Single-unit activity of paraventricular nucleus neurons in response to intero- and exteroceptive stressors in conscious, freely moving rats

Brain Research

Volumn 995, Issue 1, 2004, Pages 97-108

  Watanabe, Shoichi ^a   Kunitake, Takato ^a   Kato, Kazuo ^a   Chu, Chun Ping ^a   Nakao, Hiroyuki ^a   Qiu, De Lai ^a   Kannan, Hiroshi ^a  

^a UNIVERSITY OF MIYAZAKI   (Japan)

Author keywords

Extracellular recording; Paraventricular nucleus; Phasic type neuron; Stressor

Indexed keywords

CHOLECYSTOKININ OCTAPEPTIDE; NITROPRUSSIDE SODIUM; PHENYLEPHRINE; VASOCONSTRICTOR AGENT; VASODILATOR AGENT; VASOPRESSIN; WATER;

ACTION POTENTIAL; ANIMAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR HYPOTHALAMUS; ARTERIAL PRESSURE; ARTICLE; AUTONOMIC NERVE; BLOOD PRESSURE; CELL ACTIVITY; CONSCIOUSNESS; CONTROLLED STUDY; CYTOLOGY; DRUG EFFECT; ELECTRODE; HYPOTHALAMUS HYPOPHYSIS SYSTEM; MALE; MENTAL STRESS; MOTOR ACTIVITY; MOVEMENT (PHYSIOLOGY); NERVE CELL; NERVE CELL STIMULATION; NONHUMAN; PATHOPHYSIOLOGY; PHYSIOLOGY; PRESSORECEPTOR REFLEX; PRIORITY JOURNAL; PROTEIN SECRETION; RAT; RAT STRAIN; STIMULATION; STRESS; THALAMUS MIDLINE NUCLEUS; WATER DEPRIVATION;

EID: 0344872614     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2003.09.058     Document Type: Article

References (63)

1. Anderson J.W., Smith P.M., Ferguson A.V. Subfornical organ neurons projecting to PVN: whole-cell properties. Brain Res. 921:2001;78-85.
2. Arnauld E., Vincent J.D., Dreifuss J.J. Firing patterns of hypothalamic supraoptic neurons during water deprivation in monkeys. Science. 185:1974;535-537.
3. Barney C.C., Threatte R.M., Fregly M.J. Water deprivation-induced drinking in rats: role of angiotensin II. Am. J. Physiol. 244:1983;R244-R248.
4. Beinfeld M.C., Meyer D.K., Brownstein M.J. Cholecystokinin octapeptide in the rat hypothalamo-neurohypophysial system. Nature. 288:1980;376-378.
5. Bisset G.W., Fones N.F. Antidiuretic Hormone. Recent Advances in Renal Disease. 1975;350-416 Churchill Livingstone, Edinburgh.
6. Boudaba C., Szabó K., Tasker J.G. Physiological mapping of local inhibitory inputs to the hypothalamic paraventricular nucleus. J. Neurosci. 16:1996;7151-7160.
7. Carter D.A., Lightman S.L. A role for the area postrema in mediating cholecystokinin-stimulated oxytocin secretion. Brain Res. 435:1987;327-330.
8. Cobbet P., Smithson K.G., Hatton G.I. Immunoreactivity to vasopressin- but not oxytocin-associated neurophysin antiserum in phasic neurons of rat hypothalamic paraventricular nucleus. Brain Res. 362:1986;7-16.
9. Cross B.A., Novin D., Sundsten J.W. Antidromic activation of neurons in the paraventricular nucleus by stimulation in the neural lobe of the pituitary. J. Physiol. (Lond.). 203:1969;68P-70P.
10. Daugé V., Léna I. CCK in anxiety and cognitive processes. Neurosci. Biobehav. Rev. 22:1998;815-825.
11. Diorio D., Viau V., Meaney M.J. The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. J. Neurosci. 13:1993;3839-3847.
12. Dum F.L., Brennan T.J., Nelson A.E., Robertson G.L. The role of blood osmolality and volume in regulating vasopressin secretion in the rat. J. Clin. Invest. 52:1973;3212-3219.
13. Egan B., Grekin R., Ibsen H., Osterziel K., Julius S. Role of cardiopulmonary mechanoreceptors in ADH release in normal humans. Hypertension. 6:1984;832-836.
14. Emmert M.H., Herman J.P. Differential forebrain c-fos mRNA induction by ether inhalation and novelty: evidence for distinctive stress pathways. Brain Res. 845:1999;60-67.
15. Fekete C., Wittmann G., Liposits Z., Lechan R.M. GABA-ergic innervation of thyrotropin-releasing hormone-synthesizing neurons in the hypothalamic paraventricular nucleus of the rat. Brain Res. 957:2002;251-258.
16. Feldman S., Conforti N., Itzik A., Weidenfeld J. Differential effect of amygdaloid lesions on CRF-41, ACTH, and corticosterone responses following neural stimuli. Brain Res. 658:1994;21-26.
17. Ferguson A.V., Day T.A., Renaud L.P. Subfornical organ efferents influence the excitability of neurohypophyseal and tuberoinfundibular paraventricular nucleus neurons in the rat. Neuroendocrinology. 39:1984;423-428.
18. Harris M.C. Effects of chemoreceptor and baroreceptor stimulation on the discharge of hypothalamic supraoptic neurons in rats. J. Endocrinol. 82:1979;115-125.
19. Harris M.C., Spyer K.M. Neural regulation of vasopressin-containing hypothalamic neurons and the role of vasopressin in cardiovascular function. Loewy A.D., Spyer K.M. Central Regulation of Autonomic Functions. 1990;224-246 Oxford Univ. Press, New York.
20. Herman J.P., Schäfer M.K., Young E.A., Thompson R., Douglass J., Akil H., Watson S.J. Evidence for hippocampal regulation of neuroendocrine neurons of the hypothalamo-pituitary-adrenocortical axis. J. Neurosci. 9:1989;3072-3082.
21. Honda B.K., Negoro H., Dyball R.E.J., Higuchi T., Takano S. The osmoreceptor complex in the rat: evidence for interactions between the supraoptic and other deiencephalic nuclei. J. Physiol. 431:1990;225-241.
22. Jin Q.H., Kunitake T., Ishizuka Y., Kannan H. Increase in norepinephrine but not nitric oxide metabolite levels in the hypothalamic paraventricular nucleus region in response to air-jet and swing rotation in freely moving conscious rats. Brain Res. 876:2000;205-210.
23. Kadekaro M., Summy-long J.Y., Freeman S., Harris J.S., Terrell M.L., Eisenberg H.M. Cerebral metabolic responses and vasopressin and oxytocin secretions during progressive water deprivation in rats. Am. J. Physiol. 262:1992;R310-R317.
24. Kannan H., Yamashita H. Electrophysiological study of paraventricular nucleus neurons projecting to the dorsomedial medulla and their response to baroreceptor stimulation in rats. Brain Res. 279:1983;31-40.
25. Kannan H., Osaka T., Kasai M., Okuya S., Yamashita H. Electrophysiological properties of neurons in the caudal ventrolateral medulla projecting to the paraventricular nucleus of the hypothalamus in rats. Brain Res. 376:1986;342-350.
26. Kannan H., Hayashida Y., Yamashita H. Increase in sympathetic outflow by paraventricular nucleus stimulation in awake rats. Am. J. Physiol. 256:1989;R1325-R1330.
27. Kasai M., Osaka T., Inenaga K., Kannan H., Yamashita H. γ-Aminobutyric acid antagonist blocks baroreceptor-activated inhibition of neurosecretory cells in the hypothalamic paraventricular nucleus of rats. Neurosci. Lett. 81:1987;319-324.
28. Kõks S., Männistö P.T., Bourin M., Shlik J., Vasar V., Vasar E. Cholecystokinin-induced anxiety in rats: relevance of pre-experimental stress and seasonal variations. J. Psychiatry Neurosci. 25:2000;33-42.
29. Lawrence D., Pittman Q.J. Response of rat paraventricular neurones with central projections to suckling, haemorrhage, or osmotic stimuli. Brain Res. 341:1985;176-183.
30. Merchenthaler I., Hynes M.A., Vigh S., Schally A.V., Petrusz P. Corticotropin-releasing factor (CRF): origin and course of afferent pathways to the median eminence (ME) of the rat hypothalamus. Neuroendocrinology. 39:1984;296-306.
31. Mezey E., Reisine T.D., Skirboll L., Beinfeld M., Kiss J.Z. Cholecystokinin in the medial parvocellular subdivision of the paraventricular nucleus. Co-existence with corticotropin-releasing hormone. Ann. N. Y. Acad. Sci. 448:1985;152-156.
32. Miselis R.R. The efferent projections of the subfornical organ of the rat: a circumventricular organ within a neural network subserving water balance. Brain Res. 230:1981;1-23.
33. Morin S.M., Stotz-Potter E.H., DiMicco J.A. Injection of muscimol in dorsomedial hypothalamus and stress-induced Fos expression in paraventricular nucleus. Am. J. Physiol. 280:2001;R1276-R1284.
34. Oldfield B.J., Bicknell R.J., McAllen R.M., Weisinger R.S., McKinley M.J. Intravenous hypertonic saline induces Fos immunoreactivity in neurons throughout the lamina terminals. Brain Res. 561:1991;151-156.
35. Onaka T., Hamamura M., Yagi K. Suppression of vasopressin secretion by classically conditioned stimuli in rats. Jpn. J. Physiol. 36:1986;1261-1266.
36. Osaka T., Kannan H., Kasai M., Inenaga K., Yamashita H. Osmotic response of rat paraventricular neurons by pressure ejection method. Brain Res. Bull. 24:1990;493-497.
37. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates. 2nd ed. 1986;Academic Press, New York.
38. Poulain D.A., Wakerley J.B. Electrophysiology of hypothalamic magnocellular neurons secreting oxytocin and vasopressin. Neurosci. 7:1982;773-808.
39. Poulain D.A., Wakerley J.B., Dyball R.E.J. Electrophysiological differentiation of oxytocin- and vasopressin-secreting neurons. Proc. R. Soc. B. 196:1977;367-384.
40. Sagar S.M., Sharp F.R., Curran T. Expression of c-fos protein in brain: metabolic mapping at the cellular level. Science. 240:1988;1328-1331.
41. Sawchenko P.E., Swanson L.W., Vale W.W. Corticotropin-releasing factor: co-expression within distinct subsets of oxytocin-, vasopressin-, and neurotensin-immunoreactive neurons in the hypothalamus of the male rat. J. Neurosci. 4:1984;1118-1129.
42. Sawchenko P.E., Li H.Y., Ericsson A. Circuits and mechanisms governing hypothalamic responses to stress: a tale of two paradigms. Prog. Brain Res. 122:2000;61-78.
43. Shimokawa A., Jin Q.H., Ishizuka Y., Kunitake T., Takasaki M., Kannan H. Effects of anesthetics on norepinephrine release in the hypothalamic paraventricular nucleus region of awake rats. Neurosci. Lett. 244:1998;21-24.
44. Sladek C.D., Olschowka J.A. Dehydration induces Fos, but not increased vasopressin mRNA in the supraoptic nucleus of aged rats. Brain Res. 652:1994;207-215.
45. Smith G.P., Jerome C., Cushin B.J., Eterno R., Simansky K.J. Abdominal vagotomy blocks the satiety effect of cholecystokinin in the rat. Science. 213:1981;1036-1037.
46. Stornetta R.L., Guyenet P.G., McCarty R.C. Autonomic nervous system control of heart rate during baroreceptor activation in conscious and anesthetized rats. J. Auton. Nerv. Syst. 20:1987;121-127.
47. Stotz-Potter E.H., Morin S.M., DiMicco J.A. Effect of microinjection of muscimol into the dorsomedial or paraventricular hypothalamic nucleus on air stress-induced neuroendocrine and cardiovascular changes in rats. Brain Res. 742:1996;219-224.
48. Summerlee A.J.S., Praisley A.C., O'Byrne K.T., Fairhall K.M., Robinson I.C.A.F., Fletcher J. Aspects of the neuronal and endocrine components of reflex milk ejection in conscious rabbit. J. Endocrinol. 108:1984;143-149.
49. Swanson L.W., Sawchenko P.E. Paraventricular nucleus: a site for the integration of neuroendocrine and autonomic mechanisms. Neuroendocrinology. 31:1980;410-417.
50. Swanson L.W., Sawchenko P.E., Rind R.W. Regulation of multiple peptides in CRF parvocellular neurosecretory neurons: implications for the stress response. Prog. Brain Res. 68:1986;169-190.
51. Ter Horst G.J., Luiten P.G. Phaseolus vulgaris leuco-agglutinin tracing of intrahypothalamic connections of the lateral, ventromedial, dorsomedial, and paraventricular hypothalamic nuclei in the rat. Brain Res. Bull. 18:1987;191-203.
52. Thrivikraman K.V., Nemeroff C.B., Plotsky P.M. Sensitivity to glucocorticoid-mediated fast-feedback regulation of the hypothalamic-pituitary- adrenal axis is dependent upon stressor-specific neurocircuitry. Brain Res. 870:2000;87-101.
53. Ueta Y., Kannan H., Higuchi T., Negoro H., Yamashita H. CCK-8 excites oxytocin-secreting neurons in the paraventricular nucleus in rats - possible involvement of noradrenergic pathway. Brain Res. Bull. 32:1993;453-459.
54. Verbalis J.G., McCann M.J., McHale C.M., Stricker E.M. Oxytocin secretion in response to cholecystokinin and food: differential of nausea from satiety. Science. 232:1986;1417-1419.
55. Verbalis J.G., Stricker E.M., Robinson A.G., Hoffman G.E. Cholecystokinin activates c-fos expression in hypothalamic oxytocin and corticotropin-releasing hormone neurons. J. Neuroendocrinol. 3:1991;205-213.
56. Vincent J.D., Arnauld E., Bioulac B. Activity of osmosensitive single cells in the hypothalamus of the behaving monkey during drinking. Brain Res. 44:1972;371-384.
57. Wakerley J.B., Lincoln D.W. Phasic discharge of antidromically identified units in the paraventricular nucleus of the hypothalamus. Brain Res. 25:1971;192-194.
58. Wakerley J.B., Lincoln D.W. The milk-ejection reflex of the rat: a 20- to 40-fold acceleration in the firing of paraventricular neurones during oxytocin release. J. Endocrinol. 57:1973;477-493.
59. Wakerley J.B., Poulain D.A., Dyball R.E.J., Cross B.A. Activity of phasic neurosecretory cells during hemorrhage. Nature. 258:1975;82-84.
60. Yang Z., Coote J.H. The influence of the paraventricular nucleus on baroreceptor-dependent caudal ventrolateral medullary neurons of the rat. Pflugers Arch. 438:1999;47-52.
61. Zhang X., Fogel R., Renehan W.E. Stimulation of the paraventricular nucleus modulates the activity of gut-sensitive neurons in the vagal complex. Am. J. Physiol. 277:1999;G79-G90.
62. Zhu W., Umegaki H., Yoshimura J., Tamaya N., Suzuki Y., Miura H., Iguchi A. The elevation of plasma adrenocorticotrophic hormone and expression of c-Fos in hypothalamic paraventricular nucleus by microinjection of neostigmine into the hippocampus in rats: comparison with acute stress responses. Brain Res. 892:2001;391-395.
63. Zimpfer M., Manders W.T., Barger A.C., Vatner S.F. Pentobarbital alters compensatory neural and humoral mechanisms in response to hemorrhage. Am. J. Physiol. 243:1982;H713-H721.