Hyperresponsiveness of the rat neuroendocrine system due to repeated exposure to stress

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Abstract

Sequential exposure to stressors may elicit a period of endocrine hyperresponsiveness during which plasma hormone concentrations reach higher levels after repeated exposure to a stressor compared to levels after initial exposure. The present study was designed to further characterize hyperresponsiveness to repeated stress and determine if hyperresponsiveness is dependent upon repeated exposure to the same stressful stimuli. In Experiment 1, rats were stressed by inescapable tailshock, immobilization or exposure to shock chamber without shock for one, two, three, four or five consecutive days (15 min/day). In rats exposed to tailshock, corticosterone (CS) levels in plasma collected on days 2, 3, 4 and 5 were higher than CS levels following acute tailshock on day 1, demonstrating hyperresponsiveness to repeated tailshock. Hyperresponsiveness of CS secretion also occurred in groups of rats restrained for four or five days. No changes occurred in the CS response of animals repeatedly exposed to immobilization. Prolactin (PRL) levels were not affected by repeated exposure to the stressors. However, PRL values were different between the stress conditions and indicated that the order of stressor severity was tailshock > immobilization > exposure to shock chamber without shock.

In Experiment 2, rats were exposed to either one or two consecutive days of tailshock or immobilization. Other rats were exposed to either tailshock or immobilization on the first day, then switched to the other stressor on the next day. Hyperresponsiveness to repeated tailshock, but not immobilization, was reflected in plasma levels of CS and adrenocorticotropic hormone (ACTH), but not PRL. Hyperresponsiveness of CS and ACTH secretion also was found in rats first stressed by immobilization then switched to tailshock, demonstrating that hyperresponsiveness is not dependent upon reexposure to familiar stressful stimuli. However, hyperresponsiveness did not occur in rats first exposed to tailshock then switched to immobilization. The data suggest that both immobilization and tailshock primed the organism to hyperrespond, but only the more severe stressor (tailshock) elicited hyperresponsiveness of the neuroendocrine system.

References (28)

  • TO Bruhn et al.

    Corticotropin-releasing factor regulates proopiomelanocortin messenger ribonucleic acid levels in vivo

    Neuroendocrinology

    (1984)
  • MF Dallman et al.

    Corticosteroid feedback control of ACTH secretion: effects of stress-induced corticosteroid secretion of subsequent stress response in the rat

    Endocrinology

    (1973)
  • PW Gold et al.

    Abnormal hypothalamic-pituitary-adrenal function in anorexia nervosa: pathophysiological mechanisms in underweight and weight-recovered patients

    N Engl J Med

    (1986)
  • PW Gold et al.

    Physiology of hypercortisolism in depression and Cushing's disease

    N Engl J Med

    (1986)
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