Within-litter variation in maternal care received by individual pups correlates with adolescent social play behavior in male rats

Physiology and Behavior

Volumn 106, Issue 5, 2012, Pages 701-706

  van Hasselt, F N ^a   Tieskens, J M ^a   Trezza, V ^b,c   Krugers, H J ^a   Vanderschuren, L J M J ^b,d   Joels M ^b  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c ROMA TRE UNIVERSITY   (Italy)

^d UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Maternal care; Postnatal development; Reward; Social play behavior; Stress

Indexed keywords

ADAPTIVE BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; FEMALE; GROOMING; LATENT PERIOD; LICKING; MALE; MATERNAL CARE; NONHUMAN; PERINATAL PERIOD; PLAY; PRIORITY JOURNAL; PUP (RODENT); RAT; SEX DIFFERENCE; SOCIAL BEHAVIOR;

ANIMALS; ANIMALS, NEWBORN; FEMALE; GROOMING; MALE; MATERNAL BEHAVIOR; PLAY AND PLAYTHINGS; RATS; RATS, LONG-EVANS; REWARD; SOCIAL BEHAVIOR;

EID: 84861688496     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2011.12.007     Document Type: Article

References (51)

1. Heim C., Newport D.J., Mletzko T., Miller A.H., Nemeroff C.B. The link between childhood trauma and depression: insights from HPA axis studies in humans. Psychoneuroendocrinology 2008, 33(6):693-710.
2. Matthews K., Dalley J.W., Matthews C., Tsai T.H., Robbins T.W. Periodic maternal separation of neonatal rats produces region- and gender-specific effects on biogenic amine content in postmortem adult brain. Synapse 2001, 40(1):1-10.
3. Pryce C.R., Ruedi-Bettschen D., Dettling A.C., Weston A., Russig H., Ferger B., et al. Long-term effects of early-life environmental manipulations in rodents and primates: potential animal models in depression research. Neurosci Biobehav Rev 2005, 29(4-5):649-674.
4. Tarullo A.R., Gunnar M.R. Child maltreatment and the developing HPA axis. Horm Behav 2006, 50(4):632-639.
5. Ladd C.O., Huot R.L., Thrivikraman K.V., Nemeroff C.B., Plotsky P.M. 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(4):367-375.
6. Oomen C.A., Soeters H., Audureau N., Vermunt L., van Hasselt F.N., Manders E.M., et al. Severe early life stress hampers spatial learning and neurogenesis, but improves hippocampal synaptic plasticity and emotional learning under high-stress conditions in adulthood. J Neurosci 2010, 30(19):6635-6645.
7. Green M.F., Horan W.P. Social cognition in schizophrenia. Curr Dir Psychol Sci 2010, 19(4):243-248.
8. Franklin T.B., Linder N., Russig H., Thony B., Mansuy I.M. Influence of early stress on social abilities and serotonergic functions across generations in mice. PLoS One 2011, 6(7):e21842.
9. Stevens H.E., Leckman J.F., Coplan J.D., Suomi S.J. Risk and resilience: early manipulation of macaque social experience and persistent behavioral and neurophysiological outcomes. J Am Acad Child Adolesc Psychiatry 2009, 48(2):114-127.
10. Young L.D., Suomi S.S., Harlow H.F., McKinney W.T. Early stress and later response to separation in rhesus monkeys. Am J Psychiatry 1973, 130(4):400-405.
11. Panksepp J., Siviy S., Normansell L. The psychobiology of play: theoretical and methodological perspectives. Neurosci Biobehav Rev 1984, 8(4):465-492.
12. Pellis S.M., Pellis V.C. The playful brain: venturing to the limits of neuroscience 2009, Oneworld Publications, Oxford.
13. Spinka M., Newberry R.C., Bekoff M. Mammalian play: training for the unexpected. Q Rev Biol 2001, 76(2):141-168.
14. Vanderschuren L.J., Niesink R.J., Van Ree J.M. The neurobiology of social play behavior in rats. Neurosci Biobehav Rev 1997, 21(3):309-326.
15. Siviy S.M., Panksepp J. In search of the neurobiological substrates for social playfulness in mammalian brains. Neurosci Biobehav Rev 2011, 35(9):1821-1830.
16. Trezza V., Baarendse P.J., Vanderschuren L.J. The pleasures of play: pharmacological insights into social reward mechanisms. Trends Pharmacol Sci 2010, 31(10):463-469.
17. Vanderschuren L.J. How the brain makes play fun. Am J Play 2010, 2:315-337.
18. Trezza V., Damsteegt R., Achterberg E.J., Vanderschuren L.J. Nucleus accumbens mu-opioid receptors mediate social reward. J Neurosci 2011, 31(17):6362-6370.
19. Champagne F.A., Francis D.D., Mar A., Meaney M.J. Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol Behav 2003, 79(3):359-371.
20. Zhang T.Y., Chretien P., Meaney M.J., Gratton A. Influence of naturally occurring variations in maternal care on prepulse inhibition of acoustic startle and the medial prefrontal cortical dopamine response to stress in adult rats. J Neurosci 2005, 25(6):1493-1502.
21. Caldji C., Tannenbaum B., Sharma S., Francis D., Plotsky P.M., Meaney M.J. Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc Natl Acad Sci U S A 1998, 95(9):5335-5340.
22. Francis D., Diorio J., Liu D., Meaney M.J. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 1999, 286(5442):1155-1158.
23. Liu D., Diorio J., Tannenbaum B., Caldji C., Francis D., Freedman A., et al. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 1997, 277(5332):1659-1662.
24. Van Hasselt FN, Cornelisse S, Zhang TY, Meaney MJ, Velzing EH, Krugers HJ and Joels M. Adult hippocampal glucocorticoid receptor expression and dentate synaptic plasticity correlate with maternal care received by individuals early in life. Hippocampus in press.
25. Schneider M., Koch M. Deficient social and play behavior in juvenile and adult rats after neonatal cortical lesion: effects of chronic pubertal cannabinoid treatment. Neuropsychopharmacology 2005, 30(5):944-957.
26. Vanderschuren L.J., Spruijt B.M., Hol T., Niesink R.J., Van Ree J.M. Sequential analysis of social play behavior in juvenile rats: effects of morphine. Behav Brain Res 1995, 72(1-2):89-95.
27. Trezza V., Vanderschuren L.J. Bidirectional cannabinoid modulation of social behavior in adolescent rats. Psychopharmacology (Berl) 2008, 197(2):217-227.
28. Klein Z.A., Padow V.A., Romeo R.D. The effects of stress on play and home cage behaviors in adolescent male rats. Dev Psychobiol 2010, 52(1):62-70.
29. Parent C.I., Meaney M.J. The influence of natural variations in maternal care on play fighting in the rat. Dev Psychobiol 2008, 50(8):767-776.
30. Auger A.P., Olesen K.M. Brain sex differences and the organisation of juvenile social play behaviour. J Neuroendocrinol 2009, 21(6):519-525.
31. Panksepp J. The ontogeny of play in rats. Dev Psychobiol 1981, 14(4):327-332.
32. Spear L.P. The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 2000, 24(4):417-463.
33. Moore C.L., Morelli G.A. Mother rats interact differently with male and female offspring. J Comp Physiol Psychol 1979, 93(4):677-684.
34. Birke L.I., Sadler D. Differences in maternal behavior of rats and the sociosexual development of the offspring. Dev Psychobiol 1987, 20(1):85-99.
35. Moore C.L., Power K.L. Variation in maternal care and individual differences in play, exploration, and grooming of juvenile Norway rat offspring. Dev Psychobiol 1992, 25(3):165-182.
36. Bredy T.W., Humpartzoomian R.A., Cain D.P., Meaney M.J. Partial reversal of the effect of maternal care on cognitive function through environmental enrichment. Neuroscience 2003, 118(2):571-576.
37. Bredy T.W., Zhang T.Y., Grant R.J., Diorio J., Meaney M.J. Peripubertal environmental enrichment reverses the effects of maternal care on hippocampal development and glutamate receptor subunit expression. Eur J Neurosci 2004, 20(5):1355-1362.
38. Niesink R.J., Van Ree J.M. Involvement of opioid and dopaminergic systems in isolation-induced pinning and social grooming of young rats. Neuropharmacology 1989, 28(4):411-418.
39. Vanderschuren L.J., Trezza V., Griffioen-Roose S., Schiepers O.J., Van Leeuwen N., De Vries T.J., et al. Methylphenidate disrupts social play behavior in adolescent rats. Neuropsychopharmacology 2008, 33(12):2946-2956.
40. Pellis S.M., McKenna M.M. Intrinsic and extrinsic influences on play fighting in rats: effects of dominance, partner's playfulness, temperament and neonatal exposure to testosterone propionate. Behav Brain Res 1992, 50(1-2):135-145.
41. Van den Berg C.L., Hol T., Van Ree J.M., Spruijt B.M., Everts H., Koolhaas J.M. Play is indispensable for an adequate development of coping with social challenges in the rat. Dev Psychobiol 1999, 34(2):129-138.
42. Weintraub A., Singaravelu J., Bhatnagar S. Enduring and sex-specific effects of adolescent social isolation in rats on adult stress reactivity. Brain Res 2010, 1343:83-92.
43. Caldji C., Diorio J., Meaney M.J. Variations in maternal care alter GABA(A) receptor subunit expression in brain regions associated with fear. Neuropsychopharmacology 2003, 28(11):1950-1959.
44. Meaney M.J. The sexual differentiation of social play. Psychiatr Dev 1989, 7(3):247-261.
45. Pellis S.M., Field E.F., Smith L.K., Pellis V.C. Multiple differences in the play fighting of male and female rats. Implications for the causes and functions of play. Neurosci Biobehav Rev 1997, 21(1):105-120.
46. Pellis S.M., Pellis V.C., McKenna M.M. Feminine dimension in the play fighting of rats (Rattus norvegicus) and its defeminization neonatally by androgens. J Comp Psychol 1994, 108(1):68-73.
47. Meaney M.J., Stewart J. Neonatal-androgens influence the social play of prepubescent rats. Horm Behav 1981, 15(2):197-213.
48. Aguilar R., Caramés J.M., Espinet A. Effects of neonatal handling on playfulness by means of reversal of the desire to play in rats (Rattus norvegicus). J Comp Psychol 2009, 123(4):347-356.
49. Siviy S.M., Harrison K.A. Effects of neonatal handling on play behavior and fear towards a predator odor in juvenile rats (Rattus norvegicus). J Comp Psychol 2008, 122:1-8.
50. Lomanowska A.M., Lovic V., Rankine M.J., Mooney S.J., Robinson T.E., Kraemer G.W. Inadequate early social experience increases the incentive salience of reward-related cues in adulthood. Behav Brain Res 2011, 220(1):91-99.
51. Ruedi-Bettschen D., Pedersen E.M., Feldon J., Pryce C.R. Early deprivation under specific conditions leads to reduced interest in reward in adulthood in Wistar rats. Behav Brain Res 2005, 156(2):297-310.