Psychoneuroendocrinology
Volume 32, Issue 5 , Pages 437-450 , June 2007

Opposite effects of maternal separation on intermale and maternal aggression in C57BL/6 mice: Link to hypothalamic vasopressin and oxytocin immunoreactivity

Received 12 December 2006 ,Revised 19 February 2007 ,Accepted 20 February 2007.

References 

  1. Antoni FA. Vasopressinergic control of pituitary adrenocorticotropin secretion comes of age. Front. Neuroendocrinol. 1993;14:76–122
  2. Bale TL, Davis AM, Auger AP, Dorsa DM, McCarthy MM. CNS region-specific oxytocin receptor expression: importance in regulation of anxiety and sex behavior. J. Neurosci. 2001;21:2546–2552
  3. Bales KL, Carter CS. Developmental exposure to oxytocin facilitates partner preferences in male prairie voles (Microtus ochrogaster). Behav. Neurosci. 2003;117:854–859
  4. Barnow S, Freyberger HJ. The family environment in early life and aggressive behavior in adolescents and young adults. In:  Mattson M editors. Neurobiology of Aggression: Understanding and Preventing Violence. Totowa, NJ: Humana Press Inc.; 2003;p. 213–229
  5. Barnow S, Lucht M, Freyberger HJ. Influence of punishment, emotional rejection, child abuse, and broken home on aggression in adolescence: an examination of aggressive adolescents in Germany. Psychopathology. 2001;34:167–173
  6. Bielsky IF, Hu SB, Szegda KL, Westphal H, Young LJ. Profound impairment in social recognition and reduction in anxiety-like behavior in vasopressin V1a receptor knockout mice. Neuropsychopharmacology. 2004;29:483–493
  7. Bielsky IF, Hu SB, Young LJ. Sexual dimorphism in the vasopressin system: lack of an altered behavioral phenotype in female V1a receptor knockout mice. Behav. Brain Res. 2005;164:132–136
  8. Blanchard RJ, Wall PM, Blanchard DC. Problems in the study of rodent aggression. Horm. Behav. 2003;44:161–170
  9. Blanchard RJ, Griebel G, Farrokhi C, Markham C, Yang M, Blanchard DC. AVP V1b selective antagonist SSR149415 blocks aggressive behaviors in hamsters. Pharmacol. Biochem. Behav. 2005;80:189–194
  10. Boccia ML, Pedersen CA. Brief vs. long maternal separations in infancy: contrasting relationships with adult maternal behavior and lactation levels of aggression and anxiety. Psychoneuroendocrinology. 2001;26:657–672
  11. Bosch OJ, Kromer SA, Brunton PJ, Neumann ID. Release of oxytocin in the hypothalamic paraventricular nucleus, but not central amygdala or lateral septum in lactating residents and virgin intruders during maternal defence. Neuroscience. 2004;124:439–448
  12. Bosch OJ, Meddle SL, Beiderbeck DI, Douglas AJ, Neumann ID. Brain oxytocin correlates with maternal aggression: link to anxiety. J. Neurosci. 2005;25:6807–6815
  13. Bosch OJ, Kromer SA, Neumann ID. Prenatal stress: opposite effects on anxiety and hypothalamic expression of vasopressin and corticotropin-releasing hormone in rats selectively bred for high and low anxiety. Eur. J. Neurosci. 2006;23:541–551
  14. Brain PF. Differentiating types of attack and defence in rodents. In:  Brain PF,  Benton D editor. Multidisciplinary Approaches to Aggression Research. Amsterdam: Elsevier; 1981;p. 53–78
  15. Bufkin JL, Luttrell VR. Neuroimaging studies of aggressive and violent behavior: current findings and implications for criminology and criminal justice. Trauma Violence Abuse. 2005;6:176–191
  16. Caldji C, Francis D, Sharma S, Plotsky PM, Meaney MJ. The effects of early rearing environment on the development of GABAA and central benzodiazepine receptor levels and novelty-induced fearfulness in the rat. Neuropsychopharmacology. 2000;22:219–229
  17. Caspi A, McClay J, Moffitt TE, Mill J, Martin J, Craig IW, et al. Role of genotype in the cycle of violence in maltreated children. Science. 2002;297:851–854
  18. Caspi A, Sugden K, Moffitt TE, Taylor A, Craig IW, Harrington H, et al. Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science. 2003;301:386–389
  19. Catlett RH. An evaluation of methods for measuring fighting behaviour with specific reference to Mus musculus. Anim. Behav. 1961;9:8–10
  20. Consiglio AR, Lucion AB. Lesion of hypothalamic paraventricular nucleus and maternal aggressive behavior in female rats. Physiol. Behav. 1996;59:591–596
  21. Consiglio AR, Borsoi A, Pereira GA, Lucion AB. Effects of oxytocin microinjected into the central amygdaloid nucleus and bed nucleus of stria terminalis on maternal aggressive behavior in rats. Physiol. Behav. 2005;85:354–362
  22. Cushing BS, Kramer KM. Mechanisms underlying epigenetic effects of early social experience: the role of neuropeptides and steroids. Neurosci. Biobehav. Rev. 2005;29:1089–1105
  23. Dai J, Swaab DF, Buijs RM. Distribution of vasopressin and vasoactive intestinal polypeptide (VIP) fibers in the human hypothalamus with special emphasis on suprachiasmatic nucleus efferent projections. J. Comp. Neurol. 1997;383:397–414
  24. Davidson RJ, Putnam KM, Larson CL. Dysfunction in the neural circuitry of emotion regulation—a possible prelude to violence. Science. 2000;289:591–594
  25. de Vries GJ, Miller MA. Anatomy and function of extrahypothalamic vasopressin systems in the brain. Prog. Brain Res. 1998;119:3–20
  26. Demas GE, Kriegsfeld LJ, Blackshaw S, Huang P, Gammie SC, Nelson RJ, et al. Elimination of aggressive behavior in male mice lacking endothelial nitric oxide synthase. J. Neurosci. 1999;19:RC30
  27. Dodge KA, Bates JE, Pettit GS. Mechanisms in the cycle of violence. Science. 1990;250:1678–1683
  28. Douglas AJ, Brunton PJ, Bosch OJ, Russell JA, Neumann ID. Neuroendocrine responses to stress in mice: hyporesponsiveness in pregnancy and parturition. Endocrinology. 2003;144:5268–5276
  29. Engelmann M, Landgraf R, Wotjak CT. The hypothalamic-neurohypophysial system regulates the hypothalamic–pituitary–adrenal axis under stress: an old concept revisited. Front. Neuroendocrinol. 2004;25:132–149
  30. Ferris CF. Vasopressin/oxytocin and aggression. Novartis Found. Symp. 2005;268:190–198discussion 198–200, 242–153
  31. Ferris CF, Delville Y. Vasopressin and serotonin interactions in the control of agonistic behavior. Psychoneuroendocrinology. 1994;19:593–601
  32. Fleming AS, O’Day DH, Kraemer GW. Neurobiology of mother-infant interactions: experience and central nervous system plasticity across development and generations. Neurosci. Biobehav. Rev. 1999;23:673–685
  33. Francis DD, Young LJ, Meaney MJ, Insel TR. Naturally occurring differences in maternal care are associated with the expression of oxytocin and vasopressin (V1a) receptors: gender differences. J. Neuroendocrinol. 2002;14:349–353
  34. Frederickson D. Maltreatment of children. J. Child Fam. Nurs. 1999;2:393–401(quiz 401–392)
  35. Gammie SC, Huang PL, Nelson RJ. Maternal aggression in endothelial nitric oxide synthase-deficient mice. Horm. Behav. 2000;38:13–20
  36. Gammie SC, Hasen NS, Stevenson SA, Bale TL, D’Anna KL. Elevated stress sensitivity in corticotropin-releasing factor receptor 2 deficient mice decreases maternal, but not intermale aggression. Behav. Brain Res. 2005;160:169–177
  37. Gimpl G, Fahrenholz F. The oxytocin receptor system: structure, function, and regulation. Physiol. Rev. 2001;81:629–683
  38. Giovenardi M, Padoin MJ, Cadore LP, Lucion AB. Hypothalamic paraventricular nucleus, oxytocin, and maternal aggression in rats. Ann. NY Acad. Sci. 1997;807:606–609
  39. Giovenardi M, Padoin MJ, Cadore LP, Lucion AB. Hypothalamic paraventricular nucleus modulates maternal aggression in rats: effects of ibotenic acid lesion and oxytocin antisense. Physiol. Behav. 1998;63:351–359
  40. Gollan JK, Lee R, Coccaro EF. Developmental psychopathology and neurobiology of aggression. Dev. Psychopathol. 2005;17:1151–1171
  41. Green AH. Child maltreatment and its victims. A comparison of physical and sexual abuse. Psychiatr. Clin. North. Am. 1988;11:591–610
  42. Griebel G, Stemmelin J, Gal CS, Soubrie P. Non-peptide vasopressin V1b receptor antagonists as potential drugs for the treatment of stress-related disorders. Curr. Pharm. Des. 2005;11:1549–1559
  43. Heinrichs M, Baumgartner T, Kirschbaum C, Ehlert U. Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress. Biol. Psychiat. 2003;54:1389–1398
  44. Huot RL, Plotsky PM, Lenox RH, McNamara RK. Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats. Brain Res. 2002;950:52–63
  45. Ingram CD, Moos F. Oxytocin-containing pathway to the bed nuclei of the stria terminalis of the lactating rat brain: immunocytochemical and in vitro electrophysiological evidence. Neuroscience. 1992;47:439–452
  46. Insel TR, Shapiro LE. Oxytocin receptors and maternal behavior. Ann. NY Acad. Sci. 1992;652:122–141
  47. Itoi K, Jiang YQ, Iwasaki Y, Watson SJ. Regulatory mechanisms of corticotropin-releasing hormone and vasopressin gene expression in the hypothalamus. J. Neuroendocrinol. 2004;16:348–355
  48. Johnson RM, Kotch JB, Catellier DJ, Winsor JR, Dufort V, Hunter W, et al. Adverse behavioral and emotional outcomes from child abuse and witnessed violence. Child Maltreat. 2002;7:179–186
  49. Kalinichev M, Easterling KW, Plotsky PM, Holtzman SG. Long-lasting changes in stress-induced corticosterone response and anxiety-like behaviors as a consequence of neonatal maternal separation in Long-Evans rats. Pharmacol. Biochem. Behav. 2002;73:131–140
  50. Kane NL, Knutson JF. Influence of colony lighting conditions on home-cage spontaneous aggression. J. Comp. Physiol. Psychol. 1976;90:889–897
  51. Keck ME, Wigger A, Welt T, Muller MB, Gesing A, Reul JM, et al. Vasopressin mediates the response of the combined dexamethasone/CRH test in hyper-anxious rats: implications for pathogenesis of affective disorders. Neuropsychopharmacology. 2002;26:94–105
  52. Keverne EB, Curley JP. Vasopressin, oxytocin and social behaviour. Curr. Opin. Neurobiol. 2004;14:777–783
  53. Kirsch P, Esslinger C, Chen Q, Mier D, Lis S, Siddhanti S, et al. Oxytocin modulates neural circuitry for social cognition and fear in humans. J. Neurosci. 2005;25:11489–11493
  54. Kosfeld M, Heinrichs M, Zak PJ, Fischbacher U, Fehr E. Oxytocin increases trust in humans. Nature. 2005;435:673–676
  55. Kovacs KJ. Functional neuroanatomy of the parvocellular vasopressinergic system: transcriptional responses to stress and glucocorticoid feedback. Prog. Brain Res. 1998;119:31–43
  56. Kramer KM, Cushing BS, Carter CS. Developmental effects of oxytocin on stress response: single versus repeated exposure. Physiol. Behav. 2003;79:775–782
  57. Ladd CO, Owens MJ, Nemeroff CB. Persistent changes in corticotropin-releasing factor neuronal systems induced by maternal deprivation. Endocrinology. 1996;137:1212–1218
  58. Ladd CO, Huot RL, Thrivikraman KV, Nemeroff CB, Meaney MJ, Plotsky PM. Long-term behavioral and neuroendocrine adaptations to adverse early experience. Prog. Brain Res. 2000;122:81–103
  59. Ladd CO, Huot RL, Thrivikraman KV, Nemeroff CB, Plotsky PM. Long-term adaptations in glucocorticoid receptor and mineralocorticoid receptor mRNA and negative feedback on the hypothalamo–pituitary–adrenal axis following neonatal maternal separation. Biol. Psychiatry. 2004;55:367–375
  60. Landgraf R, Neumann ID. Vasopressin and oxytocin release within the brain: a dynamic concept of multiple and variable modes of neuropeptide communication. Front. Neuroendocrinol. 2004;25:150–176
  61. Landgraf R, Wotjak CT, Neumann ID, Engelmann M. Release of vasopressin within the brain contributes to neuroendocrine and behavioral regulation. Prog. Brain Res. 1998;119:201–220
  62. Lansford JE, Dodge KA, Pettit GS, Bates JE, Crozier J, Kaplow J. A 12-year prospective study of the long-term effects of early child physical maltreatment on psychological, behavioral, and academic problems in adolescence. Arch. Pediatr. Adolesc. Med. 2002;156:824–830
  63. Leshner AI, Korn SJ, Mixon JF, Rosenthal C, Besser AK. Effects of corticosterone on submissiveness in mice: some temporal and theoretical considerations. Physiol. Behav. 1980;24:283–288
  64. Lewis DO. From abuse to violence: psychophysiological consequences of maltreatment. J. Am. Acad. Child Adolesc. Psychiatry. 1992;31:383–391
  65. Liebsch G, Linthorst AC, Neumann ID, Reul JM, Holsboer F, Landgraf R. Behavioral, physiological, and neuroendocrine stress responses and differential sensitivity to diazepam in two Wistar rat lines selectively bred for high- and low-anxiety-related behavior. Neuropsychopharmacology. 1998;19:381–396
  66. Lightman SL, Windle RJ, Wood SA, Kershaw YM, Shanks N, Ingram CD. Peripartum plasticity within the hypothalamo–pituitary–adrenal axis. Prog. Brain Res. 2001;133:111–129
  67. Lim MM, Wang Z, Olazabal DE, Ren X, Terwilliger EF, Young LJ. Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene. Nature. 2004;429:754–757
  68. Liu D, Caldji C, Sharma S, Plotsky PM, Meaney MJ. Influence of neonatal rearing conditions on stress-induced adrenocorticotropin responses and norepinepherine release in the hypothalamic paraventricular nucleus. J. Neuroendocrinol. 2000;12:5–12
  69. Loeber R, Dishion T. Early predictors of male delinquency: a review. Psychol. Bull. 1983;94:68–99
  70. Loeber R, Stouthamer-Loeber M. Development of juvenile aggression and violence. Some common misconceptions and controversies. Am. Psychol. 1998;53:242–259
  71. Meinlschmidt, G., Heim, C., 2006. Sensitivity to intranasal oxytocin in adult men with early parental separation. Biol. Psychiatry Dec 1; [Epub ahead of print].
  72. Meaney MJ. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu. Rev. Neurosci. 2001;24:1161–1192
  73. Neumann ID. Alterations in behavioral and neuroendocrine stress coping strategies in pregnant, parturient and lactating rats. Prog. Brain Res. 2001;133:143–152
  74. Neumann ID. Brain mechanisms underlying emotional alterations in the peripartum period in rats. Depress. Anxiety. 2003;17:111–121
  75. Neumann ID, Wigger A, Torner L, Holsboer F, Landgraf R. Brain oxytocin inhibits basal and stress-induced activity of the hypothalamo–pituitary–adrenal axis in male and female rats: partial action within the paraventricular nucleus. J. Neuroendocrinol. 2000;12:235–243
  76. Neumann ID, Kromer SA, Bosch OJ. Effects of psycho-social stress during pregnancy on neuroendocrine and behavioural parameters in lactation depend on the genetically determined stress vulnerability. Psychoneuroendocrinology. 2005;30:791–806
  77. Newport DJ, Stowe ZN, Nemeroff CB. Parental depression: animal models of an adverse life event. Am. J. Psychiatry. 2002;159:1265–1283
  78. Numan M. Maternal behaviour. In:  Knobil E,  neill JD editor. The Physiology of Reproduction. second ed. New York: Raven; 1994;p. 221–301
  79. Padoin MJ, Cadore LP, Gomes CM, Barros HM, Lucion AB. Long-lasting effects of neonatal stimulation on the behavior of rats. Behav. Neurosci. 2001;115:1332–1340
  80. Parfitt DB, Levin JK, Saltstein KP, Klayman AS, Greer LM, Helmreich DL. Differential early rearing environments can accentuate or attenuate the responses to stress in male C57BL/6 mice. Brain Res. 2004;1016:111–118
  81. Parmigiani S, Brain PF, Mainardi D, Brunoni V. Different patterns of biting attack employed by lactating female mice (Mus domesticus) in encounters with male and female conspecific intruders. J. Comp. Psychol. 1988;102:287–293
  82. Parmigiani S, Ferrari PF, Palanza P. An evolutionary approach to behavioral pharmacology: using drugs to understand proximate and ultimate mechanisms of different forms of aggression in mice. Neurosci. Biobehav. Rev. 1998;23:143–153
  83. Pedersen CA. Biological aspects of social bonding and the roots of human violence. Ann. NY Acad. Sci. 2004;1036:106–127
  84. Pedersen CA, Caldwell JD, Peterson G, Walker CH, Mason GA. Oxytocin activation of maternal behavior in the rat. Ann. NY Acad. Sci. 1992;652:58–69
  85. Plotsky PM, Meaney MJ. Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Mol. Brain Res. 1993;18:195–200
  86. Politch JA, Leshner AI. Relationship between plasma corticosterone levels and levels of aggressiveness in mice. Physiol. Behav. 1977;19:775–780
  87. Popova NK. From genes to aggressive behavior: the role of serotonergic system. Bioessays. 2006;28:495–503
  88. Ring RH, Malberg JE, Potestio L, Ping J, Boikess S, Luo B, et al. Anxiolytic-like activity of oxytocin in male mice: behavioral and autonomic evidence, therapeutic implications. Psychopharmacology (Berl). 2006;185:218–225
  89. Romeo RD, Mueller A, Sisti HM, Ogawa S, McEwen BS, Brake WG. Anxiety and fear behaviors in adult male and female C57BL/6 mice are modulated by maternal separation. Horm. Behav. 2003;43:561–567
  90. Russel JW, Singer G. Relations between muricide, circadian rhythm and consummatory behaviour. Physiol. Behav. 1983;30:23–27
  91. Singewald N, Salchner P, Sharp T. Induction of c-Fos expression in specific areas of the fear circuitry in rat forebrain by anxiogenic drugs. Biol. Psychiatry. 2003;53:275–283
  92. Stern JM. Offspring-induced nurturance: animal–human parallels. Dev. Psychobiol. 1997;31:19–37
  93. Storm EE, Tecott LH. Social circuits: peptidergic regulation of mammalian social behavior. Neuron. 2005;47:483–486
  94. van Beijsterveldt CE, Bartels M, Hudziak JJ, Boomsma DI. Causes of stability of aggression from early childhood to adolescence: a longitudinal genetic analysis in Dutch twins. Behav. Genet. 2003;33:591–605
  95. van Gaalen MM, Steckler T. Behavioural analysis of four mouse strains in an anxiety test battery. Behav. Brain Res. 2000;115:95–106
  96. van Praag HM. Anxiety and increased aggression as pacemakers of depression. Acta Psychiatr. Scand. Suppl. 1998;393:81–88
  97. van Zegeren K. Variation in aggressiveness and the regulation of numbers in house mouse populations. Neth. J. Zool. 1980;30:635–770
  98. Varghese AK, Verdu EF, Bercik P, Khan WI, Blennerhassett PA, Szechtman H, et al. Antidepressants attenuate increased susceptibility to colitis in a murine model of depression. Gastroenterology. 2006;130:1743–1753
  99. Veenema AH, Blume A, Niederle D, Buwalda B, Neumann ID. Effects of early life stress on adult male aggression and hypothalamic vasopressin and serotonin. Eur. J. Neurosci. 2006;24:1711–1720
  100. Veenema AH, Torner L, Blume A, Beiderbeck DI, Neumann ID. Low inborn anxiety correlates with high intermale aggression: link to ACTH response and neuronal activation of the hypothalamic paraventricular nucleus. Horm. Behav. 2007;51:11–19
  101. Walker CD, Trottier G, Rochford J, Lavallee D. Dissociation between behavioral and hormonal responses to the forced swim stress in lactating rats. J. Neuroendocrinol. 1995;7:615–622
  102. Wersinger SR, Ginns EI, O’Carroll AM, Lolait SJ, Young 3rd WS. Vasopressin V1b receptor knockout reduces aggressive behavior in male mice. Mol. Psychiatry. 2002;7:975–984
  103. Widom CS. Child abuse, neglect, and adult behavior: research design and findings on criminality, violence, and child abuse. Am. J. Orthopsychiatry. 1989;59:355–367
  104. Wigger A, Neumann ID. Periodic maternal deprivation induces gender-dependent alterations in behavioral and neuroendocrine responses to emotional stress in adult rats. Physiol. Behav. 1999;66:293–302
  105. Wigger A, Sanchez MM, Mathys KC, Ebner K, Frank E, Liu D, et al. Alterations in central neuropeptide expression, release, and receptor binding in rats bred for high anxiety: critical role of vasopressin. Neuropsychopharmacology. 2004;29:1–14
  106. Windle RJ, Kershaw YM, Shanks N, Wood SA, Lightman SL, Ingram CD. Oxytocin attenuates stress-induced c-fos mRNA expression in specific forebrain regions associated with modulation of hypothalamo–pituitary–adrenal activity. J. Neurosci. 2004;24:2974–2982
  107. Windle RJ, Shanks N, Lightman SL, Ingram CD. Central oxytocin administration reduces stress-induced corticosterone release and anxiety behavior in rats. Endocrinology. 1997;138:2829–2834
  108. Windle RJ, Wood S, Shanks N, Perks P, Conde GL, da Costa AP, et al. Endocrine and behavioural responses to noise stress: comparison of virgin and lactating female rats during non-disrupted maternal activity. J. Neuroendocrinol. 1997;9:407–414
  109. Winslow JT, Shapiro L, Carterm CS, Insel TR. Oxytocin and complex social behavior: species comparisons. Psychopharmacol. Bull. 1993;29:409–414
  110. Winslow JT, Hearn EF, Ferguson J, Young LJ, Matzuk MM, Insel TR. Infant vocalization, adult aggression, and fear behavior of an oxytocin null mutant mouse. Horm. Behav. 2000;37:145–155
  111. Young LJ, Wang Z. The neurobiology of pair bonding. Nat. Neurosci. 2004;7:1048–1054

PII: S0306-4530(07)00040-6

doi: 10.1016/j.psyneuen.2007.02.008

Psychoneuroendocrinology
Volume 32, Issue 5 , Pages 437-450 , June 2007

Article Tools

* Image Usage & Resolution