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Current Neuropharmacology

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ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

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Review Article

Differential Hypothalamic-pituitary-adrenal Response to Stress among Rat Strains: Methodological Considerations and Relevance for Neuropsychiatric Research

Author(s): Antonio Armario*, Xavier Belda, Humberto Gagliano, Silvia Fuentes, Patricia Molina, Sara Serrano and Roser Nadal

Volume 21, Issue 9, 2023

Published on: 20 February, 2023

Page: [1906 - 1923] Pages: 18

DOI: 10.2174/1570159X21666221129102852

Price: $65

Abstract

The hormones of the hypothalamic-pituitary-adrenal (HPA) axis, particularly glucocorticoids (GCs), play a critical role in the behavioral and physiological consequences of exposure to stress. For this reason, numerous studies have described differences in HPA function between different rodent strains/lines obtained by genetic selection of certain characteristics not directly related to the HPA axis. These studies have demonstrated a complex and poorly understood relationship between HPA function and certain relevant behavioral characteristics. The present review first remarks important methodological considerations regarding the evaluation and interpretation of resting and stress levels of HPA hormones. Then, it presents works in which differences in HPA function between Lewis and Fischer rats were explored as a model for how to approach other strain comparisons. After that, differences in the HPA axis between classical strain pairs (e.g. High and Low anxiety rats, Roman high- and low-avoidance, Wistar Kyoto versus Spontaneously Hypertensive or other strains, Flinder Sensitive and Flinder Resistant lines) are described. Finally, after discussing the relationship between HPA differences and relevant behavioral traits (anxiety-like and depression-like behavior and coping style), an example for main methodological and interpretative concerns and how to test strain differences is offered.

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[1]
Vigas, M. Contribution to the Understanding of the Stress Concept. In: Catecholamines and stress: Recent advances; Usdin, E.; Kvetnansky, R.; Kopin, I., Eds.; Elsevier/North-Holland: Amsterdam, 1980; pp. 573-578.
[2]
Herman, J.P.; McKlveen, J.M.; Ghosal, S.; Kopp, B.; Wulsin, A.; Makinson, R.; Scheimann, J.; Myers, B. Regulation of the hypothalamic- pituitary-adrenocortical stress response. Compr. Physiol., 2016, 6(2), 603-621.
[http://dx.doi.org/10.1002/cphy.c150015] [PMID: 27065163]
[3]
Sapolsky, R.M.; Romero, L.M.; Munck, A.U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev., 2000, 21(1), 55-89.
[http://dx.doi.org/10.1210/er.21.1.55] [PMID: 10696570]
[4]
Finsterwald, C.; Alberini, C.M. Stress and glucocorticoid receptordependent mechanisms in long-term memory: From adaptive responses to psychopathologies. Neurobiol. Learn. Mem., 2014, 112, 17-29.
[http://dx.doi.org/10.1016/j.nlm.2013.09.017] [PMID: 24113652]
[5]
Armario, A.; Labad, J.; Nadal, R. Focusing attention on biological markers of acute stressor intensity: Empirical evidence and limitations. Neurosci. Biobehav. Rev., 2020, 111, 95-103.
[http://dx.doi.org/10.1016/j.neubiorev.2020.01.013] [PMID: 31954151]
[6]
Chrousos, G.P.; Gold, P.W. The concepts of stress and stress system disorders. Overview of physical and behavioral homeostasis. JAMA, 1992, 267(9), 1244-1252.
[http://dx.doi.org/10.1001/jama.1992.03480090092034] [PMID: 1538563]
[7]
Chrousos, G.P. Stress and disorders of the stress system. Nat. Rev. Endocrinol., 2009, 5(7), 374-381.
[http://dx.doi.org/10.1038/nrendo.2009.106] [PMID: 19488073]
[8]
Lovallo, W.R. Do low levels of stress reactivity signal poor states of health? Biol. Psychol., 2011, 86(2), 121-128.
[http://dx.doi.org/10.1016/j.biopsycho.2010.01.006] [PMID: 20079397]
[9]
Jacobson, L. Hypothalamic-pituitary-adrenocortical axis: Neuropsychiatric aspects. Compr. Physiol., 2014, 4(2), 715-738.
[http://dx.doi.org/10.1002/cphy.c130036] [PMID: 24715565]
[10]
Armario, A. The hypothalamic-pituitary-adrenal axis: What can it tell us about stressors? CNS Neurol. Disord. Drug Targets, 2006, 5(5), 485-501.
[http://dx.doi.org/10.2174/187152706778559336] [PMID: 17073652]
[11]
Spencer, R.L.; Deak, T. A users guide to HPA axis research. Physiol. Behav., 2017, 178, 43-65.
[http://dx.doi.org/10.1016/j.physbeh.2016.11.014] [PMID: 27871862]
[12]
Aguilera, G.; Rabadan-Diehl, C. Vasopressinergic regulation of the hypothalamic-pituitary-adrenal axis: Implications for stress adaptation. Regul. Pept., 2000, 96(1-2), 23-29.
[http://dx.doi.org/10.1016/S0167-0115(00)00196-8] [PMID: 11102648]
[13]
Bornstein, S.R.; Engeland, W.C.; Ehrhart-Bornstein, M.; Herman, J.P. Dissociation of ACTH and glucocorticoids. Trends Endocrinol. Metab., 2008, 19(5), 175-180.
[http://dx.doi.org/10.1016/j.tem.2008.01.009] [PMID: 18394919]
[14]
Keller-Wood, M. Hypothalamic pituitary - Adrenal axis-feedback control. Compr. Physiol., 2015, 5(3), 1161-1182.
[http://dx.doi.org/10.1002/cphy.c140065] [PMID: 26140713]
[15]
Meijer, O.C.; de Lange, E.C.M.; Breimer, D.D.; de Boer, A.G.; Workel, J.O.; de Kloet, E.R. Penetration of dexamethasone into brain glucocorticoid targets is enhanced in mdr1A P-glycoprotein knockout mice. Endocrinology, 1998, 139(4), 1789-1793.
[http://dx.doi.org/10.1210/endo.139.4.5917] [PMID: 9528963]
[16]
Mason, B.L.; Pariante, C.M.; Thomas, S.A. A revised role for Pglycoprotein in the brain distribution of dexamethasone, cortisol, and corticosterone in wild-type and ABCB1A/B-deficient mice. Endocrinology, 2008, 149(10), 5244-5253.
[http://dx.doi.org/10.1210/en.2008-0041] [PMID: 18556350]
[17]
Pruessner, J.C.; Wolf, O.T.; Hellhammer, D.H.; Buske-Kirschbaum, A.; von Auer, K.; Jobst, S.; Kaspers, F.; Kirschbaum, C. Free cortisol levels after awakening: A reliable biological marker for the assessment of adrenocortical activity. Life Sci., 1997, 61(26), 2539-2549.
[http://dx.doi.org/10.1016/S0024-3205(97)01008-4] [PMID: 9416776]
[18]
Belda, X.; Fuentes, S.; Labad, J.; Nadal, R.; Armario, A. Acute exposure of rats to a severe stressor alters the circadian pattern of corticosterone and sensitizes to a novel stressor: Relationship to pre-stress individual differences in resting corticosterone levels. Horm. Behav., 2020, 126, 104865.
[http://dx.doi.org/10.1016/j.yhbeh.2020.104865] [PMID: 32991887]
[19]
Raff, H.; Bruder, E.D.; Cullinan, W.E.; Ziegler, D.R.; Cohen, E.P. Effect of animal facility construction on basal hypothalamicpituitary- adrenal and renin-aldosterone activity in the rat. Endocrinology, 2011, 152(4), 1218-1221.
[http://dx.doi.org/10.1210/en.2010-1432] [PMID: 21248141]
[20]
Döhler, K.D.; Gärtner, K.; von zur Mühlen, A.; Döhler, U. Activation of anterior pituitary, thyroid and adrenal gland in rats after disturbance stress. Eur. J. Endocrinol., 1977, 86(3), 489-497.
[http://dx.doi.org/10.1530/acta.0.0860489] [PMID: 579019]
[21]
Armario, A.; Lopez-Calderón, A.; Jolin, T.; Castellanos, J.M. Sensitivity of anterior pituitary hormones to graded levels of psychological stress. Life Sci., 1986, 39(5), 471-475.
[http://dx.doi.org/10.1016/0024-3205(86)90527-8] [PMID: 3090393]
[22]
Vahl, T.P.; Ulrich-Lai, Y.M.; Ostrander, M.M.; Dolgas, C.M.; Elfers, E.E.; Seeley, R.J.; D’Alessio, D.A.; Herman, J.P. Comparative analysis of ACTH and corticosterone sampling methods in rats. Am. J. Physiol. Endocrinol. Metab., 2005, 289(5), E823-E828.
[http://dx.doi.org/10.1152/ajpendo.00122.2005] [PMID: 15956051]
[23]
Pecoraro, N.; Ginsberg, A.B.; Warne, J.P.; Gomez, F.; la Fleur, S.E.; Dallman, M.F. Diverse basal and stress-related phenotypes of Sprague Dawley rats from three vendors. Physiol. Behav., 2006, 89(4), 598-610.
[http://dx.doi.org/10.1016/j.physbeh.2006.07.019] [PMID: 16935312]
[24]
Akana, S.F.; Cascio, C.S.; Shinsako, J.; Dallman, M.F. Corticosterone: narrow range required for normal body and thymus weight and ACTH. Am. J. Physiol. Regul. Integr. Comp. Physiol., 1985, 249(5), R527-R532.
[http://dx.doi.org/10.1152/ajpregu.1985.249.5.R527] [PMID: 2998210]
[25]
Scorrano, F.; Carrasco, J.; Pastor-Ciurana, J.; Belda, X.; Rami-Bastante, A.; Bacci, M.L.; Armario, A. Validation of the long‐term assessment of hypothalamic‐pituitary‐adrenal activity in rats using hair corticosterone as a biomarker. FASEB J., 2015, 29(3), 859-867.
[http://dx.doi.org/10.1096/fj.14-254474] [PMID: 25398766]
[26]
Tsuchimine, S.; Matsuno, H.; O’Hashi, K.; Chiba, S.; Yoshimura, A.; Kunugi, H.; Sohya, K. Comparison of physiological and behavioral responses to chronic restraint stress between C57BL/6J and BALB/c mice. Biochem. Biophys. Res. Commun., 2020, 525(1), 33-38.
[http://dx.doi.org/10.1016/j.bbrc.2020.02.073] [PMID: 32070493]
[27]
Gentsch, C.; Lichtsteiner, M.; Driscoll, P.; Feer, H. Differential hormonal and physiological responses to stress in Roman high- and low-avoidance rats. Physiol. Behav., 1982, 28(2), 259-263.
[http://dx.doi.org/10.1016/0031-9384(82)90072-5] [PMID: 6281822]
[28]
Sternberg, E.M.; Hill, J.M.; Chrousos, G.P.; Kamilaris, T.; Listwak, S.J.; Gold, P.W.; Wilder, R.L. Inflammatory mediator-induced hypothalamic- pituitary-adrenal axis activation is defective in streptococcal cell wall arthritis-susceptible Lewis rats. Proc. Natl. Acad. Sci. USA, 1989, 86(7), 2374-2378.
[http://dx.doi.org/10.1073/pnas.86.7.2374] [PMID: 2538840]
[29]
Smith, C.C.; Hauser, E.; Renaud, N.K.; Leff, A.; Aksentijevich, S.; Chrousos, G.P.; Wilder, R.L.; Gold, P.W.; Sternberg, E.M. Increased hypothalamic [3H]flunitrazepam binding in hypothalamicpituitary- adrenal axis hyporesponsive Lewis rats. Brain Res., 1992, 569(2), 295-299.
[http://dx.doi.org/10.1016/0006-8993(92)90642-M] [PMID: 1311618]
[30]
Sternberg, E.M.; Glowa, J.R.; Smith, M.A.; Cologero, A.E.; Listwak, S.J.; Aksentijevich, S.; Chrousos, G.P.; Wilder, R.L.; Gold, P.W. Corticotropin releasing hormone related behavioral and neuroendocrine responses to stress in Lewis and Fischer rats. Brain Res., 1992, 570(1-2), 54-60.
[http://dx.doi.org/10.1016/0006-8993(92)90563-O] [PMID: 1319794]
[31]
Smith, T.; Hewson, A.K.; Quarrie, L.; Leonard, J.P.; Cuzner, L. Hypothalamic PGE2 and cAMP production and adrenocortical activation following intraperitoneal endotoxin injection: In vivo microdialysis studies in Lewis and Fischer rats. Neuroendocrinology, 1994, 59(4), 396-405.
[http://dx.doi.org/10.1159/000126683] [PMID: 8202221]
[32]
Calogero, A.E.; Sternberg, E.M.; Bagdy, G.; Smith, C.; Bernardini, R.; Aksentijevich, S.; Wilder, R.L.; Gold, P.W.; Chrousos, G.P. Neurotransmitter-induced hypothalamic-pituitary-adrenal axis responsiveness is defective in inflammatory disease-susceptible Lewis rats: In vivo and in vitro studies suggesting globally defective hypothalamic secretion of corticotropin-releasing hormone. Neuroendocrinology, 1992, 55(5), 600-608.
[http://dx.doi.org/10.1159/000126173] [PMID: 1350069]
[33]
Sternberg, E.M.; Young, W.S., III; Bernardini, R.; Calogero, A.E.; Chrousos, G.P.; Gold, P.W.; Wilder, R.L. A central nervous system defect in biosynthesis of corticotropin-releasing hormone is associated with susceptibility to streptococcal cell wall-induced arthritis in Lewis rats. Proc. Natl. Acad. Sci. USA, 1989, 86(12), 4771-4775.
[http://dx.doi.org/10.1073/pnas.86.12.4771] [PMID: 2786636]
[34]
Million, M.; Wang, L.; Martinez, V.; Taché, Y. Differential Fos expression in the paraventricular nucleus of the hypothalamus, sacral parasympathetic nucleus and colonic motor response to water avoidance stress in Fischer and Lewis rats. Brain Res., 2000, 877(2), 345-353.
[http://dx.doi.org/10.1016/S0006-8993(00)02719-0] [PMID: 10986349]
[35]
Patchev, V.K.; Mastorakos, G.; Brady, L.S.; Redwine, J.; Wilder, R.L.; Chrousos, G.P. Increased arginine vasopressin secretion may participate in the enhanced susceptibility of Lewis rats to inflammatory disease. Neuroendocrinology, 1993, 58(1), 106-110.
[http://dx.doi.org/10.1159/000126519] [PMID: 8264843]
[36]
Patchev, V.K.; Kalogeras, K.T.; Zelazowski, P.; Wilder, R.L.; Chrousos, G.P. Increased plasma concentrations, hypothalamic content, and in vitro release of arginine vasopressin in inflammatory disease-prone, hypothalamic corticotropin-releasing hormonedeficient Lewis rats. Endocrinology, 1992, 131(3), 1453-1457.
[http://dx.doi.org/10.1210/endo.131.3.1505475] [PMID: 1505475]
[37]
Zelazowski, P.; Smith, M.A.; Gold, P.W.; Chrousos, G.P.; Wilder, R.L.; Stemberg, E.M. In vitro regulation of pituitary ACTH secretion in inflammatory disease susceptible Lewis (LEW/N) and inflammatory disease resistant Fischer (F344/N) rats. Neuroendocrinology, 1992, 56(4), 474-482.
[http://dx.doi.org/10.1159/000126264] [PMID: 1335552]
[38]
Grota, L.J.; Bienen, T.; Felten, D.L. Corticosterone responses of adult Lewis and Fischer rats. J. Neuroimmunol., 1997, 74(1-2), 95-101.
[http://dx.doi.org/10.1016/S0165-5728(96)00209-3] [PMID: 9119985]
[39]
Dhabhar, F.S.; McEwen, B.S.; Spencer, R.L. Stress response, adrenal steroid receptor levels and corticosteroid-binding globulin levels a comparison between Sprague-Dawley, Fischer 344 and Lewis rats. Brain Res., 1993, 616(1-2), 89-98.
[http://dx.doi.org/10.1016/0006-8993(93)90196-T] [PMID: 8395308]
[40]
Ortiz, J.; DeCarpio, J.L.; Kosten, T.A.; Nestler, E.J. Strainselective effects of corticosterone on locomotor sensitization to cocaine and on levels of tyrosine hydroxylase and glucocorticoid receptor in the ventral tegmental area. Neuroscience, 1995, 67(2), 383-397.
[http://dx.doi.org/10.1016/0306-4522(95)00018-E] [PMID: 7675174]
[41]
Gómez, F.; Lahmame, A.; de Kloet, R.; Armario, A. Hypothalamic-pituitary-adrenal response to chronic stress in five inbred rat strains: differential responses are mainly located at the adrenocortical level. Neuroendocrinology, 1996, 63(4), 327-337.
[http://dx.doi.org/10.1159/000126973] [PMID: 8739888]
[42]
Spinedi, E.; Salas, M.; Chisari, A.; Perone, M.; Carino, M.; Gaillard, R.C. Sex differences in the hypothalamo-pituitary-adrenal axis response to inflammatory and neuroendocrine stressors. Evidence for a pituitary defect in the autoimmune disease-susceptible female Lewis rat. Neuroendocrinology, 1994, 60(6), 609-617.
[http://dx.doi.org/10.1159/000126804] [PMID: 7700504]
[43]
Armario, A.; Gavaldà, A.; Mart, J. Comparison of the behavioural and endocrine response to forced swimming stress in five inbred strains of rats. Psychoneuroendocrinology, 1995, 20(8), 879-890.
[http://dx.doi.org/10.1016/0306-4530(95)00018-6] [PMID: 8834094]
[44]
Dhabhar, F.; Miller, A.H.; McEwen, B.S.; Spencer, R.L. Differential activation of adrenal steroid receptors in neural and immune tissues of Sprague Dawley, Fischer 344, and Lewis rats. J. Neuroimmunol., 1995, 56(1), 77-90.
[http://dx.doi.org/10.1016/0165-5728(94)00135-B] [PMID: 7822484]
[45]
Marti, J.; Armario, A. Forced swimming behavior is not related to the corticosterone levels ain the test: A study with four inbred rat strains. Physiol. Behav., 1996, 59(2), 369-373.
[http://dx.doi.org/10.1016/0031-9384(95)02104-3] [PMID: 8838618]
[46]
Dhabhar, F.S.; McEwen, B.S.; Spencer, R.L. Adaptation to prolonged or repeated stress--comparison between rat strains showing intrinsic differences in reactivity to acute stress. Neuroendocrinology, 1997, 65(5), 360-368.
[http://dx.doi.org/10.1159/000127196] [PMID: 9158068]
[47]
Neeley, E.W.; Berger, R.; Koenig, J.I.; Leonard, S. Strain dependent effects of prenatal stress on gene expression in the rat hippocampus. Physiol. Behav., 2011, 104(2), 334-339.
[http://dx.doi.org/10.1016/j.physbeh.2011.02.032] [PMID: 21382392]
[48]
Chaouloff, F.; Kulikov, A.; Sarrieau, A.; Castanon, N.; Mormède, P. Male Fischer 344 and Lewis rats display differences in locomotor reactivity, but not in anxiety-related behaviours: Relationship with the hippocampal serotonergic system. Brain Res., 1995, 693(1-2), 169-178.
[http://dx.doi.org/10.1016/0006-8993(95)00733-7] [PMID: 8653405]
[49]
Michaud, D.S.; McLean, J.; Keith, S.E.; Ferrarotto, C.; Hayley, S.; Khan, S.A.; Anisman, H.; Merali, Z. Differential impact of audiogenic stressors on Lewis and Fischer rats: Behavioral, neurochemical, and endocrine variations. Neuropsychopharmacology, 2003, 28(6), 1068-1081.
[http://dx.doi.org/10.1038/sj.npp.1300149] [PMID: 12700709]
[50]
Baumann, M.H.; Elmer, G.I.; Goldberg, S.R.; Ambrosio, E. Differential neuroendocrine responsiveness to morphine in Lewis, Fischer 344, and ACI inbred rats. Brain Res., 2000, 858(2), 320-326.
[http://dx.doi.org/10.1016/S0006-8993(99)02479-8] [PMID: 10708683]
[51]
Kusnecov, A.W.; Shurin, M.R.; Armfield, A.; Litz, J.; Wood, P.; Zhou, D.; Rabin, B.S. Suppression of lymphocyte mitogenesis in different rat strains exposed to footshock during early diurnal and nocturnal time periods. Psychoneuroendocrinology, 1995, 20(8), 821-835.
[http://dx.doi.org/10.1016/0306-4530(95)00009-7] [PMID: 8834090]
[52]
Jongen-Rêlo, A.L.; Pothuizen, H.H.J.; Feldon, J.; Pryce, C.R. Comparison of central corticosteroid receptor expression in male Lewis and Fischer rats. Brain Res., 2002, 953(1-2), 223-231.
[http://dx.doi.org/10.1016/S0006-8993(02)03293-6] [PMID: 12384256]
[53]
Duclos, M.; Bouchet, M.; Vettier, A.; Richard, D. Genetic differences in hypothalamic-pituitary-adrenal axis activity and food restriction- induced hyperactivity in three inbred strains of rats. J. Neuroendocrinol., 2005, 17(11), 740-752.
[http://dx.doi.org/10.1111/j.1365-2826.2005.01367.x] [PMID: 16219003]
[54]
Ergang, P.; Vodička, M.; Soták, M.; Klusoňová, P.; Behuliak, M.; Řeháková, L.; Zach, P.; Pácha, J. Differential impact of stress on hypothalamic-pituitary-adrenal axis: Gene expression changes in Lewis and Fisher rats. Psychoneuroendocrinology, 2015, 53, 49-59.
[http://dx.doi.org/10.1016/j.psyneuen.2014.12.013] [PMID: 25591115]
[55]
Stöhr, T.; Szuran, T.; Welzl, H.; Pliska, V.; Feldon, J.; Pryce, C.R. Lewis/Fischer rat strain differences in endocrine and behavioural responses to environmental challenge. Pharmacol. Biochem. Behav., 2000, 67(4), 809-819.
[http://dx.doi.org/10.1016/S0091-3057(00)00426-3] [PMID: 11166072]
[56]
Page, G.G.; Opp, M.R.; Kozachik, S.L. Reduced sleep, stress responsivity, and female sex contribute to persistent inflammationinduced mechanical hypersensitivity in rats. Brain Behav. Immun., 2014, 40, 244-251.
[http://dx.doi.org/10.1016/j.bbi.2014.02.013] [PMID: 24594386]
[57]
Gomez-Serrano, M.; Tonelli, L.; Listwak, S.; Sternberg, E.; Riley, A.L. Effects of cross fostering on open-field behavior, acoustic startle, lipopolysaccharide-induced corticosterone release, and body weight in Lewis and Fischer rats. Behav. Genet., 2001, 31(5), 427-436.
[http://dx.doi.org/10.1023/A:1012742405141] [PMID: 11777171]
[58]
Rivest, S.; Rivier, C. Stress and interleukin-1 beta-induced activation of c-fos, NGFI-B and CRF gene expression in the hypothalamic PVN: Comparison between Sprague-Dawley, Fisher-344 and Lewis rats. J. Neuroendocrinol., 1994, 6(1), 101-117.
[http://dx.doi.org/10.1111/j.1365-2826.1994.tb00559.x] [PMID: 8025563]
[59]
Karalis, K.; Crofford, L.; Wilder, R.L.; Chrousos, G.P. Glucocorticoid and/or glucocorticoid antagonist effects in inflammatory disease- susceptible Lewis rats and inflammatory disease-resistant Fischer rats. Endocrinology, 1995, 136(7), 3107-3112.
[http://dx.doi.org/10.1210/endo.136.7.7789338] [PMID: 7789338]
[60]
Marissal-Arvy, N.; Gaumont, A.; Langlois, A.; Dabertrand, F.; Bouchecareilh, M.; Tridon, C.; Mormede, P. Strain differences in hypothalamic-pituitary-adrenocortical axis function and adipogenic effects of corticosterone in rats. J. Endocrinol., 2007, 195(3), 473-484.
[http://dx.doi.org/10.1677/JOE-07-0077] [PMID: 18000309]
[61]
Gómez, F.; De Kloet, E.R.; Armario, A. Glucocorticoid negative feedback on the HPA axis in five inbred rat strains. Am. J. Physiol. Regul. Integr. Comp. Physiol., 1998, 274(2), R420-R427.
[http://dx.doi.org/10.1152/ajpregu.1998.274.2.R420] [PMID: 9486300]
[62]
Stefferl, A.; Linington, C.; Holsboer, F.; Reul, J.M.H.M. Susceptibility and resistance to experimental allergic encephalomyelitis: relationship with hypothalamic-pituitary-adrenocortical axis responsiveness in the rat. Endocrinology, 1999, 140(11), 4932-4938.
[http://dx.doi.org/10.1210/endo.140.11.7109] [PMID: 10537116]
[63]
Oitzl, M.S.; van Haarst, A.D.; Sutanto, W.; Ron de Kloet, E. Corticosterone, brain mineralocorticoid receptors (MRS) and the activity of the hypothalamic-pituitary-adrenal (hpa) axis: The Lewis rat as an example of increased central MR capacity and a hyporesponsive HPA axis. Psychoneuroendocrinology, 1995, 20(6), 655-675.
[http://dx.doi.org/10.1016/0306-4530(95)00003-7] [PMID: 8584606]
[64]
Pardon, M.C.; Gould, G.G.; Garcia, A.; Phillips, L.; Cook, M.C.; Miller, S.A.; Mason, P.A.; Morilak, D.A. Stress reactivity of the brain noradrenergic system in three rat strains differing in their neuroendocrine and behavioral responses to stress: Implications for susceptibility to stress-related neuropsychiatric disorders. Neuroscience, 2002, 115(1), 229-242.
[http://dx.doi.org/10.1016/S0306-4522(02)00364-0] [PMID: 12401336]
[65]
Klenerova, V.; Sida, P.; Hynie, S.; Jurcovicova, J. Rat strain differences in responses of plasma prolactin and PRL mRNA expression after acute amphetamine treatment or restraint stress. Cell. Mol. Neurobiol., 2001, 21(1), 91-100.
[http://dx.doi.org/10.1023/A:1007177430146] [PMID: 11440201]
[66]
Trnečková, L.; Armario, A.; Hynie, S.; Šída, P.; Klenerová, V. Differences in the brain expression of c-fos mRNA after restraint stress in Lewis compared to Sprague–Dawley rats. Brain Res., 2006, 1077(1), 7-15.
[http://dx.doi.org/10.1016/j.brainres.2006.01.029] [PMID: 16487948]
[67]
Sarrieau, A.; Mormède, P. Hypothalamic-pituitary-adrenal axis activity in the inbred brown Norway and Fischer 344 rat strains. Life Sci., 1998, 62(16), 1417-1425.
[http://dx.doi.org/10.1016/S0024-3205(98)00080-0] [PMID: 9585169]
[68]
Uchida, S.; Nishida, A.; Hara, K.; Kamemoto, T.; Suetsugi, M.; Fujimoto, M.; Watanuki, T.; Wakabayashi, Y.; Otsuki, K.; McEwen, B.S.; Watanabe, Y. Characterization of the vulnerability to repeated stress in Fischer 344 rats: Possible involvement of microRNA- mediated down-regulation of the glucocorticoid receptor. Eur. J. Neurosci., 2008, 27(9), 2250-2261.
[http://dx.doi.org/10.1111/j.1460-9568.2008.06218.x] [PMID: 18445216]
[69]
Broadhurst, P.L. The Maudsley Reactive and Nonreactive strains of rats: A survey. Behav. Genet., 1975, 5(4), 299-319.
[http://dx.doi.org/10.1007/BF01073201] [PMID: 1191155]
[70]
Blizard, D.A. The Maudsley reactive and nonreactive strains: A North American perspective. Behav. Genet., 1981, 11(5), 469-489.
[http://dx.doi.org/10.1007/BF01070004] [PMID: 7325951]
[71]
Overstreet, D.H.; Rezvani, A.H.; Janowsky, D.S. Maudsley reactive and nonreactive rats differ only in some tasks reflecting emotionality. Physiol. Behav., 1992, 52(1), 149-152.
[http://dx.doi.org/10.1016/0031-9384(92)90444-7] [PMID: 1528998]
[72]
Paterson, A.; Whiting, P.J.; Gray, J.A.; Flint, J.; Dawson, G.R. Lack of consistent behavioural effects of Maudsley reactive and non-reactive rats in a number of animal tests of anxiety and activity. Psychopharmacology, 2001, 154(4), 336-342.
[http://dx.doi.org/10.1007/s002130000640] [PMID: 11349385]
[73]
Abel, E.L. Behavior and corticosteroid response of maudsley reactive and nonreactive rats in the open field and forced swimming test. Physiol. Behav., 1991, 50(1), 151-153.
[http://dx.doi.org/10.1016/0031-9384(91)90513-N] [PMID: 1946709]
[74]
Buda, M.; Lachuer, J.; Devauges, V.; Barbagli, B.; Blizard, D.; Sara, S.J. Central noradrenergic reactivity to stress in Maudsley rat strains. Neurosci. Lett., 1994, 167(1-2), 33-36.
[http://dx.doi.org/10.1016/0304-3940(94)91021-9] [PMID: 8177526]
[75]
Blizard, D.A.; Eldridge, J.C.; Jones, B.C. The defecation index as a measure of emotionality: Questions raised by HPA axis and prolactin response to stress in the maudsley model. Behav. Genet., 2015, 45(3), 368-373.
[http://dx.doi.org/10.1007/s10519-015-9722-x] [PMID: 25911177]
[76]
Kosti, O.; Raven, P.W.; Renshaw, D.; Hinson, J.P. Intra-adrenal mechanisms in the response to chronic stress: Investigation in a rat model of emotionality. J. Endocrinol., 2006, 189(2), 211-218.
[http://dx.doi.org/10.1677/joe.1.06638] [PMID: 16648289]
[77]
Liebsch, G.; Montkowski, A.; Holsboer, F.; Landgraf, R. Behavioural profiles of two Wistar rat lines selectively bred for high or low anxiety-related behaviour. Behav. Brain Res., 1998, 94(2), 301-310.
[http://dx.doi.org/10.1016/S0166-4328(97)00198-8] [PMID: 9722280]
[78]
Landgraf, R.; Wigger, A.; Holsboer, F.; Neumann, I.D. Hyperreactive hypothalamo-pituitary-adrenocortical axis in rats bred for high anxiety-related behaviour. J. Neuroendocrinol., 1999, 11(6), 405-407.
[http://dx.doi.org/10.1046/j.1365-2826.1999.00342.x] [PMID: 10336720]
[79]
Keck, M.E.; Welt, T.; Müller, M.B.; Uhr, M.; Ohl, F.; Wigger, A.; Toschi, N.; Holsboer, F.; Landgraf, R. Reduction of hypothalamic vasopressinergic hyperdrive contributes to clinically relevant behavioral and neuroendocrine effects of chronic paroxetine treatment in a psychopathological rat model. Neuropsychopharmacology, 2003, 28(2), 235-243.
[http://dx.doi.org/10.1038/sj.npp.1300040] [PMID: 12589376]
[80]
Frank, E.; Salchner, P.; Aldag, J.M.; Salomé, N.; Singewald, N.; Landgraf, R.; Wigger, A. Genetic predisposition to anxiety-related behavior determines coping style, neuroendocrine responses, and neuronal activation during social defeat. Behav. Neurosci., 2006, 120(1), 60-71.
[http://dx.doi.org/10.1037/0735-7044.120.1.60] [PMID: 16492117]
[81]
Brush, F.R.; Baron, S.; Froehlich, J.C.; Ison, J.R.; Pellegrino, L.J.; Phillips, D.S.; Sakellaris, P.C.; Williams, V.N. Genetic differences in avoidance learning by Rattus norvegicus: Escape/avoidance responding, sensitivity to electric shock, discrimination learning, and open-field behavior. J. Comp. Psychol., 1985, 99(1), 60-73.
[http://dx.doi.org/10.1037/0735-7036.99.1.60] [PMID: 3979029]
[82]
Brush, F.R.; del Paine, S.N.; Pellegrino, L.J.; Rykaszewski, I.M.; Dess, N.K.; Collins, P.Y. CER suppression, passive-avoidance learning, and stress-induced suppression of drinking in the Syracuse high- and low-avoidance strains of rats (Rattus norvegicus). J. Comp. Psychol., 1988, 102(4), 337-349.
[http://dx.doi.org/10.1037/0735-7036.102.4.337] [PMID: 3215010]
[83]
Brush, F.R. Selection for differences in avoidance learning: The Syracuse strains differ in anxiety, not learning ability. Behav. Genet., 2003, 33(6), 677-696.
[http://dx.doi.org/10.1023/A:1026135231594] [PMID: 14574123]
[84]
Del Paine, S.N.; Brush, F.R. Adrenal morphometry in unilateral and sham adrenalectomized syracuse high and low avoidance rats. Physiol. Behav., 1990, 48(2), 299-306.
[http://dx.doi.org/10.1016/0031-9384(90)90317-W] [PMID: 2255735]
[85]
Brush, F.R.; Isaacson, M.D.; Pellegrino, L.J.; Rykaszewski, I.M.; Shain, C.N. Characteristics of the pituitary-adrenal system in the syracuse high-and low-avoidance strains of rats (Rattus norvegicus). Behav. Genet., 1991, 21(1), 35-48.
[http://dx.doi.org/10.1007/BF01067665] [PMID: 2018462]
[86]
Gupta, P.; Brush, F.R. Differential behavioral and endocrinological effects of corticotropin-releasing hormone (CRH) in the Syracuse high- and low-avoidance rats. Horm. Behav., 1998, 34(3), 262-267.
[http://dx.doi.org/10.1006/hbeh.1998.1482] [PMID: 9878275]
[87]
Ohta, R.; Matsumoto, A.; Hashimoto, Y.; Nagao, T.; Mizutani, M. Behavioral characteristics of rats selectively bred for high and low avoidance shuttlebox response. Congenit. Anom., 1995, 35(2), 223-229.
[http://dx.doi.org/10.1111/j.1741-4520.1995.tb00614.x]
[88]
Ohta, R.; Matsumoto, A.; Nagao, T.; Mizutani, M. Comparative study of behavioral development between high and low shuttlebox avoidance rats. Physiol. Behav., 1998, 63(4), 545-551.
[http://dx.doi.org/10.1016/S0031-9384(97)00506-4] [PMID: 9523897]
[89]
Ohta, R.; Shirota, M.; Adachi, T.; Tohei, A.; Taya, K. Plasma ACTH levels during early, two-way avoidance acquisition in highand low-avoidance rats (Hatano strains). Behav. Genet., 1999, 29(2), 137-144.
[http://dx.doi.org/10.1023/A:1021616723969] [PMID: 10405463]
[90]
Asai, S.; Ohta, R.; Shirota, M.; Watanabe, G.; Taya, K. Differential responses of the hypothalamo-pituitary-adrenocortical axis to acute restraint stress in Hatano high- and low-avoidance rats. J. Endocrinol., 2004, 181(3), 515-520.
[http://dx.doi.org/10.1677/joe.0.1810515] [PMID: 15171699]
[91]
Jaroenporn, S.; Nagaoka, K.; Ohta, R.; Shirota, M.; Watanabe, G.; Taya, K. Differences in adrenocortical secretory and gene expression responses to stimulation in vitro by ACTH or prolactin between high- and low-avoidance Hatano rats. Stress, 2009, 12(1), 22-29.
[http://dx.doi.org/10.1080/10253890801976652] [PMID: 18609294]
[92]
Akieda-Asai, S.; Ohta, R.; Shirota, M.; Jaroenporn, S.; Watanabe, G.; Taya, K. Endocrinological differences between Hatano highand low-avoidance rats during early two-way avoidance acquisition. Exp. Anim., 2011, 60(5), 509-516.
[http://dx.doi.org/10.1538/expanim.60.509] [PMID: 22041288]
[93]
Bignami, G. Selection for high rates and low rates of avoidance conditioning in the rat. Anim. Behav., 1965, 13(2-3), 221-227.
[http://dx.doi.org/10.1016/0003-3472(65)90038-2] [PMID: 5835838]
[94]
Steimer, T.; Driscoll, P. Divergent stress responses and coping styles in psychogenetically selected Roman high-(RHA) and low- (RLA) avoidance rats: Behavioural, neuroendocrine and developmental aspects. Stress, 2003, 6(2), 87-100.
[http://dx.doi.org/10.1080/1025389031000111320] [PMID: 12775328]
[95]
Walker, C.D.; Rivest, R.W.; Meaney, M.J.; Aubert, M.L. Differential activation of the pituitary-adrenocortical axis after stress in the rat: Use of two genetically selected lines (Roman low- and highavoidance rats) as a model. J. Endocrinol., 1989, 123(3), 477-485.
[http://dx.doi.org/10.1677/joe.0.1230477] [PMID: 2558147]
[96]
Gentsch, C.; Lichtsteiner, M.; Feer, H. Locomotor activity, defecation score and corticosterone levels during an openfield exposure: A comparison among individually and group-housed rats, and genetically selected rat lines. Physiol. Behav., 1981, 27(1), 183-186.
[http://dx.doi.org/10.1016/0031-9384(81)90320-6] [PMID: 7196593]
[97]
Castanon, N.; Dulluc, J.; Le Moal, M.; Mormède, P. Prolactin as a link between behavioral and immune differences between the Roman rat lines. Physiol. Behav., 1992, 51(6), 1235-1241.
[http://dx.doi.org/10.1016/0031-9384(92)90314-R] [PMID: 1322543]
[98]
Steimer, T.; Escorihuela, R.M.; Fernández-teruel, A.; Driscoll, P. Long‐term behavioural and neuroendocrine changes in roman HIGH‐(RHA/Verh) and LOW‐(RLA‐Verh) avoidance rats following neonatal handling. Int. J. Dev. Neurosci., 1998, 16(3-4), 165-174.
[http://dx.doi.org/10.1016/S0736-5748(98)00032-X] [PMID: 9785113]
[99]
Aubry, J.M.; Bartanusz, V.; Driscoll, P.; Schulz, P.; Steimer, T.; Kiss, J.Z. Corticotropin-releasing factor and vasopressin mRNA levels in roman high and low-avoidance rats: Response to openfield exposure. Neuroendocrinology, 1995, 61(2), 89-97.
[http://dx.doi.org/10.1159/000126829] [PMID: 7753341]
[100]
Carrasco, J.; Márquez, C.; Nadal, R.; Tobeña, A.; Fernández-Teruel, A.; Armario, A. Characterization of central and peripheral components of the hypothalamus–pituitary–adrenal axis in the inbred Roman rat strains. Psychoneuroendocrinology, 2008, 33(4), 437-445.
[http://dx.doi.org/10.1016/j.psyneuen.2008.01.001] [PMID: 18276081]
[101]
Díaz-Morán, S.; Palència, M.; Mont-Cardona, C.; Cañete, T.; Blázquez, G.; Martínez-Membrives, E.; López-Aumatell, R.; Tobeña, A.; Fernández-Teruel, A. Coping style and stress hormone responses in genetically heterogeneous rats: Comparison with the Roman rat strains. Behav. Brain Res., 2012, 228(1), 203-210.
[http://dx.doi.org/10.1016/j.bbr.2011.12.002] [PMID: 22178313]
[102]
Okamoto, K.; Aoki, K. Development of a strain of spontaneously hypertensive rats. Jpn. Circ. J., 1963, 27(3), 282-293.
[http://dx.doi.org/10.1253/jcj.27.282] [PMID: 13939773]
[103]
Werner, S.C.; Manger, W.M.; Radichevich, I.; Wolff, M.; Estorff, I.V. Excessive thyrotropin concentrations in the circulation of the spontaneously hypertensive rat. Exp. Biol. Med., 1975, 148(4), 1013-1017.
[http://dx.doi.org/10.3181/00379727-148-38679] [PMID: 805436]
[104]
Regan, S.L.; Williams, M.T.; Vorhees, C.V. Review of rodent models of attention deficit hyperactivity disorder. Neurosci. Biobehav. Rev., 2022, 132, 621-637.
[http://dx.doi.org/10.1016/j.neubiorev.2021.11.041] [PMID: 34848247]
[105]
Aleksandrova, L.R.; Wang, Y.T.; Phillips, A.G. Evaluation of the Wistar-Kyoto rat model of depression and the role of synaptic plasticity in depression and antidepressant response. Neurosci. Biobehav. Rev., 2019, 105, 1-23.
[http://dx.doi.org/10.1016/j.neubiorev.2019.07.007] [PMID: 31336112]
[106]
Paré, W.P.; Redei, E. Depressive behavior and stress ulcer in Wistar Kyoto rats. J. Physiol. Paris, 1993, 87(4), 229-238.
[http://dx.doi.org/10.1016/0928-4257(93)90010-Q] [PMID: 8136789]
[107]
Lahmame, A.; Gomez, F.; Armario, A. Fawn-hooded rats show enhanced active behaviour in the forced swimming test, with no evidence for pituitary-adrenal axis hyperactivity. Psychopharmacology (Berl.), 1996, 125(1), 74-78.
[http://dx.doi.org/10.1007/BF02247395] [PMID: 8724451]
[108]
Lahmame, A.; del Arco, C.; Pazos, A.; Yritia, M.; Armario, A. Are Wistar-Kyoto rats a genetic animal model of depression resistant to antidepressants? Eur. J. Pharmacol., 1997, 337(2-3), 115-123.
[http://dx.doi.org/10.1016/S0014-2999(97)01276-4] [PMID: 9430405]
[109]
McCarty, R. Stress, behavior and experimental hypertension. Neurosci. Biobehav. Rev., 1983, 7(4), 493-502.
[http://dx.doi.org/10.1016/0149-7634(83)90029-5] [PMID: 6669329]
[110]
Hendley, E.D.; Cierpial, M.A.; McCarty, R. Sympathetic-adrenal medullary response to stress in hyperactive and hypertensive rats. Physiol. Behav., 1988, 44(1), 47-51.
[http://dx.doi.org/10.1016/0031-9384(88)90344-7] [PMID: 3237814]
[111]
Zhang, T.; Reid, K.; Acuff, C.G.; Jin, C.B.; Rockhold, R.W. Cardiovascular and analgesic effects of a highly palatable diet in spontaneously hypertensive and Wistar-Kyoto rats. Pharmacol. Biochem. Behav., 1994, 48(1), 57-61.
[http://dx.doi.org/10.1016/0091-3057(94)90498-7] [PMID: 8029305]
[112]
Durand, M.; Berton, O.; Aguerre, S.; Edno, L.; Combourieu, I.; Mormède, P.; Chaouloff, F. Effects of repeated fluoxetine on anxiety- related behaviours, central serotonergic systems, and the corticotropic axis in SHR and WKY rats. Neuropharmacology, 1999, 38(6), 893-907.
[http://dx.doi.org/10.1016/S0028-3908(99)00009-X] [PMID: 10465693]
[113]
Lim, D.Y.; Jang, S.J.; Park, D.G. Comparison of catecholamine release in the isolated adrenal glands of SHR and WKY rats. Auton. Autacoid Pharmacol., 2002, 22(4), 225-232.
[http://dx.doi.org/10.1046/j.1474-8673.2002.00264.x] [PMID: 12656948]
[114]
McBride, S.M.; Culver, B.; Flynn, F.W. Prenatal and early postnatal dietary sodium restriction sensitizes the adult rat to amphetamines. Am. J. Physiol. Regul. Integr. Comp. Physiol., 2006, 291(4), R1192-R1199.
[http://dx.doi.org/10.1152/ajpregu.00774.2005] [PMID: 16675632]
[115]
Vavřínová, A.; Behuliak, M.; Bencze, M.; Vodička, M.; Ergang, P.; Vaněčková, I.; Zicha, J. Sympathectomy-induced blood pressure reduction in adult normotensive and hypertensive rats is counteracted by enhanced cardiovascular sensitivity to vasoconstrictors. Hypertens. Res., 2019, 42(12), 1872-1882.
[http://dx.doi.org/10.1038/s41440-019-0319-2] [PMID: 31527789]
[116]
Nickerson, P.A. The adrenal cortex in spontaneously hypertensive rats. A quantitative ultrastructural study. Am. J. Pathol., 1976, 84(3), 545-560.
[PMID: 961826]
[117]
Nishiyama, K.; Nishiyama, A.; Frohlich, E.D. Regional blood flow in normotensive and spontaneously hypertensive rats. Am. J. Physiol., 1976, 230(3), 691-698.
[http://dx.doi.org/10.1152/ajplegacy.1976.230.3.691] [PMID: 1266971]
[118]
Ayachi, S. Increased dietary calcium lowers blood pressure in the spontaneously hypertensive rat. Metabolism, 1979, 28(12), 1234-1238.
[http://dx.doi.org/10.1016/0026-0495(79)90136-7] [PMID: 514084]
[119]
Häusler, A.; Girard, J.; Baumann, J.B.; Ruch, W.; Otten, U.H. Long-term effects of betamethasone on blood pressure and hypothalamo- pituitary-adrenocortical function in spontaneously hypertensive and normotensive rats. Horm. Res., 1983, 18(4), 191-197.
[http://dx.doi.org/10.1159/000179794] [PMID: 6642425]
[120]
Paré, W.P.; Schimmel, G.T. Stress ulcer in normotensive and spontaneously hypertensive rats. Physiol. Behav., 1986, 36(4), 699-705.
[http://dx.doi.org/10.1016/0031-9384(86)90357-4] [PMID: 3714844]
[121]
Fukuda, S.; Tsuchikura, S.; Iida, H. Age-related changes in blood pressure, hematological values, concentrations of serum biochemical constituents and weights of organs in the SHR/Izm, SHRSP/Izm and WKY/Izm. Exp. Anim., 2004, 53(1), 67-72.
[http://dx.doi.org/10.1538/expanim.53.67] [PMID: 14993746]
[122]
Gilad, G.M.; Jimerson, D.C. Modes of adaptation of peripheral neuroendocrine mechanisms of the sympatho-adrenal system to short-term stress as studied in two inbred rat strains. Brain Res., 1981, 206(1), 83-93.
[http://dx.doi.org/10.1016/0006-8993(81)90102-5] [PMID: 7470895]
[123]
Harrap, S.B.; Louis, W.J.; Doyle, A.E. Failure of psychosocial stress to induce chronic hypertension in the rat. J. Hypertens., 1984, 2(6), 653-662.
[http://dx.doi.org/10.1097/00004872-198412000-00011] [PMID: 6543222]
[124]
McCarty, R.; Kvetnansky, R.; Raymond Lake, C.; Thoa, N.B.; Kopin, I.J. Sympatho-adrenal activity of SHR and WKY rats during recovery from forced immobilization. Physiol. Behav., 1978, 21(6), 951-955.
[http://dx.doi.org/10.1016/0031-9384(78)90171-3] [PMID: 552087]
[125]
Sowers, J.; Tuck, M.; Asp, N.D.; Sollars, E. Plasma aldosterone and corticosterone responses to adrenocorticotropin, angiotensin, potassium, and stress in spontaneously hypertensive rats. Endocrinology, 1981, 108(4), 1216-1221.
[http://dx.doi.org/10.1210/endo-108-4-1216] [PMID: 6258898]
[126]
Hashimoto, K.; Makino, S.; Hirasawa, R.; Takao, T.; Sugawara, M.; Murakami, K.; Ono, K.; Ota, Z. Abnormalities in the hypothalamo- pituitary-adrenal axis in spontaneously hypertensive rats during development of hypertension. Endocrinology, 1989, 125(3), 1161-1167.
[http://dx.doi.org/10.1210/endo-125-3-1161] [PMID: 2547578]
[127]
Freeman, R.H.; Davis, J.O.; Aharon, N.V.; Ulick, S.; Weinberger, M.H. Control of aldosterone secretion in the spontaneously hypertensive rat. Circ. Res., 1975, 37(1), 66-71.
[http://dx.doi.org/10.1161/01.RES.37.1.66] [PMID: 1149188]
[128]
DeVito, W.J.; Sutterer, J.R.; Robert Brush, F. The pituitary-adrenal response to ether stress in the spontaneously hypertensive and normotensive rat. Life Sci., 1981, 28(13), 1489-1495.
[http://dx.doi.org/10.1016/0024-3205(81)90381-7] [PMID: 6264248]
[129]
Komanicky, P.; Reiss, D.L.; Dale, S.L.; Melby, J.C. Role of adrenal steroidogenesis in etiology of hypertension in the spontaneously hypertensive rat. Endocrinology, 1982, 111(1), 219-224.
[http://dx.doi.org/10.1210/endo-111-1-219] [PMID: 7084111]
[130]
Krukoff, T.L.; MacTavish, D.; Jhamandas, J.H. Hypertensive rats exhibit heightened expression of corticotropin-releasing factor in activated central neurons in response to restraint stress. Brain Res. Mol. Brain Res., 1999, 65(1), 70-79.
[http://dx.doi.org/10.1016/S0169-328X(98)00342-8] [PMID: 10036309]
[131]
Autelitano, D.J.; Van Den Buuse, M. Concomitant up-regulation of proopiomelanocortin and dopamine D2-receptor gene expression in the pituitary intermediate lobe of the spontaneously hypertensive rat. J. Neuroendocrinol., 1997, 9(4), 255-262.
[http://dx.doi.org/10.1046/j.1365-2826.1997.00576.x] [PMID: 9147288]
[132]
Braas, K.M.; Hendley, E.D.; May, V.; Cronin, K.M.; McAuley, J.A. Anterior pituitary proopiomelanocortin expression is decreased in hypertensive rat strains. Endocrinology, 1994, 134(1), 196-205.
[http://dx.doi.org/10.1210/endo.134.1.8275934] [PMID: 8275934]
[133]
Häusler, A.; Girard, J.; Baumann, J.B.; Ruch, W.; Otten, U.H. Stress-induced secretion of ACTH and corticosterone during development of spontaneous hypertension in rats. Clin. Exp. Hypertens. A, 1983, 5(1), 11-19.
[http://dx.doi.org/10.3109/10641968309048806] [PMID: 6299626]
[134]
Kvetnansky, R.; McCarty, R.; Thoa, N.B.; Lake, C.R.; Kopin, I.J. Sympatho-adrenal responses of spontaneously hypertensive rats to immobilization stress. Am. J. Physiol. Heart Circ. Physiol., 1979, 236(3), H457-H462.
[http://dx.doi.org/10.1152/ajpheart.1979.236.3.H457] [PMID: 426081]
[135]
Chiueh, C.C.; McCarty, R. Sympatho-adrenal hyperreactivity to footshock stress but not to cold exposure in spontaneously hypertensive rats. Physiol. Behav., 1981, 26(1), 85-89.
[http://dx.doi.org/10.1016/0031-9384(81)90082-2] [PMID: 7232516]
[136]
Knardahl, S.; Murison, R. Plasma corticosterone and renin activity during two-way active avoidance learning in spontaneously hypertensive and Wistar-Kyoto rats. Behav. Neural Biol., 1989, 51(3), 389-400.
[http://dx.doi.org/10.1016/S0163-1047(89)91026-1] [PMID: 2658949]
[137]
Solberg, L.C.; Olson, S.L.; Turek, F.W.; Redei, E. Altered hormone levels and circadian rhythm of activity in the WKY rat, a putative animal model of depression. Am. J. Physiol. Regul. Integr. Comp. Physiol., 2001, 281(3), R786-R794.
[http://dx.doi.org/10.1152/ajpregu.2001.281.3.R786] [PMID: 11506993]
[138]
Hauger, R.L.; Shelat, S.G.; Redei, E.E. Decreased corticotropinreleasing factor receptor expression and adrenocorticotropic hormone responsiveness in anterior pituitary cells of Wistar-Kyoto rats. J. Neuroendocrinol., 2002, 14(2), 126-134.
[http://dx.doi.org/10.1046/j.0007-1331.2001.00752.x] [PMID: 11849372]
[139]
Shepard, J.; Myers, D. Strain differences in anxiety-like behavior: Association with corticotropin-releasing factor. Behav. Brain Res., 2008, 186(2), 239-245.
[http://dx.doi.org/10.1016/j.bbr.2007.08.013] [PMID: 17904655]
[140]
Bravo, J.A.; Dinan, T.G.; Cryan, J.F. Alterations in the central CRF system of two different rat models of comorbid depression and functional gastrointestinal disorders. Int. J. Neuropsychopharmacol., 2011, 14(5), 666-683.
[http://dx.doi.org/10.1017/S1461145710000994] [PMID: 20860876]
[141]
Rittenhouse, P.A.; López-Rubalcava, C.; Stanwood, G.D.; Lucki, I. Amplified behavioral and endocrine responses to forced swim stress in the Wistar-Kyoto rat. Psychoneuroendocrinology, 2002, 27(3), 303-318.
[http://dx.doi.org/10.1016/S0306-4530(01)00052-X] [PMID: 11818168]
[142]
Redei, E.; Paré, W.P.; Aird, F.; Kluczynski, J. Strain differences in hypothalamic-pituitary-adrenal activity and stress ulcer. Am. J. Physiol. Regul. Integr. Comp. Physiol., 1994, 266(2), R353-R360.
[http://dx.doi.org/10.1152/ajpregu.1994.266.2.R353] [PMID: 8141389]
[143]
Braley, L.M.; Menachery, A.; Williams, G.H. Specificity of the alteration in aldosterone biosynthesis in the spontaneously hypertensive rat. Endocrinology, 1983, 112(2), 562-566.
[http://dx.doi.org/10.1210/endo-112-2-562] [PMID: 6293801]
[144]
Slezak, P.; Puzserova, A.; Balis, P.; Sestakova, N.; Majzunova, M.; Dovinova, I.; Kluknavsky, M.; Bernatova, I. Genotype-related effect of crowding stress on blood pressure and vascular function in young female rats. BioMed Res. Int., 2014, 2014, 1-11.
[http://dx.doi.org/10.1155/2014/413629] [PMID: 24729972]
[145]
Overstreet, D.H.; Wegener, G. The flinders sensitive line rat model of depression - 25 years and still producing. Pharmacol. Rev., 2013, 65(1), 143-155.
[http://dx.doi.org/10.1124/pr.111.005397] [PMID: 23319547]
[146]
Overstreet, D.H.; Booth, R.A.; Dana, R.; Risch, S.C.; Janowsky, D.S. Enhanced elevation of corticosterone following arecoline administration to rats selectively bred for increased cholinergic function. Psychopharmacology, 1986, 88(1), 129-130.
[http://dx.doi.org/10.1007/BF00310528] [PMID: 3080772]
[147]
Owens, M.J.; Overstreet, D.H.; Knight, D.L.; Rezvani, A.H.; Ritchie, J.C.; Bissette, G.; Janowsky, D.S.; Nemeroff, C.B. Alterations in the hypothalamic-pituitary-adrenal axis in a proposed animal model of depression with genetic muscarinic supersensitivity. Neuropsychopharmacology, 1991, 4(2), 87-93.
[PMID: 1851013]
[148]
Ayensu, W.K.; Pucilowski, O.; Mason, G.A.; Overstreet, D.H.; Rezvani, A.H.; Janowsky, D.S. Effects of chronic mild stress on serum complement activity, saccharin preference, and corticosterone levels in Flinders lines of rats. Physiol. Behav., 1995, 57(1), 165-169.
[http://dx.doi.org/10.1016/0031-9384(94)00204-I] [PMID: 7878112]
[149]
Elsenbruch, S.; Wang, L.; Hollerbach, S.; Schedlowski, M.; Tougas, G. Pseudo-affective visceromotor responses and HPA axis activation following colorectal distension in rats with increased cholinergic sensitivity. Neurogastroenterol. Motil., 2004, 16(6), 801-809.
[http://dx.doi.org/10.1111/j.1365-2982.2004.00563.x] [PMID: 15601430]
[150]
Mattsson, H.; Arani, Z.; Astin, M.; Bayati, A.; Overstreet, D.H.; Lehmann, A. Altered neuroendocrine response and gastric dysmotility in the flinders sensitive line rat. Neurogastroenterol. Motil., 2005, 17(2), 166-174.
[http://dx.doi.org/10.1111/j.1365-2982.2005.00665.x] [PMID: 15787937]
[151]
Malkesman, O.; Braw, Y.; Maayan, R.; Weizman, A.; Overstreet, D.H.; Shabat-Simon, M.; Kesner, Y.; Touati-Werner, D.; Yadid, G.; Weller, A. Two different putative genetic animal models of childhood depression. Biol. Psychiatry, 2006, 59(1), 17-23.
[http://dx.doi.org/10.1016/j.biopsych.2005.05.039] [PMID: 16095569]
[152]
Malkesman, O.; Maayan, R.; Weizman, A.; Weller, A. Aggressive behavior and HPA axis hormones after social isolation in adult rats of two different genetic animal models for depression. Behav. Brain Res., 2006, 175(2), 408-414.
[http://dx.doi.org/10.1016/j.bbr.2006.09.017] [PMID: 17069898]
[153]
Braw, Y.; Malkesman, O.; Merlender, A.; Bercovich, A.; Dagan, M.; Maayan, R.; Weizman, A.; Weller, A. Stress hormones and emotion-regulation in two genetic animal models of depression. Psychoneuroendocrinology, 2006, 31(9), 1105-1116.
[http://dx.doi.org/10.1016/j.psyneuen.2006.07.003] [PMID: 16982157]
[154]
Thiele, S.; Spehl, T.S.; Frings, L.; Braun, F.; Ferch, M.; Rezvani, A.H.; Furlanetti, L.L.; Meyer, P.T.; Coenen, V.A.; Döbrössy, M.D. Long-term characterization of the Flinders Sensitive Line rodent model of human depression: Behavioral and PET evidence of a dysfunctional entorhinal cortex. Behav. Brain Res., 2016, 300, 11-24.
[http://dx.doi.org/10.1016/j.bbr.2015.11.026] [PMID: 26658515]
[155]
Mncube, K.; Möller, M.; Harvey, B.H. Post-weaning social isolated flinders sensitive line rats display bio-behavioural manifestations resistant to fluoxetine: A model of treatment-resistant depression. Front. Psychiatry, 2021, 12, 688150.
[http://dx.doi.org/10.3389/fpsyt.2021.688150] [PMID: 34867504]
[156]
Kokras, N.; Sotiropoulos, I.; Pitychoutis, P.M.; Almeida, O.F.X.; Papadopoulou-Daifoti, Z. Citalopram-mediated anxiolysis and differing neurobiological responses in both sexes of a genetic model of depression. Neuroscience, 2011, 194, 62-71.
[http://dx.doi.org/10.1016/j.neuroscience.2011.07.077] [PMID: 21839808]
[157]
Walker, S.E.; Zanoletti, O.; Guillot de Suduiraut, I.; Sandi, C. Constitutive differences in glucocorticoid responsiveness to stress are related to variation in aggression and anxiety-related behaviors. Psychoneuroendocrinology, 2017, 84, 1-10.
[http://dx.doi.org/10.1016/j.psyneuen.2017.06.011] [PMID: 28647673]
[158]
Huzard, D.; Ghosal, S.; Grosse, J.; Carnevali, L.; Sgoifo, A.; Sandi, C. Low vagal tone in two rat models of psychopathology involving high or low corticosterone stress responses. Psychoneuroendocrinology, 2019, 101, 101-110.
[http://dx.doi.org/10.1016/j.psyneuen.2018.11.003] [PMID: 30448728]
[159]
Walker, S.E.; Sandi, C. Long-term programing of psychopathology-like behaviors in male rats by peripubertal stress depends on individual’s glucocorticoid responsiveness to stress. Stress, 2018, 21(5), 433-442.
[http://dx.doi.org/10.1080/10253890.2018.1435639] [PMID: 29415604]
[160]
Huzard, D.; Vouros, A.; Monari, S.; Astori, S.; Vasilaki, E.; Sandi, C. Constitutive differences in glucocorticoid responsiveness are related to divergent spatial information processing abilities. Stress, 2020, 23(1), 37-49.
[http://dx.doi.org/10.1080/10253890.2019.1625885] [PMID: 31187686]
[161]
Elenkov, I.J.; Kvetnansky, R.; Hashiramoto, A.; Bakalov, V.K.; Link, A.A.; Zachman, K.; Crane, M.; Jezova, D.; Rovensky, J.; Dimitrov, M.A.; Gold, P.W.; Bonini, S.; Fleisher, T.; Chrousos, G.P.; Wilder, R.L. Low versus high-baseline epinephrine output shapes opposite innate cytokine profiles: Presence of Lewis and Fischer-like neurohormonal immune phenotypes in humans? J. Immunol., 2008, 181(3), 1737-1745.
[http://dx.doi.org/10.4049/jimmunol.181.3.1737] [PMID: 18641310]
[162]
Goldstein, D.S.; Garty, M.; Bagdy, G.; Szemeredi, K.; Sternberg, E.M.; Listwak, S.; Pacak, K.; Deka-Starosta, A.; Hoffman, A.; Chang, P.C.; Stull, R.; Gold, P.W.; Kopin, I.J. Role of CRH in glucopenia-induced adrenomedullary activation in rats. J. Neuroendocrinol., 1993, 5(5), 475-486.
[http://dx.doi.org/10.1111/j.1365-2826.1993.tb00511.x] [PMID: 8680414]
[163]
Boersma, G.J.; Scheurink, A.J.W.; Wielinga, P.Y.; Steimer, T.J.; Benthem, L. The passive coping Roman Low Avoidance rat, a nonobese rat model for insulin resistance. Physiol. Behav., 2009, 97(3-4), 353-358.
[http://dx.doi.org/10.1016/j.physbeh.2009.03.005] [PMID: 19296906]
[164]
Castanon, N.; Dulluc, J.; Le Moal, M.; Mormède, P. Maturation of the behavioral and neuroendocrine differences between the Roman rat lines. Physiol. Behav., 1994, 55(4), 775-782.
[http://dx.doi.org/10.1016/0031-9384(94)90059-0] [PMID: 7986261]
[165]
Steimer, T.; la Fleur, S.; Schulz, P.E. Neuroendocrine correlates of emotional reactivity and coping in male rats from the Roman high (RHA/Verh)- and low (RLA/Verh)-avoidance lines. Behav. Genet., 1997, 27(6), 503-512.
[http://dx.doi.org/10.1023/A:1021448713665] [PMID: 9476359]
[166]
Steger, R.W.; Avila-Jimenez, R.; Amador, A.; Johns, A. Altered hypothalamic monoamine metabolism and pituitary prolactin regulation in female spontaneously hypertensive rats. Life Sci., 1984, 34(17), 1691-1697.
[http://dx.doi.org/10.1016/0024-3205(84)90641-6] [PMID: 6203002]
[167]
Amador, A.; Steger, R.W.; Bartke, A.; Johns, A.; Hayashi, R.H.; Stallings, M.H. Pituitary and testicular function in spontaneously hypertensive rats. J. Androl., 1983, 4(1), 67-70.
[http://dx.doi.org/10.1002/j.1939-4640.1983.tb00722.x] [PMID: 6302057]
[168]
Sanchís-Ollé, M.; Sánchez-Benito, L.; Fuentes, S.; Gagliano, H.; Belda, X.; Molina, P.; Carrasco, J.; Nadal, R.; Armario, A. Male long-Evans rats: An outbred model of marked hypothalamicpituitary-adrenal hyperactivity. Neurobiol. Stress, 2021, 15, 100355.
[http://dx.doi.org/10.1016/j.ynstr.2021.100355] [PMID: 34307794]
[169]
Jurcovicová, J.; Vigas, M.; Klír, P.; Jezová, D. Response of prolactin, growth hormone and corticosterone secretion to morphine administration or stress exposure in Wistar-AVN and Long Evans rats. Endocrinol. Exp., 1984, 18(4), 209-214.
[PMID: 6335081]
[170]
Vodička, M.; Vavřínová, A.; Mikulecká, A.; Zicha, J.; Behuliak, M. Hyper-reactivity of HPA axis in Fischer 344 rats is associated with impaired cardiovascular and behavioral adaptation to repeated restraint stress. Stress, 2020, 23(6), 667-677.
[http://dx.doi.org/10.1080/10253890.2020.1777971] [PMID: 32543321]
[171]
Márquez, C.; Nadal, R.; Armario, A. Responsiveness of the hypothalamic-pituitary-adrenal axis to different novel environments is a consistent individual trait in adult male outbred rats. Psychoneuroendocrinology, 2005, 30(2), 179-187.
[http://dx.doi.org/10.1016/j.psyneuen.2004.05.012] [PMID: 15471615]
[172]
Márquez, C.; Nadal, R.; Armario, A. Influence of reactivity to novelty and anxiety on hypothalamic-pituitary-adrenal and prolactin responses to two different novel environments in adult male rats. Behav. Brain Res., 2006, 168(1), 13-22.
[http://dx.doi.org/10.1016/j.bbr.2005.10.004] [PMID: 16303185]
[173]
Nadal, R.; Gabriel-Salazar, M.; Sanchís-Ollé, M.; Gagliano, H.; Belda, X.; Armario, A. Individual differences in the neuroendocrine response of male rats to emotional stressors are not trait-like and strongly depend on the intensity of the stressors. Psychoneuroendocrinology, 2021, 125, 105127.
[http://dx.doi.org/10.1016/j.psyneuen.2021.105127] [PMID: 33453596]
[174]
Armario, A. The forced swim test: Historical, conceptual and methodological considerations and its relationship with individual behavioral traits. Neurosci. Biobehav. Rev., 2021, 128, 74-86.
[http://dx.doi.org/10.1016/j.neubiorev.2021.06.014] [PMID: 34118295]
[175]
Will, C.C.; Aird, F.; Redei, E.E. Selectively bred Wistar–Kyoto rats: An animal model of depression and hyper-responsiveness to antidepressants. Mol. Psychiatry, 2003, 8(11), 925-932.
[http://dx.doi.org/10.1038/sj.mp.4001345] [PMID: 14593430]
[176]
Solberg, L.C.; Ahmadiyeh, N.; Baum, A.E.; Vitaterna, M.H.; Takahashi, J.S.; Turek, F.W.; Redei, E.E. Depressive-like behavior and stress reactivity are independent traits in a Wistar Kyoto × Fisher 344 cross. Mol. Psychiatry, 2003, 8(4), 423-433.
[http://dx.doi.org/10.1038/sj.mp.4001255] [PMID: 12740600]

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