The ontogeny of play in rats
Abstract
Play behavior, as indicated by frequency and duration of pinning behavior, was studied in young rats between 18 and 64 days of age. The incidence of play was markedly increased by social isolation. Play increased from 18-28 days of age, peaked between 32 and 40 days of age, and gradually declined thereafter. Animals developed stable "dominance hierarchies" during the course of testing so that one animal pinned the other on the average 70% of the time. Also "dominant" animals exhibited the longer pin durations. The data indicate that social play can be efficiently studied in the laboratory rat and, further, that one function of play may be to establish stable social relationships.
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After weaning, rodents show a strong orientation towards peers, actively seek peer interaction, and these interactions are important for healthy development and social learning.
“Similar to adolescent humans, after weaning, rodents show a strong orientation towards their peers.38 These animals actively seek out peer interaction and these interactions are considered to be important social input for healthy development39 and specifically for social learning.34”
From The effects of social deprivation on adolescent development and mental health (2020) · cites this paper as [39]
When play is highly motivated following social isolation and the play bout is short, there are no consistent sex differences in the structure of or time spent engaged in play.
“When play is highly motivated, as is the case following periods of social isolation, and the play bout is short, there are no consistent sex differences in the structure of or time spent engaged in play (Panksepp & Beatty, 1980; Panksepp, 1981; Thor & Holloway, 1984).”
From Developmental origins of sex differences in the neural circuitry of play (2020) · cites this paper as Panksepp, 1981
Play is most robustly expressed during the juvenile period, which in rats corresponds to postnatal days 26-40.
“Play is most robustly expressed during the juvenile period, which in rats corresponds to postnatal days 26–40 (Panksepp, 1981).”
From Developmental origins of sex differences in the neural circuitry of play (2020) · cites this paper as Panksepp, 1981
In rats, 24 h of isolation further stimulates play.
“in rats, play peaks around 30–40 days of age, and 24 h of isolation further stimulates play (Panksepp, 1981).”
From Sexually dimorphic role for vasopressin in the development of social play (2014) · cites this paper as Panksepp, 1981
Play fighting in rats emerges around 18 days of age, peaks at 30-40 days of age, and declines thereafter.
“Play fighting in rats emerges around 18 days of age, peaks at 30–40 days of age, and declines thereafter (Panksepp, 1981).”
From Sexually dimorphic role for vasopressin in the development of social play (2014) · cites this paper as Panksepp, 1981
Play first emerged around 18-19 days of age.
“As in previous studies, play first emerged around 18–19 days of age (Bolles and Woods, 1964; Panksepp, 1981; Thiels et al., 1990).”
From Sexually dimorphic role for vasopressin in the development of social play (2014) · cites this paper as Panksepp, 1981
The sex difference in play is often not detected in experiments that test animals in same-sex pairs.
“this difference is often not detected in experiments that test animals in same-sex pairs (e.g., Panksepp and Beatty, 1980; Panksepp, 1981; Thor and Holloway, 1984; Veenema et al., 2013; present results).”
From Sexually dimorphic role for vasopressin in the development of social play (2014) · cites this paper as Panksepp, 1981
Sex differences in social play disappear when rats are briefly isolated and tested for social play in resident-intruder settings.
“However, these sex differences in social play disappear when rats are briefly isolated and tested for social play in resident-intruder settings (Panksepp & Beatty, 1980; Panksepp, 1981; Thor & Holloway, 1984).”
From Sex-specific modulation of juvenile social play by vasopressin (2013) · cites this paper as Panksepp, 1981
Pinning may be indicative of dominance.
“pinning may be indicative of dominance [21, 29].”
From Sex-specific effects of neonatal progestin receptor antagonism on juvenile social play behavior in rats (2021) · cites this paper as [29]
Social play behavior is a precursor of adult social, aggressive, and sexual behavior and functions to facilitate the development of circuits involved in social behavior.
“It is thought that social play behavior is a precursor of adult social, aggressive, and sexual behavior that is displayed out of context, in exaggerated form and functions to facilitate the development of circuits involved in social behavior (Panksepp, 1981; Vanderschuren and Trezza, 2014; Pellis and Pellis, 2017).”
From Effects of Maternal Deprivation and Complex Housing on Rat Social Behavior in Adolescence and Adulthood (2018) · cites this paper as Panksepp, 1981
Spontaneous levels of play are much lower than the levels of play exhibited following some period of social isolation.
“It has been shown, however, that spontaneous levels of play are much lower than the levels of play that are exhibited following some period of social isolation (Panksepp, 1981;Pellis et al., 1997), and in the present study, rats were observed following 24 hr of social isolation.”
From Play fighting in androgen-insensitivetfm rats: Evidence that androgen receptors are necessary for the development of adult playful attack and defense (2006) · cites this paper as Panksepp, 1981
Not all test paradigms or all strains of rats show higher levels of play in males.
“Not all test paradigms (Panksepp, 1981;Panksepp & Beatty, 1980) or all strains of rats (Reinhart, McIntyre, & Pellis, 2004) show higher levels of play in males, however.”
From Play fighting in androgen-insensitivetfm rats: Evidence that androgen receptors are necessary for the development of adult playful attack and defense (2006) · cites this paper as Panksepp, 1981
The period from P26 to P40 encompasses the peak of the window in which social play is maximally expressed.
“the peak of the window in which social play is maximally expressed (Panksepp, 1981)”
From Social play experience in juvenile rats is indispensable for appropriate socio-sexual behavior in adulthood in males but not females (2023) · cites this paper as Panksepp, 1981
P45 is an age when rats of both sexes have typically entered puberty, at which point playfulness dramatically decreases.
“an age when rats of both sexes have typically entered puberty, at which point playfulness dramatically decreases (Meaney and Stewart, 1981; Panksepp, 1981).”
From Social play experience in juvenile rats is indispensable for appropriate socio-sexual behavior in adulthood in males but not females (2023) · cites this paper as Panksepp, 1981
A dyadic paradigm was developed in which rats are tested in pairs in an enclosure to which they have been habituated following a period of social isolation to increase their motivation to engage in play.
“Consequently, a dyadic paradigm was developed—rats are tested in pairs in an enclosure to which they have been habituated following a period of social isolation to increase their motivation to engage in play (Panksepp and Beatty, 1980; Panksepp, 1981).”
From The rough-and-tumble play of rats as a natural behavior suitable for studying the social brain (2022) · cites this paper as Panksepp, 1981
The social play deprivation period P21-42 is the period in life when social play is most abundant.
“Rats were deprived of social play for a period of three weeks postweaning (P21-P42), which is the period in life when social play is most abundant (Baenninger, 1967;Meaney and Stewart, 1981;Panksepp, 1981).”
From Social Play Behavior Is Critical for the Development of Prefrontal Inhibitory Synapses and Cognitive Flexibility in Rats (2022) · cites this paper as Panksepp, 1981
Differences in the timing and duration of separation may explain divergent findings on sucrose preference.
“One explanation for these divergent findings might be the existence of differences in the timing and duration of separation.”
From The effects of early life stress on reward processing (2018) · cites this paper as Panksepp, 1981
Cites
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
Social deprivation and play in rats
Panksepp, J., & Beatty, W. W. (1980) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(80)91077-8 · Cited by 409 · see citing works
Self-citationBekoff, M. (1972) · The Quarterly Review of Biology · doi:10.1086/407400 · Cited by 271 · see citing works
An 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
Notes on the Psychic Development of the Young White Rat
Small, W. S. (1899) · The American Journal of Psychology · doi:10.2307/1412730 · Cited by 174 · see citing works
Sex differences in the play behavior of prepubescent rats
Olioff, M., & Stewart, J. (1978) · Physiology & Behavior · doi:10.1016/0031-9384(78)90060-4 · Cited by 145 · see citing works
Comparison 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
Welker, W. I. (1971) · Elsevier eBooks · doi:10.1016/b978-0-12-504350-2.50010-2 · Cited by 36 · see citing works
Experimente zur Triebspezifit�t des S�ugetierspiels
M�ller-Schwarze, D. (1966) · Die Naturwissenschaften · doi:10.1007/bf00643359 · Cited by 9 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The adolescent brain and age-related behavioral manifestations
Spear, L. P. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00014-2 · Cited by 5,433 · see citing works
The effects of social deprivation on adolescent development and mental health
Orben, A., Tomova, L., & Blakemore, S.-J. (2020) · The Lancet Child & Adolescent Health · doi:10.1016/s2352-4642(20)30186-3 · Cited by 1,229 · see citing works
“The animals actively seek out peer interaction and these interactions are considered to be important social input for healthy development( 39 ) and specifically for social learning( 37 ).”
Adolescent cortical development: A critical period of vulnerability for addiction
Crews, F., He, J., & Hodge, C. (2007) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.12.001 · Cited by 1,091 · see citing works
Adolescence as a neurobiological critical period for the development of higher-order cognition
Larsen, B., & Luna, B. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.09.005 · Cited by 853 · see citing works
Laviola, G., Macrı̀, S., Morley-Fletcher, S., & Adriani, W. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00006-x · Cited by 621 · 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
Self-citationDoremus-Fitzwater, T. L., Varlinskaya, E. I., & Spear, L. P. (2010) · Brain and Cognition · doi:10.1016/j.bandc.2009.08.008 · Cited by 397 · see citing works
Douglas, L. A., Varlinskaya, E. I., & Spear, L. P. (2004) · Developmental Psychobiology · doi:10.1002/dev.20025 · Cited by 389 · see citing works
Tirelli, E., Laviola, G., & Adriani, W. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00018-6 · Cited by 362 · 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
Sensory Integration in Mouse Insular Cortex Reflects GABA Circuit Maturation
Gogolla, N., Takesian, A. E., Feng, G., Fagiolini, M., & Hensch, T. K. (2014) · Neuron · doi:10.1016/j.neuron.2014.06.033 · Cited by 310 · see citing works
Social reward among juvenile mice
Panksepp, J. B., & Lahvis, G. P. (2007) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2006.00295.x · Cited by 248 · see citing works
Self-citationLukkes, J. L. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.018.2009 · Cited by 235 · 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
Peculiar vulnerability to nicotine oral self-administration in mice during early adolescence
Adriani, W. (2002) · Neuropsychopharmacology · doi:10.1016/s0893-133x(02)00295-6 · Cited by 214 · see citing works
Stress in adolescence and drugs of abuse in rodent models: role of dopamine, CRF, and HPA axis
Burke, A. R., & Miczek, K. A. (2014) · Psychopharmacology · doi:10.1007/s00213-013-3369-1 · Cited by 207 · see citing works
The effects of early life stress on reward processing
Novick, A. M., Levandowski, M. L., Laumann, L. E., Philip, N. S., Price, L. H., & Tyrka, A. R. (2018) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2018.02.002 · Cited by 192 · see citing works
“…while the majority of studies started isolation around postnatal day (PND) 21, McCool and Chappell (2009) started isolation when rats were between PND 28 and PND 32, thus allowing the rats to have experience with peers during a longer duration within their peak play period (Panksepp, 1981).”
BackgroundVanderschuren, 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
Social Behavior and Social Motivation in Adolescent Rats
Varlinskaya, E. I., Spear, L. P., & Spear, N. E. (1999) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00285-6 · Cited by 194 · 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
Bicks, L. K., Yamamuro, K., Flanigan, M. E., Kim, J. M., Kato, D., Lucas, E. K., Koike, H., Peng, M. S., Brady, D. M., Chandrasekaran, S., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-14740-z · Cited by 150 · 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
“However, these sex differences in social play disappear when rats are briefly isolated and tested for social play in resident-intruder settings (Panksepp & Beatty, 1980; Panksepp, 1981; Thor & Holloway, 1984).”
BackgroundMethodIsolation changes the incentive value of sucrose and social behaviour in juvenile and adult rats
Van den Berg, C. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(99)00099-6 · Cited by 165 · see citing works
Life-span studies of dominance and aggression in established colonies of laboratory rats
Blanchard, R. J., Flannelly, K. J., & Blanchard, D. C. (1988) · Physiology & Behavior · doi:10.1016/0031-9384(88)90089-3 · Cited by 165 · 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
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
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
Smith, C. J. W., Poehlmann, M. L., Li, S., Ratnaseelan, A. M., Bredewold, R., & Veenema, A. H. (2017) · Brain Structure and Function · doi:10.1007/s00429-016-1260-7 · Cited by 143 · 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
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
A longitudinal study of dominance in an outdoor colony of domestic rats.
Adams, N., & Boice, R. (1983) · Journal of Comparative Psychology · doi:10.1037/0735-7036.97.1.24 · Cited by 120 · 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
Whishaw, I. Q., Metz, G. A. S., Kolb, B., & Pellis, S. M. (2001) · Developmental Psychobiology · doi:10.1002/dev.1041 · Cited by 110 · see citing works
Hermes, G., Li, N., Duman, C., & Duman, R. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.12.019 · Cited by 111 · see citing works
Environmental programming of susceptibility and resilience to stress in adulthood in male mice
Peña, C. J., Nestler, E. J., & Bagot, R. C. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00040 · Cited by 97 · 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
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-citationPlay, Curiosity, and Cognition
Chu, J., & Schulz, L. E. (2020) · Annual Review of Developmental Psychology · doi:10.1146/annurev-devpsych-070120-014806 · Cited by 93 · see citing works
Leussis, M. P., Lawson, K., Stone, K., & Andersen, S. L. (2008) · Synapse · doi:10.1002/syn.20483 · Cited by 95 · see citing works
Ontogeny of memory: an update on 40 years of work on infantile amnesia
Madsen, H. B., & Kim, J. H. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.07.030 · Cited by 92 · see citing works
Effects of genistein exposure on sexually dimorphic behaviors in rats.
Flynn, K. M. (2000) · Toxicological Sciences · doi:10.1093/toxsci/55.2.311 · Cited by 92 · see citing works
Peartree, N. A., Hood, L. E., Thiel, K. J., Sanabria, F., Pentkowski, N. S., Chandler, K. N., & Neisewander, J. L. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.10.001 · Cited by 90 · 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
Himmler, B. T., Kisko, T. M., Euston, D. R., Kolb, B., & Pellis, S. M. (2014) · Behavioural Processes · doi:10.1016/j.beproc.2014.04.014 · Cited by 87 · see citing works
Himmler, B. T., Stryjek, R., Modlinska, K., Derksen, S. M., Pisula, W., & Pellis, S. M. (2013) · Journal of Comparative Psychology · doi:10.1037/a0032187 · Cited by 82 · see citing works
Brunelli, S. A., & Hofer, M. A. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.04.014 · Cited by 80 · see citing works
Dominance status predicts social fear transmission in laboratory rats
Jones, C. E., & Monfils, M.-H. (2016) · Animal Cognition · doi:10.1007/s10071-016-1013-2 · Cited by 81 · 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
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
Thor, D. H., & Holloway, W. R. (1986) · Behavioral Neuroscience · doi:10.1037/0735-7044.100.2.275 · Cited by 73 · see citing works
Development of dominance in domestic rats in laboratory and seminatural environments
Adams, N., & Boice, R. (1989) · Behavioural Processes · doi:10.1016/0376-6357(89)90036-3 · Cited by 72 · 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
Colbert, N. K. W., Pelletier, N. C., Cote, J. M., Concannon, J. B., Jurdak, N. A., Minott, S. B., & Markowski, V. P. (2005) · Environmental Health Perspectives · doi:10.1289/ehp.7509 · Cited by 60 · see citing works
The 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
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
Prenatal protein malnutrition affects the social interactions of juvenile rats
Almeida, S. S., Tonkiss, J., & Galler, J. R. (1996) · Physiology & Behavior · doi:10.1016/0031-9384(95)02236-8 · Cited by 54 · 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
“…in mix-sex groups (Meaney and Stewart, 1981b; Olesen et al., 2005; Parent and Meaney, 2008), this difference is often not detected in experiments that test animals in same-sex pairs (e.g., Panksepp and Beatty, 1980; Panksepp, 1981; Thor and Holloway, 1984; Veenema et al., 2013; present results).”
BackgroundMethodResultInfluentialKentrop, 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
“Testing took place between 33 and 42 days of age, well within the period in which rats show abundant amounts of social play behavior (Panksepp, 1981).”
Papilloud, A., Guillot de Suduiraut, I., Zanoletti, O., Grosse, J., & Sandi, C. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0215-6 · Cited by 38 · 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
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
“the play bout is short, there are no consistent sex differences in the structure of or time spent engaged in play (Panksepp, 1981; Panksepp & Beatty, 1980; Thor & Holloway, 1984).”
BackgroundStark, R., & Pellis, S. M. (2020) · International Journal of Play · doi:10.1080/21594937.2020.1720142 · Cited by 32 · see citing works
The energetic costs of rough‐and‐tumble play in the juvenile rat
Siviy, S. M., & Atrens, D. M. (1992) · Developmental Psychobiology · doi:10.1002/dev.420250206 · Cited by 32 · see citing works
Bredewold, R., Nascimento, N. F., Ro, G. S., Cieslewski, S. E., Reppucci, C. J., & Veenema, A. H. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0100-2 · Cited by 31 · see citing works
Marquardt, 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
“…at weaning (P21) and lasting until P45, an age when rats of both sexes have typically entered puberty, at which Frontiers in Behavioral Neuroscience 15 frontiersin.org Marquardt et al. 10.3389/fnbeh.2022.1076765 point playfulness dramatically decreases (Meaney and Stewart, 1981; Panksepp, 1981).”
BackgroundMethodInfluentialCutuli, 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
Field, E. F., Whishaw, I. Q., Pellis, S. M., & Watson, N. V. (2006) · Developmental Psychobiology · doi:10.1002/dev.20121 · 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
“Consequently, a dyadic paradigm was developed—rats are tested in pairs in an enclosure to which they have been habituated following a period of social isolation to increase their motivation to engage in play (Panksepp and Beatty, 1980; Panksepp, 1981).”
BackgroundPlay in Rats: Association across Contexts and Types, and Analysis of Structure
Melotti, L., Bailoo, J., Murphy, E., Burman, O., & Wurbel, H. (2014) · Animal Behavior and Cognition · doi:10.12966/abc.11.06.2014 · Cited by 26 · see citing works
“Such properties of play have been studied extensively in rats (Douglas, Varlinskaya, & Spear, 2004; Knutson, Burgdorf, & Panksepp, 1998; Panksepp, 1981; Pellis, Field, Smith, & Pellis, 1997; Pellis & McKenna, 1992; Pellis & Pellis, 1987; Vanderschuren, 2010), and rats can serve as a promising model for the study of pl…”
BackgroundAchterberg, E. J. M., Burke, C. J., & Pellis, S. M. (2023) · Behavioural Processes · doi:10.1016/j.beproc.2023.104933 · Cited by 20 · 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
Pinning 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
Not playing by the rules: Exploratory play, rational action, and efficient search
Chu, J., & Schulz, L. (2020) · doi:10.31234/osf.io/9yra2 · Cited by 22 · see citing works
Neurexin1α knockout in rats causes aberrant social behaviour: relevance for autism and schizophrenia
Achterberg, E. J. M., Biemans, B., & Vanderschuren, L. J. M. J. (2025) · Psychopharmacology · doi:10.1007/s00213-024-06559-z · Cited by 9 · see citing works
“Social play behaviour in rats first emerges around weaning (PND21), peaks between PND28-35 and declines after the onset of puberty (around PND42), and low levels of play can still be observed in adult rats (Meaney and Stewart 1981; Panksepp 1981).”
Pesca, C., Lo Iacono, L., & Carola, V. (2025) · European Journal of Psychotraumatology · doi:10.1080/20008066.2025.2521152 · Cited by 3 · 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
“Stewart 1981; Panksepp 1981; Pellis and Pellis 1990, 1997; Thor and Holloway 1984).”
Forbes-Lorman, R. M. (2021) · Behavioral and Brain Functions · doi:10.1186/s12993-021-00183-z · Cited by 1 · see citing works
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
- Authors
- Panksepp, J.
- Affiliations
- Bowling Green State University (US)
- Corresponding author
- Panksepp, Jaak
- Venue
- Developmental Psychobiology
- Publisher
- Wiley
- Published
- 1981-07
- Volume
- 14
- Issue
- 4
- Pages
- 327-332
- ISSN
- 0012-1630 (ISSN-L)
- 1098-2302
- OpenAlex
- W2049264784
- Cited by
- 537
- References
- 9
- Citations by year
- 2026: 10 · 2025: 18 · 2024: 13 · 2023: 23 · 2022: 15 · 2021: 28 · 2020: 21 · 2019: 18 · 2018: 25 · 2017: 15 · 2016: 20 · 2015: 24 · 2014: 25 · 2013: 14 · 2012: 6
- FWCI
- 13.25
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Developmental Psychobiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Keywords
- play behavior, ontogeny, social isolation, dominance hierarchy, interpersonal relationships, laboratory rats, juvenile development
- MeSH terms
- Aging, Animals, Female, Male, Motor Activity, Play and Playthings, Social Dominance, Social Environment, Social Isolation, Rats
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