The effects of repeated corticosterone exposure on the interoceptive effects of alcohol in rats

Psychopharmacology

Volumn 220, Issue 4, 2012, Pages 809-822

  Besheer, Joyce ^a,b   Fisher, Kristen R ^a   Grondin, Julie J M ^a   Cannady, Reginald ^a,b   Hodge, Clyde W ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Alcohol; Alcoholism; Discriminative stimulus Ethanol; Drinking; Drug discrimination; HPA axis dysregulation; Interoceptive; Stress Glucocorticoids; Subjective

Indexed keywords

ALCOHOL; CORTICOSTERONE; DEXAMETHASONE; SUCROSE; WATER;

ALCOHOL ABUSE; ALCOHOL BLOOD LEVEL; ALCOHOLISM; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CORTICOSTEROID METABOLISM; CORTICOSTERONE RELEASE; DISCRIMINATION LEARNING; DISCRIMINATIVE STIMULUS; DRINKING BEHAVIOR; DRUG DISCRIMINATION TEST; HYPOPHYSIS ADRENAL SYSTEM; MALE; MEMORY; NEGATIVE FEEDBACK; NEUROBIOLOGY; NONHUMAN; PRIORITY JOURNAL; RAT; STIMULUS RESPONSE; ANIMAL; CHEMICALLY INDUCED DISORDER; COMPARATIVE STUDY; DOSE RESPONSE; DRUG EFFECT; DRUG SELF ADMINISTRATION; LONG EVANS RAT; MENTAL STRESS; PHYSIOLOGY; PSYCHOLOGICAL ASPECT;

ANIMALS; CORTICOSTERONE; DISCRIMINATION LEARNING; DOSE-RESPONSE RELATIONSHIP, DRUG; ETHANOL; MALE; RATS; RATS, LONG-EVANS; SELF ADMINISTRATION; STRESS, PSYCHOLOGICAL;

EID: 84861975683     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-011-2533-8     Document Type: Article

References (76)

1. Adinoff B, Martin PR, Bone G.H., Eckardt MJ, Roehrich L, George DT, Moss H.B., Eskay R., Linnoila M, Gold PW (1990) Hypothalamic-pituitary-adrenal axis functioning and cerebrospinal fluid corticotropin releasing hormone and corticotropin levels in alcoholics after recent and long-term abstinence. Arch Gen Psychiatry 47:325-330
2. Berman JD, Cook DM, Buchman M, Keith L.D. (1990) Diminished adrenocorticotropin response to insulin-induced hypoglycemia in nondepressed, actively drinking male alcoholics. J Clin Endocrinol Metab 71:712-717
3. Besheer J, Hodge C.W. (2005) Pharmacological and anatomical evidence for an interaction between mGluR5- and GABA(A) alpha1-containing receptors in the discriminative stimulus effects of ethanol. Neuropsychopharmacology 30:747-757
4. Besheer J, Cox AA, Hodge C.W. (2003) Coregulation of ethanol discrimination by the nucleus accumbens and amygdala. Alcohol Clin Exp Res 27:450-456
5. Besheer J, Stevenson RA, Hodge C.W. (2006) mGlu5 receptors are involved in the discriminative stimulus effects of self-administered ethanol in rats. Eur J Pharmacol 551:71-75
6. Besheer J, Schroeder JP, Stevenson R.A., Hodge C.W. (2008) Ethanol-induced alterations of c-Fos immunoreactivity in specific limbic brain regions following ethanol discrimination training. Brain Res 1232:124-131
7. Besheer J, Grondin JJ, Salling M.C., Spanos M., Stevenson RA, Hodge C.W. (2009) Interoceptive effects of alcohol require mGlu5 receptor activity in the nucleus accumbens. J Neurosci 29:9582-9591
8. Bowen CA, Purdy RH, Grant K.A. (1999) An investigation of endogenous neuroactive steroid-induced modulation of ethanol's discriminative stimulus effects. Behav Pharmacol 10:297-311
9. Brown ES, Varghese FP, McEwen B.S. (2004) Association of depression with medical illness: does cortisol play a role? Biol Psychiatry 55:1-9
10. Buffalari DM, Grace A.A. (2009) Chronic cold stress increases excitatory effects of norepinephrine on spontaneous and evoked activity of basolateral amygdala neurons. hit J Neuropsycho-pharmacol 12:95-107
11. Buwalda B, de Boer SF, Schmidt ED, Felszeghy K, Nyakas C, Sgoifo A., Van der Vegt BJ, Tilders FJ, Bohus B, Koolhaas JM (1999) Long-lasting deficient dexamethasone suppression of hypothalamic-pituitary-adrenocortical activation following peripheral CRF challenge in socially defeated rats. J Neuroendocrinol 11:513-520
12. Cannady R, Grondin JJ, Fisher K.R., Hodge CW, Besheer J. (2011) Activation of group I metabotropic glutamate receptors inhibits the discriminative stimulus effects of alcohol via selective activity within the amygdala. Neuropsychopharmacology
13. Chao HM, Choo PH, McEwen B.S. (1989) Glucocorticoid and mineralocorticoid receptor mRNA expression in rat brain. Neuroendocrinology 50:365-371
14. Childs E, O'Connor S, de Wit H (2011) Bidirectional interactions between acute psychosocial stress and acute intravenous alcohol in healthy men. Alcohol Clin Exp Res
15. Conrad CD, LeDoux JE, Magarinos A.M., McEwen B.S. (1999) Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behav Neurosci 113:902-913
16. Conrad CD, McLaughlin KJ, Harman J.S., Foltz C., Wieczorek L, Lightner E, Wright R.L. (2007) Chronic glucocorticoids increase hippocampal vulnerability to neurotoxicity under conditions that produce CA3 dendritic retraction but fail to impair spatial recognition memory. J Neurosci 27:8278-8285
17. Costa A, Bono G, Martignoni E., Merlo P, Sances G, Nappi G. (1996) An assessment of hypothalamo-pituitary-adrenal axis functioning in non-depressed, early abstinent alcoholics. Psychoneuroendocrinology 21:263-275
18. Crum RM, Pratt L.A. (2001) Risk of heavy drinking and alcohol use disorders in social phobia: a prospective analysis. Am J Psychiatry 158:1693-1700
19. Dai X, Thavundayil J, Gianoulakis C. (2002) Response of the hypothalamic-pituitary-adrenal axis to stress in the absence and presence of ethanol in subjects at high and low risk of alcoholism. Neuropsychopharmacology 27:442-452
20. Davidson JR, Kudler HS, Saunders W.B., Smith R.D. (1990) Symptom and comorbidity patterns in World War II and Vietnam veterans with posttraumatic stress disorder. Compr Psychiatry 31:162-170
21. de Kloet E.R., Joels M, Holsboer F. (2005) Stress and the brain: from adaptation to disease. Nat Rev Neurosci 6:463-475
22. de Wit H., Soderpalm AH, Nikolayev L, Young E. (2003) Effects of acute social stress on alcohol consumption in healthy subjects. Alcohol Clin Exp Res 27:1270-1277
23. Errico AL, Parsons OA, King A.C., Lovallo W.R. (1993) Attenuated cortisol response to biobehavioral stressors in sober alcoholics. J Stud Alcohol 54:393-398
24. Filip M, Nowak E, Siwanowicz J., Przegalinski E. (2000) Effects of corticosterone and its synthesis blockade on the cocaine-induced discriminative stimulus effects in rats. Pol J Pharmacol 52:411-421
25. Goeders NE (2002) The HPA axis and cocaine reinforcement. Psychoneuroendocrinology 27:13-33
26. Gold PW, Chrousos G.P. (2002) Organization of the stress system and its dysregulation in melancholic and atypical depression: high vs. low CRH/NE states. Mol Psychiatry 7:254-275
27. Gourley SL, Taylor J.R. (2009) Recapitulation and reversal of a persistent depression-like syndrome in rodents. Curr Protoc Neurosci Chapter 9: Unit 9 32
28. Griesbach GS, Hovda DA, Tio D.L., Taylor A.N. (2011) Heightening of the stress response during the first weeks after a mild traumatic brain injury. Neuroscience 178:147-158
29. Harris RB, Gu H, Mitchell T.D., Endale L., Russo M, Ryan D.H. (2004) Increased glucocorticoid response to a novel stress in rats that have been restrained. Physiol Behav 81:557-568
30. Hasin DS, Goodwin RD, Stinson F.S., Grant B.F. (2005) Epidemiology of major depressive disorder: results from the National Epidemiologic Survey on Alcoholism and Related Conditions. Arch Gen Psychiatry 62:1097-1106
31. Hatzinger M, Reul JM, Landgraf R, Holsboer F., Neumann I. (1996) Combined dexamethasone/CRH test in rats: hypothalamo-pituitary-adrenocortical system alterations in aging. Neuroendocrinology 64:349-356
32. Herman JP, Ostrander MM, Mueller N.K., Figueiredo H. (2005) Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog Neuropsychopharmacol Biol Psychiatry 29:1201-1213
33. Hernandez-Avila C.A., Oncken C, Van Kirk J, Wand G, Kranzler H.R. (2002) Adrenocorticotropin and cortisol responses to a naloxone challenge and risk of alcoholism. Biol Psychiatry 51:652-658
34. Hodge CW, Aiken A.S. (1996) Discriminative stimulus function of ethanol: role of GABAA receptors in the nucleus accumbens. Alcohol Clin Exp Res 20:1221-1228
35. Hodge CW, Cox A.A. (1998) The discriminative stimulus effects of ethanol are mediated by NMDA and GABA(A) receptors in specific limbic brain regions. Psychopharmacology (Berl) 139:95-107
36. Hoffmann JP, Su S.S. (1998) Stressful life events and adolescent substance use and depression: conditional and gender differentiated effects. Subst Use Misuse 33:2219-2262
37. Ising M, Kunzel HE, Binder E.B., Nickel T., Modell S, Holsboer F. (2005) The combined dexamethasone/CRH test as a potential surrogate marker in depression. Prog Neuropsychopharmacol Biol Psychiatry 29:1085-1093
38. Jacobsen LK, Southwick SM, Kosten T.R. (2001) Substance use disorders in patients with posttraumatic stress disorder: a review of the literature. Am J Psychiatry 158:1184-1190
39. Karatsoreos IN, Bhagat SM, Bowles N.P., Weil ZM, Pfaff DW, McEwen B.S. (2010) Endocrine and physiological changes in response to chronic corticosterone: a potential model of the metabolic syndrome in, ouse. Endocrinology 151:2117-2127
40. King A, Munisamy G, de Wit H, Lin S. (2006) Attenuated cortisol response to alcohol in heavy social drinkers. Int J Psychophysiol 59:203-209
41. Kodl MM, Fu SS, Willenbring M.L., Gravely A., Nelson DB, Joseph A.M. (2008) The impact of depressive symptoms on alcohol and cigarette consumption following treatment for alcohol and nicotine dependence. Alcohol Clin Exp Res 32:92-99
42. Koob GF (1999) Stress, corticotropin-releasing factor, and drug addiction. Ann N Y Acad Sci 897:27-45
43. Koros E, Kostowski W, Danysz W., Bienkowski P. (1999) Ethanol discrimination in the rat: lack of modulation by restraint stress and memantine. Naunyn Schmiedebergs Arch Pharmacol 359:117-122
44. Kreek MJ, Koob G.F. (1998) Drug dependence: stress and dysregulation of brain reward pathways. Drug Alcohol Depend 51:23-47
45. Lovallo WR, Dickensheets SL, Myers D.A., Thomas TL, Nixon S.J. (2000) Blunted stress cortisol response in abstinent alcoholic and polysubstance- abusing men. Alcohol Clin Exp Res 24:651-658
46. Lu L, Shepard JD, Hall F.S., Shaham Y. (2003) Effect of environmental stressors on opiate and psychostimulant reinforcement, reinstatement and discrimination in rats: a review. Neurosci Biobehav Rev 27:457-491
47. Magarinos AM, Orchinik M, McEwen B.S. (1998) Morphological changes in the hippocampal CA3 region induced by non-invasive glucocorticoid administration: a paradox. Brain Res 809:314-318
48. Majumdar SK, Shaw GK, Bridges P.K. (1988) The dexamethasone suppression test in chronic alcoholics with and without depression and its relationship to their hepatic status. Drug Alcohol Depend 21:231-235
49. Makino S, Gold PW, Schulkin J. (1994) Corticosterone effects on corticotropin-releasing hormone mRNA in the central nucleus of the amygdala and the parvocellular region of the paraventricular nucleus of the hypothalamus. Brain Res 640:105-112
50. Mantsch JR, Goeders N.E. (1998) Generalization of a restraint-induced discriminative stimulus to cocaine in rats. Psychopharmacology (Berl) 135:423-426
51. Mantsch JR, Cullinan WE, Tang L.C., Baker DA, Katz ES, Hoks MA, Ziegler D.R. (2007) Daily cocaine self-administration under long-access conditions augments restraint-induced increases in plasma corticosterone and impairs glucocorticoid receptor-mediated negative feedback in rats. Brain Res 1167:101-111
52. Marti O, Armario A. (1997) Influence of regularity of exposure to chronic stress on the pattern of habituation of pituitary-adrenal hormones, prolactin and glucose. Stress 1:179-189
53. McEwen BS (2007) Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev 87:873-904
54. McLaughlin KJ, Gomez JL, Baran S.E., Conrad C.D. (2007) The effects of chronic stress on hippocampal morphology and function: an evaluation of chronic restraint paradigms. Brain Res 1161:56-64
55. Miczek KA, Mutschler NH, van Erp AM, Blank AD, McInerney S.C. (1999) d-amphetamine "cue" generalizes to social defeat stress: behavioral sensitization and attenuated accumbens dopamine. Psychopharmacology (Berl) 147:190-199
56. Mizoguchi K, Shoji H, Ikeda R., Tanaka Y, Tabira T. (2008) Persistent depressive state after chronic stress in rats is accompanied by HPA axis dysregulation and reduced prefrontal dopaminergic neurotransmission. Pharmacol Biochem Behav 91:170-175
57. Morales-Medina J.C., Sanchez F, Flores G., Dumont Y, Quirion R. (2009) Morphological reorganization after repeated corticosterone administration in the hippocampus, nucleus accumbens and amygdala in the rat. J Chem Neuroanat
58. Otero Losada ME (1988) Changes in central GABAergic function following acute and repeated stress. Br J Pharmacol 93:483-490
59. Perrotti LI, Hadeishi Y, Ulery P.G., Barrot M., Monteggia L, Duman RS, Nestler E.J. (2004) Induction of deltaFosB in reward-related brain structures after chronic stress. J Neurosci 24:10594-10602
60. Piazza PV, Le Moal M (1998) The role of stress in drug self-administration. Trends Pharmacol Sci 19:67-74
61. Pollock VE (1992) Meta-analysis of subjective sensitivity to alcohol in sons of alcoholics. Am J Psychiatry 149:1534-1538
62. Pung T, Zimmerman K, Klein B., Ehrich M. (2003) Corticosterone in drinking water: altered kinetics of a single oral dose of corticosterone and concentrations of plasma sodium, albumin, globulin, and total protein. Toxicol Ind Health 19:171-182
63. Raone A, Cassanelli A, Scheggi S., Rauggi R, Danielli B, De Montis MG (2007) Hypothalamus-pituitary-adrenal modifications consequent to chronic stress exposure in an experimental model of depression in rats. Neuroscience 146:1734-1742
64. Romeo RD, Bellani R, Karatsoreos I.N., Chhua N., Vernov M, Conrad CD, McEwen B.S. (2006) Stress history and pubertal development interact to shape hypothalamic-pituitary-adrenal axis plasticity. Endocrinology 147:1664-1674
65. Sapolsky RM (2000) Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Arch Gen Psychiatry 57:925-935
66. Schneier FR, Foose TE, Hasin D.S., Heimberg RG, Liu SM, Grant BF, Blanco C. (2010) Social anxiety disorder and alcohol use disorder co-morbidity in the National Epidemiologic Survey on Alcohol and Related Conditions. Psychol Med 40:977-988
67. Schuckit MA (2009) An overview of genetic influences in alcoholism. J Subst Abuse Treat 36:S5-S14
68. Schuckit MA, Smith T.L. (2000) The relationships of a family history of alcohol dependence, a low level of response to alcohol and six domains of life functioning to the development of alcohol use disorders. J Stud Alcohol 61:827-835
69. Sillaber I, Henniger M.S. (2004) Stress and alcohol drinking. Ann Med 36:596-605
70. Stolerman I (1992) Drugs of abuse: behavioural principles, methods and terms. Trends Pharmacol Sci 13:170-176
71. Trim RS, Schuckit MA, Smith T.L. (2009) The relationships of the level of response to alcohol and additional characteristics to alcohol use disorders across adulthood: a discrete-time survival analysis. Alcohol Clin Exp Res 33:1562-1570
72. Uhart M, Oswald L, McCaul M.E., Chong R., Wand G.S. (2006) Hormonal responses to psychological stress and family history of alcoholism. Neuropsychopharmacology 31:2255-2263
73. Van Eekelen J.A., Jiang W, De Kloet ER, Bohn M.C. (1988) Distribution of the mineralocorticoid and the glucocorticoid receptor mRNAs in the rat hippocampus. J Neurosci Res 21:88-94
74. Waltman C, McCaul ME, Wand G.S. (1994) Adrenocorticotropin responses following administration of ethanol and ovine corticotropin-releasing hormone in the sons of alcoholics and control subjects. Alcohol Clin Exp Res 18:826-830
75. Wand GS, Dobs A.S. (1991) Alterations in the hypothalamic-pituitary- adrenal axis in actively drinking alcoholics. J Clin Endocrinol Metab 72:1290-1295
76. Wang W, Sun D, Pan B., Roberts CJ, Sun X, Hillard CJ, Liu Q.S. (2010) Deficiency in endocannabinoid signaling in the nucleus accumbens induced by chronic unpredictable stress. Neuropsychopharmacology