Comparison of the effects of single and daily repeated immobilization stress on resting activity and heterotypic sensitization of the hypothalamic–pituitary–adrenal axis

References

• Anisman H, Larry SS. (1985). Psychological and physiological interactions. In: Burchfield SR, editor. Neurochemical consequences of stress: contribution of adaptative processes. New York: Hemisphere Publishing Corp. p 68–98
   Google Scholar
• Armario A. (2006). The hypothalamic-pituitary-adrenal axis: what can it tell us about stressors? CNS & Neurol Disord Drug Targets 5:485–501
   PubMedGoogle Scholar
• Armario A, Escorihuela RM, Nadal R. (2008). Long-term neuroendocrine and behavioural effects of a single exposure to stress in adult animals. Neurosci Biobehav Rev 32:1121–35
   PubMed Web of Science ®Google Scholar
• Armario A, Gil M, Martí J, Pol O, 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 39:373–7
   PubMed Web of Science ®Google Scholar
• Armario A, Hidalgo J, Giralt M. (1988). Evidence that the pituitary-adrenal axis does not cross-adapt to stressors: comparison to other physiological variables. Neuroendocrinology 47:263–7
   PubMed Web of Science ®Google Scholar
• Armario A, Restrepo C, Castellanos JM, Balasch J. (1985). Dissociation between adrenocorticotropin and corticosterone responses to restraint after previous chronic exposure to stress. Life Sci 36:2085–92
   PubMed Web of Science ®Google Scholar
• Armario A, Vallès A, Dal-Zotto S, Márquez C, Belda X. (2004). A single exposure to severe stressors causes long-term desensitisation of the physiological response to the homotypic stressor. Stress 7:157–72
   PubMed Web of Science ®Google Scholar
• Atkinson HC, Wood SA, Kershaw YM, Bate E, Lightman SL. (2006). Diurnal variation in the responsiveness of the hypothalamic-pituitary-adrenal axis of the male rat to noise stress. J Neuroendocrinol 18:526–33
   PubMed Web of Science ®Google Scholar
• Belda X, Daviu N, Nadal R, Armario A. (2012). Acute stress-induced sensitization of the pituitary-adrenal response to heterotypic stressors: independence of glucocorticoid release and activation of CRH1 receptors. Horm Behav 62:515–24
   PubMed Web of Science ®Google Scholar
• Belda X, Fuentes S, Nadal R, Armario A. (2008). A single exposure to immobilization causes long-lasting pituitary-adrenal and behavioral sensitization to mild stressors. Horm Behav 54:654–61
   PubMed Web of Science ®Google Scholar
• Belda X, Márquez C, 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
• Berridge CW, Dunn AJ. (1989). Restraint-stress-induced changes in exploratory behavior appear to be mediated by norepinephrine-stimulated release of CRF. J Neurosci 9:3513–21
   PubMed Web of Science ®Google Scholar
• Bhatnagar S, Dallman M. (1998). Neuroanatomical basis for facilitation of hypothalamic-pituitary-adrenal responses to a novel stressor after chronic stress. Neuroscience 84:1025–39
   PubMed Web of Science ®Google Scholar
• Bhatnagar S, Vining C. (2003). Facilitation of hypothalamic-pituitary-adrenal responses to novel stress following repeated social stress using the resident/intruder paradigm. Horm Behav 43:158–65
   PubMed Web of Science ®Google Scholar
• Breslau N, Chilcoat HD, Kessler RC, Davis GC. (1999). Previous exposure to trauma and PTSD effects of subsequent trauma: results from the Detroit Area Survey of Trauma. Am J Psychiatry 156:902–7
   PubMed Web of Science ®Google Scholar
• Breslau N, Peterson EL, Schultz LR. (2008). A second look at prior trauma and the posttraumatic stress disorder effects of subsequent trauma: a prospective epidemiological study. Arch Gen Psychiatry 65:431–7
   PubMed Web of Science ®Google Scholar
• Calvo N, Martijena ID, Molina VA, Volosin M. (1998). Metyrapone pretreatment prevents the behavioral and neurochemical sequelae induced by stress. Brain Res 800:227–35
   PubMed Web of Science ®Google Scholar
• Cancela LM, Bregonzio C, Molina VA. (1995). Anxiolytic-like effect induced by chronic stress is reversed by naloxone pretreatment. Brain Res Bull 36:209–13
   PubMed Web of Science ®Google Scholar
• Chen J, Young S, Subburaju S, Sheppard J, Kiss A, Atkinson H, Wood S, et al. (2008). Vasopressin does not mediate hypersensitivity of the hypothalamic pituitary adrenal axis during chronic stress. Ann N Y Acad Sci 1148:349–59
   PubMed Web of Science ®Google Scholar
• Cox RH, Hubbard JW, Lawler JE, Sanders BJ, Mitchell VP. (1985). Cardiovascular and sympathoadrenal responses to stress in swim-trained rats. J Appl Physiol 58:1207–14
   PubMed Web of Science ®Google Scholar
• Dallman MF, Akana SF, Scribner KA, Bradbury MJ, Walker CD, Strack AM, Cascio CS. (1992). Stress, feedback and facilitation in the hypothalamo-pituitary-adrenal axis. J Neuroendocrinol 4:517–26
   PubMed Web of Science ®Google Scholar
• Dallman MF, Jones MT. (1973). Corticosteroid feedback control of ACTH secretion: effect of stress-induced corticosterone secretion on subsequent stress responses in the rat. Endocrinology 92:1367–75
   PubMed Web of Science ®Google Scholar
• Engeland WC, Miller P, Gann DS. (1989). Dissociation between changes in plasma bioactive and immunoreactive adrenocorticotropin after hemorrhage in awake dogs. Endocrinology 124:2978–85
   PubMed Web of Science ®Google Scholar
• Fernandes GA, Perks P, Cox NK, Lightman SL, Ingram CD, Shanks N. (2002). Habituation and cross-sensitization of stress-induced hypothalamic-pituitary-adrenal activity: effect of lesions in the paraventricular nucleus of the thalamus or bed nuclei of the stria terminalis. J Neuroendocrinol 14:593–602
   PubMed Web of Science ®Google Scholar
• Fleshner M, Deak T, Spencer RL, Laudenslager ML, Watkins LR, Maier SF. (1995). A long-term increase in basal levels of corticosterone and a decrease in corticosteroid-binding globulin after acute stressor exposure. Endocrinology 136:5336–42
   PubMed Web of Science ®Google Scholar
• Gagliano H, Fuentes S, Nadal R, Armario A. (2008). Previous exposure to immobilisation and repeated exposure to a novel environment demonstrate a marked dissociation between behavioral and pituitary-adrenal responses. Behav Brain Res 187:239–45
   PubMed Web of Science ®Google Scholar
• García A, Martí O, Vallès A, Dal-Zotto S, Armario A. (2000). Recovery of the hypothalamic-pituitary-adrenal response to stress. Effect of stress intensity, stress duration and previous stress exposure. Neuroendocrinology 72:114–25
   PubMed Web of Science ®Google Scholar
• Grissom N, Bhatnagar S. (2009). Habituation to repeated stress: get used to it. Neurobiol Learn Mem 92:215–24
   PubMed Web of Science ®Google Scholar
• Hardin JM, Hilbe JM. (2003). Generalized estimating equations. Boca Raton: Champan and Hall/CRC
   Google Scholar
• Hashimoto K, Suemaru S, Takao T, Sugawara M, Makino S, Ota Z. (1988). Corticotropin-releasing hormone and pituitary-adrenocortical responses in chronically stressed rats. Regul Pept 23:117–26
   PubMedGoogle Scholar
• Hauger RL, Lorang M, Irwin M, Aguilera G. (1990). CRF receptor regulation and sensitization of ACTH responses to acute ether stress during chronic intermittent immobilization stress. Brain Res 532:34–40
   PubMed Web of Science ®Google Scholar
• Hennessy JW, Levin R, Levine S. (1977). Influence of experiential factors and gonadal hormones on pituitary-adrenal response of the mouse to novelty and electric shock. J Comp Physiol Psychol 91:770–7
   PubMed Web of Science ®Google Scholar
• Heydendael W, Sharma K, Iyer V, Luz S, Piel D, Beck S, Bhatnagar S. (2011). Orexins/hypocretins act in the posterior paraventricular thalamic nucleus during repeated stress to regulate facilitation to novel stress. Endocrinology 152:4738–52
   PubMed Web of Science ®Google Scholar
• Irwin MR, Hauger RL. (1988). Adaptation to chronic stress. Temporal pattern of immune and neuroendocrine correlates. Neuropsychopharmacology 1:239–42
   PubMed Web of Science ®Google Scholar
• Johnson JD, O’Connor KA, Deak T, Spencer RL, Watkins LR, Maier SF. (2002). Prior stressor exposure primes the HPA axis. Psychoneuroendocrinology 27:353–65
   PubMed Web of Science ®Google Scholar
• Kennett GA, Chaouloff F, Marcou M, Curzon G. (1986). Female rats are more vulnerable than males in an animal model of depression: the possible role of serotonin. Brain Res 382:416–21
   PubMed Web of Science ®Google Scholar
• Kennett GA, Dickinson SL, Curzon G. (1985). Central serotonergic responses and behavioural adaptation to repeated immobilisation: the effect of the corticosterone synthesis inhibitor metyrapone. Eur J Pharmacol 119:143–52
   PubMed Web of Science ®Google Scholar
• Kim KS, Han PL. (2006). Optimization of chronic stress paradigms using anxiety- and depression-like behavioral parameters. J Neurosci Res 83:497–507
   PubMed Web of Science ®Google Scholar
• Kvetnansky R, Németh S, Vigas M, Oprsalova Z, Jurcovicova J. (1984). Stress. The role of catecholamines and other neurotransmitters. In: Usdin E, Kvetnansky R, Axelrod J, editors. Plasma catecholamines in rats during adaptation to intermittent exposure to dfferent stressors. New York: Gordon and Breach Science Publishers. p 537–62
   Google Scholar
• Kvetnansky R, Sabban EL, Palkovits M. (2009). Catecholaminergic systems in stress: structural and molecular genetic approaches. Physiol Rev 89:535–606
   PubMed Web of Science ®Google Scholar
• Le Mevel JC, Abitbol S, Beraud G, Maniey J. (1979). Temporal changes in plasma adrenocorticotropin concentration after repeated neurotropic stress in male and female rats. Endocrinology 105:812–7
   PubMed Web of Science ®Google Scholar
• Lehnert H, Reinstein DK, Strowbridge BW, Wurtman RJ. (1984). Neurochemical and behavioral consequences of acute, uncontrollable stress: effects of dietary tyrosine. Brain Res 303:215–23
   PubMed Web of Science ®Google Scholar
• Ma XM, Lightman SL. (1998). The arginine vasopressin and corticotrophin-releasing hormone gene transcription responses to varied frequencies of repeated stress in rats. J Physiol 510:605–14
   PubMed Web of Science ®Google Scholar
• Marin MT, Cruz FC, Planeta CS. (2007). Chronic restraint or variable stresses differently affect the behavior, corticosterone secretion and body weight in rats. Physiol Behav 90:29–35
   PubMed Web of Science ®Google Scholar
• Márquez C, Belda X, 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 926:181–5
   PubMed Web of Science ®Google Scholar
• Márquez C, Nadal R, Armario A. (2004). The hypothalamic-pituitary-adrenal and glucose responses to daily repeated immobilisation stress in rats: individual differences. Neuroscience 123:601–12
   PubMed Web of Science ®Google Scholar
• Martí O, Armario A. (1998). Anterior pituitary response to stress: time-related changes and adaptation. Int J Dev Neurosci 16:241–60
   PubMed Web of Science ®Google Scholar
• Martí O, García A, Vallès A, Harbuz MS, Armario A. (2001). Evidence that a single exposure to aversive stimuli triggers long-lasting effects in the hypothalamus-pituitary-adrenal axis that consolidate with time. Eur J Neurosci 13:129–36
   PubMed Web of Science ®Google Scholar
• Martí O, Gavaldà A, Jolín T, Armario A. (1993). Effect of regularity of exposure to chronic immobilization stress on the circadian pattern of pituitary adrenal hormones, growth hormone, and thyroid stimulating hormone in the adult male rat. Psychoneuroendocrinology 18:67–77
   PubMed Web of Science ®Google Scholar
• Mollica RF, McInnes K, Poole C, Tor S. (1998). Dose-effect relationships of trauma to symptoms of depression and post-traumatic stress disorder among Cambodian survivors of mass violence. Br J Psychiatry 173:482–8
   PubMed Web of Science ®Google Scholar
• Netto SM, Silveira R, Coimbra NC, Joca SR, Guimarães FS. (2002). Anxiogenic effect of median raphe nucleus lesion in stressed rats. Prog Neuropsychopharmacol Biol Psychiatry 26:1135–41
   PubMed Web of Science ®Google Scholar
• O’Connor KA, Ginsberg AB, Maksimova E, Wieseler Frank JL, Johnson JD, Spencer RL, Campeau S, et al. (2004). Stress-induced sensitization of the hypothalamic-pituitary adrenal axis is associated with alterations of hypothalamic and pituitary gene expression. Neuroendocrinology 80:252–63
   PubMed Web of Science ®Google Scholar
• O’Connor KA, Johnson JD, Hammack SE, Brooks LM, Spencer RL, Watkins LR, Maier SF. (2003). Inescapable shock induces resistance to the effects of dexamethasone. Psychoneuroendocrinology 28:481–500
   PubMed Web of Science ®Google Scholar
• Osborne B, Seggie J. (1980). Behavioral, corticosterone, and prolactin responses to novel environment in rats with fornix transections. J Comp Physiol Psychol 94:536–46
   PubMed Web of Science ®Google Scholar
• Ostrander MM, Ulrich-Lai YM, Choi DC, Richtand NM, Herman JP. (2006). Hypoactivity of the hypothalamo-pituitary-adrenocortical axis during recovery from chronic variable stress. Endocrinology 147:2008–17
   PubMed Web of Science ®Google Scholar
• Ottenweller JE, Servatius RJ, Natelson BH. (1994). Repeated stress persistently elevates morning, but not evening, plasma corticosterone levels in male rats. Physiol Behav 55:337–40
   PubMed Web of Science ®Google Scholar
• Ottenweller JE, Servatius RJ, Tapp WN, Drastal SD, Bergen MT, Natelson BH. (1992). A chronic stress state in rats: effects of repeated stress on basal corticosterone and behavior. Physiol Behav 51:689–98
   PubMed Web of Science ®Google Scholar
• Pace TW, Cole MA, Ward G, Kalman BA, Spencer RL. (2001). Acute exposure to a novel stressor further reduces the habituated corticosterone response to restraint in rats. Stress 4:319–31
   PubMedGoogle Scholar
• Pawlak R, Magarinos AM, Melchor J, McEwen B, Strickland S. (2003). Tissue plasminogen activator in the amygdala is critical for stress-induced anxiety-like behavior. Nat Neurosci 6:168–74
   PubMed Web of Science ®Google Scholar
• Pellow S, File SE. (1986). Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus-maze: a novel test of anxiety in the rat. Pharmacol Biochem Behav 24:525–9
   PubMed Web of Science ®Google Scholar
• Plaznik A, Tamborska E, Hauptmann M, Bidzinski A, Kostowski W. (1988). Brain neurotransmitter systems mediating behavioral deficits produced by inescapable shock treatment in rats. Brain Res 447:122–32
   PubMed Web of Science ®Google Scholar
• Pol O, Campmany L, Gil M, Armario A. (1992). Behavioral and neurochemical changes in response to acute stressors: influence of previous chronic exposure to immobilization. Pharmacol Biochem Behav 42:407–12
   PubMed Web of Science ®Google Scholar
• Rabasa C, Munoz-Abellán C, Daviu N, Nadal R, Armario A. (2011). Repeated exposure to immobilization or two different footshock intensities reveals differential adaptation of the hypothalamic-pituitary-adrenal axis. Physiol Behav 103:125–33
   PubMed Web of Science ®Google Scholar
• Reinstein DK, Lehnert H, Scott NA, Wurtman RJ. (1984). Tyrosine prevents behavioral and neurochemical correlates of an acute stress in rats. Life Sci 34:2225–31
   PubMed Web of Science ®Google Scholar
• Sakellaris PC, Vernikos-Danellis J. (1975). Increased rate of response of the pituitary-adrenal system in rats adapted to chronic stress. Endocrinology 97:597–602
   PubMed Web of Science ®Google Scholar
• Servatius RJ, Ottenweller JE, Bergen MT, Soldan S, Natelson BH. (1994). Persistent stress-induced sensitization of adrenocortical and startle responses. Physiol Behav 56:945–54
   PubMed Web of Science ®Google Scholar
• Spiga F, Harrison LR, MacSweeney CP, Thomson FJ, Craighead M, Lightman SL. (2009). Effect of vasopressin 1b receptor blockade on the hypothalamic-pituitary-adrenal response of chronically stressed rats to a heterotypic stressor. J Endocrinol 200:285–91
   PubMed Web of Science ®Google Scholar
• Steenbergen HL, Heinsbroek RP, Van Hest A, Van de Poll NE. (1990). Sex-dependent effects of inescapable shock administration on shuttlebox-escape performance and elevated plus-maze behavior. Physiol Behav 48:571–6
   PubMed Web of Science ®Google Scholar
• Stone EA, McCarty R. (1983). Adaptation to stress: tyrosine hydroxylase activity and catecholamine release. Neurosci Biobehav Rev 7:29–34
   PubMed Web of Science ®Google Scholar
• Ulrich-Lai YM, Arnhold MM, Engeland WC. (2006). Adrenal splanchnic innervation contributes to the diurnal rhythm of plasma corticosterone in rats by modulating adrenal sensitivity to ACTH. Am J Physiol Regul Integr Comp Physiol 290:1128–35
   PubMed Web of Science ®Google Scholar
• Ulrich-Lai YM, Ostrander MM, Thomas IM, Packard BA, Furay AR, Dolgas CM, Van Hooren DC, et al. (2007). Daily limited access to sweetened drink attenuates hypothalamic-pituitary-adrenocortical axis stress responses. Endocrinology 148:1823–34
   PubMed Web of Science ®Google Scholar
• Vahl TP, Ulrich-Lai YM, Ostrander MM, Dolgas CM, Elfers EE, Seeley RJ, D’Alessio DA, Herman JP. (2005). Comparative analysis of ACTH and corticosterone sampling methods in rats. Am J Physiol Endocrinol Metab 289:823–8
   PubMed Web of Science ®Google Scholar
• Vernikos J, Dallman MF, Bonner C, Katzen A, Shinsako J. (1982). Pituitary-adrenal function in rats chronically exposed to cold. Endocrinology 110:413–20
   PubMed Web of Science ®Google Scholar
• Vyas A, Pillai AG, Chattarji S. (2004). Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior. Neuroscience 128:667–73
   PubMed Web of Science ®Google Scholar
• Weinberg MS, Bhatt AP, Girotti M, Masini CV, Day HE, Campeau S, Spencer RL. (2009). Repeated ferret odor exposure induces different temporal patterns of same-stressor habituation and novel-stressor sensitization in both hypothalamic-pituitary-adrenal axis activity and forebrain c-fos expression in the rat. Endocrinology 150:749–61
   PubMed Web of Science ®Google Scholar
• Weiss JM, Glazer HI, Pohorecky LA, Brick J, Miller NE. (1975). Effects of chronic exposure to stressors on avoidance-escape behavior and on brain norepinephrine. Psychosom Med 37:522–34
   PubMed Web of Science ®Google Scholar
• Wotjak CT, Ganster J, Kohl G, Holsboer F, Landgraf R, 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 85:1209–22
   PubMed Web of Science ®Google Scholar
• Yehuda R, Kahana B, Schmeidler J, Southwick SM, Wilson S, Giller EL. (1995). Impact of cumulative lifetime trauma and recent stress on current posttraumatic stress disorder symptoms in holocaust survivors. Am J Psychiatry 152:1815–8
   PubMed Web of Science ®Google Scholar
• Zelena D, Mergl Z, Foldes A, Kovacs KJ, Toth Z, Makara GB. (2003). Role of hypothalamic inputs in maintaining pituitary-adrenal responsiveness in repeated restraint. Am J Physiol Endocrinol Metab 285:E1110–17
   PubMed Web of Science ®Google Scholar