The influence of natural variations in maternal care on play fighting in the rat
Abstract
Naturally occurring variations in maternal care in the rat influence the sensitivity of offspring to stress in adulthood. The offspring of mothers that show lower levels of pup licking/grooming (i.e., low‐LG mothers) demonstrate enhanced responses to stress and increased anxiety compared to those of high‐LG mothers. Low‐LG offspring are also more sensitive to the influence of environmental enrichment than high‐LG offspring. This study examined play fighting in the juvenile offspring of high‐LG and low‐LG dams in a multiple‐play partners housing environment. Male offspring from low‐LG dams demonstrated a significantly higher frequency of pouncing, pinning and aggressive social grooming than did high‐LG males and high‐LG and low‐LG females. Consistent with earlier reports, male pups engaged in more play fighting than did females and maternal care was associated with differences in play fighting but only in males. Lower levels of stimulation in the form of LG from the dam during perinatal development may thus increase sensitivity for the stimulating effects of play behavior in periadolescence, in part explaining the increased solicitation of play fighting through increased pouncing in the male offspring of the low‐LG mothers. These findings identify a possible influence of variations in maternal care on play fighting and suggest that maternal care in the perinatal period influence social interactions during periadolescence. © 2008 Wiley Periodicals, Inc. Dev Psychobiol 50: 767–776, 2008
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Early-life experience can impact later levels of juvenile play in a sex-dependent manner.
“Early-life experience can also impact later levels of juvenile play in a sex-dependent manner (Parent and Meaney, 2008).”
From Sexually dimorphic role for vasopressin in the development of social play (2014) · cites this paper as Parent and Meaney, 2008
Males are consistently found to play more than females when tested in mixed-sex groups.
“While males are consistently found to play more than females when tested in mix-sex groups (Meaney and Stewart, 1981b; Olesen et al., 2005; Parent and Meaney, 2008)”
From Sexually dimorphic role for vasopressin in the development of social play (2014) · cites this paper as Parent and Meaney, 2008
Males show more social play than females when social play is recorded among cage-mates and under undisturbed conditions.
“Males show more social play than females when social play is recorded among cage-mates and under undisturbed conditions (Poole & Fish, 1976; Meaney & Stewart, 1981; Parent & Meaney, 2008).”
From Sex-specific modulation of juvenile social play by vasopressin (2013) · cites this paper as Parent & Meaney, 2008
The motivation to play can be modified by early experiences mostly derived from the mother.
“While the motivation to play can be modified by early experiences mostly derived from the mother (Parent and Meaney, 2008; Van Hasselt et al., 2012)”
From The rough-and-tumble play of rats as a natural behavior suitable for studying the social brain (2022) · cites this paper as Parent and Meaney, 2008
Cites
Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S., Pearson, D., Plotsky, P. M., & Meaney, M. J. (1997) · Science · doi:10.1126/science.277.5332.1659 · Cited by 3,170 · see citing works
Self-citationMeaney, M. J. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1161 · Cited by 2,708 · see citing works
Self-citationCaldji, C., Tannenbaum, B., Sharma, S., Francis, D., Plotsky, P. M., & Meaney, M. J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.9.5335 · Cited by 1,437 · see citing works
Self-citationChampagne, F. A., Francis, D. D., Mar, A., & Meaney, M. J. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00149-5 · Cited by 1,021 · see citing works
Panksepp, J. (1981) · Developmental Psychobiology · doi:10.1002/dev.420140405 · Cited by 537 · see citing works
The psychobiology of play: Theoretical and methodological perspectives
Panksepp, J., Siviy, S., & Normansell, L. (1984) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(84)90005-8 · Cited by 468 · see citing works
Cameron, N. M., Champagne, F. A., Parent, C., Fish, E. W., Ozaki-Kuroda, K., & Meaney, M. J. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.03.022 · Cited by 320 · see citing works
Self-citationBredy, T. W., Humpartzoomian, R., Cain, D. P., & Meaney, M. J. (2003) · Neuroscience · doi:10.1016/s0306-4522(02)00918-1 · Cited by 248 · see citing works
Self-citationHigley, J. D., Suomi, S. J., & Linnoila, M. V. (1991) · Psychopharmacology · doi:10.1007/bf02244258 · Cited by 221 · see citing works
Intentional communication and social play: how and why animals negotiate and agree to play
Bekoff, M., & Allen, C. (1998) · Cambridge University Press eBooks · doi:10.1017/cbo9780511608575.006 · Cited by 216 · see citing works
Maternal contributions to the development of masculine sexual behavior in laboratory rats
Moore, C. (1984) · Developmental Psychobiology · doi:10.1002/dev.420170403 · Cited by 211 · see citing works
Play fighting of rats in comparative perspective: a schema for neurobehavioral analyses
Pellis, S. M., & Pellis, V. C. (1998) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(97)00071-7 · Cited by 210 · see citing works
High-Frequency Ultrasonic Vocalizations Index Conditioned Pharmacological Reward in Rats
Knutson, B. D., Burgdorf, J. S., & Panksepp, J. (1999) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00337-0 · Cited by 206 · see citing works
Bredy, T. W., Zhang, T. Y., Grant, R. J., Diorio, J., & Meaney, M. J. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03599.x · Cited by 196 · see citing works
Neonatal-androgens influence the social play of prepubescent rats
MEANEY, M. (1981) · Hormones and Behavior · doi:10.1016/0018-506x(81)90028-3 · Cited by 192 · see citing works
Self-citationAn investigation of playful behaviour in <i>Rattus norvegicus</i> and <i>Mus musculus</i> (Mammalia)
Poole, T. B., & Fish, J. (1975) · Journal of Zoology · doi:10.1111/j.1469-7998.1975.tb01391.x · Cited by 188 · see citing works
Social play in juvenile rats: A decade of methodological and experimental research
Thor, D. H., & Holloway, W. R. (1984) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(84)90004-6 · Cited by 176 · see citing works
Lester, H. A. (1977) · Scientific American · doi:10.1038/scientificamerican0277-106 · Cited by 169 · see citing works
Wallen, K. (1996) · Hormones and Behavior · doi:10.1006/hbeh.1996.0042 · Cited by 169 · see citing works
Sex Differences in Social Play: The Socialization of Sex Roles
Meaney, M. J., Stewart, J., & Beatty, W. W. (1985) · Advances in the study of behavior · doi:10.1016/s0065-3454(08)60486-6 · Cited by 168 · see citing works
Self-citationAlbert, F. W., Shchepina, O., Winter, C., Römpler, H., Teupser, D., Palme, R., Ceglarek, U., Kratzsch, J., Sohr, R., Trut, L. N., et al. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.11.010 · Cited by 157 · see citing works
Poole, T. B., & Fish, J. (1976) · Journal of Zoology · doi:10.1111/j.1469-7998.1976.tb02294.x · Cited by 149 · see citing works
Lore, R., & Flannelly, K. (1977) · Scientific American · doi:10.1038/scientificamerican0577-106 · Cited by 147 · cited 1× · see citing works
“…isolation of the animals during this period leads to altered or reduced mating activity (Gerall, Ward, & Gerall, 1967; Gruendal & Arnold, 1969; Hard & Larsson, 1968), reduced affiliative interactions in adulthood (Meaney & Stewart, 1979) and increased agonistic behaviors (Lore & Flannelly, 1977).”
BackgroundMeaney, M. J., Stewart, J., Poulin, P., & McEwen, B. S. (2008) · Neuroendocrinology · doi:10.1159/000123524 · Cited by 144 · see citing works
Self-citationThe sexual differentiation of social play
Meaney, M. J. (1988) · Trends in Neurosciences · doi:10.1016/0166-2236(88)90164-6 · Cited by 136 · see citing works
Self-citationDisruption of the male rat’s sexual behaviour induced by social isolation
Gerall, H. D., Ward, I. L., & Gerall, A. A. (1967) · Animal Behaviour · doi:10.1016/s0003-3472(67)80010-1 · Cited by 136 · see citing works
Prenatal stress feminizes juvenile play patterns in male rats
Ward, I. L., & Stehm, K. E. (1991) · Physiology & Behavior · doi:10.1016/0031-9384(91)90552-y · Cited by 125 · see citing works
Separation from the mother and the development of play in cats
Bateson, P., & Young, M. (1981) · Animal Behaviour · doi:10.1016/s0003-3472(81)80163-7 · Cited by 125 · see citing works
Meaney, M. J., & McEwen, B. S. (1986) · Brain Research · doi:10.1016/0006-8993(86)91492-7 · Cited by 122 · see citing works
Self-citationThe effects of early social isolation on the motivation for social play in juvenile rats
Ikemoto, S., & Panksepp, J. (1992) · Developmental Psychobiology · doi:10.1002/dev.420250404 · Cited by 121 · see citing works
Intermale aggression and dark/light preference in ten inbred mouse strains
Guillot, P.-V., & Chapouthier, G. (1996) · Behavioural Brain Research · doi:10.1016/0166-4328(95)00163-8 · Cited by 117 · see citing works
Play in the domestic cat is enhanced by rationing of the mother during lactation
Bateson, P., Mendl, M., & Feaver, J. (1990) · Animal Behaviour · doi:10.1016/s0003-3472(05)80532-9 · Cited by 109 · see citing works
Early weaning induces anxiety and aggression in adult mice
Kikusui, T., Takeuchi, Y., & Mori, Y. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2003.12.016 · Cited by 103 · see citing works
Moore, C., & Power, K. L. (1992) · Developmental Psychobiology · doi:10.1002/dev.420250303 · Cited by 98 · see citing works
Kikusui, T., Isaka, Y., & Mori, Y. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.03.013 · Cited by 97 · see citing works
Myers, M. M., Brunelli, S. A., Shair, H. N., Squire, J. M., & Hofer, M. A. (1989) · Developmental Psychobiology · doi:10.1002/dev.420220105 · Cited by 96 · see citing works
Meaney, M. J., & Stewart, J. (1979) · Animal Learning & Behavior · doi:10.3758/bf03209692 · Cited by 83 · see citing works
Self-citationAn environmental antiandrogen, vinclozolin, alters the organization of play behavior
Hotchkiss, A. K., Ostby, J. S., Vandenbergh, J. G., & Gray, L. E. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00093-3 · Cited by 77 · see citing works
Effects of early social deprivation on reproductive behavior of male rats
Gruendel, A. D., & Arnold, W. J. (1969) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0026667 · Cited by 76 · see citing works
Energy balance and play in juvenile rats
Siviy, S. M., & Panksepp, J. (1985) · Physiology & Behavior · doi:10.1016/0031-9384(85)90320-8 · Cited by 73 · see citing works
Thor, D. H., & Holloway, W. R. (1986) · Behavioral Neuroscience · doi:10.1037//0735-7044.100.2.275 · Cited by 73 · see citing works
Thor, D. H., & Holloway, W. R. (1986) · Behavioral Neuroscience · doi:10.1037/0735-7044.100.2.275 · Cited by 73 · see citing works
Temporal boundary of the sensitive period for hormonal organization of social play in juvenile rats.
Beatty, W. W., Dodge, A. M., Traylor, K. L., & Meaney, M. J. (1981) · Physiology & Behavior · doi:10.1016/0031-9384(81)90017-2 · Cited by 70 · see citing works
Self-citationMENARD, J., & Hakvoort, R. A. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.10.014 · Cited by 62 · see citing works
Dependence of Adult Mating Behavior in Male Rats on the Presence of Littermates in Infancy
Hȧrd, E., & Larsson, K. (2008) · Brain Behavior and Evolution · doi:10.1159/000125517 · Cited by 61 · see citing works
Differences in maternal behavior of rats and the sociosexual development of the offspring
Birke, L. I. A., & Sadler, D. (1987) · Developmental Psychobiology · doi:10.1002/dev.420200111 · Cited by 58 · see citing works
Effects of neonatal handling and maternal separation on rough‐and‐tumble play in the rat
Arnold, J. L., & Siviy, S. M. (2002) · Developmental Psychobiology · doi:10.1002/dev.10069 · Cited by 55 · see citing works
Goy, R. W., & Wallen, K. (1979) · Psychoneuroendocrinology · doi:10.1016/0306-4530(79)90035-0 · Cited by 54 · see citing works
Bateson, P., Martin, P., & Young, M. (1981) · Physiology & Behavior · doi:10.1016/0031-9384(81)90051-2 · Cited by 48 · see citing works
Shimozuru, M., Kodama, Y., Iwasa, T., Kikusui, T., Takeuchi, Y., & Mori, Y. (2007) · Developmental Psychobiology · doi:10.1002/dev.20202 · Cited by 43 · see citing works
The Influence of Early Weaning on Aggressive Behavior in Mice
Nakamura, K., Kikusui, T., Takeuchi, Y., & Mori, Y. (2003) · Journal of Veterinary Medical Science · doi:10.1292/jvms.65.1347 · Cited by 29 · see citing works
Development of Play Behavior in Neonatally Undernourished Rats
Loranca, A., Torrero, C., & Salas, M. (1999) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00235-2 · Cited by 27 · see citing works
Predatory aggression in the mink (Mustela vison): Roles of serotonin and food satiation
Nikulina, E. M., & Popova, N. K. (1988) · Aggressive Behavior · doi:10.1002/1098-2337(1988)14:2 · Cited by 12 · see citing works
Ontogeny of animal play behaviour: Bimodal age schedules
Fagen, R. M. (1980) · Animal Behaviour · doi:10.1016/s0003-3472(80)80120-5
Flagged first, then by citations
Research works printed but not linked: 2
- Burghardt G. M., 1998, Encyclopedia of comparative psychology, 725
- Wallen K., 1977, Primate bio‐social development, 439
Cited by
Sorted by citations
Feldman, R., Gordon, I., Schneiderman, I., Weisman, O., & Zagoory-Sharon, O. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.01.013 · Cited by 638 · see citing works
Daskalakis, N. P., Bagot, R. C., Parker, K. J., Vinkers, C. H., & de Kloet, E. R. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.06.008 · Cited by 579 · see citing works
Beyond allostatic load: Rethinking the role of stress in regulating human development
Ellis, B. J., & Del Giudice, M. (2014) · Development and Psychopathology · doi:10.1017/s0954579413000849 · Cited by 290 · see citing works
Maternal high fat diet consumption during the perinatal period programs offspring behavior
Sullivan, E. L., Nousen, E. K., & Chamlou, K. A. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2012.07.014 · Cited by 217 · see citing works
Sex-specific modulation of juvenile social play by vasopressin
Veenema, A. H., Bredewold, R., & De Vries, G. J. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.06.002 · Cited by 166 · see citing works
“Males show more social play than females when social play is recorded among cage-mates and under undisturbed conditions (Poole & Fish, 1976; Meaney & Stewart, 1981; Parent & Meaney, 2008).”
BackgroundBehavioural and Neurochemical Consequences of Early Weaning in Rodents
Kikusui, T., & Mori, Y. (2009) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2009.01837.x · Cited by 158 · see citing works
Peña, C. J., Neugut, Y. D., Calarco, C. A., & Champagne, F. A. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12479 · Cited by 120 · see citing works
Beery, A. K., McEwen, L. M., MacIsaac, J. L., Francis, D. D., & Kobor, M. S. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.05.022 · Cited by 81 · see citing works
Characterization of juvenile play in rats: importance of sex of self and sex of partner
Argue, K. J., & McCarthy, M. M. (2015) · Biology of Sex Differences · doi:10.1186/s13293-015-0034-x · Cited by 71 · see citing works
Himmler, S. M., Modlinska, K., Stryjek, R., Himmler, B. T., Pisula, W., & Pellis, S. M. (2014) · Journal of Comparative Psychology · doi:10.1037/a0036104 · Cited by 67 · see citing works
Sexually dimorphic role for vasopressin in the development of social play
Paul, M. J., Terranova, J. I., Probst, C. K., Murray, E. K., Ismail, N. I., & de Vries, G. J. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00058 · Cited by 51 · see citing works
“Early-life experience can also impact later levels of juvenile play in a sex-dependent manner (Parent and Meaney, 2008).”
BackgroundArgue, K. J., VanRyzin, J. W., Falvo, D. J., Whitaker, A. R., Yu, S. J., & McCarthy, M. M. (2017) · eneuro · doi:10.1523/eneuro.0344-16.2017 · Cited by 47 · see citing works
Raza, S., Harker, A., Richards, S., Kolb, B., & Gibb, R. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.12.055 · Cited by 37 · see citing works
Barrett, C. E., Modi, M. E., Zhang, B. C., Walum, H., Inoue, K., & Young, L. J. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.05.041 · Cited by 34 · see citing works
Play matters: the surprising relationship between juvenile playfulness and anxiety in later life
Richter, S. H., Kästner, N., Kriwet, M., Kaiser, S., & Sachser, N. (2016) · Animal Behaviour · doi:10.1016/j.anbehav.2016.02.003 · Cited by 33 · see citing works
Cutuli, D., Berretta, E., Caporali, P., Sampedro-Piquero, P., De Bartolo, P., Laricchiuta, D., Gelfo, F., Pesoli, M., Foti, F., Farioli Vecchioli, S., et al. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.02.015 · Cited by 30 · see citing works
The rough-and-tumble play of rats as a natural behavior suitable for studying the social brain
Pellis, S. M., Pellis, V. C., Ham, J. R., & Achterberg, E. J. M. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.1033999 · Cited by 29 · see citing works
“While themotivation to play can be modified by early experiences mostly derived from the mother (Parent and Meaney, 2008; Van Hasselt et al., 2012), once play begins at around 17 days of age, it takes about 10 days for the repertoire of tactics used during play to mature fully and this maturation appears to be little…”
BackgroundMaternal Touch Moderates Sex Differences in Juvenile Social Play Behavior
Edelmann, M. N., Demers, C. H., & Auger, A. P. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057396 · Cited by 27 · see citing works
Sex differences in juvenile play behavior differ among rat strains
Northcutt, K. V., & Nwankwo, V. C. (2018) · Developmental Psychobiology · doi:10.1002/dev.21760 · Cited by 20 · see citing works
Feng, T., An, S., Kinden, R., Zhang, X., Jia, R., & Tai, F. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.02.038 · Cited by 18 · see citing works
Orsucci, I. C., Becker, K. D., Ham, J. R., Lee, J. D. A., Bowden, S. M., & Veenema, A. H. (2025) · Physiology & Behavior · doi:10.1016/j.physbeh.2025.115080 · Cited by 3 · see citing works
Partner Choice and Context‐Dependent Sex Differences in Rat Rough‐and‐Tumble Play
Ham, J. R., Pellis, S. M., & McDonald, R. J. (2026) · European Journal of Neuroscience · doi:10.1111/ejn.70426 · Cited by 1 · see citing works
“…of male play, that drives the sex effect (Achterberg et al. 2024; Argue and McCarthy 2015; Northcutt and Nwankwo 2018; Orsucci et al. 2025; Parent and Meaney 2008; Pellis et al. 1997; Siviy 2018; Siviy et al. 1990, 2003, 2017; Siviy et al. 2017; Siviy and Panksepp 1987; Thor and Holloway…”
Ham, J. R., Iwaniuk, A. N., & Pellis, S. M. (2026) · Behavioural Brain Research · doi:10.1016/j.bbr.2026.116198 · Cited by 1 · see citing works
- Authors
- Parent, C. I., & Meaney, M. J.
- Affiliations
- Douglas Mental Health University Institute (CA)
- Corresponding author
- Meaney, Michael J.
- Venue
- Developmental Psychobiology
- Publisher
- Wiley
- Published
- 2008-10-07
- Volume
- 50
- Issue
- 8
- Pages
- 767-776
- ISSN
- 0012-1630 (ISSN-L)
- 1098-2302
- OpenAlex
- W2049175274
- Semantic Scholar
- 0458098e1e796d62a71065305985c713be6fe2a9
- Cited by
- 175
- References
- 55
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 6 · 2023: 5 · 2022: 3 · 2021: 6 · 2020: 39 · 2019: 3 · 2018: 9 · 2017: 8 · 2016: 15 · 2015: 17 · 2014: 11 · 2013: 11 · 2012: 8
- FWCI
- 12.57
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Developmental Psychobiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
- Keywords
- maternal care, play fighting, rat offspring, sex differences, periadolescence, social behavior, perinatal development, environmental enrichment, stress sensitivity, anxiety
- MeSH terms
- Aggression, Agonistic Behavior, Animals, Animals, Newborn, Arousal, Female, Grooming, Male, Maternal Behavior, Play and Playthings, Pregnancy, Sex Factors, Social Environment, Rats, Long-Evans, Rats
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