The developmental psychobiology of behavioural plasticity in mice: The role of social experiences in the family unit

Neuroscience and Biobehavioral Reviews

Volumn 23, Issue 2, 1998, Pages 197-213

  Laviola, Giovanni ^a   Terranova, M Livia ^b  

^a Sect of Behavioral Pathophysiology Lab Fisiopatol Organo Sistema I   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Affiliative and playful social behaviour; Dam care; Developmental plasticity; Individual variability; Mouse; Ontogeny of behaviour; Precocious weaning; Psychostimulants; Sexual segregation; Sibling effect

Indexed keywords

DEXAMPHETAMINE; PSYCHOSTIMULANT AGENT;

ADOLESCENT; ANIMAL EXPERIMENT; BEHAVIOR; CONFERENCE PAPER; CONTROLLED STUDY; DRUG ABUSE; FAMILY; FEMALE; LACTATION; MALE; MOTHER CHILD RELATION; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; PSYCHOBIOLOGY; SIBLING; SOCIAL INTERACTION; WEANING;

EID: 0032434602     PISSN: 01497634     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0149-7634(98)00021-9     Document Type: Conference Paper

References (123)

1. Alberts JA, Gubernick DJ. Reciprocity and resource exchange. In: Rosenblum LA, Molts H, editors. Symbiosis in parent-offspring interactions. New York: Plenum Press, 1983. pp. 7-44.
2. Alleva E., Caprioli A., Laviola G. Litter-gender-composition affects maternal behaviour of primiparous mouse dam (Mus musculus). J. Comp. Psychol. 103:1989;83-87.
3. Alleva E., Caprioli A., Laviola G. Postnatal social environment affects morphine analgesia in male mice. Physiol. Behav. 36:1986;779-781.
4. Antelman S.M., Eichler A.J., Black C.A., Kocan D. Interchangeability of stress and amphetamine in sensitization. Science. 207:1980;329-331.
5. Barbazanges A., Vallee M., Mayo W., Day J., Simon H., Le Moal M., Maccari S. Early and later adoptions have different long-term effects on male rat offspring. J. Neurosci. 16:1996;7783-7790.
6. Barrett P., Bateson P. The development of play in cats. Behaviour. 66:1978;106-120.
7. Bateson P. Ontogeny of behaviour. Br. Med. Bull. 37:1981;159-164.
8. Bateson P., Mendl M., Feaver J. Play in the domestic cat is enhanced by rationing of the mother during lactation. Anim. Behav. 40:1990;514-525.
9. Bateson P., Young M. Separation from the mother and the development of play in cats. Anim. Behav. 29:1981;173-180.
10. Bateson P., Young M. The influence of male kittens on the object play of their female siblings. Behav. Neural Biol. 27:1979;374-378.
11. Beach FA. Animal models of psychological inference. In: Katchadourian HA, editor. Human sexuality: a comparative and developmental perspective. Berkeley: University of California Press, 1979. pp. 98-112.
12. Bekoff M. Motor training and physical fitness: possible short- and long-term influences on the development of individual differences in behaviour. Develop. Psychobiol. 21:1988;601-612.
13. Birke L.I.A., Sadler D. Differences in maternal behavior of rats and the sociosexual development of the offspring. Develop. Psychobiol. 20:1987;85-99.
14. Blanchard D.C., Blanchard R.J., Tom P., Rodgers R.J. Diazepam changes risk assessment in an anxiety/defense test battery. Psychopharmacology. 101:1990;511-518.
15. Blanchard R., Zucker K.J., Hume C.S., Bradley S.J. Birth order and sibling sex ratio in homosexual male adolescents and probably prehomosexual feminine boys. Develop. Psychol. 31:1995;22-30.
16. Bowling S.L., Rowlett J.K., Bardo M.T. The effect of environmental enrichment on amphetamine-stimulated locomotor activity, dopamine synthesis and dopamine release. Neuropharmacology. 32:1993;885-893.
17. Boyle A.E., Gill K., Smith B.R., Amit Z. Differential effects of an early housing manipulation on cocaine-induced activity and self-administration in laboratory rats. Pharmacol. Biochem. Behav. 39:1991;269-274.
18. Brain C.L., Griffin G.A. The influences of the sex of litter-mates on body weight and behaviour in rat pups. Anim. Behav. 18:1970;512-516.
19. Carey G. Sibling imitation and contrast effects. Behav. Genet. 16:1986;319-340.
20. Carr G.D., White N.M. Anatomical dissociation of amphetamine's rewarding and aversive effects: an intracranial microinjection study. Psychopharmacology. 89:1986;340-346.
21. Chen C.J., Vandenbergh J.G. Cocaine attenuates puberty acceleration in female house mice. Pharmacol. Biochem. Behav. 44:1993;281-285.
22. Cirulli F., Adriani W., Laviola G. Sexual segregation in infant mice: behavioural and neuroendocrine responses to d-amphetamine administration. Psychopharmacology. 134:1997;140-152.
23. Cirulli F., Gottlieb S.L., Rosenfeld P., Levine S. Maternal factors regulate stress responsiveness in the neonatal rat. Psychobiology. 20:1992;143-152.
24. Cirulli F., Santucci D., Laviola G., Alleva E., Levine S. Behavioral and hormonal responses to stress in the newborn mouse: effects of maternal deprivation and chlordiazepoxide. Develop. Psychobiol. 27:1994;301-316.
25. Clark M.M., Karpluk P., Galef B.G. Jr. Hormonally mediated inheritance of acquired characteristics in Mongolian gerbils. Nature. 364:1993;712-713.
26. Costall B., Jones B.S., Kelly M.E., Naylor R.S., Tomkins D.M. Exploration of mice in a black and white test box: validation as a model of anxiety. Pharmacol. Biochem. Behav. 32:1989;777-785.
27. De Cabo C., Kelly M., Kitchen I., Viveros P. Effects of neonatal sexual isolation on μ-receptor development and nociceptive responses in the rat. Neurosci. Res. Comm. 10:1992;79-86.
28. De Cabo C., Kitchen I., Kelly M., Viveros M.P. Effects of B-funaltrexamine treatment and sexual isolation in the perinatal period on the development of mu-opioid receptors and nociception. Psychoneuroendocrinology. 18:1993;415-424.
29. De Kloet E.R. Steroids, stability and stress. Front Neuroendocrinol. 16:1995;416-425.
30. Deminiere J.M., Piazza P.V., Le Moal M., Simon H. Experimental approach to individual vulnerability to psychostimulant addiction. Neurosci. Biobehav. Rev. 13:1989;141-147.
31. Denenberg V.H., Morton J.R. Infantile stimulation, prepubertal sexual-social interaction, and emotionality. Anim. Behav. 12:1964;11-13.
32. Drickamer L.C. Pre- and post-weaning excretion of puberty-influencing chemosignals in house mice. Develop. Psychobiol. 25:1992;1-16.
33. Dunn J., Plomin R. Why are siblings so different? The significance of differences in sibling experiences within the family. Fam. Proc. 30:1991;271-283.
34. Dyer D.P., Southwick C.H. A possible sensitive period for juvenile socialization in mice. Behav. Biol. 12:1974;551-558.
35. Eaves L. A model for sibling effects in man. Heredity. 36:1976;205-214.
36. Fagen R. Animal play behaviour. New York: Oxford University Press, 1981.
37. Fanselow M.S., Sigmundi R.A. Species-specific danger signals, endogenous analgesia, and defensive behavior. J. Exper. Psychol. (Anim. Behav.). 12:1986;301-309.
38. Gandelman R., Vom Saal F.S., Reinish J.M. Contiguity to male foetuses affects morphology and behaviour of female mice. Nature (Lond.). 266:1977;722-724.
39. Goldfoot D.A., Wallen K., Neff D.A., Mc Brair M.C., Goy R.W. Social influence on the display of sexually dimorphic behavior in rhesus monkeys: isosexual rearing. Arch. Sexual Behav. 13:1984;395-412.
40. Gomendio M. The development of different types of play in gazelles. Implications for the nature and functions of play. Anim. Behav. 36:1988;825-836.
41. Grant E.C., Mackintosh J.H. A comparison of the social postures of some common laboratory rodents. Behaviour. 21:1963;246-259.
42. Gray J.A., Lean J., Keynes A. Infant androgen treatment and adult open-field behaviour: direct effects of injections to siblings. Physiol. Behav. 4:1969;177-181.
43. Greenough WT, Whiters GS, Wallace CS. Morphological changes in the nervous system arising from behavioral experience: what is the evidence that they are involved in learning and memory? In: Squire LR, Lindenlaub E, editors. The biology of memory, symposia medica hoechst, vol. 23. Stuttgart/New York: Schattauder Verlag, 1990. pp. 159-185.
44. Hard E., Larsson K. Dependence of adult mating behavior in male rats on the presence of littermates in infancy. Brain Behav. Evol. 1:1969;405-419.
45. Hayashi S., Kimura T. Effects of exposure to males on sexual preference in female mice. Anim. Behav. 26:1978;290-2951.
46. Henry C., Guegant G., Cador M., Arnauldt E., Arsaut J., Le Moal M., Demotes-Mainard J. Prenatal stress in rats facilitates amphetamine-induced sensitization and induces long-lasting changes in dopamine receptors in the nucleus accumbens. Brain Res. 685:1995;179-186.
47. Hofer M.A. Studies on how early maternal separation produces behavioral change in young rats. Psychosom. Med. 37:1975;245-264.
48. Janus K. Early separation of young rats from the mother and the development of play fighting. Physiol. Behav. 39:1987;471-476.
49. Kehoe P., Boylan C.B. Cocaine-induced effects on isolation stress in neonatal rats. Behav. Neurosci. 106:1992;374-379.
50. Kempermann G., Kuhn H.G., Gage F.H. More hippocampal neurons in adult mice living in an enriched environment. Nature. 386:1997;493-495.
51. Keverne EB. Sex differences in primate social behaviour. In: Haug M, Whalen RE, Aron C, Olsen KL, editors. The development of sex differences and similarities in behavior. Dordrecht: Kluwer Academic, 1993. pp. 227-240.
52. Kitchen I., Crook T.J., Muhammad B.Y., Hill R.G. Evidence that weaning stimulates the developmental expression of a delta-opioid receptor subtype in the rat. Develop. Brain Res. 78:1994;147-150.
53. Knych E.T., Eisenberg R.M. Effect of amphetamine on plasma corticosterone in the conscious rat. Neuroendocrinology. 29:1979;110-118.
54. Krackov S. Sex ratio manipulation in wild house mice: the effect of fetal resorption in relation to the mode of reproduction. Biol. Reprod. 47:1992;541-548.
55. Laviola G. On mouse pups and their lactating dams: behavioral consequences of prenatal exposure to oxazepam and interacting factors. Pharmacol. Biochem. Behav. 54:1996;459-474.
56. Laviola G., Alleva E. Ontogeny of muscimol effects on locomotor activity, habituation, and pain reactivity in mice. Psychopharmacology. 102:1990;41-48.
57. Laviola G., Alleva E. Sibling effects on the behaviour of infant mouse litters (Mus domesticus). J. Comp. Psychol. 109:1995;68-75.
58. Laviola G., De Acetis L., Bignami G., Alleva E. Prenatal oxazepam enhances mouse maternal aggression in the offspring, without modifying acute chlordiazepoxide effects. Neurotoxicol. Teratol. 13:1991;75-81.
59. Laviola G., Dell'Omo G. Precocious weaning and changes in social variables during pre-puberty affect cocaine reinforcing properties in adult mice. Psychobiology. 25:1997;163-170.
60. Laviola G., Dell'Omo G., Alleva E., Bignami G. Ontogeny of cocaine hyperactivity and conditioned place preference in mice. Psychopharmacology. 107:1992;221-228.
61. Laviola G., Dell'Omo G., Chiarotti F., Bignami G. D-amphetamine conditioned place preference in developing mice: relations with changes in activity and stereotypies. Behav. Neurosci. 108:1994;514-524.
62. Laviola G., Loggi G. Sexual segregation in infancy and bi-directional benzodiazepine effects on hot-plate response and neophobia in adult mice. Pharmacol. Biochem. Behav. 42:1992;865-870.
63. Laviola G., Renna G., Bignami G., Cuomo V. Ontogenetic and pharmacological dissociation of various components of locomotor activity and habituation in the rat. Int. J. Develop. Neurosci. 6:1988;431-438.
64. Laviola G., Terranova M.L., Sedowofia K., Clayton R., Manning A. A mouse model of early social interactions after prenatal drug exposure: a genetic investigation. Psychopharmacology. 113:1993;388-394.
65. Liu D., Diorio J., Tannenbaum B., Caldji C., Francis D., Freedman A., Sharma S., Pearson D., Plotsky P.M., Meaney D.M.J. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science. 277:1997;1659-1662.
66. Loggi G., Dell'Omo G., Laviola G. Individual differences in response to psychological stress and chlordiazepoxide in adult mice: relations with changes in early social milieu. Psychobiology. 24:1996;147-153.
67. Lupo Di Prisco C., Lucarini N., Dessi'-Fulgheri F. Testosterone aromatization in rat brain is modulated by social environment. Physiol. Behav. 20:1978;345-348.
68. Mackintosh JH. Behaviour of the house mouse. In: Berry RJ, editor. Biology of the house mouse. Symposia of the Zoological Society of London, vol. 47. London: Academic Press, 1981. pp. 337-365.
69. Maestripieri D. Litter gender composition, food availability, and maternal defence of the young in house mice (Mus domesticus). Behaviour. 116:1991;239-251.
70. Majewska D.M., Harrison N.L., Schwartz R.D., Barker J.L., Paul S.M. Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science. 232:1986;1004-1007.
71. Martin P., Bateson P. The influence of experimentally manipulating a component of weaning on the development of play in domestic cats. Anim. Behav. 33:1985;511-518.
72. Martin P., Caro T.M. On the functions of play and its role in behavioral development. Adv. Study Behav. 15:1985;59-104.
73. Matthews K., Wilkinson L.S., Robbins T.W. Repeated maternal separation of preweanling rats attenuates behavioral responses to primary and conditioned incentives in adulthood. Physiol. Behav. 59:1996;99-107.
74. McClure P.A. Sex-biased litter reduction in food-restricted wood rats (Neotoma floridana). Science. 211:1981;1058-1060.
75. Meaney M.J., Stewart J. A descriptive study of social development in the rat (Rattus norvegicus). Anim. Behav. 29:1981;34-45.
76. Meaney M.J., Stewart J. Environmental factors influencing the affiliative behavior of male and female rats (Rattus norvegicus). Anim. Learn. Behav. 7:1979;397-405.
77. Meaney M.J., Stewart J., Beatty W.W. Sex differences in social play: the socialization of sex roles. Adv. Study Behav. 15:1985;1-58.
78. Mendl M., Paul E.S. Litter composition affects parental care, offspring growth and the development of aggressive behaviour in wild house mice. Behaviour. 116:1991;90-109.
79. Mendl M., Paul E.S. Parental care, sibling relationships and the development of aggressive behaviour in two lines of wild house mice. Behaviour. 116:1991;11-42.
80. Moore C.L. An olfactory basis for maternal discrimination of sex of offspring in rats (Rattus norvegicus). Anim. Behav. 29:1981;383-386.
81. Moore C.L. Maternal contributions to the development of masculine sexual behavior in laboratory rats. Develop. Psychobiol. 17:1984;347-356.
82. Moore C.L., Chadwick-Dias A.M. Behavioral responses of infant rats to maternal licking: variations with age and sex. Develop. Psychobiol. 19:1986;427-438.
83. Moore C.L., Morelli G.A. Mother rats interact differently with male and female offspring. J. Comp. Psychol. 93:1979;677-684.
84. Moore C.L., Power K.L. Variation in maternal care and individual differences in play, exploration and grooming of juvenile Norway rat offspring. Develop. Psychobiol. 25:1992;165-182.
85. Musi B., De Acetis L., Alleva E. Influence of litter gender composition on subsequent maternal behaviour and maternal aggression. Ethology. 95:1993;43-53.
86. Naito H., Tonue T. Sex difference in ultrasound distress call by rat pups. Behav. Brain Res. 25:1987;13-21.
87. Namikas J., Wehmer F. Gender composition of the litter affects behaviour of male mice. Behav. Biol. 23:1978;219-224.
88. Panksepp J., Siviy S., Normansell L. The psychobiology of play: theoretical and methodological perspectives. Neurosci. Biobehav. Rev. 8:1984;465-492.
89. Poole T.B., Fish J. An investigation of playful behaviour in Rattus norvegicus and Mus musculus (Mammalia). J. Zool. Soc. (Lond.). 175:1975;61-71.
90. Poole T.B., Fish J. An investigation of individual, age, and sexual differences in the play of Rattus norvegicus (Mammalia: Rodentia). J. Zool. Lond. 179:1976;249-260.
91. Primus R.J., Kellogg C.K. Gonadal hormones during puberty organize environment-related social interaction in the male rat. Horm. Behav. 24:1990;311-323.
92. Richmond G., Sachs B.D. Maternal discrimination of pup sex in rats. Develop. Psychobiol. 17:1984;87-89.
93. Rosenfeld P., Ekstrand J., Olson E., Suchecki D., Levine S. Maternal regulation of adrenocortical activity in the infant rat: effects of feeding. Develop. Psychobiol. 26:1993;261-277.
94. Rosenfeld P., Suchecki D., Levine S. Multifactorial regulation of the hypothalamic-pituitary-adrenal axis during development. Neurosci. Biobehav. Rev. 16:1992;553-568.
95. Sahakian B., Robbins T.W., Morgan M.J., Iversen S.D. The effects of psychomotor stimulants on stereotypy and locomotor activity in socially-deprived and control rats. Brain Res. 84:1975;195-205.
96. Savageau M.M., Beatty W.W. Gonadectomy and sex differences in the behavioral responses to amphetamine and apomorphine of rats. Pharmacol. Biochem. Behav. 14:1981;17-21.
97. Schreiber H.L., Bell R.W., Kufner M., Villescas R. Maternal behavior: a determinant of amphetamine toxicity in rats. Psychopharmacology. 52:1977;173-176.
98. Sharpe R.M. The influence of the sex of litter-mates on subsequent maternal behaviour in Rattus norvegicus. Anim. Behav. 23:1975;551-559.
99. Sharpe R.M., Morris A., Wyatt A.C. The effect of the sex of litter-mates on the subsequent behaviour and breeding performance of cross-fostered rats. Lab. Anim. 7:1973;51-59.
100. Smith E.S.F. The influence of nutrition and postpartum mating on weaning and subsequent play behaviour of hooded rats. Anim. Behav. 41:1981;513-524.
101. Smotherman WP, Bell RW. Maternal mediation of early experience. In: Bell RW, Smotherman WP, editors. Maternal influences and early behavior. New York: Spectrum Publications, 1980. pp. 201-210.
102. Stanton M.E., Gutierrez Y.R., Levine S. Maternal deprivation potentiates pituitary-adrenal stress responses in infant rats. Behav. Neurosci. 102:1988;692-700.
103. Staton D.M., Solomon R. Microinjections of d-amphetamine into the nucleus accumbens and caudate-putamen differentially affect stereotypy and locomotion in the rat. Physiol. Behav. 12:1984;159-162.
104. Suchecki D., Rosenfeld P., Levine S. Maternal regulation of the hypothalamic-pituitary-adrenal axis in the infant rat: the roles of feeding and stroking. Develop. Brain Res. 75:1993;185-190.
105. Svare B. Maternal aggression in mice: influence of the young. Biobehav. Rev. 1:1977;151-164.
106. Swerdlow R., Koob G.F., Cador M., Lorang M., Hauger R.L. Pituitary-adrenal axis responses to acute amphetamine in the rat. Pharmacol. Biochem. Behav. 45:1993;629-637.
107. Tahakashi L.K., Lore R.K. Play-fighting and the development of agonistic behaviour in male and female rats. Aggress. Behav. 9:1983;217-227.
108. Terranova M.L., Alleva E., Laviola G. Affiliation and neophobia in developing mice prenatally exposed to oxazepam. Behav. Pharmacol. 5:1994;52-60.
109. Terranova M.L., Laviola G. Individual differences in mouse behavioural development: effects of precocious weaning and ongoing sexual segregation. Anim. Behav. 50:1995;1261-1271.
110. Terranova M.L., Laviola G., Alleva E. Ontogeny of amicable social behaviour in the mouse: gender differences and on-going isolation outcomes. Develop. Psychobiol. 26:1993;447-454.
111. Terranova M.L., Laviola G., De Acetis L., Alleva E. A description of the ontogeny of mouse agonistic behavior. J. Comp. Psychol. 112:1998;3-12.
112. Thiels E., Alberts J.R., Cramer C.P. Weaning in rats: II. Pup behavior patterns. Develop. Psychobiol. 23:1990;495-510.
113. Thor D.H., Holloway W.R. Sex and social play in juvenile rats (Rattus norvegicus). J. Comp. Psychol. 98:1984;376-384.
114. Thor D.H., Holloway W.R. Social play soliciting by male and female juvenile rats: effects of neonatal androgenization and sex of cagemates. Behav. Neurosci. 100:1986;275-279.
115. Trivers R.L., Willard D.E. Natural selection of parental ability to vary the sex ratio of offspring. Science. 179:1973;90-92.
116. Van Oortmerssen G.A. Biological significance, genetics and evolutionary origin of variability in behaviour within and between inbred strains of mice (Mus musculus). Behaviour. 38:1971;1-91.
117. Vandenbergh J.G. Coordination of social signals and ovarian function during sexual development. J. Anim. Sci. 67:1989;1841-1847.
118. Vom Saal F.S. Variation in phenotype due to random intrauterine positioning of male and female fetuses in rodents. J. Reprod. Fert. 62:1981;633-650.
119. Walker C., Byers J.A. Heritability of locomotor play in house mice, Mus domesticus. Anim. Behav. 42:1991;891-897.
120. Wender PH. The hyperactive child, adolescent and adult - attention deficit disorder through lifespan. New York: Oxford University Press, 1987.
121. Wolff R.J. Solitary and social play in wild Mus musculus (Mammalia). J. Zool. (Lond.). 195:1981;405-412.
122. Wood R.D., Bannoura M.D., Johansson I.B. Prenatal cocaine exposure: effects on play behavior in the juvenile rat. Neurotoxicol. Teratol. 16:1994;139-144.
123. Zangrossi H., File S.E. Behavioral consequences in animal tests of anxiety and exploration of exposure to cat odor. Brain Res. Bull. 29:1992;381-388.