Differential serotonergic innervation of the suprachiasmatic nucleus and the intergeniculate leaflet and its role in circadian rhythm modulation

Journal of Neuroscience

Volumn 16, Issue 6, 1996, Pages 2097-2111

  Meyer Bernstein, Elizabeth L ^a   Morin, Lawrence P ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

circadian rhythm; intergeniculate leaflet; locomotor activity; raphe nucleus; serotonin; suprachiasmatic nucleus

Indexed keywords

5,6 DIHYDROXYTRYPTAMINE; CHOLERA TOXIN B SUBUNIT; DESIPRAMINE; LEUKOAGGLUTININ; SEROTONIN;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; DORSAL RAPHE NUCLEUS; LATERAL GENICULATE BODY; LIGHT DARK CYCLE; MALE; MEDIAN RAPHE NUCLEUS; NERVE PROJECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; SEROTONINERGIC SYSTEM; SUPRACHIASMATIC NUCLEUS; SYRIAN HAMSTER;

EID: 0029880413     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-06-02097.1996     Document Type: Article

References (88)

1. Azmitia EC (1978) The serotonin-producing neurons of the midbrain median and dorsal raphe nuclei. In: Handbook of psychopharmacology, (Iversen LL, Iversen SD, Snyder SH, eds), pp 233-314. New York: Plenum.
2. Azmitia EC, Segal M (1978) An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. J Comp Neurol 179:641-668.
3. Bina KG, Rusak B, Semba K (1993) Localization of cholinergic neurons in the forebrain and brainstem that project to the suprachiasmatic nucleus of the hypothalamus in rat. J Comp Neurol 335:295-307.
4. Bobillier P, Seguin S, Petitjean F, Salvert D, Touret M, Jouvet M (1976) The raphe nuclei of the cat brainstem: a topographical atlas of their efferent projections as revealed by autoradiography. Brain Res 113:449-486.
5. Bosler O, Vuillon-Cacciuttolo G, Saïdi H (1992) Long-term serotonin reinnervation of the suprachiasmatic nucleus after 5,7-dihydroxytryptamine axotomy in the adult rat. Neurosci Lett 143:159-163.
6. Botchkina GI, Morin LP (1993) Development of the hamster serotoninergic system: cell groups and diencephalic projections. J Comp Neurol 338:405-431.
7. Bowker RM (1986) The relationship between descending serotonin projections and ascending projections in the nucleus raphe magnus: a double labeling study. Neurosci Lett 70:348-353.
8. Card JP, Moore RY (1984) The suprachiasmatic nucleus of the golden hamster: immunohistochemical analysis of cell and fiber distribution. Neuroscience 13:390-396.
9. Card JP, Moore RY (1989) Organization of lateral geniculate-hypothalamic connections in the rat. J Comp Neurol 284:135-147.
10. Conrad LCA, Leonard CM, Pfaff DW (1974) Connections of the median and dorsal raphe nuclei in the rat: an autoradiographic and degeneration study. J Comp Neurol 156:179-206.
11. DeOlmos J, Heimer L (1980) Double and triple labeling of neurons with fluorescent substances; the study of collateral pathways in the ascending raphe system. Neurosci Lett 19:7-12.
12. Edgar DM, Miller JD, Prosser RA, Dean RR, Dement WC (1993) Serotonin and the mammalian circadian system. II. Phase-shifting rat behavioral rhythms with serotonergic agonists. J Biol Rhythms 8:17-31.
13. Glass JD, Randolph WW, Ferreira SA, Rea MA, Hauser UE, Blank JL, De Vries MJ (1992) Diurnal variation in 5-hydroxyindole-acetic acid output in the suprachiasmatic region of the Siberian hamster assessed by in vivo microdialysis: evidence for nocturnal activation of serotonin release. Neuroendocrinology 56:582-590.
14. Glass JD, Hauser UE, Randolph WW, Rea MA, De Vries MJ (1993) In vivo microdialysis of 5-hydroxyindoleacetic acid and glutamic acid in the hamster suprachiasmatic nuclei. Am Zool 33:212-218.
15. 1A receptor agonists. Brain Res 638:235-242.
16. Harrington ME, Rusak B (1986) Lesions of the thalamic intergeniculate leaflet alter hamster circadian rhythms. J Biol Rhythms 1:309-325
17. Harrington ME, Rusak B (1988) Ablation of the geniculo-hypothalamic tract alters circadian activity rhythms of hamsters housed under constant light. Physiol Behav 42:183-189.
18. Harrington ME, Rusak B (1989) Photic responses of geniculo-hypothalamic tract neurons in the Syrian hamster. Vis Neurosci 2:367-375.
19. Imai H, Steindler DA, Kitai ST (1986) The organization of divergent axonal projections from the midbrain raphe nuclei in the rat. J Comp Neurol 243:363-380.
20. Jacobs BL, Azmitia EC (1992) Structure and function of the brain serotonin system. Physiol Rev 72:165-229.
21. Janik D, Mrosovsky N (1994) Intergeniculate leaflet lesions and behaviorally induced shifts of circadian rhythms. Brain Res 651:174-182.
22. 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.
23. Johnson RF, Morin LP, Moore RY (1988b) Retinohypothalamic projections in the hamster and rat demonstrated using cholera toxin. Brain Res 462:301-312.
24. Johnson RF, Moore RY, Morin LP (1989) Lateral geniculate lesions alter activity rhythms in the hamster. Brain Res Bull 22:411-422.
25. Klein DC, Moore RY, Reppert SM (1991) Suprachiasmatic nucleus: the mind's clock. New York: Oxford UP.
26. Kohler C, Chan-Palay V, Steinbusch H (1982) The distribution and origin of serotonin-containing fibers in the septal area: a combined immunohistochemical and fluorescent retrograde tracing study in the rat. J Comp Neurol 209:91-111.
27. Li Y, Jia H, Rao Z, Shi J (1990) Serotonin-, substance P- or leucine-enkephalin-containing neurons in the midbrain periaqueductal gray and nucleus raphe dorsalis send projection fibers to the central amygdaloid nucleus in the rat. Neurosci Lett 120:124-127.
28. Li Y, Takada M, Matsuzaki S, Shinonaga Y, Mizuno N (1993a) Identification of periaqueductal gray and dorsal raphe nucleus neurons projecting to both trigeminal sensory complex and forebrain structures: a fluorescent retrograde double-labeling study in the rat. Brain Res 623:267-277.
29. Li Y, Takada M, Mizuno N (1993b) Collateral projections of single neurons in the periaqueductal gray and dorsal raphe nucleus to both the trigeminal sensory complex and spinal cord in the rat. Neurosci Lett 153:153-156.
30. Lidov HGW, Molliver ME (1982a) Immunohistochemical study of the development of serotonergic neurons in the rat CNS. Brain Res Bull 9:559-604.
31. Lidov HGW, Molliver ME (1982b) An immunohistochemical study of serotonin neuron development in the rat: ascending pathways and terminals fields. Brain Res Bull 8:389-430.
32. Losier BJ, Semba K (1993) Dual projections of single cholinergic and aminergic brainstem neurons to the thalamus and basal forebrain in the rat. Brain Res 604:41-52.
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. Medanic M, Gillette MU (1992) Serotonin regulates the phase of the rat suprachiasmatic circadian pacemaker in vitro only during the subjective day. J Physiol (Lond) 450:629-642.
35. Meijer JH, Groos GA (1988) Responsiveness of suprachiasmatic and ventral lateral geniculate neurons to serotonin and imipramine: a microiontophoretic study in normal and imipramine-treated rats. Brain Res Bull 20:89-96.
36. Meyer EL, Morin LP (1995) The effects of serotonin depletion on triazolam and novel wheel induced phase shifts. Soc Neurosci Abstr 20:179
37. A/benzodiazepine receptor localization in the circadian timing system. Brain Res 531:16-24
38. Miller JD, Fuller CA (1990) The response of suprachiasmatic neurons of the rat hypothalamus to photic and serotonergic stimulation. Brain Res 515:155-162.
39. Moga MM, Moore RY (1994) An anterograde tracing study of neuronal inputs to the suprachiasmatic nucleus in the rat. Soc Neurosci Abstr 20:347.
40. Moore RY (1973) Retinohypothalamic projection in mammals: a comparative study. Brain Res 49:403-409.
41. Moore RY, Halaris AE, Jones BE (1978) Serotonin neurons of the midbrain raphe: ascending projections. J Comp Neurol 180:417-438.
42. Morin LP (1992) Serotonergic reinnervation of the hamster suprachiasmatic nucleus and intergeniculate leaflet without functional circadian rhythm recovery. Brain Res 599:98-104.
43. Morin LP (1993) Age, but not pineal status, modulates circadian periodicity of golden hamsters. J Biol Rhythms 8:189-197.
44. Morin LP, Blanchard JH (1991a) Serotonergic modulation of the hamster wheel running rhythm: response to lighting conditions and food deprivation. Brain Res 566:186-192.
45. Morin LP, Blanchard JH (1991b) Depletion of brain serotonin by 5,7-DHT modifies hamster circadian rhythm response to light. Brain Res 566:173-185.
46. Morin LP, Blanchard JH, Moore RY (1992) Intergeniculate leaflet and suprachiasmatic nucleus organization and connections in the hamster. Vis Neurosci 8:219-230.
47. Nanopoulos D, Belin MF, Maitre M, Vincendon G, Pujol JF (1982) Immunocytochemical evidence for the existence of GABAergic neurons in the nucleus raphe dorsalis: possible existence of neurons containing serotonin and GABA. Brain Res 232:375-389.
48. O'Hearn E, Battaglia G, DeSouza EB, Kuhar MJ, Molliver ME (1988) Methylenedioxyamphetamine (MDA) and methylenedioxymethamphetamine (MDMA) cause selective ablation of serotonergic axon terminals in forebrain: immunocytochemical evidence for neurotoxicity. J Neurosci 8:2788-2803.
49. Pasquier DA, Villar MJ (1982) Specific serotonergic projections to the lateral geniculate body from the lateral cell groups of the dorsal raphe nucleus. Brain Res 249:142-146.
50. Peschanski M, Besson J (1984) Diencephalic connections of the raphe nuclei of the rat brainstem: an anatomical study with reference to the somatosensory system. J Comp Neurol 224:509-534.
51. 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.
52. Pickard GE, Ralph MR, Menaker M (1987) The intergeniculate leaflet partially mediates effects of light on circadian rhythms. J Biol Rhythms 2:35-56.
53. Pierce ET, Foote WE, Hobson JA (1976) The efferent connection of the nucleus raphe dorsalis. Brain Res 107:137-144.
54. Poncet L, Denoroy L, Jouvet M (1993) Daily variations in vivo tryptophan hydroxylation and in the contents of serotonin and 5-hydroxyindoleacetic acid in discrete brain areas of the rat. J Neural Transm 92:137-150
55. Prosser RA, Miller JD, Heller HC (1990) A serotonin agonist phase shifts the circadian clock in the suprachiasmatic nuclei in vitro. Brain Res 534:336-339.
56. 2+. Brain Res 573:336-340.
57. Prosser RA, Dean RR, Edgar DM, Heller HC, Miller JD (1993) Serotonin and the mammalian circadian system. I. In vitro phase shifts by serotonergic agonists and antagonists. J Biol Rhythms 8:1-16.
58. + channel opening. Brain Res 644:67-73.
59. Prosser RA, Macdonald ES, Heller HC (1994b) c-fos mRNA in the suprachiasmatic nuclei in vitro shows a circadian rhythm and responds to a serotonergic agonist. Mol Brain Res 25:151-156.
60. Ramirez AD, Ramirez VD, Meyer DC (1987) The nature and magnitude of in vivo 5-hydroxyindoleacetic acid output from 5-hydroxytryptamine terminals is related to specific regions of the suprachiasmatic nucleus. Neuroendocrinology 46:430-438.
61. Rea MA, Glass JD, Colwell CS (1994) Serotonin modulates the photic response in the hamster suprachiasmatic nuclei. J Neurosci 14:3635-3642.
62. Selim M, Glass JD, Hauser UE, Rea MA (1993) Serotonergic inhibition of light-induced fos protein expression and extracellular glutamate in the suprachiasmatic nuclei. Brain Res 621:181-188.
63. Shibata S, Moore RY (1988) Electrical and metabolic activity of suprachiasmatic nucleus neurons in hamster hypothalamic slices. Brain Res 438:374-378.
64. Sim LJ, Joseph SA (1992) Efferent projections of the nucleus raphe magnus. Brain Res Bull 28:679-682.
65. Sim LJ, Joseph SA (1993) Dorsal raphe nucleus efferents: termination in peptidergic fields. Peptides 14:75-83.
66. Smale L, Michels KM, Moore RY, Morin LP (1990) Destruction of the hamster serotonergic system by 5,7-DHT: effects on circadian rhythm phase, entrainment and response to triazolam. Brain Res 515:9-19.
67. Steinbusch HWM (1981) Distribution of serotonin-immunoreactivity in the central nervous system of the rat-cell bodies and terminals. Neuroscience 6:557-618.
68. Stephan FK, Zucker I (1972) Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc Natl Acad Sci USA 69:1583-1586.
69. Sutin EL, Jacobowitz DM (1988) Immunocytochemical localization of peptides and other neurochemicals in the rat laterodorsal tegmental nucleus and adjacent area. J Comp Neurol 270:243-270.
70. 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.
71. 1A receptor agonists on the circadian rhythm of wheel-running activity in hamsters. Eur J Pharmacol 214:79-84.
72. Tork I (1990) Anatomy of the serotonergic system. Ann NY Acad Sci 600:9-35.
73. Turek FW (1989) Effects of stimulated physical activity on the circadian pacemaker of vertebrates. J Biol Rhythms 4:135-147.
74. van de Kar LD, Lorens SA (1979) Differential serotonergic innervation of individual hypothalamic nuclei and other forebrain regions by the dorsal and median midbrain raphe nuclei. Brain Res 162:45-54.
75. Van Reeth O, Turek FW (1989) Stimulated activity mediates phase shifts in the hamster circadian clock induced by dark pulses or benzodiazepines. Nature 339:49-51.
76. Van Reeth O, Zhang Y, Reddy A, Zee P, Turek FW (1993) Aging alters the entraining effects of an activity-inducing stimulus on the circadian clock. Brain Res 607:286-292.
77. Vaudano E, Legg CR (1992) Cerebellar connections of the ventral lateral geniculate nucleus in the rat. Anat Embryol 186:583-588.
78. Vertes RP (1984) A lectin horseradish peroxidase study of the origin of ascending fibers in the medial forebrain bundle of the rat. The lower brainstem. Neuroscience 11:651-668.
79. Vertes RP (1993) A PHA-L analysis of ascending projections of the dorsal raphe nucleus in the rat. J Comp Neurol 313:643-668.
80. Vertes RP, Martin GF (1988) Autoradiographic analysis of ascending projections from the pontine and mesencephalic reticular formation and the median raphe in the rat. J Comp Neurol 275:511-541.
81. Villar MJ, Vitale ML, Hokfelt T, Verhofstad AAJ (1988) Dorsal raphe serotoninergic branching neurons projecting both to the lateral geniculate body and superior colliculus: a combined retrograde tracing-immunohistochemical in the rat. J Comp Neurol 277:126-140.
82. Wallace JA, Lauder JM (1983) Development of the serotonergic system in the rat embryo: an immunocytochemical study. Brain Res Bull 10:459-479.
83. Waterhouse BD, Border B, Wahl L, Mihailoff GA (1993) Topographic organization of rat locus coeruleus and dorsal raphe nuclei: distribution of cells projecting to visual system structures. J Comp Neurol 336:345-361.
84. Wickland CR, Turek FW (1991) Phase-shifting effects of acute increases in activity on circadian locomotor rhythms in hamsters. Am J Physiol 261:R1109-R1117.
85. 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.
86. Ying S-W, Rusak B (1994) Effects of serotonergic agonists on firing rates of photically responsive cells in the hamster suprachiasmatic nucleus. Brain Res 651:37-46.
87. Ying S-W, Zhang D-X, Rusak B (1993) Effects of serotonin agonists and melatonin on photic responses of hamster intergeniculate leaflet neurons. Brain Res 628:8-16.
88. 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.