Stereotaxic localization of corticosterone to the amygdala enhances hypothalamo-pituitary-adrenal responses to behavioral stress

Brain Research

Volumn 963, Issue 1-2, 2003, Pages 203-213

  Shepard, Jack D ^a,b   Barron, Kirk W ^c   Myers, Dean A ^a  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^c National Institutes of Health ^*

Author keywords

Amygdala; Corticosterone; Corticotropin releasing factor; Paraventricular nucleus; Stress; Vasopressin

Indexed keywords

ARGIPRESSIN; CHOLESTEROL; CORTICOSTERONE; CORTICOTROPIN; CORTICOTROPIN RELEASING FACTOR; GLUCOCORTICOID; MESSENGER RNA;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BLOOD SAMPLING; BLOOD VESSEL CATHETERIZATION; CIRCADIAN RHYTHM; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; CORTICOSTERONE RELEASE; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS PERIVENTRICULAR NUCLEUS; IN SITU HYBRIDIZATION; MALE; MAZE TEST; NONHUMAN; PRIORITY JOURNAL; RAT; STRESS;

ADRENAL GLANDS; AMYGDALA; ANIMALS; ARGININE VASOPRESSIN; CATHETERIZATION; CORTICOSTERONE; CORTICOTROPIN-RELEASING HORMONE; DIFFUSION; DRUG IMPLANTS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; IMAGE PROCESSING, COMPUTER-ASSISTED; IN SITU HYBRIDIZATION; MALE; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PITUITARY-ADRENAL SYSTEM; RADIOIMMUNOASSAY; RATS; RATS, WISTAR; RNA, MESSENGER; STEREOTAXIC TECHNIQUES; STRESS, PSYCHOLOGICAL; THYMUS GLAND;

EID: 0037435876     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(02)03978-1     Document Type: Article

References (69)

1. Aguilera G. Regulation of pituitary ACTH secretion during chronic stress. Front. Neuroendocrinol. 15:1994;321-350.
2. Aguilera G. Corticotropin releasing hormone, receptor regulation and the stress response. Trends Endocrinol. Metab. 9:1998;329-336.
3. Akana S.F., Chu A., Soriano L., Dallman M.F. Corticosterone exerts site-specific and state dependent effects in prefrontal cortex and amygdala on regulation of adrenocorticotropic hormone, insulin and fat deposits. J. Neuroendocrinol. 13:2001;625-637.
4. Allen J.P., Allen C.F. Role of the amygdaloid complexes in the stress-induced release of ACTH in the rat. Neuroendocrinology. 15:1974;220-230.
5. Allen J.P., Allen C.F. Amygdalar participation in tonic ACTH secretion in the rat. Neuroendocrinology. 19:1975;115-125.
6. Arborelius L., Owens M.J., Plotsky P.M., Nemeroff C.B. The role of corticotropin-releasing factor in depression and anxiety disorders. J. Endocrinol. 160:1999;1-12.
7. Beaulieu S., Di Paolo T., Barden N. Control of ACTH secretion by the central nucleus of the amygdala: implication of the serotoninergic systems and its relevance to the glucocorticoid delayed negative feedback mechanism. Neuroendocrinology. 44:1986;247-254.
8. Beaulieu S., Pelletier G., Vaudry H., Barden N. Influence of the central nucleus of the amygdala on the content of corticotropin-releasing factor in the median eminence. Neuroendocrinology. 49:1989;255-261.
9. Bhatnagar S., Dallman M.F. Neuroanatomical basis for facilitation of hypothalamic-pituitary-adrenal responses to a novel stressor after chronic stress. Neuroscience. 84:1998;1025-1039.
10. Calvo N., Martijena I.D., Molina V.A., Volosin M. Metyrapone pretreatment prevents the behavioral and neurochemical sequelae induced by stress. Brain Res. 800:1998;227-235.
11. Canteras N.S., Simberly R.B., Swanson L.W. Organization of projections from the medial nucleus of the amygdala: A PHAL study in the rat. J. Comp. Neurol. 360:1995;213-245.
12. Dallman M.F. Stress Update: Adaptation of the hypothalamic-pituitary-adrenal axis to chronic stress. Trends Endocrinol. Metab. 4:1993;62-69.
13. Dallman M.F., Akana S.F., Cascio C.S., Darlington D.N., Jacobson L., Levin N. Regulation of ACTH secretion: variations on a theme of B. Recent Prog. Horm. Res. 43:1987;113-167.
14. Dallman M.F., Akana S.F., Levin N., Walker C.-D., Bradbury M.J., Suemaru S., Scribner K.S. Corticosteroids and the control of function in the hypothalamo-pituitary-adrenal (HPA) axis. Ann. NY Acad. Sci. 746:1994;22-28.
15. Davis M. Neurobiology of fear responses: the role of the amygdala. J. Neuropsychiatry Clin. Neurosci. 9:1997;382-402.
16. Dayas C.V., Buller K.M., Day T.A. Neuroendocrine responses to an emotional stressor: evidence for involvement of the medial but not the central amygdala. Eur. J. Neurosci. 11:1999;2312-2322.
17. de Olmos J.S., Heimer L. The concepts of the ventral striatopallidal system and extended amygdala. Ann. NY Acad. Sci. 877:1999;1-32.
18. 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.
19. Drevets W.C. Functional anatomical abnormalities in limbic and prefrontal cortical structures in major depression. Prog. Brain Res. 126:2000;413-431.
20. Drevets W.C. Neuroimaging and neuropathological studies of depression: implications for the cognitive-emotional features of mood disorders. Curr. Opin. Neurobiol. 11:2001;240-249.
21. Dunn J.D. Plasma corticosterone responses to electrical stimulation of the bed nucleus of the stria terminalis. Brain Res. 407:1987;327-331.
22. Feldman S., Conforti N., Itzik A., Weidenfield J. Differential effect of amygdaloid lesions on CRF-41 ACTH and corticosterone responses following neural stimuli. Brain Res. 658:1994;21-26.
23. Feldman S., Conforti N., Saphier D. The preoptic area and bed nucleus of the stria terminalis are involved in the effects of the amygdala on adrenocortical secretion. Neuroscience. 37:1990;775-779.
24. Feldman S., Weidenfeld J. The excitatory effects of the amygdala on the hypothalamo-pituitary-adrenocortical responses are mediated by hypothalamic norepinephrine, serotonin, and CRF-41. Brain Res. Bull. 45:1998;389-393.
25. Feldman S., Weidenfeld J. Glucocorticoid receptor antagonists in the hippocampus modify the negative feedback following neural stimuli. Brain Res. 821:1999;33-37.
26. File S.E., Zangrossi H., Sanders F.L., Mabbutt P.S. Raised corticosterone in the rat after exposure to the elevated plus-maze. Psychopharmacology. 113:1994;543-546.
27. Gabr R.W., Birkle D.L., Azzaro A.J. Stimulation of the amygdala by glutamate facilitates corticotropin-releasing factor release from the median eminence and activation of the hypothalamic-pituitary-adrenal axis in stressed rats. Neuroendocrinology. 62:1995;333-339.
28. Gold P.W., Chrousos G.P. The endocrinology of melancholic and atypical depression: relation to neurocircuitry and somatic consequences. Proc. Assoc. Am. Physicians. 111:1999;22-34.
29. Gold P.W., Licinio J., Wong M., Chrousos G.P. Corticotropin releasing hormone in the pathophysiology of melancholic and atypical depression and in the mechanism of action of antidepressant drugs. Ann. NY Acad. Sci. 771:1995;716-729.
30. Gray T.S., Carney M.E., Magnuson D.J. Direct projections from the central amygdaloid nucleus to the hypothalamic paraventricular nucleus: possible role in stress-induced adrenocorticotropin release. Neuroendocrinology. 50:1989;433-446.
31. Greenwood-Van M.B., Gibson M., Gunter W., Shepard J., Foreman R., Myers D. Stereotaxic delivery of corticosterone to the amygdala modulates colonic sensitivity in rats. Brain Res. 893:2001;135-142.
32. Hennessy M.B., Heybach J.P., Vernikos J., Levine S. Plasma corticosterone concentrations sensitively reflect levels of stimulus intensity in the rat. Physiol. Behav. 22:1979;821-825.
33. Hennessy M.B., Levine S. Sensitive pituitary-adrenal responsiveness to varying intensities of psychological stimulation. Physiol. Behav. 21:1978;295-297.
34. Herman J.P., Cullinan W.E. Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci. 20:1997;78-84.
35. Herman J.P., Cullinan W.E., Watson S.J. Involvement of the bed nucleus of the stria terminalis in tonic regulation of paraventricular hypothalamic CRH and AVP mRNA expression. J. Neuroendocrinol. 6:1994;433-442.
36. Herman J.P., Cullinan W.E., Morano M.I., Akil H., Watson S.J. Contribution of the ventral subiculum to inhibitory regulation of the hypothalamo-pituitary-adrenocortical axis. J. Neuroendocrinol. 7:1995;475-482.
37. Honkaniemi J., Pelto-Huikko M., Rechardt L., Isola J., Lammi A., Fuxe K., Gustafsson J., Wikstrom A., Hokfelt T. Colocalization of peptide and glucocorticoid receptor immunoreactivities in rat central amygdaloid nucleus. Neuroendocrinology. 55:1992;451-459.
38. Jacobson L., Sapolsky R. The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr. Rev. 12:1991;118-134.
39. Joels M., Vreugdenhil E. Corticosteroids in the brain. Cellular and molecular actions. Mol. Neurobiol. 17:1998;87-108.
40. Kasckow J.W., Baker D., Geracioti T.D.J. Corticotropin-releasing hormone in depression and post-traumatic stress disorder. Peptides. 22:2001;845-851.
41. Kovacs K.J., Makara G.B. Corticosterone and dexamethasone act at different brain sites to inhibit adrenalectomy-induced adrenocorticotropin hypersecretion. Brain Res. 474:1988;205-210.
42. Ledoux J.E. Fear and the brain: where have we been, and where are we going? Biol. Psychiatry. 44:1998;1229-1238.
43. Lilly M.P., Putney D.J., Carlson D.E. Potentiated response of corticotropin (ACTH) to repeated moderate hemorrhage requires amygdalar neuronal processing. Neuroendocrinology. 71:2000;88-98.
44. Ma X.M., Levy A., Lightman S.L. Emergence of an isolated arginine vasopressin (AVP) response to stress after repeated restraint: a study of both AVP and corticotropin-releasing hormone messenger ribonucleic acid (RNA) and heteronuclear RNA. Endocrinology. 138:1997;4351-4357.
45. Makino S., Shibasaki T., Yamauchi N., Nishioka T., Mimoto T., Wakabayashi I., Gold P.W., Hashimoto K. Psychological stress increased corticotropin-releasing hormone mRNA and content in the central nucleus of the amygdala but not in the hypothalamic paraventricular nucleus in the rat. Brain Res. 850:1999;136-143.
46. Makino S., Smith M.A., Gold P.W. Increased expression of corticotropin-releasing hormone and vasopressin messenger ribonucleic acid (mRNA) in the hypothalamic paraventricular nucleus during repeated stress: association with reduction in glucocorticoid receptor mRNA levels. Endocrinology. 136:(8):1995;3299-3309.
47. Marcilhac A., Siaud P. Regulation of the adrenocorticotrophin response to stress by the central nucleus of the amygdala in rats depends upon the nature of the stressor. Exp. Physiol. 81:1996;1035-1038.
48. Marcilhac A., Siaud P. Identification of projections from the central nucleus of the amygdala to the paraventricular nucleus of the hypothalamus which are immunoreactive for corticotrophin-releasing hormone in the rat. Exp. Physiol. 82:1997;273-281.
49. Meaney M.J., McEwen B.S. Testosterone implants into the amygdala during the neonatal period masculinize the social play of juvenile female rats. Brain Res. 398:1986;324-328.
50. Morimoto M., Morita N., Ozawa H., Yokoyama K., Kawata M. Distribution of glucocorticoid receptor immunoreactivity and mRNA in the rat brain: an immunohistochemical and in situ hybridization study. Neurosci. Res. 26:1996;235-269.
51. Munck A., Guyre P.M., Holbrook N.J. Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocrinol. Rev. 5:1984;25-44.
52. Myers D.A., Bell M.E., McDonald T.J., Myers T.R. Corticotropin-releasing factor receptor expression in the pituitary of fetal sheep after lesions of the hypothalamic paraventricular nucleus. Endocrinology. 140:1999;4292-4299.
53. Myers D.A., McDonald T.J., Dunn T.G., Moss G.E., Nathanielsz P.W. Effect of implantation of dexamethasone adjacent to the paraventricular nucleus on messenger ribonucleic acid for corticotropin-releasing hormone and proopiomelanocortin during late gestation in fetal sheep. Endocrinology. 130:1992;2167-2172.
54. Parkes D., Rivest S., Lee S., Rivier C., Vale W. Corticotropin-releasing factor activates c-fos, NGFI-B, and corticotropin-releasing factor gene expression within the paraventricular nucleus of the rat hypothalamus. Mol. Endocrinol. 7:1993;1357-1367.
55. Paxinos G.T., Watson C. The Rat Brain in Stereotaxic Coordinates. 1997;Academic Press, New York.
56. Pellow S., Chopin P., File S.E., Briley M. Validation of open: closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J. Neurosci. Methods. 14:1985;149-167.
57. Petrov T., Jhamandas J.H., Krukoff T.L. Electrical stimulation of the central nucleus of the amygdala induces fos-like immunoreactivity in the hypothalamus of the rat: a quantitative study. Mol. Brain Res. 22:1994;333-340.
58. Pitkanen A., Savander V., Ledoux J.E. Organization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala. Trends Neurosci. 20:1997;517-523.
59. Pittman Q.J., Blume H.W., Renaud L.P. Connections of the hypothalamic paraventricular nucleus with the neurohypophysis, median eminence, amygdala, lateral septum and midbrain periaqueductal gray: an electrophysiological study in the rat. Brain Res. 215:1981;15-28.
60. Prewitt C.M., Herman J.P. Lesion of the central nucleus of the amygdala decreases basal CRH mRNA expression and stress-induced ACTH release. Ann. NY Acad. Sci. 746:1994;438-440.
61. Prewitt C.M., Herman J.P. Hypothalamo-pituitary-adrenocortical regulation following lesions of the central nucleus of the amygdala. Stress. 1:1997;263-280.
62. Prewitt C.M., Herman J.P. Anatomical interactions between the central amygdaloid nucleus and the hypothalamic paraventricular nucleus of the rat: a dual tract-tracing analysis. J. Chem. Neuroanat. 15:1998;173-185.
63. Reul J.M.H.M., de Kloet E.R. Two receptor systems for corticosterone in rat brain: Microdistribution and differential occupation. Endocrinology. 117:1985;2505-2511.
64. Sawchenko P.E. Evidence for a local site of action for glucocorticoids in inhibiting CRF and vasopressin expression in the paraventricular nucleus. Brain Res. 403:1987;213-223.
65. Schulkin J., Gold P.W., McEwen B.S. Induction of corticotropin-releasing hormone gene expression by glucocorticoids: implication for understanding the states of fear and anxiety and allostatic load. Psychoneuroendocrinology. 23:1998;219-243.
66. Schulkin J., McEwen B.S., Gold P.W. Allostasis, amygdala, and anticipatory angst. Neurosci. Biobehav. Rev. 18:1994;385-396.
67. Shepard J.D., Barron K.W., Myers D.A. Corticosterone delivery to the amygdala increases corticotropin-releasing factor mRNA in the central amygdaloid nucleus and anxiety-like behavior. Brain Res. 861:2000;288-295.
68. Swanson L.W. Biochemical switching in hypothalamic circuits mediating responses to stress. Prog. Brain Res. 87:1991;181-200.
69. Thrivikraman K.V., Su Y., Plotsky P.M. Patterns of fos-immunoreactivity in the CNS induced by repeated hemorrhage in conscious rats: Correlations with pituitary-adrenal axis activity. Stress. 2:1997;145-158.