Involvement of the brain oxytocin system in stress coping: Interactions with the hypothalamo-pituitary-adrenal axis

Progress in Brain Research

Volumn 139, Issue , 2002, Pages 147-162

  Neumann, Inga D ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

ACTH; Anxiety; Maternal behavior; Oxytocin receptor antagonist; Retrodialysis

Indexed keywords

GLUCOCORTICOID; OXYTOCIN;

BRAIN LEVEL; BRAIN REGION; CONFERENCE PAPER; COPING BEHAVIOR; FEMALE; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS; MALE; NEUROHYPOPHYSIS; NONHUMAN; OXYTOCIN RELEASE; PRIORITY JOURNAL; RAT; STRESS; SUPRAOPTIC NUCLEUS; THALAMUS MIDLINE NUCLEUS;

EID: 0036454227     PISSN: 00796123     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0079-6123(02)39014-9     Document Type: Conference Paper

References (89)

1. Abel, E.L. (1994) A further analysis of physiological changes in rats in the forced swim test. Physiol. Behav., 56: 795-800.
2. Akana, S.F. and Dallman, M.F. (1997) Chronic cold in adrenalectomized, corticosterone (B)-treated rats: Facilitated corticotropin responses to acute restraint emerge as B increases. Endocrinology, 138: 3249-3258.
3. Argiolas, A. and Gessa, G.L. (1991) Central functions of oxytocin. Neurosci. Biobehav. Rev., 15: 217-231.
4. Arletti, R. and Bertolini, A. (1987) Oxytocin acts as an antidepressant in two animal models of depression. Life Sci., 41: 1725-1730.
5. Bale, T.L., Davis, A.M., Auger, A.P., Dorsa, D.M. and McCarthy, M.M. (2001) CNS region-specific oxytocin receptor expression: Importance in regulation of anxiety and sex behavior. J. Neurosci., 21: 2546-2552.
6. 3H]Oxytocin binding sites in the rat brain demonstrated by quantitative light microscopic autoradiography. Eur. J. Pharmacol., 102: 365-367.
7. Carter, D.A. and Lightman, S.L. (1987) Oxytocin responses to stress in lactating and hyperprolactinaemic rats. Neuroendocrinology, 46: 532-537.
8. Consiglio, A.R. and Lucion, A.B. (1996) Lesion of hypothalamic paraventricular nucleus and maternal aggressive behavior in female rats. Physiol. Behav., 59: 591-596.
9. Demotes-Mainard, J., Chauveau, J., Rodriguez, F., Vincent, J.D. and Poulain, D.A. (1986) Septal release of vasopressin in response to osmotic, hypovolemic and electrical stimulation in rats. Brain Res., 381: 314-321.
10. Dunn, F.L., Brennan, T.J., Nelson, A.E. and Robertson, G.L. (1973) The role of blood osmolality and volume in regulating vasopressin secretion in the rat. J. Clin. Invest., 52: 3212-3219.
11. Ebner, K., Wotjak, C.T., Landgraf, R. and Engelmann, M. (2000) A single social defeat experience selectively stimulates the release of oxytocin, but not vasopressin, within the septal brain area of male rats. J. Neuroendocrinol., 872: 87-92.
12. Ehlers, C.L., Reed, T.K. and Henriksen, S.J. (1986) Effects of corticotropin-releasing factor and growth hormone-releasing factor on sleep and activity in rats. Neuroendocrinology, 42: 467-474.
13. Engelmann, M., Wotjak, C.T., Ludwig, M., Neumann, I.D. and Landgraf, R. (1996) Behavioral consequences of intracerebral vasopressin and oxytocin: Focus on learning and memory. Neurosci. Biobehav. Rev., 20: 341-358.
14. Engelmann, M., Ebner, K., Wotjak, C.T. and Landgraf, R. (1998) Endogenous oxytocin is involved in short-term olfactory memory in female rats. Behav. Brain Res., 19: 89-94.
15. Engelmann, M., Ebner, K., Landgraf, R., Holsboer, F. and Wotjak, C.T. (1999) Emotional stress triggers intrahypothalamic but not peripheral release of oxytocin in male rats. J. Neuroendocrinol., 11: 867-872.
16. Engelmann, M., Ludwig, M., Singewald, N., Ebner, K., Sabatier, N., Lubec, G., Landgraf, R. and Wotjak, C.T. (2001) Taurine modulates the secretory activity of vasopressinergic neurons in conscious rats. Eur. J. Neurosci., 14: 1047-1055.
17. Fahrbach, S.E., Morrell, J.I. and Pfaff, D.W. (1985) Possible role for endogenous oxytocin in estrogen-facilitated maternal behavior in rats. Neuroendocrinology, 40: 526-532.
18. Feldman, S. and Weidenfeld, J. (1995) Neural mechanisms involved in the corticosteroid feedback effects on the hypothalamo-pituitary-adrenocortical axis. Prog. Neurobiol., 45: 129-141.
19. Feldman, S., Conforti, N. and Weidenfeld, J. (1995) Limbic pathways and hypothalamic neurotransmitters mediating adrenocortical responses to neural stimuli. Neurosci. Biobehav. Rev., 19: 235-240
20. Ferris, C.F., Foote, K.B., Meltser, H.M., Plenby, M.G., Smith, K.L. and Insel, T.R. (1992) Oxytocin in the amygdala facilitates maternal aggression. Ann. N.Y. Acad. Sci., 652: 456-457.
21. Freund-Mercier, M.J., Stoeckel, E., Palacios, J.M., Pazos, A., Reichhart, J.M., Porte, A. and Richard, P. (1987) Pharmacological characteristics and anatomical distribution of [3H]oxytocin-binding sites in the Wistar rat brain studied by autoradiography. Neuroscience, 20: 599-614.
22. Haller, I., Barna, L. and Baranyi, M. (1995) Hormonal and metabolic responses during psychosocial stimulation in aggressive and nonaggressive rats. Psychoneuroendocrinology, 20: 65-74
23. Hard, E. and Hansen, S. (1984) Reduced fearfulness in the lactating rat. Physiol. Behav., 35: 641-643.
24. Hashiguchi, H., Ye, S.H., Morris, M. and Alexander, N. (1997) Single and repeated environmental stress: Effect on plasma oxytocin, corticosterone, catecholamines, and behavior. Physiol. Behav., 61: 731-736.
25. Heinrichs, M., Meinlschmidt, G., Neumann, I., Wagner, S., Kirschbaum, C., Ehlert, U. and Hellhammer, D.H. (2001) Effects of suckling on hypothalamic-pituitary-adrenal axis responses to psychosocial stress in postpartum lactating women. J. Clin. Metab., 86: 4798-4804.
26. Herman, J.P. (1995) In situ hybridisation analysis of vasopressin gene transcription in the paraventricular and supraoptic nuclei of the rat: Regulation by stress and glucocorticoids. J. Comp. Neurol., 363: 15-27.
27. Herman, J.P. and Cullinan, W.E. (1997) Neurocircuitry of stress: Central control of the hypothalamo-pituitary-adrenocortical axia. Trends Neurosci., 20: 78-83.
28. Higuchi, T., Honda, S., Takano, S. and Negoro, H. (1988) Reduced oxytocin response to osmotic stimulus and immobilisation stress in lactating rats. J. Endocrinol., 116: 225-230.
29. Hisano, S., Li, S., Kagotani, Y. and Daikoku, S. (1992) Synaptic associations between oxytocin-containing magnocellular neurons and neurons containing corticotropin-releasing factor in the rat magnocellular paraventricular nucleus. Brain Res., 576: 311-318.
30. Hussy, N. (2002) Glial cells in the hypothalamo-neurohypophysial system: Key elements of the regulation of neuronal electrical and secretory activity. In: D. Poulain, S. Oliet and D. Theodosis (Eds.), Vasopressin and Oxytocin: From Genes to Clinical Application. Progress in Brain Research, Vol. 139. Elsevier Science, Amsterdam, pp. 95-112.
31. Insel, T.R. (1990) Regional changes in brain OT receptors postpartum: Time-course and relationship to maternal behaviour. J. Neuroendocrinol., 2: 539-545.
32. Insel, T.R. (1992) Oxytocin - A neuropeptide for affiliation: Evidence from behavioral, receptor autoradiographic, and comparative studies. Psychoneuroendocrinology, 17: 3-35.
33. Insel, T.R. and Hulihan, T.J. (1995) A gender-specific mechanism for pair bonding: Oxytocin and partner preference formation in monogamous voles. Behav. Neurosci., 109: 782-789.
34. Kasting, N.W. (1988) Simultaneous and independent release of vasopressin and oxytocin in the rat. Can. J. Physiol. Pharmacol., 66: 22-26.
35. Kendrick, K.M., Keverne, E.B., Chapman, C. and Baldwin, B.A. (1988) Intracranial dialysis measurement of oxytocin, monoamines and uric acid release from the olfactory bulb and substantia nigra of sheep during parturition, suckling, separation from lambs and eating. Brain Res., 439: 1-10.
36. King, M.G., Brown, R. and Kusnecov, A. (1985) An increase in startle response in rats administered oxytocin. Peptides, 6: 567-568.
37. Kovacs, K.J. (1998) Functional neuroanatomy of the parvocellular vasopressinergic system: Transcriptional responses to stress and glucocorticoid feedback. Prog. Brain Res., 119: 31-43.
38. Lambert, R.C., Moos, F. and Richard, P. (1993) Action of endogenous oxytocin within the paraventricular and supraoptic nuclei: A powerful link in the regulation of the bursting pattern of oxytocin neurons during the milk ejection reflex in rats. Neuroscience, 57: 1027-1038.
39. Landgraf, R. (1995) Intracerebrally released vasopressin and oxytocin: Measurement, mechanisms and behavioural consequences. J. Neuroendocrinol., 7: 243-253.
40. Landgraf, R., Neumann, I. and Schwarzberg, H. (1988) Central and peripheral release of vasopressin and oxytocin in the conscious rat after osmotic stimulation. Brain Res., 457: 219-225.
41. Landgraf, R., Neumann, I. and Pittman, Q.J. (1991) Septal and hippocampal release of vasopressin and oxytocin during late pregnancy and parturition in the rat. Neuroendocrinology, 54: 378-383.
42. Lang, R.E., Heil, J.W.E., Ganten, D., Hermann, K., Unger, T. and Rascher, W. (1983) Oxytocin unlike vasopressin is a stress hormone in the rat. Neuroendocrinology, 37: 314-316.
43. Legros, J.J. and Ansseau, M. (1992) Neurohypophyseal peptides and psychopathology. In: D.F. Swaab, M.A. Hofman, M. Mirmiran, R. Ravid and F.W. van Leeuwen (Eds.), Progress in Brain Research, Vol. 93, Elsevier, Amsterdam, pp. 455-461.
44. Leshner, A.I. and Politch, J.A. (1979) Hormonal control of submissiveness in mice: Irrelevance of the androgens and relevance of the pituitary-adrenal hormones. Physiol. Behav., 22: 531-534.
45. Lightman, S.L. (1992) Alterations in hypothalamic-pituitary responsiveness during lactation. In: C. Pedersen et al. (Eds.), Oxytocin in Maternal, Sexual and Social Behaviors. Ann. N.Y. Acad. Sci., 652: 340-346.
46. Lightman, S.L. and Young III, W.S. (1989) Lactation inhibits stress-mediated secretion of corticosterone and oxytocin and hypothalamic accumulation of corticotropin-releasing factor and enkephalin messenger ribonucleic acids. Endocrinology, 124: 2358-2364.
47. Lucki, I. (1997) The forced swim test as a model for core and component behavioral effects of antidepressant drugs. Behav. Pharmacol., 8: 523-532.
48. Ludwig, M. (1998) Dendritic release of vasopressin and oxytocin. J. Neuroendocrinol., 10: 881-895.
49. McCarthy, M.M., Chung, S.K., Ogawa, S., Kow, L.M. and Pfaff, D.W. (1991) Behavioral effects of oxytocin: Is there a unifying principle. In: S. Jard and R. Jamison (Eds.), Vasopressin, Colloque INSERM, Vol. 208, John Libbey Eurotext, pp. 195-212.
50. McCarthy, M.M., McDonald, C.H., Brooks, P.J. and Goldmann, D. (1996) An anxiolytic action of oxytocin is enhanced by estrogen in the mouse. Physiol. Behav., 60: 1209-1215.
51. Moos, F., Poulain, D.A., Rodriguez, F., Guerné, Y., Vincent, J.-D. and Richard, P. (1989) Release of oxytocin within the supraoptic nucleus during the milk ejection reflex in rats. Exp. Brain Res., 76: 593-602.
52. Moos, F. and Richard, P. (1989) Paraventricular and supraoptic bursting oxytocin cells in rat are locally regulated by oxytocin and functionally related. J. Physiol., 408: 1-18.
53. Moyer, K.E. (1968) Kinds of aggression and their physiological basis. Commun. Behav. Biol., 2: 65-87.
54. Neumann, I.D. (2001) Alterations in behavioral and neuroendocrine stress coping strategies in pregnant, parturient and lactating rats. In: Progress in Brain Research, Vol. 133. Elsevier Science, Amsterdam, pp. 143-152.
55. Neumann, I. and Landgraf, R. (1989) Septal and hippocampal release of oxytocin, but not vasopressin, in the conscious lactating rat during suckling. J. Neuroendocrinol., 1: 305-308.
56. Neumann, I., Russell, J.A. and Landgraf, R. (1993a) Oxytocin and vasopressin release within the supraoptic and paraventricular nuclei of pregnant, parturient and lactating rats: A microdialysis study. Neuroscience, 53: 65-75.
57. Neumann, I., Ludwig, M., Engelmann, M., Pittman, Q.J. and Landgraf, R. (1993b) Simultaneous microdialysis in blood and brain: Oxytocin and vasopressin release in response to central and peripheral osmotic stimulation and suckling in the rat. Neuroendocrinology, 58: 637-645.
58. Neumann, I., Koehler, E., Landgraf, R. and Summy-Long, J.Y. (1994) An oxytocin receptor antagonist infused into the supraoptic nucleus attenuates intranuclear and peripheral release of oxytocin during suckling in conscious rats. Endocrinology, 134: 141-148.
59. Neumann, I.D., Johnstone, H.A., Hatzinger, M., Liebsch, G., Shipston, M., Russell, J.A., Landgraf, R. and Douglas, A.J. (1998) Attenuated neuroendocrine responses to emotional and physical stressors in pregnant rats involve adenohypophyseal changes. J. Physiol., 508: 289-300.
60. Neumann, I.D., Wigger, A., Torner, L., Holsboer, F. and Landgraf, R. (2000a) Brain oxytocin inhibits basal and stress-induced activity of the hypothalamo-pituitary-adrenal axis in male and female rats: Partial action within the paraventricular nucleus. J. Neuroendocrinol., 12: 235-243.
61. Neumann, I., Torner, L. and Wigger, A. (2000b) Brain oxytocin: Differential inhibition of neuroendocrine stress responses and anxiety-related behaviour in virgin, pregnant and lactating rats. Neuroscience, 95: 567-575.
62. Neumann, I.D., Krömer, S.A., Toschi, N. and Ebner, K. (2000c) Brain oxytocin inhibits the (re)activity of the hypothalamopituitary-adrenal axis in male rats: Involvement of hypothalamic and limbic brain regions. Regul. Pept., 1: 31-38.
63. Neumann, I., Toschi, N., Ohl, F., Torner, L. and Kroemer, S. (2001) Maternal defence as an emotional stressor in female rats: Correlation of neuroendocrine and behavioural parameters and involvement of brain oxytocin. Eur. J. Neurosci., 13: 1016-1024.
64. Nishioka, T., Anselmofranci, J.A., Li, P., Callahan, M.F. and Morris, M. (1998) Stress increases oxytocin release within the hypothalamic paraventricular nucleus. Brain Res., 781: 57-61.
65. Opp, M.R. (1995) Corticotropin-releasing hormone involvement in stressor-induced alterations in sleep and in the regulation of waking. Adv. Neuroimmunol., 5: 127-143.
66. Popik, P., Vetulani, J. and Van Ree, J.M. (1992) Low doses of oxytocin facilitate social recognition in rats. Psychopharmacology, 106: 71-74.
67. Pedersen, C.A. and Prange, A.J. (1979) Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin. Proc. Natl. Acad. Sci. USA, 76: 6661-6665.
68. Pinnock, S.B. and Herbert, J. (2001) Corticosterone differentially modulates expression of corticotropin releasing factor and arginine vasopressin mRNA in the hypothalamic paraventricular nucleus following either acute or repeated restraint stress. Eur. J. Neurosci., 13: 576-584.
69. Rosenblatt, J.S., Factor, E. and Mayer, A.D. (1994) Relationship between maternal aggression and maternal care in the rat. Aggress. Behav., 20: 243-255.
70. Sawchenko, P.E. (1987) Adrenalectomy-induced enhancement of CRF and vasopressin immunoreactivity in parvocellular neurosecretory neurons: Anatomic peptide, and steroid specificity. J. Neurosci., 7: 1093-1106.
71. Sawchenko, P.E., Swanson, L.W. and Vale, W.W. (1984) Corticotropin-releasing factor: Co-expression within distinct subsets of oxytocin-, vasopressin-, and neurotensinimmunoreactive neurons in the hypothalamus of male rats. J. Neurosci., 4: 1118-1129.
72. Silakov, V.L., Nikitin, V.S., Moiseeva, L.A. and Losev, S.S. (1995) Influence of neuropeptides on the processes of higher nervous activity in primates. Neurosci. Behav. Physiol., 25: 386-392.
73. Torner, L., Thrivikraman, K.V., Toschi, N., Holsboer, F., Plotsky, P.M. and Neumann, I.D. (2000) Effect of adrenalectomy and corticosterone on hypothalamic and peripheral release of oxytocin and behavioral stress coping in male rats. Abstract 30th Annual Neuroscience Meeting, New Orleans, 153.12.
74. Torner, L., Toschi, N., Pohlinger, A., Landgraf, R. and Neumann, I.D. (2001) Anxiolytic and anti-stress effects of brain prolactin: Improved efficacy of antisense targeting of the prolactin receptor by molecular modeling. J. Neurosci., 21: 3207-3214.
75. Uvnäs-Moberg, K., Ahlenius, S., Hillegaart, V. and Alster, P. (1994) High doses of oxytocin cause sedation and low doses cause an anxiolytic-like effect in male rats. Pharmacol. Biochem. Behav., 49: 101-106.
76. Van Leengoed, E., Kerker, E. and Swanson, H.H. (1986) Inhibition of postpartum maternal behaviour in the rat by injecting an oxytocin antagonist into the cerebral ventricles. J. Endocrinol., 112: 275-282.
77. Verbalis, J.G. (1999) The brain oxytocin receptor(s)?. Front. Neuroendocrinol., 20: 146-156.
78. Verbalis, J.G., McHale, C.M., Gardiner, T.W. and Stricker, E.M. (1986) Oxytocin and vasopressin secretion in response to stimuli producing learned taste aversions in rat. Behav. Neurosci., 100: 466-475.
79. Wakerley, C., Foreman, C.T. and Ingram, C.D. (1989) Effect of centrally administered oxytocin on the association between cortical electroencephalogram and milk ejection in the rat. J. Neuroendocrinol., 1: 173-177.
80. Walker, C.-D., Trottier, G., Rochford, J. and Lavallée, D. (1995) Dissociation between behavioral and hormonal responses to the forced swim stress in lactating rats. J. Neuroendocrinol., 7: 615-622.
81. Welch, B.L. and Klopfer, P.H. (1961) Endocrine variability as a factor in the regulation of population density. Am. Naturalist, 95: 256-260.
82. Wigger, A. and Neumann, I.D. (2002) Endogenous opioid regulation of stress-induced oxytocin release within the hypothalamic paraventricular nucleus is reversed in late pregnancy: A microdialysis study. Neuroscience, 112: 121-129.
83. Williams, J.R., Insel, T.R., Harbaugh, C.R. and Cater, C.S. (1994) Oxytocin administered centrally facilitates formation of a partner preference in female prairie voles (Microtus ochrogaster). J. Neuroendocrinol., 6: 247-250.
84. Windle, R.J., Shanks, N., Lightman, S.L. and Ingram, C.D. (1997) Central oxytocin administration reduces stress-induced corticosterone release and anxiety behavior in rats. Endocrinology, 138: 2829-2834.
85. Winslow, J.T., Hearn, E.F., Ferguson, J., Young, L.J., Matzuk, M.M. and Insel, T.R. (2000) Infant vocalization, adult aggression, and fear behavior of an oxytocin null mutant mouse. Horm. Behav., 37: 145-155.
86. Wotjak, C.T., Masaharu, K., Liebsch, G., Montkowski, A., Holsboer, F., Neumann, I. and Landgraf, R. (1996) Release of vasopressin within the rat paraventricular nucleus in response to emotional stress: A novel mechanism of regulating adrenocorticotropic hormone secretion?. J. Neurosci., 16: 7725-7732.
87. Wotjak, C.T., Ganster, J., Kohl, G., Holsboer, F., Landgraf, R. and Engelmann, M. (1998) Dissociated central and peripheral release of vasopressin, but not oxytocin, in response to repeated swim stress: New insights into the secretory capacities of peptidergic neurons. Neuroscience, 85: 1209-1222.
88. Wotjak, C.T., Naruo, T., Muraoka, S., Simchen, R., Landgraf, R. and Engelmann, M. (2001) Swim stress stimulates the expression of vasopressin and oxytocin in magnocellular neurons of the hypothalamic paraventricular nucleus. Eur. J. Neurosci., 13: 2273-2281.
89. Yoshimura, R., Kiyama, H., Kimura, T., Araki, T., Maeno, H. and Tanizawa, O. (1993) Localization of oxytocin receptor messenger ribonucleic acid in the rat brain. Endocrinology, 133: 1239-1246.