In search of the neurobiological substrates for social playfulness in mammalian brains
Abstract
Play behavior is a fundamental and intrinsic neurobehavioral process in the mammalian brain. Using rough-and-tumble play in the juvenile rat as a model system to study mammalian playfulness, some of the relevant neurobiological substrates for this behavior have been identified, and in this review this progress. A primary-process executive circuit for play in the rat that includes thalamic intralaminar nuclei, frontal cortex and striatum can be gleaned from these data. Other neural areas that may interact with this putative circuit include amygdala, ventral hypothalamus, periaqueductal gray (PAG), and deep tectum, as well as ascending dopamine systems which participate in all types of seeking urges. At the neurochemical level, considerable evidence points to specific cholinergic and dopaminergic controls, but also endogenous opioids and cannabinoids as having a positive modulatory influence over playfulness, with all neuropeptides known to have aversive effects to reduce play. Monoamines such as norepinephrine and serotonin certainly modulate play, but they influence all psychobehavioral systems, suggesting non-specific effects. We proceed to discuss how increased insights into the neurobiological mechanisms of play can inform our understanding of normal and abnormal childhood development.
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Rough-and-tumble play in rats involves competition to gain access to the partner's nape of the neck, which is nuzzled with the snout if contacted.
“As shown in Figure 1, RTP in rats involves competition to gain access to the partner's nape of the neck, which is nuzzled with the snout if contacted (Pellis and Pellis, 1987; Siviy and Panksepp, 2011).”
From The rough-and-tumble play of rats as a natural behavior suitable for studying the social brain (2022) · cites this paper as Siviy and Panksepp, 2011
Laboratory rats have been an important model species for studying the neurobiology of rough-and-tumble play.
“Laboratory rats have been an important model species with which to study the neurobiology of RTP (Siviy and Panksepp, 2011; Siviy, 2016; Vanderschuren et al., 2016).”
From The rough-and-tumble play of rats as a natural behavior suitable for studying the social brain (2022) · cites this paper as Siviy and Panksepp, 2011
Cites
What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience?
Berridge, K. C., & Robinson, T. E. (1998) · Brain Research Reviews · doi:10.1016/s0165-0173(98)00019-8 · Cited by 4,127 · see citing works
The molecular logic of endocannabinoid signalling
Piomelli, D. (2003) · Nature Reviews Neuroscience · doi:10.1038/nrn1247 · Cited by 1,957 · see citing works
The Genesis of Animal Play: Testing the Limits
Burghardt, G. M. (2005) · doi:10.7551/mitpress/3229.001.0001 · Cited by 1,094 · see citing works
Toward a general psychobiological theory of emotions
Panksepp, J. (1982) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00012759 · Cited by 999 · see citing works
The Neuropsychopharmacology of Fronto-Executive Function: Monoaminergic Modulation
Robbins, T. W., & Arnsten, A. F. T. (2009) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135535 · Cited by 957 · see citing works
Burgdorf, J., Kroes, R. A., Moskal, J. R., Pfaus, J. G., Brudzynski, S. M., & Panksepp, J. (2008) · Journal of Comparative Psychology · doi:10.1037/a0012889 · Cited by 469 · see citing works
Self-citationThe 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
Self-citationRole of dopamine in anticipatory and consummatory aspects of sexual behavior in the male rat
Pfaus, J. G., & Phillips, A. G. (1991) · Behavioral Neuroscience · doi:10.1037/0735-7044.105.5.727 · Cited by 320 · see citing works
Thiel, K. J., Okun, A. C., & Neisewander, J. L. (2008) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2008.02.013 · Cited by 164 · 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
Expression of c-fos gene activation during rough and tumble play in juvenile rats
Gordon, N. S., Kollack-Walker, S., Akil, H., & Panksepp, J. (2002) · Brain Research Bulletin · doi:10.1016/s0361-9230(01)00762-6 · Cited by 103 · see citing works
Self-citationD₂ dopamine receptor involvement in the rough-and-tumble play behavior of juvenile rats.
Siviy, S. M., Fleischhauer, A. E., Kerrigan, L. A., & Kuhlman, S. J. (1996) · Behavioral Neuroscience · doi:10.1037/0735-7044.110.5.1168 · Cited by 47 · see citing works
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Toward a second-person neuroscience
Schilbach, L., Timmermans, B., Reddy, V., Costall, A., Bente, G., Schlicht, T., & Vogeley, K. (2013) · Behavioral and Brain Sciences · doi:10.1017/s0140525x12000660 · Cited by 1,510 · see citing works
Social re-orientation and brain development: An expanded and updated view
Nelson, E. E., Jarcho, J. M., & Guyer, A. E. (2016) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2015.12.008 · Cited by 447 · see citing works
The neurobiology of social play and its rewarding value in rats
Vanderschuren, L. J. M. J., Achterberg, E. J. M., & Trezza, V. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.07.025 · Cited by 329 · see citing works
Burke, A. R., McCormick, C. M., Pellis, S. M., & Lukkes, J. L. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.01.018 · Cited by 225 · see citing works
Endocannabinoids in Amygdala and Nucleus Accumbens Mediate Social Play Reward in Adolescent Rats
Trezza, V., Damsteegt, R., Manduca, A., Petrosino, S., Van Kerkhof, L. W. M., Pasterkamp, R. J., Zhou, Y., Campolongo, P., Cuomo, V., Di Marzo, V., et al. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.0114-12.2012 · Cited by 190 · see citing works
Individual Differences and Social Influences on the Neurobehavioral Pharmacology of Abused Drugs
Bardo, M. T., Neisewander, J. L., & Kelly, T. H. (2013) · Pharmacological Reviews · doi:10.1124/pr.111.005124 · Cited by 167 · see citing works
van Kerkhof, L. W., Damsteegt, R., Trezza, V., Voorn, P., & Vanderschuren, L. J. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.83 · Cited by 161 · see citing works
Convergence of Sex Differences and the Neuroimmune System in Autism Spectrum Disorder
McCarthy, M. M., & Wright, C. L. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.10.004 · Cited by 158 · see citing works
Bredewold, R., Smith, C. J. W., Dumais, K. M., & Veenema, A. H. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00216 · Cited by 157 · see citing works
Disrupted social development enhances the motivation for cocaine in rats
Baarendse, P. J. J., Limpens, J. H. W., & Vanderschuren, L. J. M. J. (2014) · Psychopharmacology · doi:10.1007/s00213-013-3362-8 · Cited by 87 · see citing works
Cellular activation in limbic brain systems during social play behaviour in rats
van Kerkhof, L. W. M., Trezza, V., Mulder, T., Gao, P., Voorn, P., & Vanderschuren, L. J. M. J. (2013) · Brain Structure and Function · doi:10.1007/s00429-013-0558-y · Cited by 83 · see citing works
Play 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
Ku, K. M., Weir, R. K., Silverman, J. L., Berman, R. F., & Bauman, M. D. (2016) · PLOS ONE · doi:10.1371/journal.pone.0158150 · Cited by 74 · 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
Achterberg, E. J. M., van Kerkhof, L. W. M., Damsteegt, R., Trezza, V., & Vanderschuren, L. J. M. J. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.2945-14.2015 · Cited by 58 · see citing works
Raza, S., Himmler, B. T., Himmler, S. M., Harker, A., Kolb, B., Pellis, S. M., & Gibb, R. (2015) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000169 · Cited by 37 · 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
“Laboratory rats have been an important model species with which to study the neurobiology of RTP (Siviy and Panksepp, 2011; Siviy, 2016; Vanderschuren et al., 2016).”
BackgroundPinning in the Play Fighting of Rats: A Comparative Perspective With Methodological Recommendations
Himmler, S. M., Himmler, B. T., Stryjek, R., Modlińska, K., Pisula, W., & Pellis, S. M. (2016) · International Journal of Comparative Psychology · doi:10.46867/ijcp.2016.29.00.06 · Cited by 19 · see citing works
Turano, A., McAuley, E. M., Muench, M. C., & Schwarz, J. M. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113449 · Cited by 11 · 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
- Authors
- Siviy, S. M., & Panksepp, J.
- Affiliations
- Gettysburg College (US)
- Washington State University (US)
- Corresponding author
- Siviy, Stephen M.
- ORCID
- Siviy, Stephen M.
- Venue
- Neuroscience & Biobehavioral Reviews
- Publisher
- Elsevier BV
- Published
- 2011-10
- Volume
- 35
- Issue
- 9
- Pages
- 1821-1830
- ISSN
- 0149-7634 (ISSN-L)
- OpenAlex
- W2068121174
- Cited by
- 162
- References
- 12
- Citations by year
- 2026: 6 · 2025: 8 · 2024: 10 · 2023: 11 · 2022: 6 · 2021: 6 · 2020: 13 · 2019: 6 · 2018: 12 · 2017: 11 · 2016: 17 · 2015: 20 · 2014: 9 · 2013: 16 · 2012: 6
- FWCI
- 1.44
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience & Biobehavioral Reviews (publishedVersion)
- PubMed (publishedVersion)
- The Cupola: Scholarship at Gettysburg College (Gettysburg College) (submittedVersion)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Keywords
- play behavior, rough-and-tumble play, young rats, neural correlates, frontal cortex, striatum, amygdala, ventral hypothalamus, periaqueductal gray, dopaminergic system, cholinergic modulation, endogenous opioids, cannabinoids, norepinephrine, serotonin, child development
- MeSH terms
- Animals, Brain, Competitive Behavior, Emotions, Mammals, Nervous System, Nervous System Physiological Phenomena, Play and Playthings, Social Behavior, Neurotransmitter Agents, Rats
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