A Single Exposure to Severe Stressors Causes Long-term Desensitisation of the Physiological Response to the Homotypic Stressor

References

• Adell, A., Garcia-Ma´rquez, C., Armario, A. and Gelp?´, E. (1988) Chronic stress increases serotonin and noradrenaline in rat brain and sensitizes their response to a further acute stress, J. Neurochem. 50, 1678–1681.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Armario, A. and Jolin, T. (1989) Influence of intensity and duration of exposure to various stressors on serum TSH and GH levels in adult male rats, Life Sci. 44, 215–221.
   PubMedGoogle Scholar
• Armario, A., Montero, J.L. and Balasch, J. (1986) Sensitivity of corticosterone and other metabolic variables to graded levels of low intensity stresses in adult male rats, Physiol. Behav. 37, 559–561.
   PubMedGoogle Scholar
• Armario, A., Mart?´, J. and Gil, M. (1990) The serum glucose response to acute stress is sensitive to the intensity of the stressor and to habituation, Psychoneuroendocrinology 15, 341–347.
   Google Scholar
• Armario, A., Gil, M., Marti, J., Pol, O. and Balasch, J. (1991) Influence of various acute stressors on the activity of adult male rats in a holeboard and in the forced swim test, Pharmacol. Biochem. Behav. 39, 373–377.
   PubMed Web of Science ®Google Scholar
• Armario, A., Mart?´, O., Valle`s, A., Dal-Zotto, S. and Ons, S. (2004) Longterm effects of a single exposure to immobilization on the hypothalamic–pituitary–adrenal axis: neurobiologic mechanisms, Ann. NY Acad. Sci. 1018, 162–172.
   Google Scholar
• Aubry, J.M., Bartanusz, V., Jezova, D., Belin, D. and Kiss, J.Z. (1999) Single stress induces long-lasting elevations in vasopressin mRNA levels in CRF hypophysiotrophic neurones, but repeated stress is required to modify AVP immunoreactivity, J. Neuroendocrinol. 11, 377–384.
   PubMed Web of Science ®Google Scholar
• Baker, D.G.,West, S.A., Nicholson,W.E., Ekhator, N.N., Kasckow, J.W., Hill, K.K., Bruce, A.B., Orth, D.N. and Geracioti, T.D. (1999) Serial CSF corticotropin-releasing hormone levels and adrenocortical activity in combat veterans with posttraumatic stress disorder, Am. J. Psychiat. 156, 585–588.
   PubMed Web of Science ®Google Scholar
• Belda, X., Ma´rquez, C. and Armario, A. (2004) Long-term effects of a single exposure to stress in adult rats on behavior and hypothalamic– pituitary–adrenal responsiveness: comparison of two outbred rat strains, Behav. Brain Res. 154, 399–408.
   PubMed Web of Science ®Google Scholar
• Bonaz, B. and Rivest, S. (1998) Effect of chronic stress on CRF neuronal activity and expression of its type 1 receptor in the rat brain, Am. J. Physiol. 275, R1438–R1449.
   Google Scholar
• Bremmer, J.D., Licinio, J., Darnell, A., Krystal, J.H., Owens, M.J., Southwick, S.M., Nemeroff, C.B. and Charney, D.S. (1997) Elevated CSF corticotropin-releasing factor concentrations in posttraumatic stress disorder, Am. J. Psychiat. 154, 624–629.
   Google Scholar
• Bremmer, J.D., Vythilingam, M., Vermetten, E., Adil, J., Khan, S., Nazeer, A., Afzal, N., McGlashan, T., Elzinga, B., Anderson, G.M., Heninger, G., Southwick, S.M. and Charney, D.S. (2003) Cortisol response to a cognitive stress challenge in posttraumatic stress disorder (PTSD) related to childhood abuse, Psychoneuroendocrinology 28, 733–750.
   Google Scholar
• Brennan, F.X., Ottenweller, J.E., Seifu, Y., Zhu, G. and Servatius, R.J. (2000) Persistent stress-induced elevations of urinary corticosterone in rats, Physiol. Behav. 71, 441–446.
   Google Scholar
• Buwalda, B., de Boer, S.F., Schmidt, E.D., Felszeghy, K., Nyakas, C., Sgoifo, A., Van der Vegt, B.J., Tilders, F.J., Bohus, B. and Koolhaas, J.M. (1999) Long-lasting deficient dexamethasone suppression of hypothalamic–pituitary–adrenocortical activation following peripheral CRF challenge in socially defeated rats, J. Neuroendocrinol. 11, 513–520.
   PubMedGoogle Scholar
• Campmany, L., Pol, O. and Armario, A. (1996) The effects of two chronic intermittent stressors on brain monoamines, Pharmacol. Biochem. Behav. 53, 517–523.
   PubMedGoogle Scholar
• Carobrez, S.G., Gasparotto, O.C., Buwalda, B. and Bohus, B. (2002) Long-term consequences of social stress on corticosterone and IL- 1beta levels in endotoxin-challenged rats, Physiol. Behav. 76, 99–105.
   Google Scholar
• Chautard, T., Spinedi, E., Voirol, M.-J., Pralong, F.P. and Gaillard, R.C. (1999) Role of glucocorticoids in the response of the hypothalamocorticotrope, immune and adipose systems to repeated endotoxin administration, Neuroendocrinology 69, 360–369.
   PubMed Web of Science ®Google Scholar
• Chen, X. and 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.
   PubMed Web of Science ®Google Scholar
• Cole, M.A., Kalman, B.A., Pace, T.W.W., Topczewski, F., Lowrey, M.J. and Spencer, R.L. (2000) Selective blockade of the mineralocorticoid receptor impairs hypothalamic–pituitary–adrenal axis expression of habituation, J. Neuroendocrinol. 12, 1034–1042.
   PubMed Web of Science ®Google Scholar
• Cullinan, W.E., Herman, J.P., Battaglia, D.F., Akil, H. and Watson, S.J. (1995) Pattern and time course of immediate early gene expression in rat brain following acute stress, Neuroscience 64, 477–505.
   PubMed Web of Science ®Google Scholar
• Dal-Zotto, S., Mart?´, O. and Armario, A. (2000) Influence of single or repeated experience of rats with forced swimming on behavioural and physiological responses to the stressor, Behav. Brain Res. 114, 175–181.
   Google Scholar
• Dal-Zotto, S., Mart?´, O. and Armario, A. (2002) Is repeated exposure to immobilization needed to induce adaptation of the hypothalamic– pituitary–adrenal axis? Influence of adrenal factors, Behav. Brain Res. 129, 187–195.
   Google Scholar
• Dal-Zotto, S., Mart?´, O. and Armario, A. (2003) Glucocorticoids are involved in the long-term effects of a single immobilization stress on the hypothalamic–pituitary–adrenal axis, Psychoneuroendocrinology 28, 992–1009.
   Google Scholar
• Dal-Zotto, S., Mart?´, O., Delgado, R. and Armario, A. (2004) Potentiation of glucocorticoid release does not modify the long-term effects of single exposure to immobilization stress, Psychopharmacology, (in press).
   Google Scholar
• Dallman, M.F.,Akana, S.F., Schribner, K.A.,Bradbury, M.J.,Walker, C.-D., Strack, A.M. and Cascio, C.S. (1992) Stress, feedback and facilitation in the hypothalamo–pituitary–adrenal axis, J. Neuroedocrinol. 4, 517–526.
   PubMed Web of Science ®Google Scholar
• Dayas, C.V., Buller, K.M. and Day, T.A. (1999) Neuroendocrine responses to an emotional stressor: evidence for involvement of the medial but not the central amygdala, Eur. J. Neurosci. 11, 2312–2322.
   PubMed Web of Science ®Google Scholar
• Dayas, C.V., Buller, K.M., Crane, J.W., Xu, Y. and Day, T.A. (2001) Stressor categorization: acute physical and psychological stressors elicit distinctive recruitment patterns in the amygdala and in medullary noradrenergic cell groups, Eur. J. Neurosci. 14, 1143–1152.
   PubMed Web of Science ®Google Scholar
• De Boer, S.F., Koopmans, S.J., Slangen, J.L. and Van der Gugten, J. (1990) Plasma catecholamine, corticosterone and glucose responses to repeated stress in rats: effect of interstressor interval length, Physiol. Behav. 47, 1117–1124.
   PubMed Web of Science ®Google Scholar
• De Goeij, D.C., Kvetnansky, R., Whitnall, M.H., Jezova, D., Berkenbosch, F. and Tilders, F.J. (1991) Repeated stress-induced activation of corticotropin-releasing factor neurons enhances vasopressin stores and colocalization with corticotropin-releasing factor in the median eminence of rats, Neuroendocrinology 53, 150–159.
   PubMed Web of Science ®Google Scholar
• De Goeij, D.C., Dijkstra, H. and Tilders, F.J. (1992) Chronic psychosocial stress enhances vasopressin, but not corticotropin-releasing factor, in the external zone of the median eminence of male rats: relationship to subordinate status, Endocrinology 131, 847–853.
   PubMed Web of Science ®Google Scholar
• Diorio, D., Viau, V. and Meaney, M.J. (1993) The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic– pituitary–adrenal responses to stress, J. Neurosci. 13, 3839–3847.
   PubMed Web of Science ®Google Scholar
• Dobrakovova, M., Kvetnansky, R., Oprsalova, Z. and Jezova, D. (1993) Specificity of the effect of repeated handling on sympathetic– adrenomedullary and pituitary–adrenocortical activity in rats, Psychoneuroendocrinology 18, 163–174.
   PubMed Web of Science ®Google Scholar
• Elmquist, J.K., Ackermann, M.R., Register, K.B., Rimler, R.B., Ross, L.R. and Jacobson, C.D. (1993) Induction of Fos-like immunoreactivity in the rat brain following Pasteurella multocida endotoxin administration, Endocrinology 133, 3054–3057.
   PubMed Web of Science ®Google Scholar
• Elmquist, J.K., Scammell, T.E., Jacobson, C.D. and Saper, C.B. (1996) Distribution of fos-like immunoreactivity in the rat brain following intravenous lipopolysaccharide administration, J. Comp. Neurol. 371, 85–103.
   PubMed Web of Science ®Google Scholar
• Elzinga, B.M., Schmahl, C.G., vermetten, E., van Dyck, R. and Bremmer, J.D. (2003) Higher aacortisol levels following exposure to traumatic reminders in abuse-related PTSD, Neuropsychopharmacology 28, 1656–1665.
   Google Scholar
• Emmert, M.H. and Herman, J.P. (1999) Differential forebrain c-fos mRNA induction by ether inhalation and novelty: evidence for distinctive stress pathways, Brain Res. 845, 60–67.
   PubMed Web of Science ®Google Scholar
• Figueiredo, H.F., Bruestle, A., Bodie, B., Dolgas, C.M. and Herman, J.P. (2003a) The medial prefrontal cortex differentially regulates stressinduced c-fos expression in the forebrain depending on type of stressor, Eur. J. Neurosci. 18, 2357–2364.
   PubMed Web of Science ®Google Scholar
• Figueiredo, H.F., Bodie, N.L., Tauchi, M., Dolgas, C.M. and Herman, J.P. (2003b) Stress integration after acute and chronic predator stress: differential activation of central stress circuitry and sensitization of the hypothalamic-pituitary-adrenocortical axis, Endocrinology 144, 5249–5258.
   PubMed Web of Science ®Google Scholar
• Garcia, A., Mart?´, O., Valle`s, A., Dal-Zotto, S. and Armario, A. (2000) Recovery of the hypothalamic-pituitary-adrenal response to stress. Effect of stress intensity, stress duration and previous stress exposure, Neuroendocrinology 72, 114–125.
   Google Scholar
• Goldstein, L.E., Rasmusson, A.M., Bunney, B.S. and Roth, R.H. (1996) Role of amygdala in the coordination of behavioral, neuroendocrine, and prefrontal cortical monoamine responses to psychological stress in rats, J. Neurosci. 16, 4787–4798.
   PubMed Web of Science ®Google Scholar
• Gray, T.S., Piechowski, R.A., Yracheta, J.M., Tittenhouse, P.A., Bethea, C.L. and 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.
   PubMed Web of Science ®Google Scholar
• Groves, P.M. and Thompson, R.F. (1970) Habituation: a dual-process theory, Psychol. Rev. 77, 419–450.
   PubMed Web of Science ®Google Scholar
• Hajos-Korcsok, E., Robinson, D.D., Yu, J.H., Fitch, C.S., Walke, E. and Merchant, K.M. (2003) Rapid habituation of hippocampal serotonin and norepinephrine release and anxiety-related behaviors, but not plasma corticosterone levels, to repeated footshock stress in rats, Pharmacol. Biochem. Behav. 74, 609–616.
   PubMed Web of Science ®Google Scholar
• Harbuz, M.S. and Lightman, S.L. (1989) Responses of hypothalamic and pituitary mRNA to physical and psychological stress in the rat, J. Endocrinol. 122, 705–711.
   PubMedGoogle Scholar
• Hare, A.S., Clarke, G. and Tolchard, S. (1995) Bacterial lipopolysaccharide- induced changes in FOS protein expression in the rat brain: correlation with thermoregulatory changes and plasma corticosterone, J. Neuroendocrinol. 7, 791–799.
   Google Scholar
• Hayley, S., Brebner, K., Lacosta, S., Merali, Z. and Anisman, H. (1999) Sensitization to the effects of tumor necrosis factor-alpha: neuroendocrine, central monoamine, and behavioral variations, J. Neurosci. 19, 5654–5665.
   PubMed Web of Science ®Google Scholar
• Hayley, S., Lacosta, S., Merali, Z., van Rooijen, N. and Anisman, H. (2001a) Central monoamine and plasma corticosterone changes induced by a bacterial endotoxin: sensitization and cross-sensitization effects, Eur. J. Neurosci. 13, 1155–1165.
   Google Scholar
• Hayley, S., Staines, W., Merali, Z. and Anisman, H. (2001b) Timedependent sensitization of corticotropin-releasing hormone, arginine vasopressin and c-fos immunoreactivity within the mouse brain in response to tumor necrosis factor-alpha, Neuroscience 106, 137–148.
   PubMed Web of Science ®Google Scholar
• Hayley, S., Wall, P. and Anisman, H. (2002) Sensitization to the neuroendocrine, central monoamine and behavioural effects of murine tumor necrosis factor-alpha: peripheral and central mechanisms, Eur. J. Neurosci. 15, 1061–1076.
   PubMed Web of Science ®Google Scholar
• Herman, J.P. (1995) In situ hybridization 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.
   PubMedGoogle Scholar
• Herman, J.P., Figueiredo, H., Mueller, N.K., Ulrich-Lai, Y., Ostrander, M.M., Choi, D.C. and Cullinan, W.E. (2003) Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo– pituitary–adrenocortical responsiveness, Front. Neuroendocrinol. 24, 151–180.
   PubMed Web of Science ®Google Scholar
• Imaki, T., Xiao Quan, W., Shibasaki, T., Yamada, K., Harada, S., Chikada, N., Naruse, M. and Demura, H. (1995) Stress-induced activation of neuronal activity and corticotropin-releasing factor gene expression in the paraventricular nucleus is modulated by glucocorticoids in rats, J. Clin. Investig. 96, 231–238.
   PubMed Web of Science ®Google Scholar
• Johnson, J.D., O’Connor, K.A., Deak, T., Spencer, R.L., Watkins, L.R. and Maier, S.F. (2002) Prior stressor exposure primes the HPA axis, Psychoneuroendocrinology 27, 353–365.
   PubMed Web of Science ®Google Scholar
• Kitraki, E., Karandrea, D. and Kittas, C. (1999) Long-lasting effects of stress on glucocorticoid receptor gene expression in the rat brain, Neuroendocrinology 69, 331–338.
   PubMedGoogle Scholar
• Kovacs, K.J. (1998) c-Fos as a transcription factor: a stressful (re)view from a functional map, Neurochem. Int. 33, 287–297.
   PubMed Web of Science ®Google Scholar
• Kovacs, K.J. and Sawchenko, P.E. (1996) Sequence of stress-induced alterations in indices of synaptic and transcriptional activation in parvocellular neurosecretory neurons, J. Neurosci. 16, 262–273.
   PubMed Web of Science ®Google Scholar
• Lachuer, J., Delton, I., Buda, M. and Tappaz, M. (1994) The habituation of brainstem catecholaminergic groups to chronic daily restraint stress is stress specific like that of the hypothalamo–pituitary– adrenal axis, Brain Res. 638, 196–202.
   PubMed Web of Science ®Google Scholar
• Li, H.Y. and 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.
   PubMed Web of Science ®Google Scholar
• Li, H.Y., Ericsson, A. and Sawchenko, P.E. (1996) Distinct mechanisms underlie activation of hypothalamic neurosecretory neurons and their medullary catecholaminergic afferents in categorically different stress paradigms, Proc. Natl Acad. Sci. USA 93, 2359–2364.
   PubMed Web of Science ®Google Scholar
• Liberzon, I., Krstov, M. and Young, E.A. (1997) Stress–restress: effects on ACTH and fast feedback, Psychoneuroendocrinology 22, 443–453.
   PubMed Web of Science ®Google Scholar
• Ma, X.M. and Aguilera, G. (1999) Transcriptional responses of the vasopressin and corticotropin-releasing hormone genes to acute and repeated intraperitoneal hypertonic saline injection in rats, Mol. Brain Res. 68, 129–140.
   PubMedGoogle Scholar
• Ma, X.M. and Lightman, S.L. (1998) The arginine vasopressin and corticotrophin-releasing hormone gene transcription responses to varied frequencies of repeated stress in rats, J. Physiol. 510, 605–614.
   PubMed Web of Science ®Google Scholar
• Ma, X.M., Lightman, S.L. and Aguilera, G. (1999) Vasopressin and corticotropin-releasing hormone gene responses to novel stress in rats adapted to repeated restraint, Endocrinology 140, 3623–3632.
   PubMed Web of Science ®Google Scholar
• Maier, S.F. (2001) Exposure to the stressor environment prevents the temporal dissipation of behavioral depression/learned helplessness, Biol. Psychiatry 49, 763–773.
   PubMed Web of Science ®Google Scholar
• Martinez, M., Phillips, P. and 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.
   PubMedGoogle Scholar
• Marti, O. and Armario, A. (1998) Anterior pituitary response to stress: time-related changes and adaptation, Int. J. Dev. Neurosci. 16, 241–260.
   PubMed Web of Science ®Google Scholar
• Marti, O., Mart?´, J. and Armario, A. (1994) Effects of chronic stress on food intake in rats: influence of stressor intensity and duration of daily exposure, Physiol. Behav. 55, 747–753.
   Google Scholar
• Marti, O., Gavalda`, A., Jolin, T. and Armario, A. (1996) Acute stress attenuates but does not abolish circadian rhythmicity of serum thyrotrophin and growth hormone in the rat, Eur. J. Endocrinol. 135, 703–708.
   PubMed Web of Science ®Google Scholar
• Marti, O., Garcia, A., Valle`s, A., Harbuz, M.S. and Armario, A. (2001) Evidence that a single exposure to aversive stimuli triggers longlasting effects in the hypothalamus–pituitary–adrenal axis that consolidate with time, Eur. J. Neurosci. 13, 129–136.
   PubMed Web of Science ®Google Scholar
• McFarlane, A.C., Atchison, M. and Yehuda, R. (1997) The acute stress response following motor vehicle accidents and its relation to PTSD, Ann. N.Y. Acad. Sci. 821, 437–441.
   PubMed Web of Science ®Google Scholar
• Melia, K.R., Ryabinin, A.E., Schroeder, R., Bloom, F.E. and Wilson, M.C. (1994) Induction and habituation of immediate early gene expression in rat brain by acute and repeated restraint stress, J. Neurosci. 14, 5929–5938.
   PubMed Web of Science ®Google Scholar
• Mizoguchi, K., Ishige, A., Aburada, M. and Tabira, T. (2003) Chronic stress attenuates glucocorticoid negative feedback: involvement of the prefrontal cortex and hippocampus, Neuroscience 119, 887–897.
   PubMed Web of Science ®Google Scholar
• Ma´rquez, C., Belda, X. and Armario, A. (2002) Post-stress recovery of pituitary–adrenal hormones and glucose, but not the response during exposure to the stressor, is a marker of stress intensity in highly stressful situations, Brain Res. 926, 181–185.
   PubMed Web of Science ®Google Scholar
• Ma´rquez, C., Nadal, R. and Armario, A. (2004) The hypothalamicpituitary– adrenal and glucose responses to daily repeated immobilisation stress in rats: individual differences, Neuroscience 123, 601–612.
   PubMed Web of Science ®Google Scholar
• Nisenbaum, L.K. and Abercrombie, E.D. (1992) Enhanced tyrosine hydroxylation in hippocampus of chronically stressed rats upon exposure to a novel stressor, J. Neurochem. 58, 276–281.
   PubMed Web of Science ®Google Scholar
• O’Connor, K.A., Johnson, J.D., Hammack, S.E., Brooks, L.M., Spencer, R.L., Watkins, L.R. and Maier, S.F. (2003) Inescapable shock induces resistance to the effects of dexamethasone, Psychoneuroendocrinology 28, 481–500.
   PubMed Web of Science ®Google Scholar
• Ottenweller, J.E., Servatius, R.J., Tapp,W.N., Drastal, S.D., Bergen, M.T. and Natelson, B.H. (1992) A chronic stress state in rats: effects of repeated stress on basal corticosterone and behavior, Physiol. Behav. 51, 689–698.
   PubMed Web of Science ®Google Scholar
• Pacak, K. and Palkovits, M. (2001) Stressor specificity of central neuroendocrine responses: implications for stress-related disorders, Endocr. Rev. 22, 502–548.
   PubMed Web of Science ®Google Scholar
• Pinnock, S.B. and Herbert, J. (2001)Corticosterone differentiallymodulates 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.
   Google Scholar
• Resnick, H.S., Yehuda, R., Pitman, R.K. and Foy, D.W. (1995) Effect of previous trauma on acute plasma cortisol level following rape, Am. J. Psychiatry 152, 1675–1677.
   PubMed Web of Science ®Google Scholar
• Riccio, D.C., MacArdy, E.A. and Kissinger, S.C. (1991) Associative processes in adaptation to repeated cold exposure in rats, Behav. Neurosci. 105, 599–602.
   Google Scholar
• Rivest, S. and Laflamme, N. (1995) Neuronal activity and neuropeptide gene transcription in the brains of immune-challenged rats, J. Neuroendocrinol. 7, 501–525.
   PubMed Web of Science ®Google Scholar
• Robinson, T.E., Browman, K.E., Crombag, H.S. and Badiani, A. (1998) Modulation of the induction or expression of psychostimulant sensitization by the circumstances surrounding drug administration, Neurosci. Biobehav. Rev. 22, 347–354.
   PubMedGoogle Scholar
• Schmidt, E.D., Janszen, A.W., Wouterlood, F.G. and Tilders, F.J. (1995) Interleukin-1-induced long-lasting changes in hypothalamic corticotropin- releasing hormone (CRH)–neurons and hyperresponsiveness of the hypothalamus–pituitary–adrenal axis, J. Neurosci. 15, 7417–7426.
   PubMed Web of Science ®Google Scholar
• Schmidt, E.D., Binnekade, R., Janszen, A.W. and Tilders, F.J. (1996) Short stressor induced long-lasting increases of vasopressin stores in hypothalamic corticotropin-releasing hormone (CRH) neurons in adult rats, J. Neuroendocrinol. 8, 703–712.
   PubMedGoogle Scholar
• Schmidt, E.D., Tilders, F.J., Binnekade, R., Schoffelmeer, A.N. and De Vries, T.J. (1999) Stressor- or drug-induced sensitization of the corticosterone response is not critically involved in the long-term expression of behavioural sensitization to amphetamine, Neuroscience 92, 343–352.
   PubMed Web of Science ®Google Scholar
• Schmidt, E.D., Schoffelmeer, A.N., De Vries, T.J., Wardeh, G., Dogterom, G., Bol, J.G., Binnekade, R. and Tilders, F.J. (2001) A single administration of interleukin-1 or amphetamine induces long-lasting increases in evoked noradrenaline release in the hypothalamus and sensitization of ACTH and corticosterone responses in rats, Eur. J. Neurosci. 13, 1923–1930.
   Google Scholar
• Schmidt, E.D., Aguilera, G., Binnekade, R. and Tilders, F.J. (2003) Single administration of interleukin-1 increased corticotropin releasing hormone and corticotropin releasing hormone-receptor mRNA in the hypothalamic paraventricular nucleus which paralleled long-lasting (weeks) sensitization to emotional stressors, Neuroscience 116, 275–283.
   PubMed Web of Science ®Google Scholar
• Senba, E. and Ueyama, T. (1997) Stress-induced expression of immediate early genes in the brain and peripheral organs of the rat, Neurosci. Res. 29, 183–207.
   PubMed Web of Science ®Google Scholar
• Servatius, R.J., Ottenweller, J.E. and Natelson, B.H. (1995) Delayed startle sensitization distinguishes rats exposed to one or three stress sessions: further evidence toward an animal model of PTSD, Biol. Psychiatry 38, 539–546.
   PubMed Web of Science ®Google Scholar
• Siegel, S. (1999) Drug anticipation and drug addiction. The 1998 H. David Archibald lecture, Addiction 94, 1123–1134.
   Google Scholar
• Smith, R., Lovelock, M., Owens, P.C., Chan, E.C. and Falconer, J. (1988) The effect of repetititve haemorrhage on plasma cortisol, Betaendorphin and N-terminal pro-opiomelanocortin in conscious sheep, Horm. Metabol. Res. 20, 612–615.
   Google Scholar
• Stamp, J.A. and Herbert, J. (1999) Multiple immediate-early gene expression during physiological and endocrine adaptation to repeated stress, Neuroscience 94, 1313–1322.
   PubMedGoogle Scholar
• Terrazzino, S., Perego, C. and De Simoni, M.G. (1995) Effect of development of habituation to restraint stress on the hypothalamic noradrenaline release and adrenocorticotropin secretion, J. Neurochem. 65, 263–267.
   PubMed Web of Science ®Google Scholar
• Uhlir, I., Seggie, J. and Brown, G.M. (1974) The effect of septal lesions on the threshold of adrenal stress response, Neuroendocrinology 14, 351–355.
   Google Scholar
• Umemoto, S., Kawakai, Y. and Senba, E. (1994a) Differential regulation of IEG in the rat PVH in single and repeated stress models, NeuroReport 6, 201–204.
   Google Scholar
• Umemoto, S., Noguchi, K., Kawakai, Y. and Senba, E. (1994b) Repeated stress reduces the subsequent stress-induced expression of Fos in rat brain, Neurosci. Lett. 167, 201–204.
   Google Scholar
• Umemoto, S., kawai, Y., Ueyama, T. and Senba, E. (1997) Chronic glucocorticoid administration as well as repeated stress affects the subsequent acute immobilization stress-induced expression of immediate early genes but not that of NGFI-A, Neuroscience 80, 763–773.
   Google Scholar
• Valle`s, A., Mart?´, O., Garcia, A. and Armario, A. (2000) Single exposure to stressors causes long-lasting, stress-dependent reduction of food intake in rats, Am. J. Physiol. Regul. Integr. Comp. Physiol. 279, R1138–R1144.
   Google Scholar
• Valle`s, A., Mart?´, O., Harbuz, M.S. and Armario, A. (2002) A single lipopolysaccharide administration is sufficient to induce a long-term desensitization of the hypothalamic–pituitary–adrenal axis, Neuroscience 112, 383–389.
   Google Scholar
• Valle`s, A., Mart?´, O. and Armario, A. (2003) Long-term effects of a single exposure to immobilization stress on the hypothalamic–pituitary– adrenal axis: transcriptional evidence for a progressive desensitization process, Eur. J. Neurosci. 18, 1–9.
   Google Scholar
• Van Dijken, H.H., Van der Heyden, J.A., Mos, J. and Tilders, F.J. (1992) Inescapable footshocks induce progressive and long-lasting behavioural changes in male rats, Physiol. Behav. 51, 787–794.
   PubMed Web of Science ®Google Scholar
• Van Dijken, H.H., de Goeij, D.C., Sutanto,W., Mos, J., de Kloet, E.R. and Tilders, F.J. (1993) Short inescapable stress produces long-lasting changes in the brain–pituitary–adrenal axis of adult male rats, Neuroendocrinology 58, 57–64.
   PubMed Web of Science ®Google Scholar
• Vanderschuren, L.J., Schmidt, E.D., De Vries, T.J., Van Moorsel, C.A., Tilders, F.J. and Schoffelmeer, A.N. (1999) A single exposure to amphetamine is sufficient to induce long-term behavioral, neuroendocrine, and neurochemical sensitization in rats, J. Neurosci. 19, 9579–9586.
   PubMedGoogle Scholar
• Vernikos, J., Dallman, M.F., Bonner, C., Katzen, A. and Shinsako, J. (1982) Pituitary–adrenal function in rats chronically exposed to cold, Endocrinology 110, 413–420.
   PubMed Web of Science ®Google Scholar
• Vinson, G.P., Hinson, J.P. and Toth, I.E. (1994) The neuroendocrinology of the adrenal cortex, J. Neuroendocrinol. 6, 235–246.
   PubMed Web of Science ®Google Scholar
• Watanabe,Y., Stone, E. and McEwen, B.S. (1994) Induction and habituation of c-fos and zif/268 by acute and repeated stressors, NeuroReport 5, 1321–1324.
   PubMed Web of Science ®Google Scholar
• West, M.A. and Heagy, W. (2002) Endotoxin tolerance: a review, Crit. Care Med. 30, S64–S73.
   Web of Science ®Google Scholar
• Xu, Y., Day, T.A. and Buller, K.M. (1999) The central amygdala modulates hypothalamic–pituitary–adrenal axis responses to systemic interleukin-1b administration, Neuroscience 94, 175–183.
   PubMed Web of Science ®Google Scholar
• Yehuda, R. (2001) Biology of posttraumatic stress disorder, J. Clin. Psychiatry 62(Suppl. 17), 41–46.
   Google Scholar
• Yehuda, R., Levengood, R.A., Schmeidler, J., Wilson, S., Guo, L.S. and Gerber, D. (1996) Increased pituitary activation following metyrapone administration in post-traumatic stress disorder, Psychoneuroendocrinology 21, 1–16.
   PubMed Web of Science ®Google Scholar
• Yehuda, R., Bierer, L.M., Schmeidler, J., Aferiat, D.H., Breslau, I. and Dolan, S. (2000) Low cortisol and risk for PTSD in adult offspring of holocaust survivors, Am. J. Psychiatry 157, 1252–1259.
   PubMed Web of Science ®Google Scholar
• Young, E.A., Akana, S. and Dallman, M.F. (1990) Decreased sensitivity to glucocorticoid fast feedback in chronically stressed rats, Neuroendocrinology 51, 536–542.
   PubMed Web of Science ®Google Scholar