The suprachiasmatic nucleus balances sympathetic and parasympathetic output to peripheral organs through separate preautonomic neurons

Journal of Comparative Neurology

Volumn 464, Issue 1, 2003, Pages 36-48

  Buijs, Ruud M ^a   La Fleur, Susanne E ^a   Wortel, Joke ^a   Van Heyningen, Caroline ^a   Zuiddam, Laura ^a   Mettenleiter, Thomas C ^b   Kalsbeek, Andries ^a   Nagai, Katsuya ^c   Niijima, Akira ^d  

^a NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^b FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^c OSAKA UNIVERSITY   (Japan)

^d NIIGATA UNIVERSITY   (Japan)

Author keywords

Autonomic; Brainstem; Circadian rhythm; Paraventricular nucleus; Spinal cord; Vasopressin

Indexed keywords

FLUOROGOLD;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTONOMIC DENERVATION; AUTONOMIC NERVOUS SYSTEM; BRAIN STEM; CELL SEPARATION; CONTROLLED STUDY; ELECTRIC ACTIVITY; HYPOTHALAMUS; LIVER DISEASE; NERVE CELL; NERVE DEGENERATION; NEUROANATOMY; NONHUMAN; PARASYMPATHETIC NERVE; PRIORITY JOURNAL; PSEUDORABIES HERPETOVIRUS; RAT; SIGNAL TRANSDUCTION; SLEEP WAKING CYCLE; SUPRACHIASMATIC NUCLEUS; SYMPATHETIC NERVE; VAGUS NERVE;

ADRENAL GLANDS; ANIMALS; AUTONOMIC FIBERS, PREGANGLIONIC; BETA-GALACTOSIDASE; CELL COUNT; FLUORESCENT DYES; GREEN FLUORESCENT PROTEINS; HERPESVIRUS 1, SUID; LIVER; LUMINESCENT PROTEINS; MALE; MICROSCOPY, CONFOCAL; MOTOR NEURONS; NEURAL PATHWAYS; PARASYMPATHECTOMY; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; RATS; RATS, WISTAR; SOLITARY NUCLEUS; SPINAL CORD; STILBAMIDINES; SUPRACHIASMATIC NUCLEUS; SYMPATHECTOMY;

EID: 0037978797     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10765     Document Type: Article

References (51)

1. Bartness TJ, Bamshad M. 1998. Innervation of mammalian white adipose tissue: implications for the regulation of total body fat. Am J Physiol 275:R1399-R1411.
2. Buijs RM, Kalsbeek A. 2001. Hypothalamic integration of central and peripheral clocks. Nat Rev Neurosci 2:521-526.
3. Buijs RM, Wortel J, Hou YX. 1995. Colocalization of gamma-aminobutyric acid with vasopressin, vasoactive intestinal peptide, and somatostatin in the rat suprachiasmatic nucleus. J Comp Neurol 358:343-352.
4. Buijs RM, Wortel J, Van Heerikhuize JJ, Feenstra MG, Ter Horst GJ, Romijn HJ, Kalsbeek A. 1999. Anatomical and functional demonstration of a multisynaptic suprachiasmatic nucleus adrenal (cortex) pathway. Eur J Neurosci 11:1535-1544.
5. Buijs RM, Chun SJ, Niijima A, Romijn HJ, Nagai K. 2001. Parasympathetic and sympathetic control of the pancreas: a role for the suprachiasmatic nucleus and other hypothalamic centers that are involved in the regulation of food intake. J Comp Neurol 431:405-423.
6. Cannon WB, Rosenblueth A. 1933. Studies on activities in endocrine organs. XXIX. Am J Physiol 104:557-574.
7. Card JP. 1995. Pseudorabies virus replication and assembly in the rodent central nervous system. In: Kaplitt MG and Loewy AD, editors. Viral vectors: gene therapy and neuroscience applications. San Diego: Academic Press. p 319-347.
8. Card JP, Rinaman L, Lynn RB, Lee BH, Meade RP, Miselis RR, Enquist LW. 1993. Pseudorabies virus infection of the rat central nervous system: ultrastructural characterization of viral replication, transport, and pathogenesis. J Neurosci 13:2515-2539.
9. Castel M, Morris JF. 2000. Morphological heterogeneity of the GABAergic network in the suprachiasmatic nucleus, the brain's circadian pacemaker. J Anat 196:1-13.
10. Choi S, Wong LS, Yamat C, Dallman MF. 1998. Hypothalamic ventromedial nuclei amplify circadian rhythms: do they contain a food-entrained endogenous oscillator? J Neurosci 18:3843-3852.
11. Craig AD. 2002. Opinion: how do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci 3:655-666.
12. 3H]D-aspartate autoradiography. Neuroscience 2000;101:637-655.
13. Cui LN, Coderre E, Renaud LP. 2002. Glutamate and GABA mediate suprachiasmatic nucleus inputs to spinal-projecting paraventricular neurons. Am J Physiol Regul Integr Comp Physiol 281:R1283-R1290.
14. Damasio AR. 1998. Emotion in the perspective of an integrated nervous system. Brain Res Brain Res Rev 26:83-86.
15. Darlington DN, Miyamoto M, Keil LC, Dallman MF. 1989. Paraventricular stimulation with glutamate elicits bradycardia and pituitary responses. Am J Physiol 256:R112-R119.
16. Diz DI, Jacobowitz DM. 1984. Cardiovascular effects of discrete intrahypothalamic and preoptic injections of bradykinin. Brain Res Bull 12:409-417.
17. Elmquist JK, Maratos Flier E, Saper CB, Flier JS. 1998. Unraveling the central nervous system pathways underlying responses to leptin. Nat Neurosci 1:445-450.
18. Elmquist JK, Elias CF, Saper CB. 1999. From lesions to leptin: hypothalamic control of food intake and body weight. Neuron 22:221-232.
19. Enquist LW. 1994. Infection of the mammalian nervous system by pseudorabies virus (PRV). Semin Virol 5:221-231.
20. Gerendai I, Toth IE, Kocsis K, Boldogkoi Z, Medveczky I, Halasz B. 2002. Transneuronal labelling of nerve cells in the CNS of female rat from the mammary gland by viral tracing technique. Neuroscience 108:103-118.
21. Guan JL, Uehara K, Lu S, Wang QP, Funahashi H, Sakurai T, Yanagizawa M, Shioda S. 2002. Reciprocal synaptic relationships between orexin- and melanin-concentrating hormone-containing neurons in the rat lateral hypothalamus: a novel circuit implicated in feeding regulation. Int J Obes Relat Metab Disord 26:1523-1532.
22. Hamada T, Lesauter J, Venuti JM, Silver R. 2001. Expression of Period genes: rhythmic and nonrhythmic compartments of the suprachiasmatic nucleus pacemaker. J Neurosci 21:7742-7750.
23. Hermes ML, Ruijter JM, Klop A, Buijs RM, Renaud LP. 2000. Vasopressin increases GABAergic inhibition of rat hypothalamic paraventricular nucleus neurons in vitro. J Neurophysiol 83:705-711.
24. Hermes MLHJ, Coderre EM, Buijs RM, Renaud LP. 1996. GABA and glutamate mediate rapid neurotransmission from suprachiasmatic nucleus to hypothalamic paraventricular nucleus in rat. J Physiol Lond 496:749-757.
25. Holstege G. 1987. Some anatomical observations on the projections from the hypothalamus to brainstem and spinal cord: an HRP and autoradiographic tracing study in the cat. J Comp Neurol 260:98-126.
26. Kalsbeek A, Vanheerikhuize JJ, Wortel J, Buijs RM. 1996. A diurnal rhythm of stimulatory input to the hypothalamo-pituitary-adrenal system as revealed by timed intrahypothalamic administration of the vasopressin V-1 antagonist. J Neurosci 16:5555-5565.
27. Kalsbeek A, Fliers E, Franke AN, Wortel J, and Buijs RM. 2000. Functional connections between the suprachiasmatic nucleus and the thyroid gland as revealed by lesioning and viral tracing techniques in the rat. Endocrinology 141:3832-3841.
28. Kannan H, Niijima A, Yamashita H. 1987. Inhibition of renal sympathetic nerve activity by electrical stimulation of the hypothalamic paraventricular nucleus in anesthetized rats. J Auton Nerv Syst 21:83-86.
29. Kannan H, Hayashida Y, Yamashita H. 1989. Increase in sympathetic outflow by paraventricular nucleus stimulation in awake rats. Am J Physiol 256:R1325-R1330.
30. la Fleur SE, Kalsbeek A, Wortel J, Fekkes ML, Buijs RM. 2001. A daily rhythm in glucose tolerance: a role for the suprachiasmatic nucleus. Diabetes 50:1237-1243.
31. LeDoux J. 1998. Fear and the brain: where have we been, and where are we going? [see comments]. Biol Psychiatry 44:1229-1238.
32. Lesauter J, Silver R. 1999. Localization of a suprachiasmatic nucleus subregion regulating locomotor rhythmicity. J Neurosci 19:5574-5585.
33. Menetrey D, Basbaum AI. 1987. Spinal and trigeminal projections to the nucleus of the solitary tract: a possible substrate for somatovisceral and viscerovisceral reflex activation. J Comp Neurol 255:439-450.
34. Mtui EP, Anwar M, Gomez R, Reis DJ, Ruggiero DA. 1993. Projections from the nucleus tractus solitarii to the spinal cord. J Comp Neurol 337:231-252.
35. Norgren R. 1978. Projections from the nucleus of the solitary tract in the rat. Neuroscience 3:207-218.
36. Palm IF, Van Der Beek EM, Swarts HJ, Vliet Jv, Wiegant VM, Buijs RM, Kalsbeek A. 2001. Control of the estradiol-induced prolactin surge by the suprachiasmatic nucleus. Endocrinology 142:2296-302.
37. Pickard GE, Smeraski CA, Tomlinson CC, Banfield BW, Kaufman J, Wilcox CL, Enquist LW, Sollars PJ. 2002. Intravitreal injection of the attenuated pseudorabies virus PRV Bartha results in infection of the hamster suprachiasmatic nucleus only by retrograde transsynaptic transport via autonomic circuits. J Neurosci 22:2701-2710.
38. Romijn HJ, Sluiter AA, Wortel J, van Uum JF, Buijs RM. 1998. Immunocytochemical evidence for a diurnal rhythm of neurons showing colocalization of VIP with GRP in the rat suprachiasmatic nucleus. J Comp Neurol 391:397-405.
39. Sakurada S, Shido O, Sugimoto N, Hiratsuka Y, Yoda T, Kanosue K. 2000. Autonomic and behavioural thermoregulation in starved rats. J Physiol 526:417-424.
40. Saper CB, Loewy AD, Swanson LW, Cowan WM. 1976. Direct hypothalamo-autonomic connections. Brain Res 117:305-12.
41. Sawchenko PE, Swanson LW. 1982. Immunohistochemical identification of neurons in the paraventricular nucleus of the hypothalamus that project to the medulla or to the spinal cord in the rat. J Comp Neurol 205:260-272.
42. Strack AM, Sawyer WB, Marubio LM, Loewy AD. 1988. Spinal origin of sympathetic preganglionic neurons in the rat. Brain Res 455:187-191.
43. Strack AM, Loewy AD. 1990. Pseudorabies virus: a highly specific transneuronal cell body marker in the sympathetic nervous system. J Neurosci 10:2139-2147.
44. Swanson LW. 1987. The hypothalamus. In: Björklund A, Hökfelt T, Swanson LW, editors. Integrated systems of the CNS, Part I. Hypothalamus, hippocampus, amygdala, retina. Amsterdam: Elsevier. p 1-124.
45. Swanson LW, Kuypers HGJM. 1980. The paraventricular nucleus of the hypothalamus: cytoarchitectonic subdivisions and organization of projections to the pituitary, dorsal vagal complex, and spinal cord as demonstrated by retrograde fluorescence double-labeling methods. J Comp Neurol 194:555-570.
46. Swanson LW, Sawchenko PE. 1980. Paraventricular nucleus: a site for the integration of neuroendocrine and autonomic mechanisms. Neuroendocrinology 31:410-417.
47. Ter Horst GJ, De Boer P, Luiten PGM, Van Willigen JD. 1989. Ascending projections from the solitary tract nucleus to the hypothalamus. A Phaseolus vulgaris lectin tracing study in the rat. Neuroscience 31:785-797.
48. Tucker DC, Saper CB. 1985. Specificity of spinal projections from hypothalamic and brainstem areas which innervate sympathetic preganglionic neurons. Brain Res 360:159-64.
49. Ueyama T, Krout KE, Nguyen XV, Karpitskiy V, Kollert A, Mettenleiter TC, Loewy AD. 1999. Suprachiasmatic nucleus: a central autonomic clock. Nat Neurosci 2:1051-1053.
50. Van Den Pol AN. 1982. The magnocellular and parvocellular paraventricular nucleus of rat: intrinsic organization. J Comp Neurol 206:317-345.
51. Zhang YH, Lu J, Elmquist JK, Saper CB. 2000. Lipopolysaccharide activates specific populations of hypothalamic and brainstem neurons that project to the spinal cord. J Neurosci 20:6578-6586.