The DOI matches its Crossref record; 72 of the 72 references it cites were found in a registry or an index.
Juvenile peer play experience and the development of the orbitofrontal and medial prefrontal cortices
Abstract
The experience of peer play during the juvenile phase in rats is known to be important for the development of adult social competence. Adult social competence is also compromised by damage to the orbitofrontal cortex (OFC), an area known to be involved in social behavior. We therefore hypothesized that the functioning of the OFC in social behavior is facilitated through the experience of peer play during the juvenile period. Further, because the OFC and medial prefrontal cortex (mPFC) are known to be reciprocally responsive to a variety of manipulations, we suspected that the functioning of the mPFC is also responsive to the experience of peer play during development. Female Long-Evans rats were raised in conditions that varied with respect to the experience of peer play, and Golgi techniques were used to examine the neuronal morphology of the OFC and mPFC. The results indicated that the neurons of the OFC responded to the number of peers present, not whether those peers engaged in play or not, whereas the neurons of the mPFC responded specifically to the experience of play.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“Even if not completely isolated, but instead deprived of peer contact by being reared solely with an adult animal, adolescent rodents show brain-level changes including reduced synaptic pruning in the prefrontal cortex.53”
From The effects of social deprivation on adolescent development and mental health (2020) · cites this paper as [53]
In the citing paper
“The same lesions, however, broadly impair social cognition and thus may not be specific to play (Bell et al., 2010).”
From Developmental origins of sex differences in the neural circuitry of play (2020) · cites this paper as Bell et al., 2010
In the citing paper
“The dendritic complexity of cortical pyramidal neurons is reduced in animals given multiple play partners over an extended period of time compared to those either socially deprived or given only limited access to the same partner (Bell et al., 2010).”
From Developmental origins of sex differences in the neural circuitry of play (2020) · cites this paper as Bell et al., 2010
In the citing paper
“The mPFC is also changed in response to play experience.”
From Developmental origins of sex differences in the neural circuitry of play (2020) · cites this paper as Bell et al., 2010
In the citing paper
“Rats demonstrate enhanced cognitive abilities and a rich social repertoire paired with neural complexity, particularly in brain regions implicated in ASD pathology such as the frontal cortex [10–12].”
From Behavioral Phenotyping of Juvenile Long-Evans and Sprague-Dawley Rats: Implications for Preclinical Models of Autism Spectrum Disorders (2016) · cites this paper as [10]
In the citing paper
“the development of the medial prefrontal cortex (mPFC) and associated socio-cognitive skills is influenced by the experience of RTP with peers in the juvenile period (about 28–40 days post birth; Bell et al., 2010; Baarendse et al., 2013; Schneider 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 Bell et al., 2010
In the citing paper
“Lack of social play experience during postweaning development has been reported to cause long-lasting changes in PFC circuitry and function (Leussis et al., 2008;Bell et al., 2010;Baarendse et al., 2013;Vanderschuren and Trezza, 2014).”
From Social Play Behavior Is Critical for the Development of Prefrontal Inhibitory Synapses and Cognitive Flexibility in Rats (2022) · cites this paper as Bell et al., 2010
Citations
Cites
(1995) · Cited by 1,979
Self-citationThe cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat
Krettek, J. E., & Price, J. L. (1977) · The Journal of Comparative Neurology · doi:10.1002/cne.901710204 · Cited by 1,277
Structural plasticity associated with exposure to drugs of abuse
Robinson, T. E., & Kolb, B. E. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2004.06.025 · Cited by 1,130
Self-citationListon, C., Miller, M. M., Goldwater, D. S., Radley, J. J., Rocher, A. B., Hof, P. R., Morrison, J. H., & McEwen, B. S. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.1184-06.2006 · Cited by 968
Functions of the frontal cortex of the rat: A comparative review
Kolb, B. E. (1984) · Brain Research Reviews · doi:10.1016/0165-0173(84)90018-3 · Cited by 897
Self-citationHeidbreder, C. A., & Groenewegen, H. J. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2003.09.003 · Cited by 882
Fagen, R. M. (1981) · Cited by 860
Repeated Stress Induces Dendritic Spine Loss in the Rat Medial Prefrontal Cortex
Radley, J. J., Rocher, A. B., Miller, M., Janssen, W. G. M., Liston, C., Hof, P. R., McEwen, B. S., & Morrison, J. H. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhi104 · Cited by 820
The Organization of the Cerebral Cortex
Sholl, D. A. (1957) · The American Journal of the Medical Sciences · doi:10.1097/00000441-195711000-00015 · Cited by 771
Robinson, T. E., & Kolb, B. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-21-08491.1997 · Cited by 704
Self-citation
Cited by
Sorted by citations
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 1,383
“Even if not completely isolated, but instead deprived of peer contact by being reared solely with an adult animal, adolescent rodents show brain-level changes including reduced synaptic pruning in the prefrontal cortex( 54 ).”
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
“, 2013) and induces plastic changes in the mPFC that persist into adulthood (Bell et al., 2010; Himmler et al., 2013).”
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
“ 66 Whether these effects are specific to play deprivation or merely reflect the generic effect of a lack of stimulation requires further study.”
BackgroundInfluentialExperience and the developing prefrontal cortex
Kolb, B., Mychasiuk, R., Muhammad, A., Li, Y., Frost, D. O., & Gibb, R. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1121251109 · Cited by 564
“In contrast, the neurons of mPFC showed a decrease in spine density proportional to the amount of play but not the number of conspecifics (59).”
BackgroundSelf-citationStress and the developing adolescent brain
Eiland, L. R., & Romeo, R. D. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.10.048 · Cited by 539
“In contrast, in the mPFC, no peer play groups had significantly greater dendritic length and more complex arbors than the single or multiple peer play groups (Bell et al., 2010).”
BackgroundBrain plasticity and behaviour in the developing brain.
Kolb, B. E., & Gibb, R. L. (2011) · Europe PMC (PubMed Central) · Cited by 470
Self-citationSocial 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
“The experience of social play during the juvenile hase appears to affect the maturation of the medial prefrontal e Neuroscience 17 (2016) 118–127 cortex, and the flexible engagement of this region in social encounters later in development (Bell et al., 2010; Himmler et al., 2013, 2014).”
InfluentialBurke, 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
Self-citationThe development of the ventral prefrontal cortex and social flexibility
Nelson, E. E., & Guyer, A. E. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.01.002 · Cited by 201
Play, Playfulness, Creativity and Innovation
Bateson, P. (2014) · Animal Behavior and Cognition · doi:10.12966/abc.05.02.2014 · Cited by 220
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
“This issue can be addressed using somewhat more sophisticated approaches, such as allowing the animals a limited amount of (playful) social interaction every day (e.g., Einon et al. 1978), or housing them with non-playful, adult females (e.g., Bell et al. 2010).”
Principles of plasticity in the developing brain
Kolb, B. E., Harker, A., & Gibb, R. L. (2017) · Developmental Medicine & Child Neurology · doi:10.1111/dmcn.13546 · Cited by 224
Self-citationSearching for the principles of brain plasticity and behavior
Kolb, B. E., & Gibb, R. L. (2013) · Cortex · doi:10.1016/j.cortex.2013.11.012 · Cited by 170
Self-citationBehavioural profiles are shaped by social experience: when, how and why
Sachser, N., Kaiser, S., & Hennessy, M. B. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0344 · Cited by 163
“In rats, for example, play is indispensable for an adequate development of coping with social challenges and it influences both behaviour [73] and neural organization [74].”
BackgroundRough-and-Tumble Play and the Development of the Social Brain
Pellis, S. M., Himmler, B. T., Himmler, S. M., & Pellis, V. C. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-804036-2.00012-1 · Cited by 151
Self-citationStress during development alters dendritic morphology in the nucleus accumbens and prefrontal cortex
Muhammad, A., Carroll, C., & Kolb, B. E. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.04.041 · Cited by 146
Self-citationWhat 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
“Given that being reared with a nonplayful partner leads to atypical development of the medial prefrontal cortex (mPFC; Bell et al., 2010; B. T. Himmler, Pellis, & Kolb, 2013), some of the changes in behavioral and cognitive deficits in play-deprived rats may arise from altered development of this…”
BackgroundSelf-citationDow-Edwards, D. L., MacMaster, F. P., Peterson, B. S., Niesink, R. J. M., Andersen, S. L., & Braams, B. R. (2019) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2019.106834 · Cited by 160
“the medial PFC and nucleus accumbens (Trezza et al., 2008; Trezza et al., 2014; Bell et al., 2010).”
Why Do the Children (Pretend) Play?
Lillard, A. S. (2017) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2017.08.001 · Cited by 145
“In addition, play deprivation influences the development of the medial prefrontal cortex [45], reducing long-range inhibitory circuits (for a discussion see [46]).”
BackgroundBrain Plasticity in the Developing Brain
Kolb, B. E., Mychasiuk, R., Muhammad, A., & Gibb, R. L. (2013) · Progress in brain research · doi:10.1016/b978-0-444-63327-9.00005-9 · Cited by 121
“Neurons of the mPFC region respond to the amount of play but not the number of playmates, whereas the OFC responds to the number of playmates and not the amount of play (Bell et al., 2010).”
BackgroundSelf-citationThe 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
Self-citationWall, V. L., Fischer, E. K., & Bland, S. T. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2012.09.002 · Cited by 123
“Of special importance during adolescence is the development of social play behaviors, and deprivation of play behavior in adolescent rats impairs subsequent social behavior and decreases the dendritic complexity of themPFC [34].”
Watt, M. J., Weber, M. A., Davies, S. R., & Forster, G. L. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.06.015 · Cited by 97
A brain motivated to play: insights into the neurobiology of playfulness
Siviy, S. M. (2016) · Behaviour · doi:10.1163/1568539x-00003349 · Cited by 113
“Dendritic complexity of pyramidal cells within the medial prefrontal cortex has also been shown to be sensitive to play experience as a juvenile (Bell et al., 2010).”
BackgroundFarrell, M. R., Holland, F. H., Shansky, R. M., & Brenhouse, H. C. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.05.009 · Cited by 95
Ahn, Y., Narous, M., Tobias, R., Rho, J. M., & Mychasiuk, R. (2014) · Developmental Neuroscience · doi:10.1159/000362645 · Cited by 94
Schneider, 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
“Molecular analysis revealed increased CB1 receptor (CB1R) protein levels and CP55, 940 stimulated [35S]GTPγS binding activity specifically in the amygdala and thalamus in previously peer-rejected rats.”
BackgroundOntogenetic trajectories of chimpanzee social play: similarities with humans
Cordoni, G., & Palagi, E. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027344 · Cited by 87
Age, experience, injury, and the changing brain
Kolb, B. E., & Teskey, G. C. (2010) · Developmental Psychobiology · doi:10.1002/dev.20515 · Cited by 86
Self-citationRichards, S., Mychasiuk, R., Kolb, B. E., & Gibb, R. L. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.02.043 · Cited by 84
Self-citationCellular 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
A Brief Glimpse at the Long Evolutionary History of Play
Burghardt, G. M. (2014) · Animal Behavior and Cognition · doi:10.12966/abc.05.01.2014 · Cited by 82
Himmler, B. T., Pellis, S. M., & Kolb, B. E. (2013) · Neuroscience Letters · doi:10.1016/j.neulet.2013.09.061 · Cited by 79
Self-citationHarnessing the power of neuroplasticity for intervention
Kolb, B. E., & Muhammad, A. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00377 · Cited by 85
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
Self-citationKu, 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
Connections during crisis: Adolescents’ social dynamics and mental health during COVID-19.
Polack, R. G., Sened, H., Aubé, B. S. S., Zhang, A., Joormann, J., & Hedy Kober, A. (2021) · Developmental Psychology · doi:10.1037/dev0001211 · Cited by 81
Plasticity in the prefrontal cortex of adult rats
Kolb, B. E., & Gibb, R. L. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00015 · Cited by 73
“Bell et al. (2010) manipulated the amount of play behavior that rats could experience by housing them with either 1 or 3 siblings or 1 or 3 adults. Adult rats do not play with juveniles or adolescents so although there would be social interaction if youngsters were housed with adults, there is virtually no play. Furth…”
BackgroundInfluentialSelf-citationBlumstein, D. T., Chung, L. K., & Smith, J. E. (2013) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2013.0485 · Cited by 72
“A fundamental and ethical challenge in studying play is that it is difficult to deprive animals only of play (but see [10,11]) and that deprivation of play typically impedes normal development [12,13].”
BackgroundFair 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 76
Stress, sensitive periods, and substance abuse
Andersen, S. L. (2019) · Neurobiology of Stress · doi:10.1016/j.ynstr.2018.100140 · Cited by 92
“development of the prefrontal cortex to respond to social cues (Bell et al. 2009; Bell et al. 2010), increase behavioral flexibility (Himmler et al.”
BackgroundMuhammad, A., & Kolb, B. E. (2011) · Developmental Neuroscience · doi:10.1159/000324744 · Cited by 73
“The experience-dependent modulation of social behavior could be attributed to underlying altered neurocircuits. For example, PS reorganized the mPFC by decreasing the spine density described below in the anatomical findings. Similarly, PFC exhibited play-dependent structural reorganization in rats [”
BackgroundSelf-citationBrain plasticity and recovery from early cortical injury
Kolb, B. E., Mychasiuk, R., Williams, P. T. J. A., & Gibb, R. L. (2011) · Developmental Medicine & Child Neurology · doi:10.1111/j.1469-8749.2011.04054.x · Cited by 70
“Complex housing prenatally Decreased dendritic length; increased spine density R Gibb, C Gonzalez, B Kolb Postnatal ‘handling’ Decreased dendritic length; spines unchanged Gibb and Kolb(3) Postnatal tactile stimulation Decreased dendritic length; decreased spine density Kolb and Gibb(4) Prenatal tactile stimulation De…”
BackgroundSelf-citationCharacterization 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
“For defensive strategies, the choice to use rotation over evasion is mediated by cortical regions [43, 44].”
BackgroundShapiro, L. P., Parsons, R. G., Koleske, A. J., & Gourley, S. L. (2016) · Journal of Neuroscience Research · doi:10.1002/jnr.23960 · Cited by 69
“For example, social play during adolescence modestly increases dendrite arborization in the OFC while decreasing arborization in the mPFC, an effect that could be interpreted as enhanced pruning (Bell et al., 2010).”
BackgroundPlay therapy in children with autism: Its role, implications, and limitations
Elbeltagi, R. M., Al‐Beltagi, M., Saeed, N. K., & Alhawamdeh, R. (2023) · World Journal of Clinical Pediatrics · doi:10.5409/wjcp.v12.i1.1 · Cited by 69
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
Tzanoulinou, S., & Sandi, C. (2015) · Current topics in behavioral neurosciences · doi:10.1007/7854_2015_430 · Cited by 75
“Play behaviors in rodents have been shown to be rewarding [reviewed in Trezza et al. (2010)], and playing has been hypothesized to be important for learning motor sequences and behaviors that will be essential to the animals as adults (the motor-training hypothesis) (Bell et al. 2010).”
BackgroundUnderstanding the links between social ties and fitness over the life cycle in primates
González, N. T. (2019) · Behaviour · doi:10.1163/1568539x-00003552 · Cited by 69
“In many cases, the higher frequency and quality of play during development correlate with important fitnessrelated traits, such as increased motor-skills (rats, Assamese macaques, and ground squirrels, Nunes et al., 2004; Bell et al., 2010; Berghänel et al., 2015; Schneider et al., 2016), appropriate submissive behavi…”
BackgroundInfluentialMychasiuk, R., Hehar, H., Ma, I., Candy, S., & Esser, M. J. (2016) · European Journal of Neuroscience · doi:10.1111/ejn.13360 · Cited by 63
“Studies have shown that juveniles reared with adults have little opportunity to engage in roughand-tumble play as adults avoid this type of play with younger rats (Bell et al., 2010).”
BackgroundMychasiuk, R., Hehar, H., Farran, A., & Esser, M. J. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.10.048 · Cited by 67
Antidepressants and the adolescent brain
Cousins, L., & Goodyer, I. M. (2015) · Journal of Psychopharmacology · doi:10.1177/0269881115573542 · Cited by 61
“Adolescent rats housed with multiple peers showed greater dendritic length and more complicated dendritic arbours in the orbitofrontal cortex and reduced dendritic length in the medial PFC compared with rats housed with either one adult or one peer (Bell et al., 2010).”
BackgroundSocial Competence at Two Years after Childhood Traumatic Brain Injury
Anderson, V. A., Beauchamp, M. H., Yeates, K. O., Crossley, L. H., Ryan, N. P., Hearps, S. J. C., & Catroppa, C. (2017) · Journal of Neurotrauma · doi:10.1089/neu.2016.4692 · Cited by 67
“…confirmed associations between such environmental factors and social and behavioral adjustment in juvenile animals under experimental conditions, 45–47 describing links between negative environmental conditions (e.g., low levels of stimulation and parent contact) and reduced brain development…”
The impact of adolescent stress experiences on neurobiological development
Iacono, L. L., & Carola, V. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.09.040 · Cited by 64
Hinton, E. A., Li, D. C., Allen, A. G., & Gourley, S. L. (2019) · eneuro · doi:10.1523/eneuro.0318-19.2019 · Cited by 60
“Our findings are consistent with evidence that social play, other environmental stimuli, and stress hormones all contribute to neuron refinement during early-life critical periods (Zuo et al., 2005; Bell et al., 2010; Liston and Gan, 2011).”
ResultBijlsma, 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
Synaptic Cytoskeletal Plasticity in the Prefrontal Cortex Following Psychostimulant Exposure
DePoy, L. M., & Gourley, S. L. (2015) · Traffic · doi:10.1111/tra.12295 · Cited by 52
Dean, S. L., Wright, C. L., Hoffman, J. F., Wang, M., Alger, B. E., & McCarthy, M. M. (2012) · Endocrinology · doi:10.1210/en.2012-1350 · Cited by 51
Modeling play: distinguishing between origins and current functions
Pellis, S. M., Burghardt, G. M., Palagi, E., et al. (2015) · Adaptive Behavior · doi:10.1177/1059712315596053 · Cited by 50
Self-citationSexual Differentiation of the Brain and ADHD: What Is a Sex Difference in Prevalence Telling Us?
Waddell, J., & McCarthy, M. M. (2010) · Current topics in behavioral neurosciences · doi:10.1007/7854_2010_114 · Cited by 53
“This may relate to the maturation of the frontal cortex which modulates response inhibition, impulsivity, and dopaminergic reward circuits (Bell et al. 2010; Bock et al. 2008).”
BackgroundGrowing pains and pleasures: how emotional learning guides development
Nelson, E. E., Lau, J. Y. F., & Jarcho, J. M. (2014) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2013.11.003 · Cited by 48
Bambico, F. R., Lacoste, B., Hattan, P. R., & Gobbi, G. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht310 · Cited by 48
Muhammad, A., Hossain, S., Pellis, S. M., & Kolb, B. E. (2011) · Behavioral Neuroscience · doi:10.1037/a0022628 · Cited by 47
Self-citationPlay, 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
Self-citationMychasiuk, R., Hehar, H., Ma, I. W. Y., Kolb, B. E., & Esser, M. J. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.12.034 · Cited by 50
“Theypostulated that becauseplay involves complex and dynamic movements that are often made in response to external stimuli, one of play’s primary goals may be to ‘fine-tune’ regions of themPFC typically involved in the accurate sequencing and execution of movements (Bell et al., 2010).”
BackgroundSelf-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
Self-citationDeveloping Self‐Directed Executive Functioning: Recent Findings and Future Directions
Barker, J. E., & Munakata, Y. (2015) · Mind Brain and Education · doi:10.1111/mbe.12071 · Cited by 49
Play behavior and responses to novel situations in juvenile ground squirrels
Marks, K. A., Vizconde, D. L., Gibson, E. S., Rodriguez, J. R., & Nunes, S. (2017) · Journal of Mammalogy · doi:10.1093/jmammal/gyx049 · Cited by 46
The physiology of play: potential relevance for higher education
Koeners, M. P., & Francis, J. (2020) · International Journal of Play · doi:10.1080/21594937.2020.1720128 · Cited by 52
Nunes, S. (2014) · Journal of Ethology · doi:10.1007/s10164-014-0403-7 · Cited by 39
“…been proposed for play behavior in young animals including the promotion of motor, cognitive, and social development, and acquisition of behavioral plasticity in responses to unfamiliar situations (Bekoff 1972, 1988; Poirier and Smith 1974; Bekoff and Byers 1998; Lewis 2000; Špinka et al. 2001).”
BackgroundBrain development, experience, and behavior
Kolb, B. E., Mychasiuk, R., & Gibb, R. L. (2013) · Pediatric Blood & Cancer · doi:10.1002/pbc.24908 · Cited by 47
Self-citationNeurobiological mechanisms supporting experience-dependent resistance to social stress
Cooper, M. A., Clinard, C. T., & Morrison, K. E. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.01.072 · Cited by 39
“Also, restricting social play alters dendritic morphology in brain regions that regulate coping with stress such as the mPFC (Bell et al., 2010).”
BackgroundSearching for factors underlying cerebral plasticity in the normal and injured brain
Kolb, B. E., Muhammad, A., & Gibb, R. L. (2011) · Journal of Communication Disorders · doi:10.1016/j.jcomdis.2011.04.007 · Cited by 49
Self-citationColonnello, V., Petrocchi, N., Farinelli, M., & Ottaviani, C. (2016) · Current Neuropharmacology · doi:10.2174/1570159x14666160816120209 · Cited by 36
The evolution of two types of play
Smaldino, P. E., Palagi, E., Burghardt, G. M., & Pellis, S. M. (2019) · Behavioral Ecology · doi:10.1093/beheco/arz090 · Cited by 43
“, 1981), suggesting that only those species capable of the requisite investment in play gain this more sophisticated benefit (e.g., rats, Syrian hamsters; Baarendse et al., 2014; Bell et al., 2010; Burleson et al., 2016).”
BackgroundSelf-citationHamilton, D. A., Candelaria‐Cook, F. T., Akers, K. G., Rice, J. P., Maes, L. I., Rosenberg, M. J., Valenzuela, C. F., & Savage, D. D. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.05.048 · Cited by 38
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
“The dendritic complexity of cortical pyramidal neurons is reduced in animals given multiple play partners over an extended period of time compared to those either socially deprived or given only limited access to the same partner (Bell et al., 2010).”
BackgroundThe development of socio-sexual behavior in belugas (Delphinapterus leucas) under human care
Lilley, M. K., Ham, J. R., & Hill, H. M. M. (2019) · Behavioural Processes · doi:10.1016/j.beproc.2019.104025 · Cited by 34
Cumming, M. J., Thompson, M. A., & McCormick, C. M. (2014) · Developmental Psychobiology · doi:10.1002/dev.21252 · Cited by 36
Stark, R., & Pellis, S. M. (2020) · International Journal of Play · doi:10.1080/21594937.2020.1720142 · Cited by 32
“from being reared with an adult has been for females (Bell et al., 2010; Burleson et al., 2016; Himmler, Pellis, & Kolb, 2013).”
BackgroundInfluentialSelf-citationPlayful handling as social enrichment for individually- and group-housed laboratory rats
Cloutier, S., Baker, C., Wahl, K., Panksepp, J., & Newberry, R. C. (2012) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2012.10.006 · Cited by 29
“Therefore, keeping rats in appropriate ocial groups, whenever possible, is important to ensure roper brain and social skills development and meet their evelopmental needs (Bell et al., 2010; Krohn et al., 2006).”
BackgroundResultInfluentialBowlby's “Environment of Evolutionary Adaptedness”
Schore, A. N. (2012) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199755059.003.0002 · Cited by 31
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
Self-citationPellis, S. M., Williams, L. A., & Pellis, V. C. (2017) · International Journal of Comparative Psychology · doi:10.46867/ijcp.2017.30.00.14 · Cited by 30
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
“For example, the development of the medial prefrontal cortex (mPFC) and associated socio-cognitive skills is influenced by the experience of RTP with peers in the juvenile period (about 28–40 days post birth; Bell et al., 2010; Baarendse et al., 2013; Schneider et al., 2016), and the mPFC has a crucial role in coordin…”
BackgroundSelf-citationAnimal play and evolution: Seven timely research issues about enigmatic phenomena
Burghardt, G. M., Pellis, S. M., Schank, J. C., Smaldino, P. E., Vanderschuren, L. J. M. J., & Palagi, E. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105617 · Cited by 32
Self-citationComparing the ontogeny, neurobiology, and function of social play in hamsters and rats
Cooper, M. A., Grizzell, J. A., Whitten, C. J., & Burghardt, G. M. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105102 · Cited by 28
Ahmadi, B. B. M., Afarinesh, M. R., Jafaripour, L., & Sheibani, V. (2022) · Brain and Behavior · doi:10.1002/brb3.2993 · Cited by 27
“Therefore, the extent and nature of play in juvenile rats modify the prefrontal cortex organization in adulthood (Bell et al., 2010).”
BackgroundMuhammad, A., & Kolb, B. E. (2011) · Brain Research · doi:10.1016/j.brainres.2011.05.038 · Cited by 29
“In addition, the PFC is altered structurally and functionally (Lu et al., 2009) by early experiences and is a key player in modulating behaviors such as play behavior (Bell et al., 2010).”
Self-citationBrain Plasticity and Experience
Kolb, B. E. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-804036-2.00013-3 · Cited by 31
Self-citationCarter, R. N., Romanow, C. A., Pellis, S. M., & Lingle, S. (2019) · Animal Behaviour · doi:10.1016/j.anbehav.2019.06.032 · Cited by 30
Self-citationde Melo, S. R., Antoniazzi, C. T. D. D., Hossain, S., & Kolb, B. E. (2018) · Developmental Neuroscience · doi:10.1159/000486619 · Cited by 28
Self-citationDouble Helix: Reciprocity between juvenile play and brain development
Cooke, B. M., & Shukla, D. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.07.001 · Cited by 27
Context-dependent individual differences in playfulness in male rats
Lampe, J. F., Burman, O., Würbel, H., & Melotti, L. (2017) · Developmental Psychobiology · doi:10.1002/dev.21509 · Cited by 30
Hodges, T. E., Eltahir, A. M., Patel, S. D., Bredewold, R., Veenema, A. H., & McCormick, C. M. (2019) · Hormones and Behavior · doi:10.1016/j.yhbeh.2019.104579 · Cited by 28
Domestication 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
“…development and sociocognitive development in the juvenile period has been demonstrated across several of rat strains (Baarendse et al., 2013; Bell et al., 2010; Einon et al., 1978; Himmler, Pellis, & Kolb, 2013; Himmler et al., 2018; Schneider, Bindila, et al., 2016; Schneider, Pätz, et…”
BackgroundMethodInfluentialSelf-citationHimmler, B. T., Mychasiuk, R., Nakahashi, A., Himmler, S. M., Pellis, S. M., & Kolb, B. E. (2017) · Synapse · doi:10.1002/syn.22022 · Cited by 25
“Whereas the play-induced pruning of the mPFC has been replicated multiple times (Bell et al., 2010; Burleson et al., 2016; Himmler et al., 2013), the partner-induced proliferation of complexity in the OFC has yielded conflicting results—it was replicated twice in Bell et al. (2010), but not by…”
BackgroundMethodResultInfluentialSelf-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 24
Self-citationIntergenerational Sex-Specific Transmission of Maternal Social Experience
Faraji, J., Karimi, M., Soltanpour, N., Rouhzadeh, Z., Roudaki, S., Hosseini, S. A., Jafari, S. Y., Abdollahi, A. A., Soltanpour, N., Moeeini, R., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-28729-8 · Cited by 25
Wang, H., Li, J., Wang, H., Sun, Y., Liu, R., Wang, X., Su, Y., & Si, T. (2020) · Neuroscience Bulletin · doi:10.1007/s12264-020-00499-2 · Cited by 22
Metadata
- Authors
- Bell, H. C., Pellis, S. M., & Kolb, B.
- Affiliations
- University of Lethbridge (CA)
- Corresponding author
- Bell, Heather C.
- Venue
- Behavioural Brain Research
- Publisher
- Elsevier BV
- Published
- 2010-02-11
- Volume
- 207
- Issue
- 1
- Pages
- 7-13
- ISSN
- 0166-4328 (ISSN-L)
- OpenAlex
- W2159471102
- Semantic Scholar
- 42bad78d1e7212e62089b41a5ef8861c76be5794
- Cited by
- 217
- References
- 72
- Citations by year
- 2026: 5 · 2025: 8 · 2024: 14 · 2023: 19 · 2022: 12 · 2021: 10 · 2020: 11 · 2019: 14 · 2018: 15 · 2017: 17 · 2016: 14 · 2015: 15 · 2014: 14 · 2013: 18 · 2012: 11
- FWCI
- 13.06
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Behavioural Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Natural Sciences and Engineering Research Council of Canada
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- peer play, orbitofrontal cortex, medial prefrontal cortex, neuronal morphology, social behavior development, rat development, Golgi staining
- MeSH terms
- Analysis of Variance, Animals, Dendrites, Female, Neuronal Plasticity, Peer Group, Play and Playthings, Social Behavior, Social Isolation, Silver Staining, Prefrontal Cortex, Rats, Long-Evans, Dendritic Spines, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
