Escalated or suppressed cocaine reward, tegmental BDNF, and accumbal dopamine caused by episodic versus continuous social stress in rats

Journal of Neuroscience

Volumn 31, Issue 27, 2011, Pages 9848-9857

  Miczek, Klaus A ^a,b   Nikulina, Ella M ^a,c   Shimamoto, Akiko ^a   Covington, Herbert E ^a,d  

^a TUFTS UNIVERSITY   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^d DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; COCAINE; DOPAMINE;

ADAPTATION; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; HABITUATION; IMMUNOHISTOCHEMISTRY; MALE; MOTOR ACTIVITY; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; RAT; REINFORCEMENT; REWARD; SENSITIZATION; SIGNAL TRANSDUCTION; SOCIAL INTERACTION; SOCIAL STRESS; TEGMENTUM;

ANALYSIS OF VARIANCE; ANIMALS; BODY WEIGHT; BRAIN-DERIVED NEUROTROPHIC FACTOR; COCAINE; CONDITIONING, OPERANT; DOPAMINE; DOPAMINE UPTAKE INHIBITORS; ELECTROCHEMISTRY; FOOD HANDLING; GENE EXPRESSION REGULATION; MALE; MICRODIALYSIS; MOTOR ACTIVITY; NUCLEUS ACCUMBENS; ONCOGENE PROTEINS V-FOS; RATS; RATS, LONG-EVANS; REINFORCEMENT SCHEDULE; REWARD; SELF ADMINISTRATION; STRESS, PSYCHOLOGICAL; SUCROSE; TIME FACTORS; VENTRAL TEGMENTAL AREA;

EID: 79960043825     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0637-11.2011     Document Type: Article

References (79)

1. Abumaria N, Rygula R, Havemann-Reinecke U, Ruther E, Bodemer W, Roos C, Flügge G (2006) Identification of genes regulated by chronic social stress in the rat dorsal raphe nucleus. Cell Mol Neurobiol 26:145-162.
2. Aguilar-Valles A, Sánchez E, de Gortari P, Balderas I, Ramrez-Amaya V, Bermúdez-Rattoni F, Joseph-Bravo P (2005) Analysis of the stress response in rats trained in the water-maze: differential expression of corticotropin-releasing hormone, CRH-R1, glucocorticoid receptors and brain-derived neurotrophic factor in limbic regions. Neuroendocrinology 82:306-319.
3. Ahmed SH, Cador M (2006) Dissociation of psychomotor sensitization from compulsive cocaine consumption. Neuropsychopharmacology 31: 563-571.
4. Altar CA, Boylan CB, Jackson C, Hershenson S, Miller J, Wiegand SJ, Lindsay RM, Hyman C (1992) Brain-derived neurotrophic factor augments rotational behavior and nigrostriatal dopamine turnover in vivo. Proc Natl Acad Sci U S A 89:11347-11351.
5. Amat J, Baratta MV, Paul E, Bland ST, Watkins LR, Maier SF (2005) Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nat Neurosci 8:365-371.
6. Amat J, Paul E, Zarza C, Watkins LR, Maier SF (2006) Previous experience with behavioral control over stress blocks the behavioral and dorsal raphe nucleus activating effects of later uncontrollable stress: role of the ventral medial prefrontal cortex. J Neurosci 26:13264-13272.
7. Anstrom KK, Miczek KA, Budygin EA (2009) Increased phasic dopamine signaling in the mesolimbic pathway during social defeat in rats. Neuroscience 161:3-12.
8. Antelman SM, Eichler AJ, Black CA, Kocan D (1980) Interchangeability of stress and amphetamine in sensitization. Science 207:329-331.
9. Arborelius L, Owens MJ, Plotsky PM, Nemeroff CB (1999) The role of corticotropin-releasing factor in depression and anxiety disorders. J Endocrinol 160:1-12.
10. Barnett SA (1975) The rat. A study in behavior. Chicago: University of Chicago. Berdoy M, Drickamer LC (2007) Comparative social organization and life history of Rattus and Mus. In: Rodent societies: an ecological and evolutionary perspective (Wolff JO, Sherman PW, eds), pp 380-392.Chicago: University of Chicago.
11. Berton O, McClung CA, Dileone RJ, Krishnan V, Renthal W, Russo SJ, Graham D, Tsankova NM, Bolanos CA, Rios M, Monteggia LM, Self DW, Nestler EJ (2006) Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311:864-868.
12. Blanchard DC, Sakai RR, McEwen B, Weiss SM, Blanchard RJ (1993) Subordination stress- behavioral, brain, and neuroendocrine correlates. Behav Brain Res 58:113-121.
13. Blanchard RJ, Blanchard DC, Flannelly KJ (1985) Social stress, mortality and aggression in colonies and burrowing habitats. Behav Processes 11:209-213.
14. Brady KT, Sinha R (2005) Co-occurring mental and substance use disorders: the neurobiological effects of chronic stress. Am J Psychiatry 162:1483-1493.
15. Cao JL, Covington HE III, Friedman AK, Wilkinson MB, Walsh JJ, Cooper DC, Nestler EJ, Han MH (2010) Mesolimbic dopamine neurons in the brain reward circuit mediate susceptibility to social defeat and antidepressant action. J Neurosci 30:16453-16458.
16. Carlezon WA, Thome J, Olson VG, Lane-Ladd SB, Brodkin ES, Hiroi N, Duman RS, Neve RL, Nestler EJ (1998) Regulation of cocaine reward by CREB. Science 282:2272-2275.
17. Cordeira JW, Frank L, Sena-Esteves M, Pothos EN, Rios M (2010) Brainderived neurotrophic factor regulates hedonic feeding by acting on the mesolimbic dopamine system. J Neurosci 30:2533-2541.
18. Covington HE, Miczek KA (2001) Repeated social-defeat stress, cocaine or morphine. Effects on behavioral sensitization and intravenous cocaine self-administration "binges." Psychopharmacology 158:388-398.
19. Covington HE, Miczek KA (2005) Intense cocaine self-administration after episodic social defeat stress, but not after aggressive behavior: dissociation from corticosterone activation. Psychopharmacology 183:331-340.
20. Covington HE, Kikusui T, Goodhue J, Nikulina EM, Hammer RP Jr, Miczek KA (2005) Brief social defeat stress: long lasting effects on cocaine taking during a binge and zif268mRNAexpression in the amygdala and prefrontal cortex. Neuropsychopharmacology 30:310-321.
21. Covington HE, Tropea TF, Rajadhyaksha AM, Kosofsky BE, Miczek KA(2008) NMDA receptors in the rat VTA: a critical site for social stress to intensify cocaine taking. Psychopharmacology 197:203-216.
22. De Kloet ER, Joels M, Holsboer F (2005) Stress and the brain: from adaptation to disease. Nat Rev Neurosci 6:463-475.
23. Duman RS, Monteggia LM (2006) A neurotrophic model for stress-related mood disorders. Biol Psychiatry 59:1116-1127.
24. Fanous S, Hammer RP Jr, Nikulina EM (2010) Short- and long-term effects of intermittent social defeat stress on BDNF expression in mesocorticolimbic brain regions. Neuroscience 167:598-607.
25. Ferrari PF, Van Erp AMM, Tornatzky W, Miczek KA (2003) Accumbal dopamine and serotonin in anticipation of the next aggressive episode in rats. Eur J Neurosci 17:371-378.
26. Fish EW, Shahrokh D, Bagot R, Caldji C, Bredy T, Szyf M, Meaney MJ (2004) Epigenetic programming of stress responses through variations in maternal care. Ann N Y Acad Sci 1036:167-180.
27. Fuchs E, Czeh B, Flugge G (2004) Examining novel concepts of the pathophysiology of depression in the chronic psychosocial stress paradigm in tree shrews. Behav Pharmacol 15:315-325.
28. Grace AA (1991) Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: a hypothesis for the etiology of schizophrenia. Neuroscience 41:1-24.
29. GraceAA (1995) The tonic/phasic model of dopamine system regulation: its relevance for understanding how stimulant abuse can alter basal ganglia function. Drug Alcohol Depend 37:111-129.
30. Grace AA, Floresco SB, Goto Y, Lodge DJ (2007) Regulation of firing of dopaminergic neurons and control of goal-directed behaviors. Trends Neurosci 30:220-227.
31. Graham DL, Edwards S, Bachtell RK, DiLeone RJ, Rios M, Self DW (2007) Dynamic BDNF activity in nucleus accumbens with cocaine use increases self-administration and relapse. Nat Neurosci 10:1029-1037.
32. Grimm JW, Lu L, Hayashi T, Hope BT, Su TP, Shaham Y (2003) Timedependent increases in brain-derived neurotrophic factor protein levels within the mesolimbic dopamine system after withdrawal from cocaine: implications for incubation of cocaine craving. J Neurosci 23:742-747.
33. HodosW (1961) Progressive ratio as a measure of reward strength. Science 134:943-944.
34. Katz RJ (1981) Possible muscarinic-cholinergic mediation of patterned aggressive reflexes in the cat. Prog Neuropsychopharmacol 5:49-56.
35. Koob G, Kreek MJ (2007) Stress, dysregulation of drug reward pathways, and the transition to drug dependence. Am J Psychiatry 164:1149-1159.
36. Koolhaas JM, Korte SM, de Boer SF, Van Der Vegt BJ, Van Reenen CG, Hopster H, De Jong IC, Ruis MAW,Blokhuis HJ (1999) Coping styles in animals: current status in behavior and stress-physiology. Neurosci Biobehav Rev 23:925-935.
37. Koolhaas JM, Bartolomucci A, Buwalda B, de Boer SF, Flügge G, Korte SM, Meerlo P, Murison R, Olivier B, Palanza P, Richter-Levin G, Sgoifo A, Steimer T, Stiedl O, van Dijk G, Wöhr M, Fuchs E (2011) Stress revisited: a critical evaluation of the stress concept. Neurosci Biobehav Rev 35:1291-1301.
38. Kozorovitskiy Y, Gould E (2004) Dominance hierarchy influences adult neurogenesis in the dentate gyrus. J Neurosci 24:6755-6759.
39. Krishnan V, Han MH, Graham DL, Berton O, Renthal W, Russo SJ, Laplant Q, Graham A, Lutter M, Lagace DC, Ghose S, Reister R, Tannous P, Green TA, Neve RL, Chakravarty S, Kumar A, Eisch AJ, Self DW, Lee FS, et al. (2007) Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 131:391-404.
40. Miczek KA (1974) Intraspecies aggression in rats: effects of d-amphetamine and chlordiazepoxide. Psychopharmacologia 39:275-301.
41. Miczek KA (1979) A new test for aggression in rats without aversive stimulation: differential effects of d-amphetamine and cocaine. Psychopharmacology 60:253-259.
42. Miczek KA, de Almeida RMM (2001) Oral drug self-administration in the home cage of mice: alcohol-heightened aggression and inhibition by the 5-HT1B agonist anpirtoline. Psychopharmacology 157:421-429.
43. Miczek KA, de Boer SF (2005) Aggressive, defensive, and submissive behavior. In: The behavior of the laboratory rat: a handbook with tests (Whishaw IQ, Kolb B, eds), pp 344-352.New York: Oxford UP.
44. Miczek KA, Nikulina E, Kream RM, Carter G, Espejo EF (1999a) Behavioral sensitization to cocaine after a brief social defeat stress: c-fos expression in the PAG. Psychopharmacology 141:225-234.
45. Miczek KA, Mutschler NH, Van Erp AMM, Blank AD, McInerney SC (1999b) d-Amphetamine "cue" generalizes to social defeat stress: sensi-tization and role of accumbens dopamine. Psychopharmacology 147:190-199.
46. Nair A, Vaidya VA (2006) Cyclic AMP response element binding protein and brain-derived neurotrophic factor: molecules that modulate our mood? J Biosci 31:423-434.
47. Narita M, Aoki K, Takagi M, Yajima Y, Suzuki T (2003) Implication of brain-derived neurotrophic factor in the release of dopamine and dopamine-related behaviors induced by methamphetamine. Neuroscience 119:767-775.
48. National Research Council (1996) Guide for the care and use of laboratory animals. Washington DC: National Academy.
49. Nikulina EM, Covington HE III, Ganschow L, Hammer RP Jr, Miczek KA (2004) 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 123:857-865.
50. Numakawa T, Kumamaru E, Adachi N, Yagasaki Y, Izumi A, Kunugi H (2009) Glucocorticoid receptor interaction with TrkB promotes BDNFtriggered PLC-γ signaling for glutamate release via a glutamate transporter. Proc Natl Acad Sci U S A 106:647-652
51. Pacchioni AM, Cador M, Bregonzio C, Cancela LM (2007) A glutamatedopamine interaction in the persistent enhanced response to amphetamine in nucleus accumbens core but not shell following a single restraint stress. Neuropsychopharmacology 32:682-692.
52. Paxinos G, Watson C (1997) The rat brain in stereotaxic coordinates, Ed 3. San Diego: Academic.
53. Pierce RC, Bell K, Duffy P, Kalivas PW (1996) Repeated cocaine augments excitatory amino acid transmission in the nucleus accumbens only in rats having developed behavioral sensitization. J Neurosci 16:1550-1560.
54. Pizarro JM, Lumley LA, Medina W, Robison CL, Chang WE, Alagappan A, Bah MJ, Dawood MY, Shah JD, Mark B, Kendall N, Smith MA, Saviolakis GA, Meyerhoff JL (2004) Acute social defeat reduces neurotrophin expression in brain cortical and subcortical areas in mice. Brain Res 1025:10-20.
55. Pu L, Liu QS, Poo MM (2006) BDNF-dependent synaptic sensitization in midbrain dopamine neurons after cocaine withdrawal. Nat Neurosci 9:605-607.
56. Quadros IM, Miczek KA (2009) Two modes of intense cocaine bingeing: increased persistence after social defeat stress and increased rate of intake due to extended access conditions in rats. Psychopharmacology 206: 109-121.
57. Razzoli M, Carboni L, Guidi A, Gerrard P, Arban R (2007) Social defeatinduced contextual conditioning differentially imprints behavioral and adrenal reactivity: a time-course study in the rat. Physiol Behav 92: 734-740.
58. Remie R, van Dongen JJ, Rensema JW (1990) Permanent cannulation of the jugular vein (acc. to Steffens). In: Manual of microsurgery on the laboratory rat (van Dongen JJ, ed), pp 159-169.Amsterdam: Elsevier.
59. Richardson NR, Roberts DCS (1996) Progressive ratio schedules in drug self-administration studies in rats: a method to evaluate reinforcing efficacy. J Neurosci Methods 66:1-11.
60. Robinson TE, Berridge KC (1993) The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Brain Res Rev 18:247-291.
61. Rygula R, Abumaria N, Flugge G, Fuchs E, Ruther E, Havemann-Reinecke U(2005) Anhedonia and motivational deficits in rats: Impact of chronic social stress. Behav Brain Res 162:127-134.
62. Seligman ME, Maier SF (1967) Failure to escape traumatic shock. J Exp Psychol 74:1-9.
63. Seroogy KB, Lundgren KH, Tran TM, Guthrie KM, Isackson PJ, Gall CM (1994) Dopaminergic neurons in rat ventral midbrain express brainderived neurotrophic factor and neurotrophin-3 mRNAs. J Comp Neurol 342:321-334.
64. Sgoifo A, Pozzato C, Costoli T, Manghi M, Stilli D, Ferrari PF, Ceresini G, Musso E (2001) Cardiac autonomic responses to intermittent social conflict in rats. Physiol Behav 73:343-349.
65. Shaham Y, Erb S, Stewart J (2000) Stress-induced relapse to heroin and cocaine seeking in rats: a review. Brain Res Rev 33:13-33.
66. Shaham Y, Shalev U, Lu L, de Wit H, Stewart J (2003) The reinstatement model of drug relapse: history, methodology and major findings. Psychopharmacology 168:3-20.
67. Smith MA, Makino S, Kvetnansky R, Post RM (1995) Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. J Neurosci 15:1768-1777.
68. Tidey JW, Miczek KA (1996) Social defeat stress selectively alters mesocorticolimbic dopamine release: an in vivo microdialysis study. Brain Res 721:140-149.
69. Tornatzky W, Miczek KA (1993) Long-term impairment of autonomic circadian rhythms after brief intermittent social stress. Physiol Behav 53:983-993.
70. Tornatzky W, Miczek KA (2000) Cocaine self-administration "binges": transition from behavioral and autonomic regulation toward homeostatic dysregulation in rats. Psychopharmacology 148:289-298.
71. Tsankova NM, Berton O, Renthal W, Kumar A, Neve RL, Nestler EJ (2006) Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat Neurosci 9:519-525.
72. Tsankova N, Renthal W, Kumar A, Nestler EJ (2007) Epigenetic regulation in psychiatric disorders. Nat Rev Neurosci 8:355-367.
73. van der Poel AM, Miczek KA (1991) Long ultrasonic calls in male rats following mating, defeat and aversive stimulation: frequency modulation and bout structure. Behaviour 119:127-142.
74. Van Erp AMM, Miczek KA (2000) Aggressive behavior, increased accumbal dopamine, and decreased cortical serotonin in rats. J Neurosci 20:9320-9325.
75. Vanderschuren LJMJ, Kalivas PW (2000) Alterations in dopaminergic and glutamatergic transmission in the induction and expression of behavioral sensitization: a critical review of preclinical studies. Psychopharmacology 151:99-120.
76. Von Holst D (1985) Coping behaviour and stress physiology in male tree shrews (Tupaia belangeri). In: Experimental behavioral ecology and sociobiology (Hölldobler B, Lindberg I, eds), pp 461-470.Sunderland, MA: Sinauer Associates.
77. Von Holst D (1998) The concept of stress and its relevance for animal behavior. In: Advances in the study of behavior, Vol 27, Stress and behavior (Møller AP, Milinski M, Slater PJB, eds), pp 1-131.New York: Academic.
78. Willner P, Muscat R, Papp M (1992) Chronic mild stress-induced anhedonia- a realistic animal-model of depression. Neurosci Biobehav Rev 16:525-534.
79. Yap JJ, Miczek KA (2007) Social defeat stress, sensitization, and intravenous cocaine self-administration in mice. Psychopharmacology 192:261-273.