Neuroendocrine responses to an emotional stressor: Evidence for involvement of the medial but not the central amygdala

European Journal of Neuroscience

Volumn 11, Issue 7, 1999, Pages 2312-2322

  Dayas, C V ^a   Buller, K M ^a   Day, T A ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Amygdala; Emotional stress; Hypothalamic pituitary adrenal axis; Oxytocin; Paraventricular nucleus; Restraint

Indexed keywords

CORTICOTROPIN RELEASING FACTOR; OXYTOCIN;

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY LABELING; ARTICLE; CONTROLLED STUDY; EMOTIONAL STRESS; GENE EXPRESSION; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMOBILIZATION STRESS; MALE; NERVE PROJECTION; NEUROENDOCRINE SYSTEM; NEUROSECRETORY CELL; NONHUMAN; ONCOGENE C FOS; PRIORITY JOURNAL; RAT; SUPRAOPTIC NUCLEUS; THALAMUS MIDLINE NUCLEUS; TUBEROHYPOPHYSEAL TRACT;

EID: 0033046214     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.1999.00645.x     Document Type: Article

References (59)

1. Adolphs, R., Tranel, D., Damasio, A.R. 1998 The human amygdala in social judgment. Nature, 393, 470 474.
2. Arnold, F.J., De Lucas Bueno, M., Shiers, H., Hancock, D.C., Evan, G.I., Herbert, J. 1992 Expression of c‐ fos in regions of the basal limbic forebrain following intracerebroventricular corticotropin‐releasing factor in unstressed or stressed male rats. Neuroscience, 51, 377 390.
3. Beaulieu, S., Di Paolo, T., Barden, N. 1986 Control of ACTH secretion by the central nucleus of the amygdala: implication of the serotoninergic system and its relevance to the glucocorticoid delayed negative feedback mechanism. Neuroendocrinology, 44, 247 254.
4. Beaulieu, S., Di Paolo, T., Cote, J., Barden, N. 1987 Participation of the central amygdaloid nucleus in the response of adrenocorticotropin secretion to immobilization stress: opposing roles of the noradrenergic and dopaminergic systems. Neuroendocrinology, 45, 37 46.
5. Bhatnagar, S. & Dallman, M. 1998 Neuroanatomical basis for facilitation of hypothalamic‐pituitary‐adrenal responses to a novel stressor after chronic stress. Neuroscience, 84, 1025 1039.
6. Bohus, B., Koolhaas, J.M., Luiten, P.G., Korte, S.M., Roozendaal, B., Wiersma, A. 1996 The neurobiology of the central nucleus of the amygdala in relation to neuroendocrine and autonomic outflow. Prog. Brain Res., 107, 447 460.
7. Bonaz, B. & Tache, Y. 1997 Corticotropin‐releasing factor and systemic capsaicin‐sensitive afferents are involved in abdominal surgery‐induced Fos expression in the paraventricular nucleus of the hypothalamus. Brain Res., 748, 12 20.
8. Buller, K.M., Xu, Y., Day, T.A. 1998 Indomethacin attenuates oxytocin and hypothalamic‐pituitary‐adrenal axis responses to systemic interleukin‐1β. J. Neuroendocrinol., 10, 519 528.
9. Buma, P. & Nieuwenhuys, R. 1987 Ultrastructural demonstration of oxytocin and vasopressin release sites in the neural lobe and median eminence of the rat by tannic acid and immunogold methods. Neurosci. Lett., 74, 151 157.
10. Callahan, M.F., Da Rocha, M.J., Morris, M. 1992 Sinoaortic denervation does not increase cardiovascular/endocrine responses to stress. Neuroendocrinology, 56, 735 744.
11. Campeau, S. & Watson, S.J. 1997 Neuroendocrine and behavioral responses and brain pattern of c‐ fos induction associated with audiogenic stress. J. Neuroendocrinol., 9, 577 588.
12. Canteras, N.S., Simerly, R.B., Swanson, L.W. 1995 Organization of projections from the medial nucleus of the amygdala: a PHAL study in the rat. J. Comp Neurol., 360, 213 245.
13. Carter, D.A. & Lightman, S.L. 1987 Oxytocin stress responses are dependent upon emotionality. Psychoneuroendocrinology, 12, 219 223.
14. Champagne, D., Beaulieu, J., Drolet, G. 1998 CRFergic innervation of the paraventricular nucleus of the rat hypothalamus: a tract‐tracing study. J. Neuroendocrinol., 10, 119 131.
15. Chen, X. & Herbert, J. 1995 Regional changes in c‐ fos expression in the basal forebrain and brainstem during adaptation to repeated stress: correlations with cardiovascular, hypothermic and endocrine responses. Neuroscience, 64, 675 685.
16. Cirino, M. & Renaud, L.P. 1985 Influence of lateral septum and amygdala stimulation on the excitability of hypothalamic supraoptic neurons. An electrophysiological study in the rat. Brain Res., 326, 357 361.
17. Coffey, P.J., Perry, V.H., Rawlins, J.N. 1990 An investigation into the early stages of the inflammatory response following ibotenic acid‐induced neuronal degeneration. Neuroscience, 35, 121 132.
18. Cullinan, W.E., Herman, J.P., Battaglia, D.F., Akil, H., Watson, S.J. 1995 Pattern and time course of immediate early gene expression in rat brain following acute stress. Neuroscience, 64, 477 505.
19. Cunningham, E.T. Jr & Sawchenko, P.E. 1988 Anatomical specificity of noradrenergic inputs to the paraventricular and supraoptic nuclei of the rat hypothalamus. J. Comp. Neurol., 274, 60 76.
20. Duncan, G.E., Knapp, D.J., Breese, G.R. 1996 Neuroanatomical characterization of Fos induction in rat behavioral models of anxiety. Brain Res., 713, 79 91.
21. Dunn, J.D. & Whitener, J. 1986 Plasma corticosterone responses to electrical stimulation of the amygdaloid complex: cytoarchitectural specificity. Neuroendocrinology, 42, 211 217.
22. Ericsson, A., Kovacs, K.J., Sawchenko, P.E. 1994 A functional anatomical analysis of central pathways subserving the effects of interleukin‐1 on stress‐related neuroendocrine neurons. J. Neurosci., 14, 897 913.
23. Feldman, S., Conforti, N., Itzik, A., Weidenfeld, J. 1994 Differential effect of amygdaloid lesions on CRF‐41, ACTH and corticosterone responses following neural stimuli. Brain Res., 658, 21 26.
24. Feldman, S., Conforti, N., Weidenfeld, J. 1995 Limbic pathways and hypothalamic neurotransmitters mediating adrenocortical responses to neural stimuli. Neurosci. Biobehav. Rev., 19, 235 240.
25. Galeno, T.M., Van Hoesen, H.G., Brody, M.J. 1984 Central amygdaloid nucleus lesion attenuates exaggerated hemodynamic responses to noise stress in the spontaneously hypertensive rat. Brain Res., 291, 249 259.
26. Gibbs, D.M. 1984 Dissociation of oxytocin, vasopressin and corticotropin secretion during different types of stress. Life Sci., 35, 487 491.
27. Gibbs, D.M. 1986 Stress‐specific modulation of ACTH secretion by oxytocin. Neuroendocrinology, 42, 456 458.
28. Gray, T.S. 1996 Amygdala: role in autonomic and neuroendocrine responses to stress. In: McCubbin, J.A., Kaufmann, P.G. & Nemeroff, C.B, eds. Stress, Neuropeptides, and Systemic Disease. Academic Press, San Diego, pp. 37 53.
29. Gray, T.S., Carney, M.E., Magnuson, D.J. 1989 Direct projections from the central amygdaloid nucleus to the hypothalamic paraventricular nucleus: Possible role in stress‐induced adrenocorticotropin release. Neuroendocrinology, 50, 433 446.
30. Gray, T.S., Piechowski, R.A., Yracheta, J.M., Rittenhouse, P.A., Bethea, C.L., Van de Kar, L.D. 1993 Ibotenic acid lesions in the bed nucleus of the stria terminalis attenuate conditioned stress‐induced increases in prolactin, ACTH and corticosterone. Neuroendocrinology, 57, 517 524.
31. Herman, J.P. & Cullinan, W.E. 1997 Neurocircuitry of stress: central control of the hypothalamo‐pituitary‐adrenocortical axis. Trends Neurosci., 20, 78 84.
32. Herman, J.P., Cullinan, W.E., Watson, S.J. 1994 Involvement of the bed nucleus of the stria terminalis in tonic regulation of paraventricular hypothalamic CRH and AVP mRNA expression. J. Neuroendocrinol., 6, 433 442.
33. Honkaniemi, J., Kainu, T., Ceccatelli, S., Rechardt, L., Hokfelt, T., Pelto‐Huikko, M. 1992 Fos and jun in rat central amygdaloid nucleus and paraventricular nucleus after stress. Neuroreport, 3, 849 852.
34. Imaki, T., Shibasaki, T., Hotta, M., Demura, H. 1993 Intracerebroventricular administration of corticotropin‐releasing factor induces c‐ fos mRNA expression in brain regions related to stress responses: comparison with pattern of c‐ fos mRNA induction after stress. Brain Res., 616, 114 125.
35. Johnson, E.O., Kamilaris, T.C., Chrousos, G.P., Gold, P.W. 1992 Mechanisms of stress: a dynamic overview of hormonal and behavioral homeostasis. Neurosci. Biobehav. Rev., 16, 115 130.
36. Jolkkonen, E. & Pitkanen, A. 1998 Intrinsic connections of the rat amygdaloid complex: projections originating in the central nucleus. J. Comp. Neurol., 395, 53 72.
37. Killcross, S., Robbins, T.W., Everitt, B.J. 1997 Different types of fear‐conditioned behaviour mediated by separate nuclei within amygdala. Nature, 388, 377 380.
38. Lang, R.E., Heil, J.W.E., Ganten, D., Hermann, K., Unger, T., Rascher, W. 1983 Oxytocin unlike vasopressin is a stress hormone in the rat. Neuroendocrinology, 37, 314 316.
39. Li, Y. & Dampney, R.A.L. 1994 Expression of fos‐like protein in brain following sustained hypertension and hypotension in conscious rabbits. Neuroscience, 61, 613 634.
40. Li, H.Y. & Sawchenko, P.E. 1998 Hypothalamic effector neurons and extended circuitries activated in ‘neurogenic’ stress: a comparison of footshock effects exerted acutely, chronically, and in animals with controlled glucocorticoid levels. J. Comp. Neurol., 393, 244 266.
41. Martinez, M., Phillips, P.J., Herbert, J. 1998 Adaptation in patterns of c‐ fos expression in the brain associated with exposure to either single or repeated social stress in male rats. Eur. J. Neurosci., 10, 20 33.
42. Miyata, S., Itoh, T., Lin, S.H., Ishiyama, M., Nakashima, T., Kiyohara, T. 1995 Temporal changes of c‐ fos expression in oxytocinergic magnocellular neuroendocrine cells of the rat hypothalamus with restraint stress. Brain Res. Bull., 37, 391 395.
43. Petrov, T., Jhamandas, J.H., Krukoff, T.L. 1994 Electrical stimulation of the central nucleus of the amygdala induces fos‐like immunoreactivity in the hypothalamus of the rat: a quantitative study. Brain Res. Mol. Brain Res., 22, 333 340.
44. Pezzone, M.A., Lee, W.S., Hoffman, G.E., Rabin, B.S. 1992 Induction of c‐ Fos immunoreactivity in the rat forebrain by conditioned and unconditioned aversive stimuli. Brain Res., 597, 41 50.
45. Pitkanen, A., Savander, V., LeDoux, J.E. 1997 Organization of intra‐amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala [published erratum appears in Trends Neurosci., 1998, 21 (2), 52]. Trends Neurosci., 20, 517 523.
46. Prewitt, C.M. & Herman, J.P. 1994 Lesion of the central nucleus of the amygdala decreases basal CRH mRNA expression and stress‐induced ACTH release. Ann. NY Acad. Sci., 746, 438 440.
47. Prewitt, C.M. & Herman, J.P. 1997 Hypothalamo‐pituitary‐adrenocortical regulation following lesions of the central nucleus of the amygdala. Stress, 1, 263 280.
48. Roozendaal, B., Koolhaas, J.M., Bohus, B. 1991 Attenuated cardiovascular, neuroendocrine, and behavioral responses after a single footshock in central amygdaloid lesioned male rats. Physiol. Behav., 50, 771 775.
49. Roozendaal, B., Koolhaas, J.M., Bohus, B. 1992 Central amygdaloid involvement in neuroendocrine correlates of conditioned stress responses. J. Neuroendocrinol., 4, 483 489.
50. Roozendaal, B., Koolhaas, J.M., Bohus, B. 1997 The role of the central amygdala in stress and adaption. Acta Physiol. Scand. (Suppl.640), 51 54.
51. Sawchenko, P.E. & Swanson, L.W. 1983 The organisation of forebrain afferents to the paraventricular and supraoptic nuclei of the rat. J. Comp. Neurol., 218, 121 144.
52. Silverman, A.J., Hoffman, D.L., Zimmerman, E.A. 1981 The descending afferent connections of the paraventricular nucleus of the hypothalamus (PVN). Brain Res. Bull., 6, 47 61.
53. Smith, D.W., Buller, K.M., Day, T.A. 1995 Role of ventrolateral medulla catecholamine cells in hypothalamic neuroendocrine cell responses to systemic hypoxia. J. Neurosci., 15, 7979 7988.
54. Swanson, L.W. & Petrovich, G.D. 1998 What is the amygdala? Trends Neurosci., 21, 323 331.
55. Swanson, L.W., Sawchenko, P.E., Rivier, J., Vale, W.W. 1983 Organization of ovine corticotropin‐releasing factor immunoreactive cells and fibers in the rat brain: an immunohistochemical study. Neuroendocrinology, 36, 165 186.
56. Traub, R.J., Silva, E., Gebhart, G.F., Solodkin, A. 1996 Noxious colorectal distention induced‐c‐Fos protein in limbic brain structures in the rat. Neurosci. Lett., 215, 165 168.
57. Tribollet, E. & Dreifuss, J.J. 1981 Localization of neurones projecting to the hypothalamic paraventricular nucleus area of the rat: a horseradish peroxidase study. Neuroscience, 6, 1315 1328.
58. Van de Kar, L.D., Piechowski, R.A., Rittenhouse, P.A., Gray, T.S. 1991 Amygdaloid lesions: differential effect on conditioned stress and immobilization‐induced increases in corticosterone and renin secretion. Neuroendocrinology, 54, 89 95.
59. Xu, Y., Buller, K.M., Day, T.A. 1998 Role of the central amygdala in HPA axis, oxytocin and central catecholamine responses to systemic IL‐1β. Eur. J. Neurosci, 10 (Suppl. 10), 295 (Abstract).