NUCLEUS;

CRICETINAE; MESOCRICETUS AURATUS;

EID: 24944495468     PISSN: 07487304     EISSN: None     Source Type: Journal    
DOI: 10.1177/0748730405278443     Document Type: Article

References (60)

1. Abe H, Rusak B, and Robertson HA (1991) Photic induction of Fos protein in the suprachiasmatic nucleus is inhibited by the NMDA receptor antagonist MK-801. Neurosci Lett 127:9-12.
2. Abe H, Rusak B, and Robertson HA (1992) NMDA and non-NMDA receptor antagonists inhibit photic induction of Fos protein in the hamster suprachiasmatic nucleus. Brain Res Bull 28:831-835.
3. Antle MC, Kriegsfeld LJ, and Silver R (2005) Signaling within the master clock of the brain: localized activation of mitogen-activated protein kinase by gastrin-releasing peptide. J Neurosci 25:2447-2454.
4. Boulos Z and Morin LP (1985) Entrainment of split circadian activity rhythms in hamsters. J Biol Rhythms 1:1-15.
5. Chambille I, Doyle S, and Serviere J (1993) Photic induction and circadian expression of Fos-like protein: immunohistochemical study in the retina and suprachiasmatic nuclei of hamster. Brain Res 612:138-150.
6. Chastrette N, Pfaff DW, and Gibbs RB (1991) Effects of daytime and nighttime stress on Fos-like immunoreactivity in the paraventricular nucleus of the hypothalamus, the habenula, and the posterior paraventricular nucleus of the thalamus. Brain Res 563:339-344.
7. Cheng MY, Bullock CM, Li C, Lee AG, Bermak JC, Belluzzi J, Weaver DR, Leslie FM, and Zhou Q-Y (2002) Prokineticin 2 transmits the behavioural circadian rhythm of the suprachiasmatic nucleus. Nature 417:405-410.
8. Cole AJ, Saffen DW, Baraban JM, and Worley PF (1989) Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature 340:474-476.
9. Coogan AN and Piggins HD (2003) Circadian and photic regulation of phosphorylation of ERK1/2 and Elk-1 in the suprachiasmatic nuclei of the Syrian hamster. J Neurosci 23:3085-3093.
10. Davis FC and Menaker M (1980) Hamsters through time's window: temporal structure of hamster locomotor rhythmicity. Am J Physiol 239:R149-R155.
11. de la Iglesia HO, Meyer J, Carpino A Jr, and Schwartz WJ (2000) Antiphase oscillation of the left and right suprachiasmatic nuclei. Science 290:799-801.
12. de la Iglesia HO, Meyer J, and Schwartz WJ (2003) Lateralization of circadian pacemaker output: activation of left- and right-sided luteinizing hormone-releasing hormone neurons involves a neural rather than a humoral pathway. J Neurosci 23:7412-7414.
13. Ebling FJP, Maywood ES, Staley K, Humby T, Hancock DC, Waters CM, Evan GI, and Hastings MH (1991) The role of NMDA-type glutamatergic neurotransmission in the photic induction of immediate-early gene expression in the suprachiasmatic nuclei of the Syrian hamster. J Neuroendocrinol 3:641-652.
14. Guido ME, de Guido L, Goguen D, Robertson HA, and Rusak B (1999a) Differential effects of glutamatergic blockade on circadian and photic regulation of gene expression in the hamster suprachiasmatic nucleus. Mol Brain Res 67:247-257.
15. Guido ME, Goguen D, De Guido L, Robertson HA, and Rusak B (1999b) Circadian and photic regulation of immediate-early gene expression in the hamster suprachiasmatic nucleus. Neuroscience 90:555-571.
16. Hamada T, Antle MC, and Silver R (2004) Temporal and spatial expression patterns of canonical clock genes and clock-controlled genes in the suprachiasmatic nucleus. Eur J Neurosci 19:1741-1748.
17. Harrington ME, Eskes GA, Dickson P, and Rusak B (1990) Lesions dorsal to the suprachiasmatic nuclei abolish split activity rhythms of hamsters. Brain Res Bull 24:593-597.
18. Hoorneman EMD and Buijs RM (1982) Vasopressin fiber pathways in the rat brain following suprachiasmatic nucleus lesioning. Brain Res 243:235-241.
19. Kalsbeek A, Teclemariam-Mesbah R, and Pévet P (1993) Efferent projections of the suprachiasmatic nucleus in the golden hamster (Mesocricetus auratus). J Comp Neurol 332:293-314.
20. Kornhauser JM, Nelson DE, Mayo KE, and Takahashi JS (1990) Photic and circadian regulation of c-fos gene expression in the hamster suprachiasmatic nucleus. Neuron 5:127-134.
21. Kramer A, Yang F-C, Snodgrass P, Li X, Scammell TE, Davis FC, and Weitz CJ (2001) Regulation of daily locomotor activity and sleep by hypothalamic EGF receptor signalling. Science 294:2511-2515.
22. Kriegsfeld LJ, Leak RK, Yackulic CR, LeSauter J, and Silver R (2004) Organization of suprachiasmatic nucleus projections in Syrian hamsters (Mesocricetus auratus): an anterograde and retrograde analysis. J Comp Neurol 468:361-379.
23. Lee HS, Nelms JL, Nguyen M, Silver R, and Lehman MN (2003) The eye is necessary for a circadian rhythm in the suprachiasmatic nucleus. Nat Neurosci 6:111-112.
24. Lees JG, Hallonquist JD, and Mrosovsky N (1983) Differential effects of dark pulses on the two components of split circadian activity rhythms in golden hamsters. J Comp Physiol A 153:123-132.
25. Maywood ES, Mrosovsky N, Field MD, and Hastings MH (1999) Rapid downregulation of mammalian Period genes during behavioral resetting of the circadian clock. Proc Natl Acad Sci USA 96:15211-15216.
26. Meijer JH, Daan S, Overkamp GJF, and Hermann PM (1990) The two-oscillator circadian system of tree shrews (Tupaia belangeri) and its response to light and dark pulses. J Biol Rhythms 5:1-16.
27. Meijer JH, van der Zee EA, and Dietz M (1988) The effects of intraventricular carbachol injections on the free-running activity rhythm of the hamster. J Biol Rhythms 3:333-348.
28. Morin LP, Blanchard JH, and 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.
29. Morin LP, Goodless-Sanchez N, Smale L, and Moore RY (1994) Projections of the suprachiasmatic nuclei, subparaventricular zone and retrochiasmatic area in the golden hamster. Neuroscience 61:391-410.
30. Morin LP and Wood RI (2001) A Stereotaxic Atlas of the Golden Hamster Brain. San Diego, CA: Academic Press.
31. Muscat L, Huberman AD, Jordan CL, and Morin LP (2003) Crossed and uncrossed retinal projection to the hamster circadian system. J Comp Neurol 466:513-524.
32. Nunez AA, Bult A, McElhinny TL, and Smale L (1999) Daily rhythms of Fos expression in hypothalamic targets of the suprachiasmatic nucleus in diurnal and nocturnal rodents. J Biol Rhythms 14:300-306.
33. Ohta H, Yamazaki S, and McMahon DG (2005) Constant light desynchronizes mammalian clock neurons. Nat Neurosci 8:267-269.
34. Olucha-Bordonau FE, Teruel V, Barcia-González J, Ruiz-Torner A, Valverde-Navarro AA, and Martínez-Soriano F (2003) Cytoarchitecture and efferent projections of the nucleus incertus of the rat. J Comp Neurol 464:62-97.
35. 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.
36. Pickard GE, Kahn R, and Silver R (1984) Splitting of the circadian rhythm of body temperature in the golden hamster. Physiol Behav 32:763-766.
37. Pickard GE and Turek FW (1982) Splitting of the circadian rhythm of activity is abolished by unilateral lesions of the suprachiasmatic nuclei. Science 215:1119-1121.
38. Pittendrigh CS and Daan S (1976) A functional analysis of circadian pacemakers in nocturnal rodents. V. Pacemaker structure: a clock for all seasons. J Comp Physiol A 106:333-355.
39. Quintero JE, Kuhlman SJ, and McMahon DG (2003) The biological clock nucleus: a multiphasic oscillator network regulated by light. J Neurosci 23:8070-8076.
40. Rea MA (1992) Different populations of cells in the suprachiasmatic nuclei express c-fos in association with light-induced phase delays and advances of the free-running activity rhythm in hamsters. Brain Res 579:107-112.
41. Rea MA, Buckley B, and Lutton LM (1993) Local administration of EAA antagonists blocks light-induced phase shifts and c-fos expression in hamster SCN. Am J Physiol 265:R1191-R1198.
42. Rusak B, Robertson HA, Wisden W, and Hunt SP (1990) Light pulses that shift rhythms induce gene expression in the suprachiasmatic nucleus. Science 248:1237-1240.
43. Saeb-Parsy K and Dyball REJ (2003) Defined cell groups in the rat suprachiasmatic nucleus have different day/night rhythms of single-unit activity in vivo. J Biol Rhythms 18:26-42.
44. Schaap J, Albus H, van der Leest HT, Eilers PHC, Détári L, and Meijer JH (2003) Heterogeneity of rhythmiclight-induced phase delays and advances of the free-r suprachiasmatic nucleus neurons: implications for circadian waveform and photoperiodic encoding. Proc Natl Acad Sci USA 100:15994-15999.
45. Schwartz MD, Nunez AA, and Smale L (2004) Differences in the suprachiasmatic nucleus and lower subparaventricular zone of diurnal and nocturnal rodents. Neuroscience 127:13-23.
46. Shibuya CA, Melnyk RB, and Mrosovsky N (1980) Simultaneous splitting of drinking and locomotor activity rhythms in a golden hamster. Naturwissenschaften 67:45-47.
47. Sofroniew MV and Weindl A (1978) Projections from the parvocellular vasopressin- and neurophysin-containing neurons of the suprachiasmatic nucleus. Am J Anat 153:391-430.
48. Sutherland RJ (1982) The dorsal diencephalic conduction system: a review of the anatomy and functions of the habenular complex. Neurosci Biobehav Rev 6:1-13.
49. Swann JM and Turek FW (1985) Multiple circadian oscillators regulate the timing of behavioral and endocrine rhythms in female golden hamsters. Science 228:898-900.
50. Treep JA, Abe H, Rusak B, and Goguen DM (1995) Two distinct retinal projections to the hamster suprachiasmatic nucleus. J Biol Rhythms 10:299-307.
51. Vindlacheruvu RR, Ebling FJP, Maywood ES, and Hastings MH (1992) Blockade of glutamatergic neurotransmission in the suprachiasmatic nucleus prevents cellular and behavioural responses of the circadian system to light. Eur J Neurosci 4:673-679.
52. Vogelbaum MA and Menaker M (1992) Temporal chimeras produced by hypothalamic transplants. J Neurosci 12:3619-3627.
53. Vuillez P, Jacob N, Teclemariam-Mesbah R, Van Rossum A, Vivien-Roels B, and Pévet P (1998) Effect of NMDA receptor antagonist MK-801 on light-induced Fos expression in the suprachiasmatic nuclei and on melatonin production in the Syrian hamster. J Neuroendocrinol 10:671-677.
54. Watts AG and Swanson LW (1987) Efferent projections of the suprachiasmatic nucleus: II. Studies using retrograde transport of fluorescent: dyes and simultaneous peptide immunohistochemistry in the rat. J Comp Neurol 258:230-252.
55. Weaver DR, Rivkees SA, and Reppert SM (1989) Localization and characterization of melatonin receptors in rodent brain by in vitro autoradiography. J Neurosci 9:2581-2590.
56. Wirtshafter D, Asin KE, and Pitzer MR (1994) Dopamine agonists and stress produce different patterns of Fos-like immunoreactivity in the lateral habenula. Brain Res 633:21-26.
57. Wisden W, Errington ML, Williams S, Dunnett SB, Walters C, Hitchcock D, Evan G, Bliss TVP, and Hunt SP (1990) Differential expression of immediate early genes in the hippocampus and spinal cord. Neuron 4:603-614.
58. Yamaguchi S, Isejima H, Matsuo T, Okura R, Yagita K, Kobayashi M, Okamura H (2003) Synchronization of cellular clocks in the suprachiasmatic nucleus. Science 302:1408-1412.
59. Yan L and Okamura H (2002) Gradients in the circadian expression of Per1 and Per2 genes in the rat suprachiasmatic nucleus. Eur J Neurosci 15:1153-1162.
60. Zhao H and Rusak B (2005) Circadian firing-rate rhythms and light responses of rat habenular nucleus neurons in vivo and in vitro. Neuroscience 132:519-528.