Expression of c-fos gene activation during rough and tumble play in juvenile rats
Abstract
Rough and tumble (R&T) play is an intrinsic behavior in most mammals. However, unlike sex and aggression, play has not been well characterized in terms of neuronal circuitry. We employed in situ hybridization to explore the differences of c-fos mRNA activation in juvenile rats that had been allowed R&T play for a total of 30 min before sacrifice contrasted to animals with comparable histories that had received no play. Densitometric estimates of c-fos gene activation revealed that the deep and dorsolateral tectum, inferior colliculus, dorsal periaquaductal gray, ventromedial hypothalamus, dorsal and ventral striatum, and somatosensory cortex were significantly more activated in animals that had played than those that had not. Prior play dominance and amount of social experience had no clear effects on the levels of c-fos gene expression. This provides a variety of new hypotheses concerning the role of various brain areas in the elaboration of R&T play behavior, but the important role of other types of motor arousal in the differential effects were not evaluated in this study.
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The activation patterns in many of these regions correlated with one another, suggesting that the coordinated activity, rather than individual activation, of specific brain circuits is necessary for proper play behavior.
“The activation patterns in many of these regions correlated with one another, suggesting that the coordinated activity, rather than individual activation, of specific brain circuits is necessary for proper play behavior.”
From Developmental origins of sex differences in the neural circuitry of play (2020) · cites this paper as Gordon et al., 2002
Play activates several distinct brain regions, including those involved in motivation, reward, sensory, and motor processing.
“Using this methodology, two leading play research groups demonstrated that play activates several distinct brain regions, including those involved in motivation, reward, sensory, and motor processing (Gordon et al., 2002; van Kerkhof et al., 2014).”
From Developmental origins of sex differences in the neural circuitry of play (2020) · cites this paper as Gordon et al., 2002
Social play enhances neuronal activity in a broad network of limbic and corticostriatal structures.
“Social play enhances neuronal activity in a broad network of limbic and corticostriatal structures”
From Social Play Behavior Is Critical for the Development of Prefrontal Inhibitory Synapses and Cognitive Flexibility in Rats (2022) · cites this paper as Gordon et al., 2002
Cites
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
Affective Neuroscience: The Foundations of Human and Animal Emotions
Panksepp, J. (1998) · doi:10.1093/oso/9780195096736.001.0001 · Cited by 4,428 · see citing works
Self-citationIkemoto, S., & Panksepp, J. (1999) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00023-5 · Cited by 1,450 · see citing works
Self-citationThe 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
Panksepp, J. (1981) · Developmental Psychobiology · doi:10.1002/dev.420140405 · Cited by 537 · see citing works
Self-citationThe psychobiology of play: Theoretical and methodological perspectives
Panksepp, J., Siviy, S., & Normansell, L. (1984) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(84)90005-8 · Cited by 468 · see citing works
Self-citationAnticipation of play elicits high-frequency ultrasonic vocalizations in young rats.
Knutson, B. D., Burgdorf, J. S., & Panksepp, J. (1998) · Journal of comparative psychology · doi:10.1037/0735-7036.112.1.65 · Cited by 456 · see citing works
Self-citation(1998) · Journal of Consciousness Studies · Cited by 332 · see citing works
Self-citationKollack‐Walker, S., & Newman, S. W. (1995) · Neuroscience · doi:10.1016/0306-4522(94)00563-k · Cited by 315 · see citing works
Self-citationPlace conditioning reveals the rewarding aspect of social interaction in juvenile rats
Calcagnetti, D. J., & Schechter, M. D. (1992) · Physiology & Behavior · doi:10.1016/0031-9384(92)90101-7 · Cited by 284 · see citing works
Neurochemical mechanisms of the defensive behavior in the dorsal midbrain
Brandão, M. L., Anseloni, V. Z., Pandóssio, J. E., De Araújo, J. E., & Castilho, V. M. (1999) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(99)00038-x · Cited by 280 · see citing works
Social Stress in Hamsters: Defeat Activates Specific Neurocircuits within the Brain
Kollack‐Walker, S., Watson, S. J., & Akil, H. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-22-08842.1997 · Cited by 253 · see citing works
Self-citationAnticipation of rewarding electrical brain stimulation evokes ultrasonic vocalization in rats.
Burgdorf, J. S., Knutson, B. D., & Panksepp, J. (2000) · Behavioral Neuroscience · doi:10.1037/0735-7044.114.2.320 · Cited by 244 · see citing works
Self-citationForebrain expression of c-fos due to active maternal behaviour in lactating rats
Lonstein, J. S., Simmons, D. A., Swann, J. M., & Stern, J. M. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00283-2 · Cited by 237 · see citing works
PELLIS, S. M., FIELD, E. F., SMITH, L. K., & PELLIS, V. C. (1997) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(95)00060-7 · Cited by 234 · 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
Self-citationPlay as a reinforcer for maze-learning in juvenile rats
Humphreys, A. P., & Einon, D. F. (1981) · Animal Behaviour · doi:10.1016/s0003-3472(81)80173-x · Cited by 199 · see citing works
Lonstein, J. S., & Stern, J. M. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-09-03364.1997 · Cited by 183 · see citing works
Bandler, R. J., Depaulis, A., & Vergnes, M. (1985) · Behavioural Brain Research · doi:10.1016/0166-4328(85)90058-0 · Cited by 181 · see citing works
Sensory modulation of juvenile play in rats
Siviy, S. M., & Panksepp, J. (1987) · Developmental Psychobiology · doi:10.1002/dev.420200108 · Cited by 181 · see citing works
Self-citationSocial play in juvenile rats: A decade of methodological and experimental research
Thor, D. H., & Holloway, W. R. (1984) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(84)90004-6 · Cited by 176 · see citing works
Kinchla, R. A. (1992) · Annual Review of Psychology · doi:10.1146/annurev.ps.43.020192.003431 · Cited by 175 · see citing works
Numan, M., & Numan, M. J. (1995) · Behavioral Neuroscience · doi:10.1037//0735-7044.109.1.135 · Cited by 136 · see citing works
Neural substrates of aggression and flight in the cat
Siegel, A., & Pott, C. B. (1988) · Progress in Neurobiology · doi:10.1016/0301-0082(88)90015-9 · Cited by 130 · see citing works
Effects of morphine and naloxone on play‐rewarded spatial discrimination in juvenile rats
Normansell, L., & Panksepp, J. (1990) · Developmental Psychobiology · doi:10.1002/dev.420230108 · Cited by 126 · see citing works
Self-citationThe effects of early social isolation on the motivation for social play in juvenile rats
Ikemoto, S., & Panksepp, J. (1992) · Developmental Psychobiology · doi:10.1002/dev.420250404 · Cited by 121 · see citing works
Self-citationKollack‐Walker, Don, Watson, & Akil (1999) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1999.00354.x · Cited by 113 · see citing works
Panksepp, J. (1998) · Current Directions in Psychological Science · doi:10.1111/1467-8721.ep10774709 · Cited by 104 · see citing works
Self-citationSeeger, T., Sforzo, G. A., Pert, C. B., & Pert, A. (1984) · Brain Research · doi:10.1016/0006-8993(84)90436-0 · Cited by 100 · see citing works
Social play alters regional brain opioid receptor binding in juvenile rats
Vanderschuren, L. J. M. J., Stein, E. A., Wiegant, V. M., & Van Ree, J. M. (1995) · Brain Research · doi:10.1016/0006-8993(95)00256-p · Cited by 88 · see citing works
c-Fos expression in female hamster brain following sexual and aggressive behaviors
Joppa, M. A., Meisel, R. L., & Garber, M. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00179-m · Cited by 68 · see citing works
Pellis, S. M., Castañeda, E., McKenna, M. M., Tran-Nguyen, L. T. L., & Whishaw, I. Q. (1993) · Neuroscience Letters · doi:10.1016/0304-3940(93)90600-p · Cited by 68 · see citing works
Dorsomedial diencephalic involvement in the juvenile play of rats.
Siviy, S. M., & Panksepp, J. (1985) · Behavioral Neuroscience · doi:10.1037//0735-7044.99.6.1103 · Cited by 45 · see citing works
Self-citationMedial hypothalamic lesions and play fighting in juvenile rats.
Beatty, W., & Costello, K. B. (1983) · Physiology and Behavior · doi:10.1016/0031-9384(83)90110-5 · Cited by 17 · see citing works
Pellis, S. M. (1993) · doi:10.1002/1098-2337(1993)19:5
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Empathy: its ultimate and proximate bases
Preston, S. D., & de Waal, F. B. M. (2002) · Behavioral and Brain Sciences · doi:10.1017/s0140525x02000018 · Cited by 4,126 · see citing works
Consciousness without a cerebral cortex: A challenge for neuroscience and medicine
Merker, B. (2007) · Behavioral and Brain Sciences · doi:10.1017/s0140525x07000891 · Cited by 868 · see citing works
The power of play: A pediatric role in enhancing development in young children
Yogman, M., Garner, A., Hutchinson, J., Hirsh-Pasek, K., Golinkoff, R. M., COMMITTEE ON PSYCHOSOCIAL ASPECTS OF CHILD AND FAMILY HEALTH, & COUNCIL ON COMMUNICATIONS AND MEDIA (2018) · Pediatrics · doi:10.1542/peds.2018-2058 · Cited by 758 · see citing works
Evidence-based Kernels: Fundamental Units of Behavioral Influence
Embry, D. D., & Biglan, A. (2008) · Clinical Child and Family Psychology Review · doi:10.1007/s10567-008-0036-x · Cited by 396 · see citing works
Wöhr, M., & Schwarting, R. K. W. (2013) · Cell and Tissue Research · doi:10.1007/s00441-013-1607-9 · Cited by 371 · see citing works
Panteleimon Ekkekakis, A., Hall, E. E., & Petruzzello, S. J. (2005) · Journal of Sports Sciences · doi:10.1080/02640410400021492 · Cited by 375 · see citing works
Isgor, C., Kabbaj, M., Akil, H., & Watson, S. J. (2004) · Hippocampus · doi:10.1002/hipo.10207 · Cited by 341 · see citing works
Self-citationThe 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
Alexander, R., Aragón, O. R., Bookwala, J., Cherbuin, N., Gatt, J. M., Kahrilas, I. J., Kästner, N., Lawrence, A. B., Lowe, L. J., Morrison, R., et al. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.12.002 · Cited by 329 · see citing works
Bolaños, C. A., Barrot, M., Berton, O., Wallace-Black, D., & Nestler, E. J. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00570-5 · Cited by 267 · see citing works
Halperin, J. M., & Healey, D. M. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.07.006 · Cited by 237 · see citing works
Of Mice and Men: Natural Kinds of Emotions in the Mammalian Brain? A Response to Panksepp and Izard
Barrett, L. F., Lindquist, K. A., Bliss‐Moreau, E., Duncan, S., Gendron, M., Mize, J., & Brennan, L. E. (2007) · Perspectives on Psychological Science · doi:10.1111/j.1745-6916.2007.00046.x · Cited by 227 · 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
Vanderschuren, L. J. M. J., & Trezza, V. (2013) · Current Topics in Behavioral Neurosciences · doi:10.1007/978-3-662-45758-0_268 · Cited by 200 · see citing works
Panksepp, J. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.02.015 · Cited by 184 · see citing works
Self-citationSadananda, M., Wöhr, M., & Schwarting, R. K. W. (2008) · Neuroscience Letters · doi:10.1016/j.neulet.2008.02.002 · Cited by 169 · 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
Dopaminergic Neurotransmission in the Nucleus Accumbens Modulates Social Play Behavior in Rats
Manduca, A., Servadio, M., Damsteegt, R., Campolongo, P., Vanderschuren, L. J., & Trezza, V. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2016.22 · Cited by 149 · 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
Self-citationAn insular view of the social decision-making network
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Holland, F. H., Ganguly, P., Potter, D. N., Chartoff, E. H., & Brenhouse, H. C. (2014) · Neuroscience Letters · doi:10.1016/j.neulet.2014.02.023 · Cited by 125 · see citing works
Brain Sex Differences and the Organisation of Juvenile Social Play Behaviour
Auger, A. P., & Olesen, K. M. (2009) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2009.01871.x · Cited by 142 · see citing works
Supekar, K., Kochalka, J., Schaer, M., Wakeman, H. N., Qin, S., Padmanabhan, A., & Menon, V. (2018) · Brain · doi:10.1093/brain/awy191 · Cited by 118 · see citing works
A brain motivated to play: insights into the neurobiology of playfulness
Siviy, S. M. (2016) · Behaviour · doi:10.1163/1568539x-00003349 · Cited by 113 · see citing works
Gordon, N. S., Burke, S., Akil, H., Watson, S. J., & Panksepp, J. (2003) · Neuroscience Letters · doi:10.1016/s0304-3940(03)00158-7 · Cited by 106 · see citing works
Self-citationModeling depression: social dominance–submission gene expression patterns in rat neocortex
Kroes, R. A., Panksepp, J., Burgdorf, J. S., Otto, N. J., & Moskal, J. R. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.08.076 · Cited by 101 · see citing works
Self-citationStress, sensitive periods, and substance abuse
Andersen, S. L. (2019) · Neurobiology of Stress · doi:10.1016/j.ynstr.2018.100140 · Cited by 92 · see citing works
Cellular activation in limbic brain systems during social play behaviour in rats
van Kerkhof, L. W. M., Trezza, V., Mulder, T., Gao, P., Voorn, P., & Vanderschuren, L. J. M. J. (2013) · Brain Structure and Function · doi:10.1007/s00429-013-0558-y · Cited by 83 · see citing works
Is play a behavior system, and, if so, what kind?
Pellis, S. M., Pellis, V. C., Pelletier, A. N., & Leca, J. (2019) · Behavioural Processes · doi:10.1016/j.beproc.2018.12.011 · Cited by 77 · see citing works
Lewis, K. P., & Barton, R. A. (2006) · Journal of comparative psychology · doi:10.1037/0735-7036.120.1.31 · Cited by 77 · see citing works
Play fighting and the development of the social brain: The rat’s tale
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Stress during adolescence alters behavioral sensitization to amphetamine
Kabbaj, M., Isgor, C., Watson, S. J., & Akil, H. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00188-4 · Cited by 76 · see citing works
Self-citationManduca, A., Lassalle, O., Sepers, M., Campolongo, P., Cuomo, V., Marsicano, G., Kieffer, B., Vanderschuren, L. J. M. J., Trezza, V., & Manzoni, O. J. J. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00211 · Cited by 73 · see citing works
Play 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 · see citing works
Johnson, N. L., Carini, L. M., Schenk, M. E., Stewart, M., & Byrnes, E. M. (2011) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2011.00029 · Cited by 67 · see citing works
Comparative approaches in evolutionary psychology: molecular neuroscience meets the mind.
Panksepp, J., Moskal, J. R., Panksepp, J. B., & Kroes, R. A. (2002) · PubMed · Cited by 64 · see citing works
Self-citationBijlsma, 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
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
Lawrence, R. C., Bonner, H., Newsom, R. J., & Kelly, S. J. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.10.028 · Cited by 46 · see citing works
Dysfunctional play and dopamine physiology in the Fischer 344 rat
Siviy, S. M., Crawford, C. A., Akopian, G. K., & Walsh, J. P. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.02.009 · Cited by 44 · see citing works
Harro, J., Kanarik, M., Matrov, D., & Panksepp, J. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.02.016 · Cited by 44 · see citing works
Self-citationRicci, L. A., Grimes, J. M., & MELLONIJR, R. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.10.025 · Cited by 38 · see citing works
Bell, M. R., Hart, B. G., & Gore, A. C. (2015) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2015.11.024 · Cited by 37 · see citing works
Analysis of c-Fos induction in response to social interaction in male and female Fisher 344 rats
Perkins, A. E., Woodruff, E. R., Chun, L. E., Spencer, R. L., Varlinskaya, E. I., & Terrence Deak, B. (2017) · Brain Research · doi:10.1016/j.brainres.2017.07.022 · 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
Activation of limbic system structures by replay of ultrasonic vocalization in rats
Wöhr, M., & Schwarting, R. K. W. (2010) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-374593-4.00012-7 · Cited by 34 · see citing works
Sylvester, M. A., Goodell, D. J., Adams, J., & Bland, S. T. (2015) · Brain Research · doi:10.1016/j.brainres.2015.11.006 · Cited by 33 · see citing works
Siviy, S. M., & Harrison, K. A. (2008) · Journal of comparative psychology · doi:10.1037/0735-7036.122.1.1 · Cited by 32 · see citing works
Female juvenile play elicits Fos expression in dopaminergic neurons of the VTA.
Northcutt, K. V., & Nguyen, J. M. K. (2014) · Behavioral Neuroscience · doi:10.1037/a0035964 · Cited by 31 · see citing works
Hodges, T. E., Green, M. R., Simone, J. J., & McCormick, C. M. (2014) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2014.03.001 · Cited by 30 · see citing works
Mu opioid receptors in the medial preoptic area govern social play behavior in adolescent male rats
Zhao, C., Chang, L., Auger, A. P., Gammie, S. C., & Riters, L. V. (2020) · Genes Brain & Behavior · doi:10.1111/gbb.12662 · Cited by 28 · see citing works
Moore, H., Craft, T. K. S., Grimaldi, L. M., Babic, B., Brunelli, S. A., & Vannucci, S. J. (2010) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2009.11.013 · Cited by 29 · see citing works
Delville, Y., Newman, M. L., Wommack, J. C., Taravosh‐Lahn, K., & Cervantes, M. (2005) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195168761.003.0014 · Cited by 28 · see citing works
Double 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 · see citing works
Persistent activation of select forebrain regions in aggressive, adolescent cocaine-treated hamsters
Knyshevski, I., Connor, D. F., Harrison, R. J., Ricci, L. A., & Melloni, R. H. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.11.027 · Cited by 27 · see citing works
Achterberg, E. J. M., Trezza, V., & Vanderschuren, L. J. M. J. (2014) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000039 · Cited by 26 · see citing works
Reppucci, C. J., Gergely, C. K., & Veenema, A. H. (2018) · Journal of Neuroendocrinology · doi:10.1111/jne.12582 · Cited by 26 · see citing works
Vitor-Vieira, F., Vilela, F. C., & Giusti‐Paiva, A. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113503 · Cited by 24 · see citing works
Yamamuro, T., Senzaki, K., Iwamoto, S., Nakagawa, Y., Hayashi, T., Hori, M., Sakamoto, S., Murakami, K., Shiga, T., & Urayama, O. (2010) · Neuroscience Research · doi:10.1016/j.neures.2010.09.001 · Cited by 24 · see citing works
A comparison of tests for restricted orderings in the three‐class case
Alonzo, T. A., Nakas, C. T., Yiannoutsos, C. T., & Bucher, S. (2009) · Statistics in Medicine · doi:10.1002/sim.3536 · Cited by 24 · see citing works
Perkins, A. E., Varlinskaya, E. I., & Deak, T. (2019) · International review of neurobiology · doi:10.1016/bs.irn.2019.08.001 · Cited by 22 · see citing works
Sex differences in monoamines following amphetamine and social reward in adolescent rats.
Weiss, V. G., Hofford, R. S., Yates, J. R., Jennings, F. C., & Bardo, M. T. (2015) · Experimental and Clinical Psychopharmacology · doi:10.1037/pha0000026 · Cited by 22 · see citing works
A New Bioinformatics Paradigm for the Theory, Research, and Practice of Therapeutic Hypnosis
Atkinson, D., Iannotti, S., Cozzolino, M., Castiglione, S., Cicatelli, A., Vyas, B., Blake-Mortimer, J. S., Hill, R., Chovanec, E., Chiamberlando, A., et al. (2010) · American Journal of Clinical Hypnosis · doi:10.1080/00029157.2010.10401745 · Cited by 21 · see citing works
Social context induces two unique patterns of c‐Fos expression in adolescent and adult rats
Varlinskaya, E. I., Vogt, B. A., & SPEAR, L. P. (2012) · Developmental Psychobiology · doi:10.1002/dev.21064 · Cited by 20 · see citing works
Play and tickling responses map to the lateral columns of the rat periaqueductal gray
Gloveli, N., Simonnet, J., Tang, W., Concha‐Miranda, M., Maier, E., Dvorzhak, A., Schmitz, D., & Brecht, M. (2023) · Neuron · doi:10.1016/j.neuron.2023.06.018 · Cited by 20 · see citing works
Neale, D., Clackson, K., Georgieva, S., Dedetaş, H., Scarpate, M., Wass, S. V., & Leong, V. (2018) · Frontiers in Psychology · doi:10.3389/fpsyg.2018.00273 · Cited by 19 · see citing works
Hearing, touching, and multisensory integration during mate choice
Lenschow, C., Mendes, A. R. P., & Lima, S. Q. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.943888 · Cited by 17 · see citing works
Amygdala circuit transitions supporting developmentally-appropriate social behavior
Ferrara, N. C., & Opendak, M. M. (2023) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2023.107762 · Cited by 17 · see citing works
Social play behavior shapes the development of prefrontal inhibition in a region-specific manner
Bijlsma, A., Vanderschuren, L. J. M. J., & Wierenga, C. J. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhad212 · Cited by 16 · see citing works
The Value of Using an Evolutionary Framework for Gauging Children’s Well-Being
Narvaez, D. F., Panksepp, J., & Schore, A. N. (2013) · Cited by 14 · see citing works
Self-citationMarler, C. A., Trainor, B. C., Gleason, E. D., Bester‐Meredith, J. K., & Becker, E. A. (2008) · Elsevier eBooks · doi:10.1016/b978-012374285-8.00028-7 · Cited by 14 · see citing works
Cozzolino, M., & Celia, G. (2021) · American Journal of Clinical Hypnosis · doi:10.1080/00029157.2021.1947767 · Cited by 15 · see citing works
Playful genes: what do we know about the epigenetics of play behaviour?
Sgro, M., & Mychasiuk, R. (2020) · International Journal of Play · doi:10.1080/21594937.2020.1720139 · Cited by 12 · see citing works
Playback of Ultrasonic Vocalizations to Juvenile and Adult Rats: Behavioral and Neuronal Effects
Schwarting, R. K. W., Kisko, T. M., & Wöhr, M. (2018) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-809600-0.00034-2 · Cited by 13 · see citing works
The Value of Using an Evolutionary Framework for Gauging Children's Well-Being
Narvaez, D. F., Panksepp, J., Schore, A. N., & Gleason, T. R. (2012) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199755059.003.0001 · Cited by 13 · see citing works
Self-citationThe Role of Play in Contemporary Child Psychotherapy: A Developmental Perspective
Barish, K. (2020) · Journal of Infant Child and Adolescent Psychotherapy · doi:10.1080/15289168.2020.1756031 · Cited by 11 · see citing works
Social play behavior is driven by glycine-dependent mechanisms
Dvorzhak, A., Brecht, M., & Schmitz, D. (2024) · Current Biology · doi:10.1016/j.cub.2024.06.073 · Cited by 9 · see citing works
Kanarik, M., & Harro, J. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.08.049 · Cited by 9 · see citing works
Mild environmental intervention in mother-infant interactions reduces social play behavior in rats.
Karkow, A. R. M., & Lucion, A. B. (2013) · Psychology & Neuroscience · doi:10.3922/j.psns.2013.1.07 · Cited by 9 · see citing works
Basal ganglia involvement in the playfulness of juvenile rats
Siviy, S. M. (2019) · Journal of Neuroscience Research · doi:10.1002/jnr.24475 · Cited by 8 · see citing works
Spitzer, M. (2008) · Nervenheilkunde · doi:10.1055/s-0038-1627331 · Cited by 8 · see citing works
Borland, J. M. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105809 · Cited by 8 · see citing works
Bastle, R. M., Peartree, N. A., Goenaga, J. G., Hatch, K. N., Henricks, A. M., Scott, S. N., Hood, L. E., & Neisewander, J. L. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.07.024 · Cited by 7 · see citing works
Berg, E. L., & Silverman, J. L. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-816393-1.00010-5 · Cited by 4 · see citing works
Early Experience and Triune Ethics Orientations
Narvaez, D. F. (2016) · Palgrave Macmillan UK eBooks · doi:10.1057/978-1-137-55399-7_4 · Cited by 4 · see citing works
The meaning of barks: vocal communication of fearful and playful affective states in pigs
Chan, W. Y. (2011) · Research Exchange (Washington State University) · Cited by 4 · 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. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.05.01.070540 · Cited by 4 · see citing works
McKinney, J. E., Ludington, S. C., Butler, J. M., & O’Connell, L. A. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.11.28.518266 · Cited by 4 · see citing works
Advances in ethological approaches to explore rodent vocal communication
Abud, A., Wang, Y., Hafter, R., Tavakoli, E., Wu, C. S.-Y., Atapattu, S., Raza, A., Ali, M. H., Al-Hadi, A., Khalid, H., et al. (2025) · Frontiers in Ethology · doi:10.3389/fetho.2025.1563374 · Cited by 2 · see citing works
Panksepp, J., & Pincus, D. I. (2004) · Neuropsychoanalysis · doi:10.1080/15294145.2004.10773462 · Cited by 1 · see citing works
Self-citationThe Importance of Affective Neuroscience for Child Psychotherapy
Barish, K. (2023) · Journal of Infant Child and Adolescent Psychotherapy · doi:10.1080/15289168.2023.2178820 · Cited by 1 · see citing works
The brain at play: neural substrates of social play behaviour in adolescent rats
van Kerkhof, L. W. M. (2013) · Utrecht University Repository (Utrecht University) · Cited by 1 · see citing works
Vanderschuren, L. J. M. J., & Achterberg, E. J. M. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-819641-0.00021-9 · Cited by 1 · see citing works
The role of the amygdala in social behavior and alcoholism
Kosse, R. C. (2014) · Utrecht University Repository (Utrecht University)
Kanarik, M. (2007) · DSpace repository (University of Tartu)
Corrections to Panksepp (2008)
Barrett, L. F., & Lindquist, K. A. (2008)
The Value of Using an Evolutionary Framework for Gauging Children's
Narvaez, D. F., Panksepp, J., Schore, A. N., & Gleason, T. R. (2013)
Self-citationMartins, G. W., Chagas, G. S., Patrício, F. C., Lira, A. D. O., Fragoso, J., Santos, A. B., & Leandro, C. G. (2020) · Behavioural Processes · doi:10.1016/j.beproc.2020.104151
Measuring Social Communication in Rodent Models of Neurodevelopmental Disorders
Berg, E. L., & Silverman, J. L. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-819641-0.00002-5
- Authors
- Gordon, N. S., Kollack-Walker, S., Akil, H., & Panksepp, J.
- Affiliations
- Bowling Green State University (US)
- University of Michigan (US)
- Corresponding author
- Panksepp, Jaak
- Venue
- Brain Research Bulletin
- Publisher
- Elsevier BV
- Published
- 2002-03
- Volume
- 57
- Issue
- 5
- Pages
- 651-659
- ISSN
- 0361-9230 (ISSN-L)
- OpenAlex
- W2078189006
- Cited by
- 103
- References
- 36
- Citations by year
- 2025: 1 · 2024: 2 · 2023: 8 · 2022: 4 · 2021: 2 · 2020: 9 · 2019: 4 · 2018: 6 · 2017: 3 · 2016: 6 · 2015: 5 · 2014: 5 · 2013: 8 · 2012: 2
- FWCI
- 5.97
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain Research Bulletin (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- rough-and-tumble play, c-fos gene expression, young rats, neuronal activation, brain regions, tectum, inferior colliculus, hypothalamus, striatum, somatosensory cortex, social experience
- MeSH terms
- Aging, Animals, Arousal, Behavior, Animal, Brain, Brain Stem, Male, Motor Activity, Neurons, Play and Playthings, RNA, Messenger, Social Behavior, Up-Regulation, Proto-Oncogene Proteins c-fos, Rats, Long-Evans, Rats
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