Adolescent social defeat alters neural, endocrine and behavioral responses to amphetamine in adult male rats

Brain Research

Volumn 1352, Issue , 2010, Pages 147-156

  Burke, Andrew R ^a   Renner, Kenneth J ^a,b   Forster, Gina L ^a   Watt, Michael J ^a  

^a UNIVERSITY OF SOUTH DAKOTA   (United States)

^b W O Farber Center for Civic Leadership   (United States)

Author keywords

Adolescence; Corticosterone; Dopamine; Psychostimulant; Social stress

Indexed keywords

AMPHETAMINE; CORTICOSTERONE; DOPAMINE; MONOAMINE;

ADDICTION; ADOLESCENCE; ADOLESCENT DEVELOPMENT; ADULTHOOD; AGE; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR MODIFICATION; DOPAMINERGIC SYSTEM; ENDOCRINE FUNCTION; ENVIRONMENT; ENVIRONMENTAL FACTOR; HORMONE RELEASE; LIMBIC SYSTEM; LOCOMOTION; MALE; MATURATION; NONHUMAN; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; SOCIAL ASPECT; SOCIAL STRESS;

ADOLESCENT; AGING; AMPHETAMINE; ANIMALS; BEHAVIOR, ANIMAL; BIOGENIC MONOAMINES; CORTICOSTERONE; DOPAMINE; HUMANS; LIMBIC SYSTEM; LOCOMOTION; MALE; RATS; REWARD;

RATTUS;

EID: 77956180106     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2010.06.062     Document Type: Article

References (82)

1. S.L. Andersen Trajectories of brain development: point of vulnerability or window of opportunity? Neurosci. Biobehav. Rev. 27 2003 3 18
2. S.L. Andersen, and M.H. Teicher Desperately driven and no brakes: developmental stress exposure and subsequent risk for substance abuse Neurosci. Biobehav. Rev. 33 2009 516 524
3. C.E. Beyer, and J.D. Steketee Dopamine depletion in the medial prefrontal cortex induces sensitized-like behavioral and neurochemical responses to cocaine Brain Res. 833 1999 133 141
4. K. Björkqvist Social defeat as a stressor in humans Physiol. Behav. 73 2001 435 442
5. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254
6. B. Buwalda, M.H. Kole, A.H. Veenema, M. Huininga, S.F. de Boer, S.M. Korte, and J.M. Koolhaas Long-term effects of social stress on brain and behavior: a focus on hippocampal functioning Neurosci. Biobehav. Rev. 29 2005 83 97
7. S. Caccia, C. Fracasso, S. Garattini, G. Guiso, and S. Sarati Effects of short- and long-term administration of fluoxetine on the monoamine content of rat brain Neuropharmacology 31 1992 343 347
8. W.J. Chen, S.E. Maier, and J.R. West Prenatal alcohol treatment attenuated postnatal cocaine-induced elevation of dopamine concentration in nucleus accumbens: a preliminary study Neurotoxicol. Teratol. 19 1997 39 46
9. H.E. Covington III, and K.A. Miczek Repeated social-defeat stress, cocaine or morphine. Effects on behavioral sensitization and intravenous cocaine self-administration "binges" Psychopharmacology (Berl) 158 2001 388 398
10. H.E. Covington III, and K.A. Miczek Intense cocaine self-administration after episodic social defeat stress, but not after aggressive behavior: dissociation from corticosterone activation Psychopharmacology (Berl) 183 2005 331 340
11. B. Czeh, J.I. Muller-Keuker, R. Rygula, N. Abumaria, C. Hiemke, E. Domenici, and E. Fuchs Chronic social stress inhibits cell proliferation in the adult medial prefrontal cortex: hemispheric asymmetry and reversal by fluoxetine treatment Neuropsychopharmacology 32 2007 1490 1503
12. A. Del Arco, and F. Mora Prefrontal cortex-nucleus accumbens interaction: in vivo modulation by dopamine and glutamate in the prefrontal cortex Pharmacol. Biochem. Behav. 90 2008 226 235
13. V. Deroche, P.V. Piazza, P. Casolini, S. Maccari, M. Le Moal, and H. Simon Stress-induced sensitization to amphetamine and morphine psychomotor effects depend on stress-induced corticosterone secretion Brain Res. 598 1992 343 348
14. G. Di Chiara, and A. Imperato Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats Proc. Natl Acad. Sci. USA 85 1988 5274 5278
15. M.D. Doherty, and A. Gratton Medial prefrontal cortical D1 receptor modulation of the meso-accumbens dopamine response to stress: an electrochemical study in freely-behaving rats Brain Res. 715 1996 86 97
16. L.A. Douglas, E.I. Varlinskaya, and L.P. Spear Novel-object place conditioning in adolescent and adult male and female rats: effects of social isolation Physiol. Behav. 80 2003 317 325
17. C.J. Farmer, T.R. Isakson, D.J. Coy, and K.J. Renner In vivo evidence for progesterone dependent decreases in serotonin release in the hypothalamus and midbrain central grey: relation to the induction of lordosis Brain Res. 711 1996 84 92
18. G. Flores, G.K. Wood, J.J. Liang, R. Quirion, and L.K. Srivastava Enhanced amphetamine sensitivity and increased expression of dopamine D2 receptors in postpubertal rats after neonatal excitotoxic lesions of the medial prefrontal cortex J. Neurosci. 16 1996 7366 7375
19. G.L. Forster, A.J. Falcon, A.D. Miller, G.A. Heruc, and C.D. Blaha Effects of laterodorsal tegmentum excitotoxic lesions on behavioral and dopamine responses evoked by morphine and d-amphetamine Neuroscience 114 2002 817 823
20. G.L. Forster, R.B. Pringle, N.J. Mouw, S.M. Vuong, M.J. Watt, A.R. Burke, C.A. Lowry, C.H. Summers, and K.J. Renner Corticotropin-releasing factor in the dorsal raphe nucleus increases medial prefrontal cortical serotonin via type 2 receptors and median raphe nucleus activity Eur. J. Neurosci. 28 2008 299 310
21. G.L. Gladstone, G.B. Parker, and G.S. Malhi Do bullied children become anxious and depressed adults?: a cross-sectional investigation of the correlates of bullying and anxious depression J. Nerv. Ment. Dis. 194 2006 201 208
22. N.E. Goeders The HPA axis and cocaine reinforcement Psychoneuroendocrinology 27 2002 13 33
23. H.W. Gordon Early environmental stress and biological vulnerability to drug abuse Psychoneuroendocrinology 27 2002 115 126
24. A.W. Grossman, J.D. Churchill, B.C. McKinney, I.M. Kodish, S.L. Otte, and W.T. Greenough Experience effects on brain development: possible contributions to psychopathology J. Child Psychol. Psychiatry 44 2003 33 63
25. M. Haney, S. Maccari, M. Le Moal, H. Simon, and P.V. Piazza Social stress increases the acquisition of cocaine self-administration in male and female rats Brain Res. 698 1995 46 52
26. J.P. Hoffmann, F.G. Cerbone, and S.S. Su A growth curve analysis of stress and adolescent drug use Subst. Use Misuse 35 2000 687 716
27. M.S. Hooks, G.H. Jones, A.D. Smith, D.B. Neill, and J.B. Justice Jr. Response to novelty predicts the locomotor and nucleus accumbens dopamine response to cocaine Synapse 9 1991 121 128
28. M.S. Hooks, G.H. Jones, A.D. Smith, D.B. Neill, and J.B. Justice Jr. Individual differences in locomotor activity and sensitization Pharmacol. Biochem. Behav. 38 1991 467 470
29. M.S. Hooks, G.H. Jones, D.B. Neill, and J.B. Justice Jr. Individual differences in amphetamine sensitization: dose-dependent effects Pharmacol. Biochem. Behav. 41 1992 203 210
30. G.E. Jaskiw, F. Karoum, W.J. Freed, I. Phillips, J.E. Kleinman, and D.R. Weinberger Effect of ibotenic acid lesions of the medial prefrontal cortex on amphetamine-induced locomotion and regional brain catecholamine concentrations in the rat Brain Res. 534 1990 263 272
31. K. Johnson, L. Churchill, M.A. Klitenick, M.S. Hooks, and P.W. Kalivas Involvement of the ventral tegmental area in locomotion elicited from the nucleus accumbens or ventral pallidum J. Pharmacol. Exp. Ther. 277 1996 1122 1131
32. M. Kabbaj Individual differences in vulnerability to drug abuse: The high responders/low responders model CNS Neurol. Disord. Drug Targets 5 2006 513 520
33. M. Kabbaj, C. Isgor, S.J. Watson, and H. Akil Stress during adolescence alters behavioral sensitization to amphetamine Neuroscience 113 2002 395 400
34. P.W. Kalivas, and C. O'Brien Drug addiction as a pathology of staged neuroplasticity Neuropsychopharmacology 33 2008 166 180
35. R. Kaltiala-Heino, M. Rimpela, P. Rantanen, and A. Rimpela Bullying at school-an indicator of adolescents at risk for mental disorders J. Adolesc. 23 2000 661 674
36. R.C. Kessler, G.P. Amminger, S. Aguilar-Gaxiola, J. Alonso, S. Lee, and T.B. Ustun Age of onset of mental disorders: a review of recent literature Curr. Opin. Psychiatry 20 2007 359 364
37. D. King, M.J. Zigmond, and J.M. Finlay Effects of dopamine depletion in the medial prefrontal cortex on the stress-induced increase in extracellular dopamine in the nucleus accumbens core and shell Neuroscience 77 1997 141 153
38. J.E. Klebaur, and M.T. Bardo Individual differences in novelty seeking on the playground maze predict amphetamine conditioned place preference Pharmacol. Biochem. Behav. 63 1999 131 136
39. G.F. Koob, and M. Le Moal Addiction and the brain antireward system Annu. Rev. Psychol. 59 2008 29 53
40. J.M. Koolhaas, S.F. De Boer, A.J. De Rutter, P. Meerlo, and A. Sgoifo Social stress in rats and mice Acta Physiol. Scand. Suppl. 640 1997 69 72
41. M.J. Kreek, and G.F. Koob Drug dependence: stress and dysregulation of brain reward pathways Drug Alcohol Depend. 51 1998 23 47
42. L.R. Lucas, Z. Celen, K.L. Tamashiro, R.J. Blanchard, D.C. Blanchard, C. Markham, R.R. Sakai, and B.S. McEwen Repeated exposure to social stress has long-term effects on indirect markers of dopaminergic activity in brain regions associated with motivated behavior Neuroscience 124 2004 449 457
43. M. Marinelli, and P.V. Piazza Interaction between glucocorticoid hormones, stress and psychostimulant drugs Eur. J. Neurosci. 16 2002 387 394
44. M. Martinez, A. Calvo-Torrent, and J. Herbert Mapping brain response to social stress in rodents with c-fos expression: a review Stress 5 2002 3 13
45. I.Z. Mathews, R.G. Mills, and C.M. McCormick Chronic social stress in adolescence influenced both amphetamine conditioned place preference and locomotor sensitization Dev. Psychobiol. 50 2008 451 459
46. C.M. McCormick, D. Robarts, K. Kopeikina, and J.E. Kelsey Long-lasting, sex- and age-specific effects of social stressors on corticosterone responses to restraint and on locomotor responses to psychostimulants in rats Horm. Behav. 48 2005 64 74
47. K.A. Miczek A new test for aggression in rats without aversive stimulation: differential effects of d-amphetamine and cocaine Psychopharmacology (Berl) 60 1979 253 259
48. K.A. Miczek, H.E. Covington III, E.M. Nikulina Jr., and R.P. Hammer Aggression and defeat: persistent effects on cocaine self-administration and gene expression in peptidergic and aminergic mesocorticolimbic circuits Neurosci. Biobehav. Rev. 27 2004 787 802
49. J.B. Mitchell, and A. Gratton Partial dopamine depletion of the prefrontal cortex leads to enhanced mesolimbic dopamine release elicited by repeated exposure to naturally reinforcing stimuli J. Neurosci. 12 1992 3609 3618
50. T.R. Nansel, M. Overpeck, R.S. Pilla, W.J. Ruan, B. Simons-Morton, and P. Scheidt Bullying behaviors among US youth: prevalence and association with psychosocial adjustment Jama 285 2001 2094 2100
51. M.L. Newman, G.W. Holden, and Y. Delville Isolation and the stress of being bullied J. Adolesc. 28 2005 343 357
52. E.M. Nikulina, H.E. Covington III, L. Ganschow, R.P. Hammer Jr., and K.A. Miczek Long-term behavioral and neuronal cross-sensitization to amphetamine induced by repeated brief social defeat stress: Fos in the ventral tegmental area and amygdala Neuroscience 123 2004 857 865
53. M.J. Park, T. Paul Mulye, S.H. Adams, C.D. Brindis, and C.E. Irwin Jr. The health status of young adults in the United States J. Adolesc. Health 39 2006 305 317
54. T. Pascucci, R. Ventura, E.C. Latagliata, S. Cabib, and S. Puglisi-Allegra The medial prefrontal cortex determines the accumbens dopamine response to stress through the opposing influences of norepinephrine and dopamine Cereb. Cortex 17 2007 2796 2804
55. J.R. Pauly, S.F. Robinson, and A.C. Collins Chronic corticosterone administration enhances behavioral sensitization to amphetamine in mice Brain Res. 620 1993 195 202
56. G. Paxinos, and C. Watson The rat brain in stereotaxic coordinates. Vol 1998 Academic Press San Diego
57. P.V. Piazza, and M. Le Moal The role of stress in drug self-administration Trends Pharmacol. Sci. 19 1998 67 74
58. P.V. Piazza, J.M. Deminiere, M. Le Moal, and H. Simon Factors that predict individual vulnerability to amphetamine self-administration Science 245 1989 1511 1513
59. P.V. Piazza, S. Maccari, J.M. Deminiere, M. Le Moal, P. Mormede, and H. Simon Corticosterone levels determine individual vulnerability to amphetamine self-administration Proc. Natl Acad. Sci. USA 88 1991 2088 2092
60. P.V. Piazza, F. Rouge-Pont, J.M. Deminiere, M. Kharoubi, M. Le Moal, and H. Simon Dopaminergic activity is reduced in the prefrontal cortex and increased in the nucleus accumbens of rats predisposed to develop amphetamine self-administration Brain Res. 567 1991 169 174
61. A.J. Pijnenburg, and J.M. van Rossum Letter: Stimulation of locomotor activity following injection of dopamine into the nucleus accumbens J. Pharm. Pharmacol. 25 1973 1003 1005
62. R.J. Primus, and C.K. Kellogg Pubertal-related changes influence the development of environment-related social interaction in the male rat Dev. Psychobiol. 22 1989 633 643
63. K.J. Renner, and V.N. Luine Determination of monoamines in brain nuclei by high performance liquid chromatography with electrochemical detection: young vs. middle aged rats Life Sci. 34 1984 2193 2199
64. K. Rigby, and P.T. Slee Dimensions of interpersonal relation among Australian children and implications for psychological well-being J. Soc. Psychol. 133 1993 33 42
65. I. Rossow, and G. Lauritzen Shattered childhood: a key issue in suicidal behavior among drug addicts? Addiction 96 2001 227 240
66. R. Rygula, N. Abumaria, G. Flugge, E. Fuchs, E. Ruther, and U. Havemann-Reinecke Anhedonia and motivational deficits in rats: impact of chronic social stress Behav. Brain Res. 162 2005 127 134
67. S. Schenk, B.A. Horger, R. Peltier, and K. Shelton Supersensitivity to the reinforcing effects of cocaine following 6-hydroxydopamine lesions to the medial prefrontal cortex in rats Brain Res. 543 1991 227 235
68. J.L. Scholl, N. Feng, M.J. Watt, K.J. Renner, and G.L. Forster Individual differences in amphetamine sensitization, behavior and central monoamines Physiol. Behav. 96 2009 493 504
69. L.H. Sellings, and P.B. Clarke Segregation of amphetamine reward and locomotor stimulation between nucleus accumbens medial shell and core J. Neurosci. 23 2003 6295 6303
70. L.H. Sellings, and P.B. Clarke 6-Hydroxydopamine lesions of nucleus accumbens core abolish amphetamine-induced conditioned activity Synapse 59 2006 374 377
71. W. Slikker Jr., S.F. Ali, A.C. Scallet, C.H. Frith, G.D. Newport, and J.R. Bailey Neurochemical and neurohistological alterations in the rat and monkey produced by orally administered methylenedioxymethamphetamine (MDMA) Toxicol. Appl. Pharmacol. 94 1988 448 457
72. L.P. Spear The adolescent brain and age-related behavioral manifestations Neurosci. Biobehav. Rev. 24 2000 417 463
73. S. Tharp-Taylor, A. Haviland, and E.J. D'Amico Victimization from mental and physical bullying and substance use in early adolescence Addict. Behav. 34 2009 561 567
74. J.W. Tidey, and K.A. Miczek Acquisition of cocaine self-administration after social stress: role of accumbens dopamine Psychopharmacology (Berl) 130 1997 203 212
75. L.J. Vanderschuren, E.D. Schmidt, T.J. De Vries, C.A. Van Moorsel, F.J. Tilders, and A.N. Schoffelmeer A single exposure to amphetamine is sufficient to induce long-term behavioral, neuroendocrine, and neurochemical sensitization in rats J. Neurosci. 19 1999 9579 9586
76. E.I. Varlinskaya, and L.P. Spear Social interactions in adolescent and adult Sprague-Dawley rats: impact of social deprivation and test context familiarity Behav. Brain Res. 188 2008 398 405
77. R. Ventura, A. Alcaro, S. Cabib, D. Conversi, L. Mandolesi, and S. Puglisi-Allegra Dopamine in the medial prefrontal cortex controls genotype-dependent effects of amphetamine on mesoaccumbens dopamine release and locomotion Neuropsychopharmacology 29 2004 72 80
78. M. Wals, and F. Verhulst Child and adolescent antecedents of adult mood disorders Curr. Opin. Psychiatry 18 2005 15 19
79. M.J. Watt, G.L. Forster, W.J. Korzan, K.J. Renner, and C.H. Summers Rapid neuroendocrine responses evoked at the onset of social challenge Physiol. Behav. 90 2007 567 575
80. M.J. Watt, A.R. Burke, K.J. Renner, and G.L. Forster Adolescent male rats exposed to social defeat exhibit altered anxiety behavior and limbic monoamines as adults Behav. Neurosci. 123 2009 564 576
81. R.A. Wise Neurobiology of addiction Curr. Opin. Neurobiology 6 1996 243 251
82. J. Zhu, M.T. Bardo, R.C. Bruntz, D.J. Stairs, and L.P. Dwoskin Individual differences in response to novelty predict prefrontal cortex dopamine transporter function and cell surface expression Eur. J. Neurosci. 26 2007 717 728