Behavior Genetics

, 41:787 | Cite as

Gene Expression in Aminergic and Peptidergic Cells During Aggression and Defeat: Relevance to Violence, Depression and Drug Abuse

  • Klaus A. Miczek
  • Ella M. Nikulina
  • Aki Takahashi
  • Herbert E. CovingtonIII
  • Jasmine J. Yap
  • Christopher O. Boyson
  • Akiko Shimamoto
  • Rosa M. M. de Almeida
Original Research


In this review, we examine how experiences in social confrontations alter gene expression in mesocorticolimbic cells. The focus is on the target of attack and threat due to the prominent role of social defeat stress in the study of coping mechanisms and victimization. The initial operational definition of the socially defeated mouse by Ginsburg and Allee (1942) enabled the characterization of key endocrine, cardiovascular, and metabolic events during the initial response to an aggressive opponent and during the ensuing adaptations. Brief episodes of social defeat stress induce an augmented response to stimulant challenge as reflected by increased locomotion and increased extracellular dopamine (DA) in the nucleus accumbens (NAC). Cells in the ventral tegmental area (VTA) that project to the NAC were more active as indicated by increased expression of c-fos and Fos-immunoreactivity and BDNF. Intermittent episodes of social defeat stress result in increased mRNA for MOR in brainstem and limbic structures. These behavioral and neurobiological indices of sensitization persist for several months after the stress experience. The episodically defeated rats also self-administered intravenous cocaine during continuous access for 24 h (“binge”). By contrast, continuous social stress, particularly in the form of social subordination stress, leads to reduced appetite, compromised endocrine activities, and cardiovascular and metabolic abnormalities, and prefer sweets less as index of anhedonia. Cocaine challenges in subordinate rats result in a blunted psychomotor stimulant response and a reduced DA release in NAC. Subordinate rats self-administer cocaine less during continuous access conditions. These contrasting patterns of social stress result from continuous vs. intermittent exposure to social stress, suggesting divergent neuroadaptations for increased vulnerability to cocaine self-administration vs. deteriorated reward mechanisms characteristic of depressive-like profiles.


Social stress Defeat Ventral tegmental area Dorsal raphe Amphetamine Cocaine Sensitization Tolerance Anhedonia 



The authors would like to thank Mr. J. Thomas Sopko for his exceptional technical assistance. Preparation of this review and the original research from our own laboratory were supported by USPHS research grants AA05122, DA02632, DA026451 (EMN) and grants from the Alcoholic Beverage Medical Research Foundation (KAM, PI).


  1. Adams DB, Baccelli G, Mancia G, Zanchetti A (1969) Cardiovascular changes during naturally elicited fighting behavior in the cat. Am J Physiol 216:1226–1235PubMedGoogle Scholar
  2. Albeck DS, McKittrick CR, Blanchard DC, Blanchard RJ, Nikulina J, McEwen BS, Sakai RR (1997) Chronic Social Stress Alters Levels of Corticotropin-Releasing Factor and Arginine Vasopressin mRNA in Rat Brain. J Neurosci 17:4895–4903PubMedGoogle Scholar
  3. Amorim MC, Almada VC (2005) The outcome of male-male encounters affects subsequent sound production during courtship in the cichlid fish Oreochromis mossambicus. Anim Behav 69:595–601CrossRefGoogle Scholar
  4. Antelman SM, Eichler AJ, Black CA, Kocan D (1980) Interchangeability of stress and amphetamine in sensitization. Science 207:329–331PubMedCrossRefGoogle Scholar
  5. Barnett SA (1975) The Rat. A Study in Behavior. University of Chicago Press, ChicagoGoogle Scholar
  6. Barnett SA, Hocking WE, Munro KMH, Walker KZ (1975) Socially induced renal pathology of captive wild rats. Aggress Behav 1:123–133CrossRefGoogle Scholar
  7. Baum MJ, Everitt BJ (1992) Increased expression of C-Fos in the medial preoptic area after Mating in male-rats—role of afferent inputs from the Medial Amygdala and Midbrain Central Tegmental Field. Neuroscience 50:627–646PubMedCrossRefGoogle Scholar
  8. Berdoy M, Drickamer LC (2007) Comparative social organization and life history of Rattus and Mus. In: Wolff JO, Sherman PW (eds) Rodent societies: an ecological and evolutionary perspective. University of Chicago Press, Chciago, pp 380–392Google Scholar
  9. Björkqvist K (2001) Social defeat as a stressor in humans. Physiol Behav 73:435–442PubMedCrossRefGoogle Scholar
  10. Blanchard RJ, Blanchard CD (1977) Aggressive behavior in the rat. Behav Biol 21:197–224PubMedCrossRefGoogle Scholar
  11. Blanchard RJ, Blanchard DC, Flannelly KJ (1985) Social stress, mortality and aggression in colonies and burrowing habitats. Behav Process 11:209–213CrossRefGoogle Scholar
  12. Brain PF (1972) Endocrine and behavioral differences between dominant and subordinate male house mice housed in pairs. Psychonom Sci 28:260–262Google Scholar
  13. Brodkin ES, Goforth SA, Keene AH, Fossella JA, Silver LM (2002) Identification of quantitative trait Loci that affect aggressive behavior in mice. J Neurosci 22:1165–1170PubMedGoogle Scholar
  14. Bronson FH (1973) Establishment of social rank among grouped male mice: Relative effects on circulating FSH, LH, and corticosterone. Physiol Behav 10:947–951PubMedCrossRefGoogle Scholar
  15. Caspi A, McClay J, Moffitt TE, Mill J, Martin J, Craig IW, Taylor A, Poulton R (2002) Role of genotype in the cycle of violence in maltreated children. Science 297:851–854PubMedCrossRefGoogle Scholar
  16. Chen X, Herbert J (1995) Regional changes in c-fos expression in the basal forebrain and brainstem during adaptation to repeated stress: correlation with cardiovascular, hypothermic and endocrine responses. Neuroscience 64:675–685PubMedCrossRefGoogle Scholar
  17. Coates JM, Herbert J (2008) Endogenous steroids and financial risk taking on a London trading floor. Proc Natl Acad Sci USA 105:6167–6172PubMedCrossRefGoogle Scholar
  18. Cooper MA, Grober MS, Nicholas CR, Huhman KL (2009) Aggressive encounters alter the activation of serotonergic neurons and the expression of 5-HT1A mRNA in the hamster dorsal raphe nucleus. Neuroscience 161:680–690PubMedCrossRefGoogle Scholar
  19. Covington HE III, Miczek KA (2001) Repeated social-defeat stress, cocaine or morphine. Effects on behavioral sensitization and intravenous cocaine self-administration “binges”. Psychopharmacology 158:388–398PubMedCrossRefGoogle Scholar
  20. Covington HE III, Miczek KA (2005) Intense cocaine self-administration after episodic social defeat stress, but not after aggressive behavior: dissociation from corticosterone activation. Psychopharmacology 183:331–340PubMedCrossRefGoogle Scholar
  21. Covington HE III, 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 zif268 mRNA expression in the amygdala and prefrontal cortex. Neuropsychopharmacology 30:310–321PubMedCrossRefGoogle Scholar
  22. Craig IW, Halton KE (2009) Genetics of human aggressive behaviour. Hum Genet 126:101–113PubMedCrossRefGoogle Scholar
  23. Crowcroft P, Rowe FP (1963) Social organization and territorial behaviour in the wild house mouse. Proc Zool Soc London 140:517–531CrossRefGoogle Scholar
  24. Day DE, Cooper MA, Markham CM, Huhman KL (2011) NR2B subunit of the NMDA receptor in the basolateral amygdala is necessary for the acquisition of conditioned defeat in Syrian hamsters. Behav Brain Res 217:55–59PubMedCrossRefGoogle Scholar
  25. de Jong JG, Wasilewski M, Van Der Vegt BJ, Buwalda B, Koolhaas JM (2005) A single social defeat induces short-lasting behavioral sensitization to amphetamine. Physiol Behav 83:805–811PubMedCrossRefGoogle Scholar
  26. Delville Y, De Vries GJ, Ferris CF (2000) Neural connections of the anterior hypothalamus and agonistic behavior in golden hamsters. Brain Behav Evolution 55:53–76CrossRefGoogle Scholar
  27. Deroche V, Piazza PV, Casolini P, Maccari S, Le Moal M, Simon H (1992) Stress-induced sensitization to amphetamine and morphine psychomotor effects depend on stress-induced corticosterone secretion. Brain Res 598:343–348PubMedCrossRefGoogle Scholar
  28. Dhingra NK, Raju TR, Meti BL (1997) Selective reduction of monoamine oxidase A and B in the frontal cortex of subordinate rats. Brain Res 758:237–240PubMedCrossRefGoogle Scholar
  29. Dow HC, Kreibich AS, Kaercher KA, Sankoorikal GM, Pauley ED, Lohoff FW, Ferraro TN, Li H, Brodkin ES (2011) Genetic dissection of intermale aggressive behavior in BALB/cJ and A/J mice. Genes Brain Behav 10:57–68PubMedCrossRefGoogle Scholar
  30. Ely DL (1981) Hypertension, social rank, and aortic arteriosclerosis in CBA/J mice. Physiol Behav 26:655–661PubMedCrossRefGoogle Scholar
  31. Fekete EM, Zhao Y, Li C, Sabino V, Vale WW, Zorrilla EP (2009) Social defeat stress activates medial amygdala cells that express type 2 corticotropin-releasing factor receptor mRNA. Neuroscience 162:5–13PubMedCrossRefGoogle Scholar
  32. 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 17:371–378PubMedCrossRefGoogle Scholar
  33. Fleshner M, Laudenslager ML, Simons L, Maier SF (1989) Reduced serum antibodies associated with social defeat in rats. Physiol Behav 45:1183–1187PubMedCrossRefGoogle Scholar
  34. Frischknecht HR, Siegfried B (1989) Relationship between behavioral and nociceptive changes in attacked mice: effects of opiate antagonists. Psychopharmacology 97:160–162PubMedCrossRefGoogle Scholar
  35. Fuxjager MJ, Forbes-Lorman RM, Coss DJ, Auger CJ, Auger AP, Marler CA (2010) Winning territorial disputes selectively enhances androgen sensitivity in neural pathways related to motivation and social aggression. Proc Natl Acad Sci USA 107:12393–12398PubMedCrossRefGoogle Scholar
  36. Garzon M, Pickel VM (2001) Plasmalemmal μ-opioid receptor distribution mainly in nondopaminergic neurons in the rat ventral tegmental area. Synapse 41:311–328PubMedCrossRefGoogle Scholar
  37. Ginsburg BE (1967) Genetic parameters in behavioral research. In: Hirsch J (ed) Behavior-genetic analysis. McGraw-Hill, New York, pp 135–153Google Scholar
  38. Ginsburg B, Allee WC (1942) Some effects of conditioning on social dominance and subordination in inbred strains of mice. Physiol Zool 15:485–506Google Scholar
  39. Grant KA, Shively CA, Nader MA, Ehrenkaufer RL, Line SW, Morton TE, Gage HD, Mach RH (1998) Effect of social status on striatal dopamine D2 receptor binding characteristics in cynomolgus monkeys assessed with positron emission tomography. Synapse 29:80–83PubMedCrossRefGoogle Scholar
  40. Halasz J, Liposits Z, Kruk MR, Haller J (2002) Neural background of glucocorticoid dysfunction-induced abnormal aggression in rats: involvement of fear- and stress- related structures. Eur J Neurosci 15:561–569PubMedCrossRefGoogle Scholar
  41. Haney M, Miczek KA (1995) Delta opioid receptors: reflexive, defensive and vocal affective responses in female rats. Psychopharmacology 121:204–212PubMedCrossRefGoogle Scholar
  42. Hen R (1996) Mean genes. Neuron 16:17–21PubMedCrossRefGoogle Scholar
  43. Henry JP, Stephens PM (1977) The social environment and essential hypertension in mice: possible role of inervation of the adrenal cortex. In: de Jong W, Provoost AP, Shapiro AP (eds) Progress in brain research, vol. 47: hypertension and brain mechanisms. Elsevier, New York, pp 263–273CrossRefGoogle Scholar
  44. Herman JP, Stinus L, Le Moal M (1984) Repeated stress increases locomotor response to amphetamine. Psychopharmacology 84:431–435PubMedCrossRefGoogle Scholar
  45. Hsu Y, Earley RL, Wolf LL (2006) Modulation of aggressive behaviour by fighting experience: mechanisms and contest outcomes. Biol Rev Camb Philos Soc 81:33–74PubMedGoogle Scholar
  46. Hucklebridge FH, Gamal-El-Din L, Brain PF (1981) Social status and the adrenal medulla in the house mouse (Mus musculus, L.). Behav Neural Biol 33:345–363CrossRefGoogle Scholar
  47. Johnson SW, North RA (1992) Opioids excite dopamine neurons by hyperpolarization of local interneurons. J Neurosci 12:483–488PubMedGoogle Scholar
  48. Joppa MA, Meisel RL, Garber MA (1995) c-Fos expression in female hamster brain following sexual and aggressive behaviors. Neuroscience 68:783–792PubMedCrossRefGoogle Scholar
  49. Kalivas PW, Stewart J (1991) Dopamine transmission in the initiation and expression of drug- and stress-induced sensitization of motor activity. Brain Res Rev 16:223–244PubMedCrossRefGoogle Scholar
  50. Kirkpatrick B, Kim JW, Insel TR (1994) Limbic system fos expression associated with paternal behavior. Brain Res 658:112–118PubMedCrossRefGoogle Scholar
  51. Kollack-Walker S, Newman SW (1995) Mating and agonistic behavior produce different patterns of Fos immunolabeling in the male Syrian hamster brain. Neuroscience 66:721–736PubMedCrossRefGoogle Scholar
  52. Kollack-Walker S, Watson SJ, Akil H (1997) Social stress in hamsters: Defeat activates specific neurocircuits within the brain. J Neurosci 17:8842–8855PubMedGoogle Scholar
  53. Kollack-Walker S, Don C, Watson SJ, Akil H (1999) Differential expression of c-fos mRNA within neurocircuits of male hamsters exposed to acute or chronic defeat. J Neuroendocrinol 11:547–559PubMedCrossRefGoogle Scholar
  54. Koolhaas JM, Everts H, de Ruiter AJH, de Boer SF, Bohus B (1998) Coping with stress in rats and mice: Differential peptidergic modulation of the amygdala-lateral septum complex. Prog Brain Res 119:437–448PubMedCrossRefGoogle Scholar
  55. 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 23:925–935PubMedCrossRefGoogle Scholar
  56. Kreek MJ, Koob GF (1998) Drug dependence: Stress and dysregulation of brain reward pathways. Drug Alcohol Depend 51:23–47PubMedCrossRefGoogle Scholar
  57. Külling P, Frischknecht HR, Pasi A, Waser PG, Siegfried B (1988) Social conflict-induced changes in nociception and beta-endorphin-like immunoreactivity in pituitary and discrete brain areas of C57BL/6 and DBA/2 mice. Brain Res 450:237–246PubMedCrossRefGoogle Scholar
  58. Lesch KP, Merschdorf U (2000) Impulsivity, aggression, and serotonin: a molecular psychobiological perspective. Behav Sci Law 18:581–604PubMedCrossRefGoogle Scholar
  59. Liu D, Diorio J, Tannenbaum B, Caldji C, Francis D, Freedman A, Sharma S, Pearson D, Plotsky PM, Meaney MJ (1997) Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277:1659–1662PubMedCrossRefGoogle Scholar
  60. Lore R, Nikoletseas M, Takahashi L (1984) Colony aggression in laboratory rats: a review and some recommendations. Aggress Behav 10:59–71CrossRefGoogle Scholar
  61. Lucion AB, de Almeida RMM, DaSilva RSM (1996) Territorial aggression, body weight, carbohydrate metabolism and testosterone levels of wild rats maintained in laboratory colonies. Braz J Med Biol Res 29:1657–1662PubMedGoogle Scholar
  62. Magendzo K, Bustos G (2003) Expression of amphetamine-induced behavioral sensitization after short- and long-term withdrawal periods: participation of mu- and delta-opioid receptors. Neuropsychopharmacology 28:468–477PubMedCrossRefGoogle Scholar
  63. Maier SF, Seligman MEP (1976) Learned helplessness—theory and evidence. J Exp Psychol Gen 105:3–46CrossRefGoogle Scholar
  64. Martinez M, Calvo-Torrent A, Pico-Alfonso MA (1998a) Social defeat and subordination as models of social stress in laboratory rodents: A review. Aggress Behav 24:241–256CrossRefGoogle Scholar
  65. Martinez M, Phillips PJ, Herbert J (1998b) Adaptation in patterns of c-fos expression in the brain associated with exposure to either single or repeated social stress in male rats. Eur J Neurosci 10:20–33PubMedCrossRefGoogle Scholar
  66. Martinez M, Calvo-Torrent A, Herbert J (2002) Mapping brain response to social stress in rodents with c-fos expression: a review. Stress 5:3–13PubMedCrossRefGoogle Scholar
  67. Matsuda S, Peng H, Yoshimura H, Wen TC, Fukuda T, Sakanaka M (1996) Persistent c-fos expression in the brains of mice with chronic social stress. Neurosci Res 26:157–170PubMedCrossRefGoogle Scholar
  68. Maxson SC (1996) Searching for candidate genes with effects on an agonistic behavior, offense, in mice. Behav Genet 26:471–475PubMedCrossRefGoogle Scholar
  69. McKittrick CR, Blanchard DC, Blanchard RJ, McEwen BS, Sakai RR (1995) Serotonin receptor binding in a colony model of chronic social stress. Biol Psychiatry 37:383–393PubMedCrossRefGoogle Scholar
  70. Meehan WP, Tornatzky W, Miczek KA (1995) Blood pressure via telemetry during social confrontations in rats: Effects of clonidine. Physiol Behav 58:81–88PubMedCrossRefGoogle Scholar
  71. Meerlo P, de Boer SF, Koolhaas JM, Daan S, van den Hoofdakker RH (1996) Changes in daily rhythms of body temperature and activity after a single social defeat in rats. Physiol Behav 59:735–739PubMedCrossRefGoogle Scholar
  72. Melia KR, Ryabinin AE, Schroeder R, Bloom FE, Wilson MC (1994) Induction and habituation of immediate early gene expression in rat brain by acute and repeated restraint stress. J Neurosci 14:5929–5938PubMedGoogle Scholar
  73. Meyer-Lindenberg A, Buckholtz JW, Kolachana B, Hariri AR, Pezawas L, Blasi G, Wabnitz A, Honea R, Verchinski B, Callicott JH, Egan M, Mattay V, Weinberger DR (2006) Neural mechanisms of genetic risk for impulsivity and violence in humans. Proc Nat Acad Sci U S A 103:6269–6274CrossRefGoogle Scholar
  74. Miczek KA (1991) Tolerance to the analgesic, but not discriminative stimulus effects of morphine after brief social defeat in rats. Psychopharmacology 104:181–186PubMedCrossRefGoogle Scholar
  75. Miczek KA, de Boer SF (2005) Aggressive, defensive, and submissive behavior. In: Whishaw IQ, Kolb B (eds) The Behavior of the Laboratory Rat: A Handbook with Tests. Oxford University Press, New York, pp 344–352Google Scholar
  76. Miczek KA, Winslow JT (1987) Psychopharmacological research on aggressive behavior. In: Greenshaw AJ, Dourish CT (eds) Experimental psychopharmacology: concepts and methods. Humana Press, Clifton, pp 27–113CrossRefGoogle Scholar
  77. Miczek KA, Thompson ML, Shuster L (1982) Opioid-like analgesia in defeated mice. Science 215:1520–1522PubMedCrossRefGoogle Scholar
  78. Miczek KA, Thompson ML, Shuster L (1985) Naloxone injections into periaqueductal grey area and arcuate nucleus block analgesia in defeated mice. Psychopharmacology 87:39–42PubMedCrossRefGoogle Scholar
  79. Miczek KA, Thompson ML, Shuster L (1986) Analgesia following defeat in an aggressive encounter: development of tolerance and changes in opioid receptors. In: Kelly DD (ed) Stress-induced Analgesia. Ann N Y Acad Sci, New York, pp 14–29Google Scholar
  80. Miczek KA, Thompson ML, Tornatzky W (1991) Subordinate animals: behavioral and physiological adaptations and opioid tolerance. In: Brown MR (ed) Stress: neurobiology and neuroendocrinology. Marcel Dekker, New York, pp 323–357Google Scholar
  81. Miczek KA, Mutschler NH, Van Erp AMM, Blank AD, McInerney SC (1999a) d-Amphetamine “cue” generalizes to social defeat stress: sensitization and role of accumbens dopamine. Psychopharmacology 147:190–199PubMedCrossRefGoogle Scholar
  82. Miczek KA, Nikulina E, Kream RM, Carter G, Espejo EF (1999b) Behavioral sensitization to cocaine after a brief social defeat stress: c-fos expression in the PAG. Psychopharmacology 141:225–234PubMedCrossRefGoogle Scholar
  83. Miczek KA, Maxson SC, Fish EW, Faccidomo S (2001) Aggressive behavioral phenotypes in mice. Behav Brain Res 125:167–181PubMedCrossRefGoogle Scholar
  84. Miczek KA, Covington HE, Nikulina EM, Hammer RP (2004) Aggression and defeat: persistent effects on cocaine self-administration and gene expression in peptidergic and aminergic mesocorticolimbic circuits. Neurosci Biobehav Rev 27:787–802PubMedCrossRefGoogle Scholar
  85. Miczek KA, Yap JJ, Covington HE III (2008) Social stress, therapeutics and drug abuse: preclinical models of escalated and depressed intake. Pharmacol Ther 120:102–128PubMedCrossRefGoogle Scholar
  86. Miczek KA, Nikulina EM, Shimamoto A, Covington HE III (2011) Escalated or suppressed cocaine reward, tegmental BDNF and accumbal dopamine due to episodic vs. continuous social stress in rats. J Neurosci (in press)Google Scholar
  87. Nehrenberg DL, Wang S, Buus RJ, Perkins J, de Villena FP, Pomp D (2010) Genomic mapping of social behavior traits in a F2 cross derived from mice selectively bred for high aggression. BMC Genet 11:113PubMedCrossRefGoogle Scholar
  88. Nikulina EM, Marchand JE, Kream RM, Miczek KA (1998) Behavioral sensitization to cocaine after a brief social stress is accompanied by changes in fos expression in the murine brainstem. Brain Res 810:200–210PubMedCrossRefGoogle Scholar
  89. Nikulina EM, Hammer RP Jr, Miczek KA, Kream RM (1999) Social defeat stress increases expression of mu-opioid receptor mRNA in rat ventral tegmental area. NeuroReport 10:3015–3019PubMedCrossRefGoogle Scholar
  90. 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 123:857–865PubMedCrossRefGoogle Scholar
  91. Nikulina EM, Miczek KA, Hammer RP Jr (2005) Prolonged effects of repeated social defeat stress on mRNA expression and function of mu-opioid receptors in the ventral tegmental area of rats. Neuropsychopharmacology 30:1096–1103PubMedCrossRefGoogle Scholar
  92. Nikulina EM, Arrillaga-Romany I, Miczek KA, Hammer RP Jr (2008) Long-lasting alteration in mesocorticolimbic structures after repeated social defeat stress in rats: time course of Δ-opioid receptor mRNA and FosB/ΔFosB immunoreactivity. Eur J Neurosci 27:2272–2284PubMedCrossRefGoogle Scholar
  93. Ogawa S, Lubahn DB, Korach KS, Pfaff EW (1997) Behavioral effects of estrogen receptor gene disruption in male mice. Proc Natl Acad Sci USA 94:1476–1481PubMedCrossRefGoogle Scholar
  94. Oliveira RF, Silva A, Canario AV (2009) Why do winners keep winning? Androgen mediation of winner but not loser effects in cichlid fish. Proc Biol Sci 276:2249–2256PubMedCrossRefGoogle Scholar
  95. Oyegbile TO, Marler CA (2005) Winning fights elevates testosterone levels in California mice and enhances future ability to win fights. Horm Behav 48:259–267PubMedCrossRefGoogle Scholar
  96. Panksepp J, Herman B, Conner R, Bishop P, Scott JP (1978) The biology of social attachments: opiates alleviate separation distress. Biol Psychiatry 13:607–618PubMedGoogle Scholar
  97. Parfitt DB, Newman SW (1998) Fos-immunoreactivity within the extended amygdala is correlated with the onset of sexual satiety. Horm Behav 34:17–29PubMedCrossRefGoogle Scholar
  98. Pitkow LJ, Sharer CA, Ren X, Insel TR, Terwilliger EF, Young LJ (2001) Facilitation of affiliation and pair-bond formation by vasopressin receptor gene transfer into the ventral forebrain of a monogamous vole. J Neurosci 21:7392–7396PubMedGoogle Scholar
  99. Post RM, Weiss SR, Pert A, Uhde TW (1987) Chronic cocaine administration: sensitization and kindling effects. In: Fisher S, Raskin A, Uhlenhuth EH (eds) Cocaine: Clinical and Biobehavioral Aspects. Oxford University Press, New York, pp 109–173Google Scholar
  100. Potegal M, Ferris CF, Hebert M, Meyerhoff J, Skaredoff L (1996) Attack priming in female Syrian golden hamsters is associated with a c-fos-coupled process within the corticomedial amygdala. Neuroscience 75:869–880PubMedCrossRefGoogle Scholar
  101. Raab A, Dantzer R, MIchaud B, Mormede P, Taghzouti K, Simon H, Lemoal M (1986) Behavioural, physiological and immunological consequences of social status and aggression in chronically coexisting resident-intruder dyads of male rats. Physiol Behav 36:223–228PubMedCrossRefGoogle Scholar
  102. Ribeiro Do Couto B, Aguilar MA, Manzanedo C, Rodríguez-Arias M, Armario A, Miñarro J (2006) Social stress is as effective as physical stress in reinstating morphine-induced place preference in mice. Psychopharmacology 185:459–470PubMedCrossRefGoogle Scholar
  103. Robinson TE (2010) Sensitization to drugs. In: Stolerman IP (ed) Encyclopedia of psychopharmacology. Springer, HeidelbergGoogle Scholar
  104. Rodgers RJ, Hendrie CA (1983) Social conflict activates status-dependent endogenous analgesic or hyperalgesic mechanisms in male mice: effects of naloxone on nociception and behaviour. Physiol Behav 30:775–780PubMedCrossRefGoogle Scholar
  105. Rodgers RJ, Randall JI (1985) Social conflict analgesia: Studies on naloxone antagonism and morphine cross-tolerance in male DBA/2 mice. Pharmacol Biochem Behav 23:883–887PubMedCrossRefGoogle Scholar
  106. Rodgers RJ, Randall JI (1988) Blockade of non-opioid analgesia in intruder mice by selective neuronal and non-neuronal benzodiazepine recognition site ligands. Psychopharmacology 96:45–54PubMedCrossRefGoogle Scholar
  107. Roubertoux PL, Guillot PV, Mortaud S, Pratte M, Jamon M, Cohen-Salmon C, Tordjman S (2005) Attack behaviors in mice: from factorial structure to quantitative trait loci mapping. Eur J Pharmacol 526:172–185PubMedCrossRefGoogle Scholar
  108. Sapolsky RM (1996) Stress, glucorticoids, and damage to the nervous system: the current state of confusion. Stress 1:1–19PubMedCrossRefGoogle Scholar
  109. Schuurman T (1980) Hormonal correlates of agonistic behavior in adult male rats. In: McConnel PS, Boer GJ, Romijn HJ, Van de Poll NE, Corner MA (eds) Progress in brain research, vol. 53: adaptive capabilities of the nervous system. Elsevier Biomedical Press, Amsterdam, pp 415–420Google Scholar
  110. Scott JP (1958) Aggression. The University of Chicago Press, ChicagoGoogle Scholar
  111. Segal DS, Mandell AJ (1974) Long-term administration of d-amphetamine: progressive augmentation of motor activity and stereotypy. Pharmacol Biochem Behav 2:249–255PubMedCrossRefGoogle Scholar
  112. Sgoifo A, deBoer SF, Haller J, Koolhaas JM (1996) Individual differences in plasma catecholamine and corticosterone stress responses of wild-type rats: relationship with aggression. Physiol Behav 60(6):1403–1407PubMedCrossRefGoogle Scholar
  113. Siegfried B, Frischknecht HR (1989) Place avoidance learning and stress-induced analgesia in the attacked mouse: role of endogenous opioids. Behav Neural Biol 52:95–107PubMedCrossRefGoogle Scholar
  114. Siegfried B, Frischknecht HR, Waser PG (1984) Defeat, learned submissiveness, and analgesia in mice: effect of genotype. Behav Neural Biol 42:91–97PubMedCrossRefGoogle Scholar
  115. Sorg BA, Kalivas PW (1991) Effects of cocaine and footshock stress on extracellular dopamine levels in the ventral striatum. Brain Res 559:29–36PubMedCrossRefGoogle Scholar
  116. Stefanski V (2001) Social stress in laboratory rats. Behavior, immune function, and tumor metastasis. Physiol Behav 73:385–391PubMedCrossRefGoogle Scholar
  117. Takahashi A, Shimamoto A, Boyson CO, DeBold JF, Miczek KA (2010) GABA(B) receptor modulation of serotonin neurons in the dorsal raphe nucleus and escalation of aggression in mice. J Neurosci 30:11771–11780PubMedCrossRefGoogle Scholar
  118. Taylor A, Kim-Cohen J (2007) Meta-analysis of gene–environment interactions in developmental psychopathology. Dev Psychopathol 19:1029–1037PubMedCrossRefGoogle Scholar
  119. Tecott LH, Barondes SH (1996) Genes and aggressiveness. Behavioral genetics. Curr Biol 6:238–240PubMedCrossRefGoogle Scholar
  120. Teskey GC, Kavaliers M, Hirst M (1984) Social conflict activates opioid analgesic and ingestive behaviors in male mice. Life Sci 35:303–315PubMedCrossRefGoogle Scholar
  121. Thomas DA, Howard SB, Barfield RJ (1982) Male-produced postejaculatory 22-kHz vocalizations and the mating behavior of estrous female rats. Behav Neural Biol 36:403–410PubMedCrossRefGoogle Scholar
  122. Tornatzky W, Miczek KA (1993) Long-term impairment of autonomic circadian rhythms after brief intermittent social stress. Physiol Behav 53:983–993PubMedCrossRefGoogle Scholar
  123. Tornatzky W, Miczek KA (1994) Behavioral and autonomic responses to intermittent social stress: Differential effects of clonidine and metoprolol. Psychopharmacology 116:346–356PubMedCrossRefGoogle Scholar
  124. Umemoto S, Noguchi K, Kawai Y, Senba E (1994) Repeated stress reduces the subsequent stress-induced expression of Fos in rat brain. Neurosci Lett 167:101–104PubMedCrossRefGoogle Scholar
  125. 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 119:127–142CrossRefGoogle Scholar
  126. Van Der Vegt BJ, Lieuwes N, van de Wall EHEM, Kato K, Moya-Albiol L, Martinez-Sanchis S, de Boer SF, Koolhaas JM (2003) Activation of serotonergic neurotransmission during the performance of aggressive behaviour in rats. Behav Neurosci 117:667–674PubMedCrossRefGoogle Scholar
  127. Van Erp AMM, Miczek KA (2000) Aggressive behavior, increased accumbal dopamine and decreased cortical serotonin in rats. J Neurosci 15:9320–9325Google Scholar
  128. Vezina P, Lorrain DS, Arnold GM, Austin JD, Suto N (2002) Sensitization of midbrain dopamine neuron reactivity promotes the pursuit of amphetamine. J Neurosci 22:4654–4662PubMedGoogle Scholar
  129. Vivian JA, Miczek KA (1998) Effects of mu and delta opioid agonists and antagonists on affective vocal and reflexive pain responses during social stress in rats. Psychopharmacology 139:364–375PubMedCrossRefGoogle Scholar
  130. Von Holst D (1985) Coping behaviour and stress physiology in male tree shrews (Tupaia belangeri). In: Hölldobler B, Lindberg I (eds) Experimental behavioral ecology and sociobiology. Sinauer Associates, Sunderland, pp 461–470Google Scholar
  131. Von Holst D (1998) The concept of stress and its relevance for animal behavior. In: Moller AP, Milinski M, Slater PJB (eds) Advances in the study of behavior, vol. 27: stress and behavior. Academic Press, New York, pp 1–131Google Scholar
  132. Watanabe Y, McKittrick CR, Blanchard DC, Blanchard RJ, McEwen BS, Sakai RR (1995) Effects of chronic social stress on tyrosine hydroxylase mRNA and protein levels. Mol Brain Res 32:176–180PubMedCrossRefGoogle Scholar
  133. Weiss JM, Pohorecky LA, Salman S, Gruenthal M (1976) Attenuation of gastric lesions by psychological aspects of aggression in rats. J Comp Physiol Psychol 90:252–259PubMedCrossRefGoogle Scholar
  134. Winslow JT, Hastings N, Carter CS, Harbaugh CR, Insel TR (1993) A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 365:545–548PubMedCrossRefGoogle Scholar
  135. Young LJ, Wang Z (2004) The neurobiology of pair bonding. Nat Neurosci 7:1048–1054PubMedCrossRefGoogle Scholar
  136. Young LJ, Winslow JT, Wang Z, Gingrich B, Guo Q, Matzuk MM, Insel TR (1997) Gene targeting approaches to neuroendocrinology: oxytocin, maternal behavior, and affiliation. Horm Behav 31:221–231PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Klaus A. Miczek
    • 1
    • 2
    • 3
  • Ella M. Nikulina
    • 2
    • 4
  • Aki Takahashi
    • 5
  • Herbert E. CovingtonIII
    • 6
  • Jasmine J. Yap
    • 7
  • Christopher O. Boyson
    • 1
  • Akiko Shimamoto
    • 1
  • Rosa M. M. de Almeida
    • 8
  1. 1.Department of PsychologyTufts UniversityMedfordUSA
  2. 2.Department of PsychiatryTufts University School of MedicineBostonUSA
  3. 3.Departments of Pharmacology and NeuroscienceTufts UniversityBostonUSA
  4. 4.Department of Basic Medical SciencesUniversity of Arizona College of MedicinePhoenixUSA
  5. 5.Mouse Genomics Resource LaboratoryNational Institute of GeneticsShizuokaJapan
  6. 6.Departments of Psychology and NeuroscienceDuke UniversityDurhamUSA
  7. 7.Center for NeuroscienceUniversity of ColoradoBoulderUSA
  8. 8.Instituto de PsicologiaUFRGSPorto AlegreBrazil

Personalised recommendations