Juvenile social play and the development of socio-cognitive skills in male rats: Does everyone benefit?
Open accessAbstract
Social play during early life is important for brain and behavioral development. In rats, rough-and-tumble play (RTP)-their main form of social play-enhances socio-cognitive flexibility and refines the medial prefrontal cortex (mPFC) through dendritic pruning. While restricting RTP impairs these outcomes, it remains unclear whether all individuals benefit equally when play opportunities are abundant. To test this, we reared 54 male rats in large social groups from weaning to adulthood, ensuring rich RTP experiences. Despite these conditions, 20.4% later escalated playful encounters into aggression, indicating reduced social competence. These "incompetent" rats did not differ in play frequency or defensive tactics, suggesting similar juvenile RTP exposure. However, their mPFC layer III pyramidal neurons showed larger dendritic arbors and greater distal spine density, consistent with reduced pruning. These neural and behavioral traits parallel those in play-deprived rats, indicating that some individuals fail to gain RTP's socio-cognitive benefits. This variation mirrors patterns in humans, where not all children benefit equally from play-based interventions, underscoring the need to identify early-life predictors and neural mechanisms underlying individual differences.
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Fitting Linear Mixed-Effects Models Using <b>lme4</b>
Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015) · Journal of Statistical Software · doi:10.18637/jss.v067.i01 · Cited by 86,835 · see citing works
Preschool Program Improves Cognitive Control
Diamond, A., Barnett, W. S., Thomas, J., & Munro, S. (2007) · Science · doi:10.1126/science.1151148 · Cited by 2,025 · see citing works
The power of play: A pediatric role in enhancing development in young children
Yogman, M., Garner, A., Hutchinson, J., Hirsh-Pasek, K., Golinkoff, R. M., COMMITTEE ON PSYCHOSOCIAL ASPECTS OF CHILD AND FAMILY HEALTH, & COUNCIL ON COMMUNICATIONS AND MEDIA (2018) · Pediatrics · doi:10.1542/peds.2018-2058 · Cited by 758 · see citing works
A method for vibratome sectioning of Golgi–Cox stained whole rat brain
Gibb, R. L., & Kolb, B. E. (1998) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(97)00163-5 · Cited by 618 · see citing works
The ontogeny of behaviour in the albino rat
Bolles, R. C., & Woods, P. J. (1964) · Animal Behaviour · doi:10.1016/0003-3472(64)90062-4 · Cited by 570 · see citing works
Aggressive behavior in the rat
Blanchard, R. J., & Blanchard, D. C. (1977) · Behavioral Biology · doi:10.1016/s0091-6773(77)90308-x · Cited by 554 · see citing works
Nijhof, S. L., Vinkers, C. H., van Geelen, S. M., Duijff, S. N., Achterberg, E. J. M., van der Net, J., Veltkamp, R. C., Grootenhuis, M. A., van de Putte, E. M., Hillegers, M. H. J., et al. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.09.024 · Cited by 363 · see citing works
Pellis, S. M., & Pellis, V. C. (1990) · Developmental Psychobiology · doi:10.1002/dev.420230303 · Cited by 255 · see citing works
Self-citationUsing the tube test to measure social hierarchy in mice
Fan, Z., Zhu, H. L., Zhou, T., Wang, S., Wu, Y., & Hu, H. (2019) · Nature Protocols · doi:10.1038/s41596-018-0116-4 · Cited by 227 · see citing works
Bell, H. C., Pellis, S. M., & Kolb, B. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.09.029 · Cited by 217 · see citing works
Self-citationBaarendse, P. J. J., Counotte, D. S., O'Donnell, P., & Vanderschuren, L. J. M. J. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.47 · Cited by 206 · see citing works
Elementary-school children's rough-and-tumble play and social competence.
Pellegrini, A. D. (1988) · Developmental Psychology · doi:10.1037/0012-1649.24.6.802 · Cited by 203 · see citing works
Vanderschuren, L. J. M. J., & Trezza, V. (2013) · Current Topics in Behavioral Neurosciences · doi:10.1007/978-3-662-45758-0_268 · Cited by 200 · see citing works
Veenema, A. H., & Neumann, I. D. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.10.017 · Cited by 191 · see citing works
Thomas, D. A., Takahashi, L. K., & Barfield, R. J. (1983) · Journal of Comparative Psychology · doi:10.1037/0735-7036.97.3.201 · Cited by 187 · see citing works
Developmental Benefits of Play for Children
Barnett, L. (1990) · Journal of Leisure Research · doi:10.1080/00222216.1990.11969821 · Cited by 186 · see citing works
Sensory modulation of juvenile play in rats
Siviy, S. M., & Panksepp, J. (1987) · Developmental Psychobiology · doi:10.1002/dev.420200108 · Cited by 181 · see citing works
The influence of natural variations in maternal care on play fighting in the rat
Parent, C. I., & Meaney, M. J. (2008) · Developmental Psychobiology · doi:10.1002/dev.20342 · Cited by 175 · see citing works
What is play fighting and what is it good for?
Pellis, S. M., & Pellis, V. C. (2017) · Learning & Behavior · doi:10.3758/s13420-017-0264-3 · Cited by 160 · see citing works
Self-citationComparison of behavioural development in socially isolated and grouped rats
Baenninger, L. P. (1967) · Animal Behaviour · doi:10.1016/0003-3472(67)90018-8 · Cited by 139 · see citing works
The role of the medial prefrontal cortex in the play fighting of rats.
Bell, H. C., McCaffrey, D. R., Forgie, M. L., Kolb, B., & Pellis, S. M. (2009) · Behavioral Neuroscience · doi:10.1037/a0017617 · Cited by 114 · see citing works
Self-citationA brain motivated to play: insights into the neurobiology of playfulness
Siviy, S. M. (2016) · Behaviour · doi:10.1163/1568539x-00003349 · Cited by 113 · see citing works
Structure of Rat Ultrasonic Vocalizations and Its Relevance to Behavior
Takahashi, N., Kashino, M., & Hironaka, N. (2010) · PLoS ONE · doi:10.1371/journal.pone.0014115 · Cited by 111 · see citing works
Developmental analyses of social play behavior in juvenile rats
Thor, D. H., & Holloway, W. R. (1984) · Bulletin of the Psychonomic Society · doi:10.3758/bf03333916 · Cited by 105 · see citing works
Uptight and Laid-Back Monkeys: Individual Differences in the Response to Social Challenges
Suomi, S. J. (1991) · The MIT Press eBooks · doi:10.7551/mitpress/5415.003.0005 · Cited by 94 · see citing works
Structure-function interface in the analysis of play fighting
Pellis, S. M., & Pellis, V. C. (1998) · Cambridge University Press eBooks · doi:10.1017/cbo9780511608575.007 · Cited by 91 · see citing works
Self-citationSchneider, P., Bindila, L., Schmahl, C., Bohus, M., Meyer-Lindenberg, A., Lutz, B., Spanagel, R., & Schneider, M. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00203 · Cited by 89 · see citing works
Manifestations of domination: Assessments of social dominance in rodents
Fulenwider, H. D., Caruso, M. A., & Ryabinin, A. E. (2021) · Genes Brain & Behavior · doi:10.1111/gbb.12731 · Cited by 82 · see citing works
Peering into the Dynamics of Social Interactions: Measuring Play Fighting in Rats
Himmler, B. T., Pellis, V. C., & Pellis, S. M. (2013) · Journal of Visualized Experiments · doi:10.3791/4288 · Cited by 81 · see citing works
Self-citationHimmler, B. T., Pellis, S. M., & Kolb, B. E. (2013) · Neuroscience Letters · doi:10.1016/j.neulet.2013.09.061 · Cited by 79 · see citing works
Self-citationPlay fighting and the development of the social brain: The rat’s tale
Pellis, S. M., Pellis, V. C., Ham, J. R., & Stark, R. A. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105037 · Cited by 76 · see citing works
Self-citationThe development of “roughness” in the play fighting of rats: A Laban Movement Analysis perspective
Foroud, A., & Pellis, S. M. (2002) · Developmental Psychobiology · doi:10.1002/dev.10088 · Cited by 72 · see citing works
Self-citationFair play and its connection with social tolerance, reciprocity and the ethology of peace
Palagi, E., Cordoni, G., Demuru, E., & Bekoff, M. (2016) · Behaviour · doi:10.1163/1568539x-00003336 · Cited by 72 · see citing works
Cologon, K. (2020) · Research Papers in Education · doi:10.1080/02671522.2020.1849372 · Cited by 72 · see citing works
Burleson, C. A., Pedersen, R. W., Seddighi, S., DeBusk, L. E., Burghardt, G. M., & Cooper, M. A. (2016) · Behavioral Neuroscience · doi:10.1037/bne0000148 · Cited by 69 · see citing works
Playful defensive responses in adult male rats depend on the status of the unfamiliar opponent
Smith, L. K., Fantella, S.-L. N., & Pellis, S. M. (1999) · Aggressive Behavior · doi:10.1002/(sici)1098-2337(1999)25:2 · Cited by 65 · see citing works
Self-citationHewes, J. (2014) · Children · doi:10.3390/children1030280 · Cited by 58 · see citing works
Play, variation in play and the development of socially competent rats
Himmler, S. M., Himmler, B. T., Pellis, V. C., & Pellis, S. M. (2016) · Behaviour · doi:10.1163/1568539x-00003307 · Cited by 57 · see citing works
Self-citationKisko, T. M., Euston, D. R., & Pellis, S. M. (2015) · Behavioural Processes · doi:10.1016/j.beproc.2015.01.016 · Cited by 57 · see citing works
Self-citationThe neurobiology of social play behaviour: Past, present and future
Achterberg, E. J. M., & Vanderschuren, L. J. M. J. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105319 · Cited by 56 · see citing works
Promoting Executive Function Skills in Preschoolers Using a Play-Based Program
Gibb, R. L., Coelho, L. A., van Rootselaar, N. A., Halliwell, C., MacKinnon, M., Plomp, I., & Gonzalez, C. L. R. (2021) · Frontiers in Psychology · doi:10.3389/fpsyg.2021.720225 · Cited by 55 · see citing works
Bijlsma, A., Omrani, A., Spoelder, M., Verharen, J. P. H., Bauer, L., Cornelis, C., de Zwart, B., van Dorland, R., Vanderschuren, L. J. M. J., & Wierenga, C. J. (2022) · The Journal of Neuroscience · doi:10.1523/jneurosci.0524-22.2022 · Cited by 54 · see citing works
Avoiding escalation from play to aggression in adult male rats: The role of ultrasonic calls
Burke, C. J., Kisko, T. M., Pellis, S. M., & Euston, D. R. (2017) · Behavioural Processes · doi:10.1016/j.beproc.2017.09.014 · Cited by 48 · see citing works
Self-citationBehavioral Variability in the Service of Constancy
Bell, H. C. (2014) · International Journal of Comparative Psychology · doi:10.46867/ijcp.2014.27.02.02 · Cited by 45 · see citing works
Kentrop, J., Smid, C. R., Achterberg, E. J. M., van IJzendoorn, M. H., Bakermans-Kranenburg, M. J., Joëls, M., & van der Veen, R. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00193 · Cited by 41 · see citing works
Chapter 24 Social behaviour and the prefrontal cortex
de Bruin, J. P. C. (1991) · Progress in brain research · doi:10.1016/s0079-6123(08)62696-5 · Cited by 41 · see citing works
Schneider, P., Hannusch, C., Schmahl, C., Bohus, M., Spanagel, R., & Schneider, M. (2014) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2013.04.004 · Cited by 39 · see citing works
Adolescent social rejection alters pain processing in a CB1 receptor dependent manner
Schneider, P., Pätz, M., Spanagel, R., & Schneider, M. (2016) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2016.04.007 · Cited by 37 · see citing works
Developmental origins of sex differences in the neural circuitry of play
VanRyzin, J. W., Marquardt, A. E., & McCarthy, M. M. (2020) · International Journal of Play · doi:10.1080/21594937.2020.1723370 · Cited by 34 · see citing works
Measuring play fighting in rats: a multilayered approach
Pellis, S. M., Pellis, V. C., Burke, C. J., Stark, R. A., Ham, J. R., Euston, D. R., & Achterberg, E. J. M. (2022) · Current Protocols · doi:10.1002/cpz1.337 · Cited by 33 · see citing works
Self-citationDomestication and the Role of Social Play on the Development of Sociocognitive Skills in Rats
Pellis, S. M., Pellis, V. C., Himmler, B. T., Modlinska, K., Stryjek, R., Kolb, B., & Pisula, W. (2019) · International Journal of Comparative Psychology · doi:10.46867/ijcp.2019.32.00.17 · Cited by 32 · see citing works
Self-citationStark, R., & Pellis, S. M. (2020) · International Journal of Play · doi:10.1080/21594937.2020.1720142 · Cited by 32 · see citing works
Self-citationMarquardt, A. E., VanRyzin, J. W., Fuquen, R. W., & McCarthy, M. M. (2023) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.1076765 · Cited by 31 · see citing works
Pellis, S. M., Williams, L. A., & Pellis, V. C. (2017) · International Journal of Comparative Psychology · doi:10.46867/ijcp.2017.30.00.14 · Cited by 29 · see citing works
Self-citationThe 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
Self-citationStark, R. A., Brinkman, B., Gibb, R. L., Iwaniuk, A. N., & Pellis, S. M. (2022) · Behavioural Brain Research · doi:10.1016/j.bbr.2022.114222 · Cited by 23 · see citing works
Self-citationHam, J., & Pellis, S. (2023) · Animal Behavior and Cognition · doi:10.26451/abc.10.04.02.2023 · Cited by 22 · see citing works
Self-citationStark, R. A. M., Ramkumar, R., & Pellis, S. M. (2021) · International Journal of Comparative Psychology · doi:10.46867/ijcp.2021.34.5592 · Cited by 20 · see citing works
Self-citationMultiple benefits of juvenile play: A ground squirrel's perspective
Nunes, S., & Montemayor, M. P. M. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105099 · Cited by 19 · see citing works
Ham, J. R., Szabo, M., Annor‐Bediako, J., Stark, R. A., Iwaniuk, A. N., & Pellis, S. M. (2024) · Developmental Psychobiology · doi:10.1002/dev.22456 · Cited by 18 · see citing works
Self-citationStark, R. A., & Pellis, S. M. (2021) · Behavioural Processes · doi:10.1016/j.beproc.2021.104492 · Cited by 17 · see citing works
Self-citationSocial play behavior shapes the development of prefrontal inhibition in a region-specific manner
Bijlsma, A., Vanderschuren, L. J. M. J., & Wierenga, C. J. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhad212 · Cited by 16 · see citing works
Pellis, S. M., Pellis, V. C., & Ham, J. R. (2024) · Frontiers in Ethology · doi:10.3389/fetho.2024.1362052 · Cited by 15 · see citing works
Self-citationPlay partner preferences among groups of unfamiliar juvenile male rats
Ham, J. R., & Pellis, S. M. (2024) · Scientific Reports · doi:10.1038/s41598-024-66988-w · Cited by 13 · see citing works
Self-citationPredatory 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
Grange, D. A., Hood, K. E., Ikeda, S. C., Reed, C. L., Jones, B. C., & Block, M. L. (1997) · Aggressive Behavior · doi:10.1002/(sici)1098-2337(1997)23:2 · Cited by 12 · see citing works
Brinkman, B., Ngwenya, A., Fjordbotten, K., Stephen, O., & Iwaniuk, A. N. (2022) · Brain Structure and Function · doi:10.1007/s00429-022-02528-4 · Cited by 7 · see citing works
Self-citationHam, J. R., & Pellis, S. M. (2025) · iScience · doi:10.1016/j.isci.2025.112562 · Cited by 5 · see citing works
Self-citationJuvenile male rats form preferences based on strain when playing in groups but not in pairs
Ham, J. R., Jaiswal, D., Waner-Mariquito, R., Pellis, S. M., & Achterberg, E. J. M. (2025) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2025.1617178 · Cited by 5 · see citing works
Self-citationEscribano-Cadena, Y., Tendilla‐Beltrán, H., & Flores, G. (2025) · Neuroscience · doi:10.1016/j.neuroscience.2025.07.041 · Cited by 2 · see citing works
Homing and feral pigeons differ in hippocampal formation neuron size: a Golgi study
Brinkman, B. E., Irvine, S. D., Ham, J. R., & Iwaniuk, A. N. (2025) · Brain Structure and Function · doi:10.1007/s00429-025-03030-3 · Cited by 2 · see citing works
Self-citationBailey (1999) · doi:10.1002/(sici)1098-2302(199909)35:2
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Evaluating the play fighting of rats: A sociological perspective
Ham, J. R., Pellis, S. M., Pellis, V. C., & Achterberg, E. J. M. (2026) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2026.110836
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- Authors
- Ham, J. R., Iwaniuk, A. N., & Pellis, S. M.
- Affiliations
- University of Lethbridge (CA)
- Corresponding author
- Ham, Jackson R.
- Venue
- Behavioural Brain Research
- Publisher
- Elsevier BV
- Published
- 2026-06
- Volume
- 508
- Pages
- 116198
- ISSN
- 0166-4328 (ISSN-L)
- OpenAlex
- W7153500257
- Semantic Scholar
- 7f9ac9b07fab91af7d1f8cae5ea927bdb8fa885f
- Cited by
- 1
- References
- 77
- Citations by year
- 2026: 1
- FWCI
- 8.74
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Behavioural Brain Research (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- Canada Research Chairs Program (CRC-2018\u201300023)
- Canada Foundation for Innovation (ANI: 30215)
- Natural Sciences and Engineering Research Council of Canada (2024\u201303978, 2018\u201303706)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- rough-and-tumble play, social play, medial prefrontal cortex, dendritic pruning, individual differences, social aggression, social competence, dendritic spine density, play deprivation
- MeSH terms
- Social Cognition, Cognitive Flexibility, Aggression, Animals, Behavior, Animal, Cognition, Dendrites, Individuality, Male, Neuronal Plasticity, Play and Playthings, Social Behavior, Prefrontal Cortex, Pyramidal Cells, Rats, Long-Evans, Rats, Social Skills
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