Adolescent social isolation increases anxiety-like behavior and ethanol intake and impairs fear extinction in adulthood: Possible role of disrupted noradrenergic signaling

Neuropharmacology

Volumn 97, Issue , 2015, Pages 149-159

  Skelly, M J ^a   Chappell, A E ^a   Carter, E ^a   Weiner, J L ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Duloxetine; Fear potentiated startle; Prazosin; Propranolol; Social isolation

Indexed keywords

DULOXETINE; PRAZOSIN; PROPRANOLOL; ALCOHOL; ANXIOLYTIC AGENT; CENTRAL DEPRESSANT AGENT; NORADRENALIN;

ADOLESCENT; ALCOHOL CONSUMPTION; ALCOHOL USE DISORDER; ALCOHOLISM; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; CONDITIONING; CONTROLLED STUDY; FEAR; MALE; NONHUMAN; NORADRENERGIC SYSTEM; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; RAT; REINFORCEMENT; SOCIAL ISOLATION; STARTLE REFLEX; SYMPTOM; AGING; ANIMAL; DRINKING BEHAVIOR; DRUG SELF ADMINISTRATION; DRUG THERAPY; LONG EVANS RAT; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY; RANDOMIZATION;

AGING; ALCOHOL DRINKING; ANIMALS; ANTI-ANXIETY AGENTS; ANXIETY; CENTRAL NERVOUS SYSTEM DEPRESSANTS; CONDITIONING (PSYCHOLOGY); DULOXETINE HYDROCHLORIDE; ETHANOL; EXTINCTION, PSYCHOLOGICAL; FEAR; MALE; NOREPINEPHRINE; PRAZOSIN; PROPRANOLOL; RANDOM ALLOCATION; RATS, LONG-EVANS; SELF ADMINISTRATION; SOCIAL ISOLATION;

EID: 84934973802     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2015.05.025     Document Type: Article

References (86)

1. G. Aston-Jones, and G.C. Harris Brain substrates for increased drug seeking during protracted withdrawal Neuropharmacology 47 Suppl. 1 2004 167 179
2. D. Bailly, D. Servant, N. Blandin, R. Beuscart, and P.J. Parquet Effects of beta-blocking drugs in alcohol withdrawal: a double-blind comparative study with propranolol and diazepam Biomed. Pharmacother. 46 1992 419 424
3. M. Barad Fear extinction in rodents: basic insight to clinical promise Curr. Opin. Neurobiol. 15 2005 710 715
4. H.C. Becker Effects of alcohol dependence and withdrawal on stress responsiveness and alcohol consumption Alcohol Res. 34 2012 448 458
5. H.C. Becker, M.F. Lopez, and T.L. Doremus-Fitzwater Effects of stress on alcohol drinking: a review of animal studies Psychopharmacology (Berl.) 218 2011 131 156
6. C.W. Berridge, and B.D. Waterhouse The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes Brain Res. Brain Res. Rev. 42 2003 33 84
7. E. Berrocoso, and J.A. Mico In vivo effect of venlafaxine on locus coeruleus neurons: role of opioid, alpha(2)- adrenergic, and 5-hydroxytryptamine(1A) receptors J. Pharmacol. Exp. Ther. 322 2007 101 107
8. B. Bingham, K. McFadden, X. Zhang, S. Bhatnagar, S. Beck, and R. Valentino Early adolescence as a critical window during which social stress distinctly alters behavior and brain norepinephrine activity Neuropsychopharmacology 36 2011 896 909
9. J.K. Boehnlein, and J.D. Kinzie Pharmacologic reduction of CNS noradrenergic activity in PTSD: the case for clonidine and prazosin J. Psychiatr. Pract. 13 2007 72 78
10. C.O. Bondi, G. Barrera, M.D. Lapiz, T. Bedard, A. Mahan, and D.A. Morilak Noradrenergic facilitation of shock-probe defensive burying in lateral septum of rats, and modulation by chronic treatment with desipramine Prog. Neuropsychopharmacol. Biol. Psychiatry 31 2007 482 495
11. K.T. Brady, and R. Sinha Co-occurring mental and substance use disorders: the neurobiological effects of chronic stress Am. J. Psychiatry 162 2005 1483 1493
12. O. Brawman-Mintzer, and R.B. Lydiard Biological basis of generalized anxiety disorder J. Clin. Psychiatry 58 Suppl. 3 1997 16 25 discussion 26
13. G.R. Breese, R. Sinha, and M. Heilig Chronic alcohol neuroadaptation and stress contribute to susceptibility for alcohol craving and relapse Pharmacol. Ther. 129 2011 149 171
14. S.E. Bruce, K.A. Yonkers, M.W. Otto, J.L. Eisen, R.B. Weisberg, M. Pagano, M.T. Shea, and M.B. Keller Influence of psychiatric comorbidity on recovery and recurrence in generalized anxiety disorder, social phobia, and panic disorder: a 12-year prospective study Am. J. Psychiatry 162 2005 1179 1187
15. S. Carnicella, D. Ron, and S. Barak Intermittent ethanol access schedule in rats as a preclinical model of alcohol abuse Alcohol 48 2014 243 252
16. A.M. Chappell, E. Carter, B.A. McCool, and J.L. Weiner Adolescent rearing conditions influence the relationship between initial anxiety-like behavior and ethanol drinking in male Long Evans rats Alcohol Clin. Exp. Res. 37 Suppl. 1 2013 E394 E403
17. F.C. Cruz, I.M. Quadros, S. Planeta Cda, and K.A. Miczek Maternal separation stress in male mice: long-term increases in alcohol intake Psychopharmacology (Berl.) 201 2008 459 468
18. T.A. Davis, T. Jovanovic, S.D. Norrholm, E.M. Glover, M. Swanson, S. Spann, and B. Bradley Substance use attenuates physiological responses associated with PTSD among individuals with co-morbid PTSD and SUDs J. Psychol. Psychother. Suppl. 7 2013
19. G.A. Deehan, M.E. Cain, and S.W. Kiefer Differential rearing conditions alter operant responding for ethanol in outbred rats Alcohol. Clin. Exp. Res. 31 2007 1692 1698
20. J.M. Delfs, Y. Zhu, J.P. Druhan, and G. Aston-Jones Noradrenaline in the ventral forebrain is critical for opiate withdrawal-induced aversion Nature 403 2000 430 434
21. M. Driessen, S. Meier, A. Hill, T. Wetterling, W. Lange, and K. Junghanns The course of anxiety, depression and drinking behaviours after completed detoxification in alcoholics with and without comorbid anxiety and depressive disorders Alcohol Alcohol. 36 2001 249 255
22. C.L. Ehlers, B.M. Walker, J.P. Pian, J.L. Roth, and C.J. Slawecki Increased alcohol drinking in isolate-housed alcohol-preferring rats Behav. Neurosci. 121 2007 111 119
23. M.A. Enoch The role of early life stress as a predictor for alcohol and drug dependence Psychopharmacology (Berl.) 214 2011 17 31
24. R. Famularo, R. Kinscherff, and T. Fenton Propranolol treatment for childhood posttraumatic stress disorder, acute type. A pilot study Am. J. Dis. Child. 142 1988 1244 1247
25. H.C. Fox, G.M. Anderson, K. Tuit, J. Hansen, A. Kimmerling, K.M. Siedlarz, P.T. Morgan, and R. Sinha Prazosin effects on stress- and cue-induced craving and stress response in alcohol-dependent individuals: preliminary findings Alcohol. Clin. Exp. Res. 36 2012 351 360
26. T.D. Geracioti Jr., D.G. Baker, N.N. Ekhator, S.A. West, K.K. Hill, A.B. Bruce, D. Schmidt, B. Rounds-Kugler, R. Yehuda, P.E. Keck Jr., and J.W. Kasckow CSF norepinephrine concentrations in posttraumatic stress disorder Am. J. Psychiatry 158 2001 1227 1230
27. C.F. Gillespie, J. Phifer, B. Bradley, and K.J. Ressler Risk and resilience: genetic and environmental influences on development of the stress response Depress Anxiety 26 2009 984 992
28. N.W. Gilpin, and G.F. Koob Effects of beta-adrenoceptor antagonists on alcohol drinking by alcohol-dependent rats Psychopharmacology (Berl.) 212 2010 431 439
29. S. Goswami, O. Rodriguez-Sierra, M. Cascardi, and D. Pare Animal models of post-traumatic stress disorder: face validity Front. Neurosci. 7 2013 89
30. C. Grillon Models and mechanisms of anxiety: evidence from startle studies Psychopharmacology (Berl.) 199 2008 421 437
31. C. Grillon, and C.A. Morgan 3rd Fear-potentiated startle conditioning to explicit and contextual cues in Gulf War veterans with posttraumatic stress disorder J. Abnorm. Psychol. 108 1999 134 142
32. F.S. Hall, S. Huang, G.W. Fong, A. Pert, and M. Linnoila Effects of isolation-rearing on voluntary consumption of ethanol, sucrose and saccharin solutions in Fawn Hooded and Wistar rats Psychopharmacology (Berl.) 139 1998 210 216
33. F.S. Hall, S. Huang, G.W. Fong, A. Pert, and M. Linnoila Effects of isolation rearing on locomotion, anxiety and responses to ethanol in Fawn Hooded and Wistar rats Psychopharmacology (Berl.) 139 1998 203 209
34. C. Heim, and C.B. Nemeroff The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies Biol. Psychiatry 49 2001 1023 1039
35. K.G.C. Hellemans, L.C. Benge, and M.C. Olmstead Adolescent enrichment partially reverses the social isolation syndrome Dev. Brain Res. 150 2004 103 115
36. A. Holmes, P.J. Fitzgerald, K.P. MacPherson, L. DeBrouse, G. Colacicco, S.M. Flynn, S. Masneuf, K.E. Pleil, C. Li, C.A. Marcinkiewcz, T.L. Kash, O. Gunduz-Cinar, and M. Camp Chronic alcohol remodels prefrontal neurons and disrupts NMDAR-mediated fear extinction encoding Nat. Neurosci. 15 2012 1359 1361
37. R.L. Huot, K.V. Thrivikraman, M.J. Meaney, and P.M. Plotsky Development of adult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long Evans rats and reversal with antidepressant treatment Psychopharmacology (Berl.) 158 2001 366 373
38. L.K. Jacobsen, S.M. Southwick, and T.R. Kosten Substance use disorders in patients with posttraumatic stress disorder: a review of the literature Am. J. Psychiatry 158 2001 1184 1190
39. R. Jankord, M.B. Solomon, J. Albertz, J.N. Flak, R. Zhang, and J.P. Herman Stress vulnerability during adolescent development in rats Endocrinology 152 2011 629 638
40. H.P. Jedema, J.M. Finlay, A.F. Sved, and A.A. Grace Chronic cold exposure potentiates CRH-evoked increases in electrophysiologic activity of locus coeruleus neurons Biol. Psychiatry 49 2001 351 359
41. D. Ji, N.W. Gilpin, H.N. Richardson, C.L. Rivier, and G.F. Koob Effects of naltrexone, duloxetine, and a corticotropin-releasing factor type 1 receptor antagonist on binge-like alcohol drinking in rats Behav. Pharmacol. 19 2008 1 12
42. T. Jovanovic, S.D. Norrholm, N.Q. Blanding, M. Davis, E. Duncan, B. Bradley, and K.J. Ressler Impaired fear inhibition is a biomarker of PTSD but not depression Depress Anxiety 27 2010 244 251
43. T. Jovanovic, K.M. Nylocks, and K.L. Gamwell Translational neuroscience measures of fear conditioning across development: applications to high-risk children and adolescents Biol. Mood Anxiety Disord. 3 2013 17
44. J. Juarez, and C. Vazquez-Cortes Alcohol intake in social housing and in isolation before puberty and its effects on voluntary alcohol consumption in adulthood Dev. Psychobiol. 43 2003 200 207
45. A.N. Karkhanis, B.A. McCool, J.L. Weiner, and S.R. Jones Social isolation stress augments dopamine and norepinephrine responses to ethanol in the nucleus accumbens and the basolateral amygdala Alcohol. Clin. Exp. Res. 38 2014 81a-81a
46. J. Kaufman, B.Z. Yang, H. Douglas-Palumberi, M. Crouse-Artus, D. Lipschitz, J.H. Krystal, and J. Gelernter Genetic and environmental predictors of early alcohol use Biol. Psychiatry 61 2007 1228 1234
47. W. Kim, C.U. Pae, J.H. Chae, T.Y. Jun, and W.M. Bahk The effectiveness of mirtazapine in the treatment of post-traumatic stress disorder: a 24-week continuation therapy Psychiatry Clin. Neurosci. 59 2005 743 747
48. G.F. Koob Theoretical frameworks and mechanistic aspects of alcohol addiction: alcohol addiction as a reward deficit disorder Curr. Top. Behav. Neurosci. 13 2013 3 30
49. G.F. Koob, and M. Le Moal Plasticity of reward neurocircuitry and the 'dark side' of drug addiction Nat. Neurosci. 8 2005 1442 1444
50. M.G. Kushner, K. Abrams, and C. Borchardt The relationship between anxiety disorders and alcohol use disorders: a review of major perspectives and findings Clin. Psychol. Rev. 20 2000 149 171
51. M. Lader Beta-adrenoceptor antagonists in neuropsychiatry: an update J. Clin. Psychiatry 49 1988 213 223
52. C. Lanteri, L. Salomon, Y. Torrens, J. Glowinski, and J.P. Tassin Drugs of abuse specifically sensitize noradrenergic and serotonergic neurons via a non-dopaminergic mechanism Neuropsychopharmacology 33 2008 1724 1734
53. A.D. Le, S. Harding, W. Juzytsch, D. Funk, and Y. Shaham Role of alpha-2 adrenoceptors in stress-induced reinstatement of alcohol seeking and alcohol self-administration in rats Psychopharmacology (Berl.) 179 2005 366 373
54. M. Leeies, J. Pagura, J. Sareen, and J.M. Bolton The use of alcohol and drugs to self-medicate symptoms of posttraumatic stress disorder Depress Anxiety 27 2010 731 736
55. J. Liappas, T. Paparrigopoulos, E. Tzavellas, and A. Rabavilas Mirtazapine and venlafaxine in the management of collateral psychopathology during alcohol detoxification Prog. Neuropsychopharmacol. Biol. Psychiatry 29 2005 55 60
56. B.A. McCool, and A.M. Chappell Early social isolation in male Long-Evans rats alters both appetitive and consummatory behaviors expressed during operant ethanol self-administration Alcohol. Clin. Exp. Res. 33 2009 273 282
57. E.M. Meyer, V. Long, M.S. Fanselow, and I. Spigelman Stress increases voluntary alcohol intake, but does not alter established drinking habits in a rat model of posttraumatic stress disorder Alcohol. Clin. Exp. Res. 37 2013 566 574
58. M.R. Milad, S.P. Orr, N.B. Lasko, Y. Chang, S.L. Rauch, and R.K. Pitman Presence and acquired origin of reduced recall for fear extinction in PTSD: results of a twin study J. Psychiatr. Res. 42 2008 515 520
59. D. Mochizuki, R. Tsujita, S. Yamada, K. Kawasaki, Y. Otsuka, S. Hashimoto, T. Hattori, Y. Kitamura, and N. Miki Neurochemical and behavioural characterization of milnacipran, a serotonin and noradrenaline reuptake inhibitor in rats Psychopharmacology (Berl.) 162 2002 323 332
60. D.A. Morilak, G. Barrera, D.J. Echevarria, A.S. Garcia, A. Hernandez, S. Ma, and C.O. Petre Role of brain norepinephrine in the behavioral response to stress Prog. Neuropsychopharmacol. Biol. Psychiatry 29 2005 1214 1224
61. A. Naert, Z. Callaerts-Vegh, and R. D'Hooge Nocturnal hyperactivity, increased social novelty preference and delayed extinction of fear responses in post-weaning socially isolated mice Brain Res. Bull. 85 2011 354 362
62. A.A. Patkar, C.A. Marsden, P.C. Naik, D.A. Kendall, R. Gopalakrishnan, M.J. Vergare, and S.P. Weinstein Differences in peripheral noradrenergic function among actively drinking and abstinent alcohol-dependent individuals Am. J. Addict. 13 2004 225 235
63. L.A. Pavcovich, L.M. Cancela, M. Volosin, V.A. Molina, and O.A. Ramirez Chronic stress-induced changes in locus coeruleus neuronal activity Brain Res. Bull. 24 1990 293 296
64. L.A. Pavcovich, and O.A. Ramirez Time course effects of uncontrollable stress in locus coeruleus neuronal activity Brain Res. Bull. 26 1991 17 21
65. I.L. Petrakis, E. Ralevski, N. Desai, L. Trevisan, R. Gueorguieva, B. Rounsaville, and J.H. Krystal Noradrenergic vs serotonergic antidepressant with or without naltrexone for veterans with PTSD and comorbid alcohol dependence Neuropsychopharmacology 37 2012 996 1004
66. D.D. Rasmussen, L.L. Alexander, M.A. Raskind, and J.C. Froehlich The alpha1-adrenergic receptor antagonist, prazosin, reduces alcohol drinking in alcohol-preferring (P) rats Alcohol. Clin. Exp. Res. 33 2009 264 272
67. D.D. Rasmussen, C.W. Wilkinson, and M.A. Raskind Chronic daily ethanol and withdrawal: 6. Effects on rat sympathoadrenal activity during "abstinence" Alcohol 38 2006 173 177
68. K.J. Ressler, and C.B. Nemeroff Role of norepinephrine in the pathophysiology of neuropsychiatric disorders CNS Spectr. 6 2001 663-666, 670
69. J. Robinson, J. Sareen, B.J. Cox, and J.M. Bolton Role of self-medication in the development of comorbid anxiety and substance use disorders: a longitudinal investigation Arch. Gen. Psychiatry 68 2011 800 807
70. E. Roman, and I. Nylander The impact of emotional stress early in life on adult voluntary ethanol intake-results of maternal separation in rats Stress 8 2005 157 174
71. R.D. Romeo Adolescence: a central event in shaping stress reactivity Dev. Psychobiol. 52 2010 244 253
72. R.D. Romeo, R. Bellani, I.N. Karatsoreos, N. Chhua, M. Vernov, C.D. Conrad, and B.S. McEwen Stress history and pubertal development interact to shape hypothalamic-pituitary-adrenal axis plasticity Endocrinology 147 2006 1664 1674
73. E. Saglam, I.T. Uzbay, H. Kayir, T. Celik, and M. Beyazyurek Effects of venlafaxine on ethanol withdrawal syndrome in rats Fundam. Clin. Pharmacol. 18 2004 693 698
74. E.M. Sellers, D.H. Zilm, and N.C. Degani Comparative efficacy of propranolol and chlordiazepoxide in alcohol withdrawal J. Stud. Alcohol 38 1977 2096 2108
75. J.A. Simms, P. Steensland, B. Medina, K.E. Abernathy, L.J. Chandler, R. Wise, and S.E. Bartlett Intermittent access to 20% ethanol induces high ethanol consumption in Long-Evans and Wistar rats Alcohol. Clin. Exp. Res. 32 2008 1816 1823
76. E. Simon O'Brien, R. Legastelois, H. Houchi, C. Vilpoux, S. Alaux-Cantin, O. Pierrefiche, E. Andre, and M. Naassila Fluoxetine, desipramine, and the dual antidepressant milnacipran reduce alcohol self-administration and/or relapse in dependent rats Neuropsychopharmacology 36 2011 1518 1530
77. T.L. Simpson, A.J. Saxon, C.W. Meredith, C.A. Malte, B. McBride, L.C. Ferguson, C.A. Gross, K.L. Hart, and M. Raskind A pilot trial of the alpha-1 adrenergic antagonist, prazosin, for alcohol dependence Alcohol. Clin. Exp. Res. 33 2009 255 263
78. M.J. Skelly, and J.L. Weiner Chronic treatment with prazosin or duloxetine lessens concurrent anxiety-like behavior and alcohol intake: evidence of disrupted noradrenergic signaling in anxiety-related alcohol use Brain Behav. 4 2014 468 483
79. R.J. Smith, and G. Aston-Jones Noradrenergic transmission in the extended amygdala: role in increased drug-seeking and relapse during protracted drug abstinence Brain Struct. Funct. 213 2008 43 61
80. L.P. Spear Heightened stress responsivity and emotional reactivity during pubertal maturation: implications for psychopathology Dev. Psychopathol. 21 2009 87 97
81. R.J. Valentino, S.L. Foote, and G. Aston-Jones Corticotropin-releasing factor activates noradrenergic neurons of the locus coeruleus Brain Res. 270 1983 363 367
82. V. Vengeliene, S. Siegmund, M.V. Singer, J.D. Sinclair, T.K. Li, and R. Spanagel A comparative study on alcohol-preferring rat lines: effects of deprivation and stress phases on voluntary alcohol intake Alcohol. Clin. Exp. Res. 27 2003 1048 1054
83. T.L. Verplaetse, D.D. Rasmussen, J.C. Froehlich, and C.L. Czachowski Effects of prazosin, an alpha1-adrenergic receptor antagonist, on the seeking and intake of alcohol and sucrose in alcohol-preferring (P) rats Alcohol. Clin. Exp. Res. 36 2012 881 886
84. B.M. Walker, D.D. Rasmussen, M.A. Raskind, and G.F. Koob alpha1-noradrenergic receptor antagonism blocks dependence-induced increases in responding for ethanol Alcohol 42 2008 91 97
85. K. Yamamoto, T. Shinba, and M. Yoshii Psychiatric symptoms of noradrenergic dysfunction: a pathophysiological view Psychiatry Clin. Neurosci. 68 2014 1 20
86. J.T. Yorgason, R.A. Espana, J.K. Konstantopoulos, J.L. Weiner, and S.R. Jones Enduring increases in anxiety-like behavior and rapid nucleus accumbens dopamine signaling in socially isolated rats Eur. J. Neurosci. 37 2013 1022 1031