Social play in juvenile hamsters alters dendritic morphology in the medial prefrontal cortex and attenuates effects of social stress in adulthood

Burleson, Cody A.; Pedersen, Robert W.; Seddighi, Sahba; DeBusk, Lauren E.; Burghardt, Gordon M.; Cooper, Matthew A.

doi:10.1037/bne0000148

Cited by 69Stress Responses and CortisolNeuroendocrine regulation and behaviorMemory and Neural Mechanisms

Social play in juvenile hamsters alters dendritic morphology in the medial prefrontal cortex and attenuates effects of social stress in adulthood

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Burleson, Cody A., Pedersen, Robert W., Seddighi, Sahba, DeBusk, Lauren E., Burghardt, Gordon M., Cooper, Matthew A.·2016·Behavioral Neuroscience

DOI 10.1037/bne0000148PMC PMC4961604

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Abstract

Social play is a fundamental aspect of behavioral development in many species. Social play deprivation in rats alters dendritic morphology in the ventromedial prefrontal cortex (vmPFC) and we have shown that this brain region regulates responses to social defeat stress in Syrian hamsters. In this study, we tested whether play deprivation during the juvenile period disrupts dendritic morphology in the prefrontal cortex and potentiates the effects of social defeat stress. At weaning, male hamsters were either group-housed with peers or pair-housed with their mother, with whom they do not play. In adulthood, animals received acute social defeat stress or no-defeat control treatment. The hamsters were then tested for a conditioned defeat response in a social interaction test with a novel intruder, and were also tested for social avoidance of a familiar opponent. Brains were collected for Golgi-Cox staining and analysis of dendritic morphology in the infralimbic (IL), prelimbic (PL), and orbitofrontal cortex (OFC). Play-deprived animals showed an increased conditioned defeat response and elevated avoidance of a familiar opponent compared with play-exposed animals. Furthermore, play-deprived animals showed increased total length and branch points in apical dendrites of pyramidal neurons in the IL and PL cortices, but not in the OFC. These findings suggest that social play deprivation in juvenile hamsters disrupts neuronal development in the vmPFC and increases vulnerability to the effects of social stress in adulthood. Overall, these results suggest that social play is necessary for the natural dendritic pruning process during adolescence and promotes coping with stress in adulthood. (PsycINFO Database Record

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The convergence of evidence from this study and others using different manipulations points to play experience being the critical driver of the impairments observed.
“Nevertheless, the convergence of evidence from our study and others using different manipulations (e.g., reducing play by rearing juveniles with an adult or a peer from a less playful strain) points to play experience being the critical driver of the impairments observed (Schneider et al., 2016; Burleson et al., 2016; Pellis et al., 2017; Stark and Pellis, 2020, 2021).”
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 Burleson et al., 2016

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Giedd, J. N., Blumenthal, J., Jeffries, N. O., Castellanos, F. X., Liu, H., Zijdenbos, A., Paus, T., Evans, A. C., & Rapoport, J. L. (1999) · Nature Neuroscience · doi:10.1038/13158 · Cited by 5,552 · see citing works
Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex
Rakic, P., Bourgeois, J.-P., Eckenhoff, M. F., Zecevic, N., & Goldman-Rakic, P. S. (1986) · Science · doi:10.1126/science.3952506 · Cited by 1,133 · 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
Self-citation
The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive
Goldman-Rakic, P. S. (1996) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.1996.0129 · Cited by 1,072 · see citing works
Chronic behavioral stress induces apical dendritic reorganization in pyramidal neurons of the medial prefrontal cortex
Radley, J. J., Sisti, H. M., Hao, J., Rocher, A. B., McCall, T., Hof, P. R., McEwen, B. S., & Morrison, J. H. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.01.006 · Cited by 769 · see citing works
Synaptic and Behavioral Profile of Multiple Glutamatergic Inputs to the Nucleus Accumbens
Britt, J. P., Benaliouad, F., McDevitt, R. A., Stuber, G. D., Wise, R. A., & Bonci, A. (2012) · Neuron · doi:10.1016/j.neuron.2012.09.040 · Cited by 716 · 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 neurobiology of social play behavior in rats
Vanderschuren, L. J. M. J., Niesink, R. J. M., & Van Pee, J. M. (1997) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(96)00020-6 · Cited by 559 · see citing works
The Role of the Medial Prefrontal Cortex in the Conditioning and Extinction of Fear
Giustino, T. F., & Maren, S. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00298 · Cited by 519 · see citing works
Social buffering of the stress response: diversity, mechanisms, and functions
Hennessy, M. B., Kaiser, S., & Sachser, N. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.06.001 · Cited by 477 · 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
A role for synaptic plasticity in the adolescent development of executive function
Selemon, L. D. (2013) · Translational Psychiatry · doi:10.1038/tp.2013.7 · Cited by 439 · cited 1× · see citing works
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Background
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Do-Monte, F. H., Manzano-Nieves, G., Quiñones-Laracuente, K., Ramos-Medina, L., & Quirk, G. J. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.3137-14.2015 · Cited by 385 · see citing works
On the Functions of Play and Its Role in Behavioral Development
Martin, P., & Caro, T. (1985) · Advances in the study of behavior · doi:10.1016/s0065-3454(08)60487-8 · Cited by 369 · see citing works
stereotaxic atlas of the golden hamster brain
Morin, L. P., & Wood, R. I. (2001) · Academic eBooks · Cited by 312 · see citing works
Role of the medial prefrontal cortex in coping and resilience
Maier, S. F., & Watkins, L. R. (2010) · Brain Research · doi:10.1016/j.brainres.2010.08.039 · Cited by 292 · see citing works
Neural Mechanisms of the Testosterone–Aggression Relation: The Role of Orbitofrontal Cortex
Mehta, P. H., & Beer, J. S. (2009) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21389 · Cited by 286 · see citing works
Prefrontal Cortical Circuit for Depression- and Anxiety-Related Behaviors Mediated by Cholecystokinin: Role of ΔFosB
Vialou, V., Bagot, R. C., Cahill, M. E., Ferguson, D., Robison, A. J., Dietz, D. M., Fallon, B., Mazei-Robison, M., Ku, S. M., Harrigan, E., et al. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.1787-13.2014 · Cited by 283 · cited 1× · see citing works
“…(Do-Monte, Manzano-Nieves, QuinonesLaracuente, Ramos-Medina, & Quirk, 2015; Giustino & Maren, 2015), the neuroendocrine stress response (Radley, Gosselink, & Sawchenko, 2009), acquisition of anxiety and depression-like behavior (Vialou et al., 2014), and drug seeking behavior (Britt et al., 2012).”
Background
A Discrete GABAergic Relay Mediates Medial Prefrontal Cortical Inhibition of the Neuroendocrine Stress Response
Radley, J. J., Gosselink, K. L., & Sawchenko, P. E. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5924-08.2009 · Cited by 268 · see citing works
Differential rates of attack, defense, and counterattack during the developmental decrease in play fighting by male and female rats
Pellis, S. M., & Pellis, V. C. (1990) · Developmental Psychobiology · doi:10.1002/dev.420230303 · Cited by 255 · see citing works
Stress-Induced Dendritic Remodeling in the Prefrontal Cortex is Circuit Specific
Shansky, R. M., Hamo, C., Hof, P. R., McEwen, B. S., & Morrison, J. H. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp003 · Cited by 248 · see citing works
Peripuberty stress leads to abnormal aggression, altered amygdala and orbitofrontal reactivity and increased prefrontal MAOA gene expression
Márquez, C., Poirier, G. L., Cordero, M. I., Larsen, M. H., Groner, A., Marquis, J., Magistretti, P. J., Trono, D., & Sandi, C. (2013) · Translational Psychiatry · doi:10.1038/tp.2012.144 · Cited by 245 · see citing works
Conditioned defeat in male and female syrian hamsters
Huhman, K. L., Solomon, M. B., Janicki, M., Harmon, A. C., Lin, S. M., Israel, J. E., & Jasnow, A. M. (2003) · Hormones and Behavior · doi:10.1016/j.yhbeh.2003.05.001 · Cited by 239 · see citing works
Role of Prefrontal Cortex Glucocorticoid Receptors in Stress and Emotion
McKlveen, J. M., Myers, B., Flak, J. N., Bundzikova, J., Solomon, M. B., Seroogy, K. B., & Herman, J. P. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.03.024 · Cited by 237 · see citing works
Environmental Enrichment Confers Stress Resiliency to Social Defeat through an Infralimbic Cortex-Dependent Neuroanatomical Pathway
Lehmann, M. L., & Herkenham, M. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.0577-11.2011 · Cited by 234 · see citing works
Brief periods of socialization and later behavior in the rat
Einon, D. F., Morgan, M. J., & Kibbler, C. C. (1978) · Developmental Psychobiology · doi:10.1002/dev.420110305 · Cited by 232 · see citing works
Current Perspectives on the Biological Study of Play: Signs of Progress
Graham, K. L., & Burghardt, G. M. (2010) · The Quarterly Review of Biology · doi:10.1086/656903 · Cited by 229 · see citing works
Self-citation
Neural mechanisms of the testosterone-aggression relation: The role of the orbito-frontal cortex
Mehta, P. H. (2010) · PsycEXTRA Dataset · doi:10.1037/e554362012-158 · Cited by 221 · see citing works
Juvenile peer play experience and the development of the orbitofrontal and medial prefrontal cortices
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
Isolation during the play period in infancy decreases adult social interactions in rats
Hol, T., Van den Berg, C. L., Van Ree, J. M., & Spruijt, B. M. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(98)00116-8 · Cited by 212 · see citing works
Play fighting of rats in comparative perspective: a schema for neurobehavioral analyses
Pellis, S. M., & Pellis, V. C. (1998) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(97)00071-7 · Cited by 210 · see citing works
Early social experience is critical for the development of cognitive control and dopamine modulation of prefrontal cortex function
Baarendse, 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
Effects of neonatal decortication on the social play of juvenile rats
Panksepp, J., Normansell, L., Cox, J. F., & Siviy, S. M. (1994) · Physiology & Behavior · doi:10.1016/0031-9384(94)90285-2 · Cited by 204 · see citing works
Chronic juvenile stress produces corticolimbic dendritic architectural remodeling and modulates emotional behavior in male and female rats
Eiland, L. R., Ramroop, J. R., Hill, M. N., Manley, J., & McEwen, B. S. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.04.015 · Cited by 203 · see citing works
Comparison of the effects of bilateral orbital prefrontal cortex lesions and amygdala lesions on emotional responses in rhesus monkeys
Izquierdo, A., Suda, R. K., & Murray, E. A. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1232-05.2005 · Cited by 186 · see citing works
Untitled work
(2010) · American journal of play · Cited by 179 · see citing works
Contributions of the orbitofrontal cortex to impulsive choice: interactions with basal levels of impulsivity, dopamine signalling, and reward-related cues
Zeeb, F. D., Floresco, S., & Winstanley, C. A. (2010) · Psychopharmacology · doi:10.1007/s00213-010-1871-2 · Cited by 177 · see citing works
Behavioural rigidity and rule-learning deficits following isolation-rearing in the rat: neurochemical correlates
Jones, G. H., Marsden, C. A., & Robbins, T. W. (1991) · Behavioural Brain Research · doi:10.1016/s0166-4328(05)80050-6 · Cited by 172 · see citing works
In search of the neurobiological substrates for social playfulness in mammalian brains
Siviy, S. M., & Panksepp, J. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.03.006 · Cited by 162 · see citing works
Dendritic pruning of the medial amygdala during pubertal development of the male Syrian hamster
Zehr, J. L., Todd, B. J., Schulz, K. M., McCarthy, M. M., & Sisk, C. L. (2006) · Journal of Neurobiology · doi:10.1002/neu.20251 · Cited by 145 · see citing works
The Role of the Cortex in Play Fighting by Rats: Developmental and Evolutionary Implications
Pellis, S. M., Pellis, V. C., & Whishaw, I. Q. (2008) · Brain Behavior and Evolution · doi:10.1159/000114124 · Cited by 132 · see citing works
Prefrontal cortex reactivity underlies trait vulnerability to chronic social defeat stress
Kumar, S., Hultman, R. C., Hughes, D. N., Michel, N., Katz, B. M., & Dzirasa, K. (2014) · Nature Communications · doi:10.1038/ncomms5537 · Cited by 130 · see citing works
Chronic stress alters inhibitory networks in the medial prefrontal cortex of adult mice
Gilabert-Juan, J., Castillo-Gomez, E., Guirado, R., Moltó, M. D., & Nacher, J. (2013) · Brain Structure and Function · doi:10.1007/s00429-012-0479-1 · Cited by 125 · see citing works
Behavioural changes following lesions of the orbital prefrontal cortex in male rats
de Bruin, J. P. C., van Oyen, H. G., & van de Poll, N. E. (1983) · Behavioural Brain Research · doi:10.1016/0166-4328(83)90032-3 · Cited by 124 · see citing works
Scent marking and the maintenance of dominant/subordinate status in male golden hamsters
Ferris, C. F., Axelson, J. F., Shinto, L. H., & Albers, H. E. (1987) · Physiology & Behavior · doi:10.1016/0031-9384(87)90114-4 · Cited by 119 · see citing works
Plasticity and functions of the orbital frontal cortex
Kolb, B. E., Pellis, S. M., & Robinson, T. E. (2004) · Brain and Cognition · doi:10.1016/s0278-2626(03)00278-1 · Cited by 116 · see citing works
Individual housing during the play period results in changed responses to and consequences of a psychosocial stress situation in rats
Von Frijtag, J. C., Schot, M., van den Bos, R., & Spruijt, B. M. (2002) · Developmental Psychobiology · doi:10.1002/dev.10057 · Cited by 116 · see citing works
The effects of orbital frontal cortex damage on the modulation of defensive responses by rats in playful and nonplayful social contexts.
Pellis, S. M., Hastings, E., Shimizu, T., Kamitakahara, H., Komorowska, J., Forgie, M. L., & Kolb, B. (2006) · Behavioral Neuroscience · doi:10.1037/0735-7044.120.1.72 · Cited by 116 · 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
Recognition of Familiar Individuals in Golden Hamsters: A New Method and Functional Neuroanatomy
Lai, W., Ramiro, L.-L. R., Yu, H. A., & Johnston, R. E. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2124-05.2005 · Cited by 104 · see citing works
MicroRNAs as biomarkers of resilience or vulnerability to stress
Chen, R. J., Kelly, G., Sengupta, A., Heydendael, W., Nicholas, B., Beltrami, S., Luz, S., Peixoto, L., Abel, T. G., & Bhatnagar, S. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.07.045 · Cited by 100 · see citing works
Cortical Region Interactions and the Functional Role of Apical Dendrites
Spratling, M. (2002) · Behavioral and Cognitive Neuroscience Reviews · doi:10.1177/1534582302001003003 · Cited by 99 · see citing works
Play‐fighting in the Syrian golden hamster Mesocricetus auratus waterhouse, and its relationship to serious fighting during postweaning development
Pellis, S. M., & Pellis, V. C. (1988) · Developmental Psychobiology · doi:10.1002/dev.420210404 · Cited by 96 · see citing works
Stress and the development of agonistic behavior in golden hamsters
Delville, Y., David, J. T., Taravosh‐Lahn, K., & Wommack, J. C. (2003) · Hormones and Behavior · doi:10.1016/s0018-506x(03)00130-2 · Cited by 93 · see citing works
Individual Housing From Rearing Modifies the Performance of Young Rats on the Elevated Plus-Maze Apparatus
SILVA, N. L. D., Ferreira, V. M. M., Carobrez, A. P., & Morato, G. S. (1996) · Physiology & Behavior · doi:10.1016/s0031-9384(96)00254-5 · Cited by 90 · see citing works
Peripubertal stress-induced behavioral changes are associated with altered expression of genes involved in excitation and inhibition in the amygdala
Tzanoulinou, S., Riccio, O., de Boer, M. W., & Sandi, C. (2014) · Translational Psychiatry · doi:10.1038/tp.2014.54 · Cited by 87 · see citing works
Juvenile play experience primes neurons in the medial prefrontal cortex to be more responsive to later experiences
Himmler, 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
Increased corticosterone in peripubertal rats leads to long-lasting alterations in social exploration and aggression
Veenit, V., Cordero, M. I., Tzanoulinou, S., & Sandi, C. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00026 · Cited by 68 · see citing works
Ventral medial prefrontal cortex inactivation impairs impulse control but does not affect delay-discounting in rats
Feja, M., & Koch, M. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.02.013 · Cited by 62 · see citing works
Neural circuitry of play fighting in golden hamsters
Cheng, S.-Y., Taravosh-Lahn, K., & Delville, Y. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.07.048 · Cited by 59 · see citing works
Social status alters defeat-induced neural activation in Syrian hamsters
Morrison, K. E., Curry, D. W., & Cooper, M. A. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.03.002 · Cited by 44 · see citing works
Self-citation
Alterations in neuronal morphology in infralimbic cortex predict resistance to fear extinction following acute stress
Moench, K. M., Maroun, M., Kavushansky, A., & Wellman, C. (2016) · Neurobiology of Stress · doi:10.1016/j.ynstr.2015.12.002 · Cited by 41 · see citing works
Maintenance of dominance status is necessary for resistance to social defeat stress in Syrian hamsters
Morrison, K. E., Bader, L. R., Clinard, C. T., Gerhard, D. M., Gross, S. E., & Cooper, M. A. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.05.041 · Cited by 41 · see citing works
Self-citation
Social housing conditions around puberty determine later changes in plasma cortisol levels and behavior
Kaiser, S., Harderthauer, S., Sachser, N., & Hennessy, M. B. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.10.002 · Cited by 41 · see citing works
Perturbations in reward-related decision-making induced by reduced prefrontal cortical GABA transmission: Relevance for psychiatric disorders
Piantadosi, P. T., Khayambashi, S., Schluter, M. G., Kutarna, A., & Floresco, S. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.10.007 · Cited by 40 · see citing works
Learned stressor resistance requires extracellular signal-regulated kinase in the prefrontal cortex
Christianson, J. P., Flyer-Adams, J. G., Drugan, R. C., Amat, J., Daut, R. A., Foilb, A. R., Watkins, L. R., & Maier, S. F. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00348 · Cited by 39 · see citing works
The medial prefrontal cortex is both necessary and sufficient for the acquisition of conditioned defeat
Markham, C. M., Luckett, C., & Huhman, K. L. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.09.026 · Cited by 32 · see citing works
Glucocorticoids and the Development of Agonistic Behaviour during Puberty in Male Golden Hamsters
Wommack, J. C., Salinas, A. G., & Delville, Y. (2005) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2005.01369.x · Cited by 31 · see citing works
The modulation of play fighting in rats: Role of the motor cortex.
Kamitakahara, H., Monfils, M., Forgie, M. L., Kolb, B. E., & Pellis, S. M. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.1.164 · Cited by 29 · see citing works
Social isolation and cohabitation with haloperidol- treated partners: Effect on density of striatal dopamine D2 receptors in the developing rat brain
Bean, G., & Lee, T. (1991) · Psychiatry Research · doi:10.1016/0165-1781(91)90029-o · Cited by 26 · see citing works
Defeat-induced activation of the ventral medial prefrontal cortex is necessary for resistance to conditioned defeat
Morrison, K. E., Bader, L. R., McLaughlin, C. N., & Cooper, M. A. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.01.006 · Cited by 21 · see citing works
Self-citation
Characterization of offensive responses during the maturation of play‐fighting into aggression in male golden hamsters
Cervantes, M., Taravosh‐Lahn, K., Wommack, J. C., & Delville, Y. (2006) · Developmental Psychobiology · doi:10.1002/dev.20183 · Cited by 21 · see citing works
5-HT1A receptor activation reduces fear-related behavior following social defeat in Syrian hamsters
Bader, L. R., Carboni, J. D., Burleson, C. A., & Cooper, M. A. (2014) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2014.03.024 · Cited by 17 · see citing works
Self-citation
Play fighting of juvenile golden hamsters (Mesocricetus auratus): effects of two types of social deprivation and days of testing
Guerra, R. F., Takase, E., & Nunes, C. R. D. O. (1999) · Behavioural Processes · doi:10.1016/s0376-6357(99)00058-3 · Cited by 13 · see citing works
Effects of different opportunities for social interaction on the play fighting behavior in male and female golden hamsters (Mesocricetus auratus)
Vieira, M. L., Garcia, M. P., Rau, D. D. W., & Prado, A. B. (2005) · Developmental Psychobiology · doi:10.1002/dev.20101 · Cited by 6 · see citing works
Untitled work
(1999) · doi:10.1002/(sici)1098-2302(199903)34:2

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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
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Galaj, E., Barrera, E. D., & Ranaldi, R. (2019) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2019.172829 · Cited by 55 · see citing works
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Wooddell, L. J., Hamel, A. F., Murphy, A. M., Byers, K. L., Kaburu, S., Meyer, J. S., Suomi, S. J., & Dettmer, A. M. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.06.018 · Cited by 48 · see citing works
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Heintz, M. R., Murray, C. M., Markham, A. C., Pusey, A. E., & Lonsdorf, E. V. (2017) · American Journal of Primatology · doi:10.1002/ajp.22716 · Cited by 48 · see citing works
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 41 · see citing works
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“, reducing play by rearing juveniles with an adult or a peer from a less playful strain) points to play experience being the critical driver of the impairments observed (Schneider et al., 2016; Burleson et al., 2016; Pellis et al., 2017; Stark and Pellis, 2020, 2021).”
Background
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From Play Date to Stress Fate: Juvenile Social Play Rescues Stress‐Induced Changes in Adult Social Behavior
Whitten, C. J., Kelly, J. R., Gillespie, A. L., Brooks, H. J. B., Hooker, M. K., Temple, A., Hennon, L. M., Kilgore, B. J., Singamaneni, Y. B., Schulz, K. M., et al. (2025) · Developmental Psychobiology · doi:10.1002/dev.70020 · Cited by 7 · see citing works
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Comparing 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 · see citing works
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Development of social play in hamsters: Sex differences and their possible functions
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Alterations in dendritic spine plasticity in the prefrontal cortex induced by social play restrictions in male rats
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Authors: Burleson, C. A., Pedersen, R. W., Seddighi, S., DeBusk, L. E., Burghardt, G. M., & Cooper, M. A.
ORCID: Seddighi, Sahba
DeBusk, Lauren E.
Burghardt, Gordon M.
Cooper, Matthew A.
Venue: Behavioral Neuroscience
Publisher: American Psychological Association (APA)
Published: 2016-08
Volume: 130
Issue: 4
Pages: 437-447
ISSN: 0735-7044 (ISSN-L)
1939-0084
DOI: 10.1037/bne0000148
PMC: PMC4961604
OpenAlex: W2380856064
Cited by: 69
References: 76
Citations by year: 2026: 4 · 2025: 6 · 2024: 9 · 2023: 11 · 2022: 4 · 2021: 7 · 2020: 5 · 2019: 5 · 2018: 7 · 2017: 9 · 2016: 2
FWCI: 4.90
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: other-oa
www.apa.org/pubs/journals/resources/open-access.aspx (am, 284 d)
Locations: Behavioral Neuroscience (publishedVersion, other-oa)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health (R21 MH098190)
University of Tennessee
Topics: Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords: social play, play deprivation, medial prefrontal cortex, dendritic morphology, social defeat stress, social avoidance, infralimbic cortex, prelimbic cortex, orbitofrontal cortex, dendritic pruning, stress coping
MeSH terms: Animals, Brain, Dendrites, Female, Male, Mesocricetus, Neuronal Plasticity, Social Behavior, Prefrontal Cortex, Rats

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Social play in juvenile hamsters alters dendritic morphology in the medial prefrontal cortex and attenuates effects of social stress in adulthood

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