Cellular activation in limbic brain systems during social play behaviour in rats

van Kerkhof, Linda W. M.; Trezza, Viviana; Mulder, Tessa; Gao, Ping; Voorn, Pieter; Vanderschuren, Louk J. M. J.

doi:10.1007/s00429-013-0558-y

Cited by 83Neuroendocrine regulation and behaviorMemory and Neural MechanismsNeurotransmitter Receptor Influence on Behavior

Cellular activation in limbic brain systems during social play behaviour in rats

Open access

van Kerkhof, Linda W. M., Trezza, Viviana, Mulder, Tessa, Gao, Ping, Voorn, Pieter, Vanderschuren, Louk J. M. J.·2013·Brain Structure and Function

DOI 10.1007/s00429-013-0558-yPMC PMC3770763

Open this paper in CoChat — free account

Abstract

Positive social interactions during the juvenile and adolescent phases of life are essential for proper social and cognitive development in mammals, including humans. During this developmental period, there is a marked increase in peer-peer interactions, signified by the abundance of social play behaviour. Despite its importance for behavioural development, our knowledge of the neural underpinnings of social play behaviour is limited. Therefore, the purpose of this study was to map the neural circuits involved in social play behaviour in rats. This was achieved by examining cellular activity after social play using the immediate early gene c-Fos as a marker. After a session of social play behaviour, pronounced increases in c-Fos expression were observed in the medial prefrontal cortex, medial and ventral orbitofrontal cortex, dorsal striatum, nucleus accumbens core and shell, lateral amygdala, several thalamic nuclei, dorsal raphe and the pedunculopontine tegmental nucleus. Importantly, the cellular activity patterns after social play were topographically organized in this network, as indicated by play-specific correlations in c-Fos activity between regions with known direct connections. These correlations suggest involvement in social play behaviour of the projections from the medial prefrontal cortex to the striatum, and of amygdala and monoaminergic inputs to frontal cortex and striatum. The analyses presented here outline a topographically organized neural network implicated in processes such as reward, motivation and cognitive control over behaviour, which mediates social play behaviour in rats.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1007/s00429-013-0558-y

Cites

127 of 127 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

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?

A pronounced increase in c-Fos expression has been observed in both the NAc core and shell following play fighting in rats.
“A pronounced increase in c-Fos expression has been observed in both the NAc core and shell following play fighting in rats54; however, only pharmacological inactivation of the NAc core, but not shell, interfered with social play behavior55.”
From Peripubertal stress increases play fighting at adolescence and modulates nucleus accumbens CB1 receptor expression and mitochondrial function in the amygdala (2018) · cites this paper as [54]
Substantial evidence supports the involvement of both NAc shell and core in play fighting.
“Substantial evidence supports the involvement of both NAc shell and core in play fighting.”
From Peripubertal stress increases play fighting at adolescence and modulates nucleus accumbens CB1 receptor expression and mitochondrial function in the amygdala (2018) · cites this paper as [54]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Primer3 on the WWW for General Users and for Biologist Programmers
Rozen, S., & Skaletsky, H. (2003) · Humana Press eBooks · doi:10.1385/1-59259-192-2:365 · Cited by 14,952 · see citing works
The adolescent brain and age-related behavioral manifestations
Spear, L. P. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00014-2 · Cited by 5,433 · see citing works
The reward circuit: linking primate anatomy and human imaging
Haber, S. N., & Knutson, B. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.129 · Cited by 3,718 · see citing works
The rat nervous system
Paxinos, G. (1985) · Cited by 3,715 · see citing works
Contributions of the Amygdala to Emotion Processing: From Animal Models to Human Behavior
Phelps, E. A., & LeDoux, J. E. (2005) · Neuron · doi:10.1016/j.neuron.2005.09.025 · Cited by 3,203 · cited 1× · see citing works
“It is widely accepted that the amygdala is important for the processing of negative emotions (Maren and Quirk 2004; Morrison and Salzman 2010; Phelps and Ledoux 2005).”
Why do many psychiatric disorders emerge during adolescence?
Paus, T., Keshavan, M., & Giedd, J. N. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2513 · Cited by 3,123 · see citing works
Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun.
Morgan, J., & Curran, T. (1991) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.14.030191.002225 · Cited by 2,689 · see citing works
Understanding adolescence as a period of social–affective engagement and goal flexibility
Crone, E. A., & Dahl, R. E. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3313 · Cited by 2,507 · see citing works
The debate over dopamine’s role in reward: the case for incentive salience
Berridge, K. C. (2007) · Psychopharmacology · doi:10.1007/s00213-006-0578-x · Cited by 2,347 · see citing works
Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex
Cardinal, R. N., Parkinson, J. A., Hall, J., & Everitt, B. J. (2002) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(02)00007-6 · Cited by 2,129 · see citing works
The social brain in adolescence
Blakemore, S.-J. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2353 · Cited by 1,896 · see citing works
The principal features and mechanisms of dopamine modulation in the prefrontal cortex
Seamans, J. K., & Yang, C. R. (2004) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2004.05.006 · Cited by 1,592 · see citing works
Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex
Ikemoto, S. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.05.004 · Cited by 1,477 · see citing works
The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking
Ikemoto, S., & Panksepp, J. (1999) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00023-5 · Cited by 1,450 · see citing works
Neuronal signalling of fear memory
Maren, S., & Quirk, G. J. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1535 · Cited by 1,428 · see citing works
Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates
Dalley, J. W., Cardinal, R. N., & Robbins, T. W. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.09.006 · Cited by 1,329 · see citing works
Affective neuroscience of pleasure: reward in humans and animals
Berridge, K. C., & Kringelbach, M. L. (2008) · Psychopharmacology · doi:10.1007/s00213-008-1099-6 · Cited by 1,254 · see citing works
Whole-Brain Mapping of Direct Inputs to Midbrain Dopamine Neurons
Watabe‐Uchida, M., Zhu, L., Ogawa, S. K., Vamanrao, A., & Uchida, N. (2012) · Neuron · doi:10.1016/j.neuron.2012.03.017 · Cited by 1,221 · see citing works
The amygdala and reward
Baxter, M. G., & Murray, E. A. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn875 · Cited by 1,200 · see citing works
Putting a spin on the dorsal-ventral divide of the striatum
Voorn, P., Vanderschuren, L. J. M. J., Groenewegen, H. J., Robbins, T. W., & Pennartz, C. M. A. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.06.006 · Cited by 1,188 · see citing works
Self-citation
The social re-orientation of adolescence: a neuroscience perspective on the process and its relation to psychopathology
NELSON, E. E., LEIBENLUFT, E., McCLURE, E. B., & PINE, D. S. (2005) · Psychological Medicine · doi:10.1017/s0033291704003915 · Cited by 1,075 · see citing works
Pattern and time course of immediate early gene expression in rat brain following acute stress
Cullinan, W. E., Herman, J. P., Battaglia, D. F., Akil, H., & Watson, S. J. (1995) · Neuroscience · doi:10.1016/0306-4522(94)00355-9 · Cited by 1,056 · see citing works
The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness
Van der Werf, Y. D., Witter, M. P., & Groenewegen, H. J. (2002) · Brain Research Reviews · doi:10.1016/s0165-0173(02)00181-9 · Cited by 994 · see citing works
Cortico-Basal Ganglia Reward Network: Microcircuitry
Sesack, S. R., & Grace, A. A. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.93 · Cited by 985 · see citing works
Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system
Lammel, S., Hetzel, A., Häckel, O., Jones, I., Liss, B., & Roeper, J. (2008) · Neuron · doi:10.1016/j.neuron.2008.01.022 · Cited by 976 · see citing works
The Neuropsychopharmacology of Fronto-Executive Function: Monoaminergic Modulation
Robbins, T. W., & Arnsten, A. F. T. (2009) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135535 · Cited by 957 · see citing works
Ventral striatal control of appetitive motivation: role in ingestive behavior and reward-related learning
Kelley, A. E. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2003.11.015 · Cited by 942 · see citing works
Basal ganglia
Alexander, G. E. (1998) · Cited by 891 · see citing works
The amygdalostriatal projection in the rat—an anatomical study by anterograde and retrograde tracing methods
Kelley, A. E., Domesick, V. B., & Nauta, W. J. H. (1982) · Neuroscience · doi:10.1016/0306-4522(82)90067-7 · Cited by 888 · see citing works
Prefrontal Glutamate Release into the Core of the Nucleus Accumbens Mediates Cocaine-Induced Reinstatement of Drug-Seeking Behavior
McFarland, K., Lapish, C. C., & Kalivas, P. W. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-08-03531.2003 · Cited by 884 · see citing works
Animal Play Behavior
Fagen, R. M. (1981) · Cited by 860 · see citing works
Mammalian Play: Training for the Unexpected
Spinka, M., Newberry, R. C., & Bekoff, M. (2001) · The Quarterly Review of Biology · doi:10.1086/393866 · Cited by 817 · see citing works
The neostriatal mosaic: II. Patch- and matrix-directed mesostriatal dopaminergic and non-dopaminergic systems
Gerfen, C. R., Herkenham, M. A., & Thibault, J. (1987) · Journal of Neuroscience · doi:10.1523/jneurosci.07-12-03915.1987 · Cited by 804 · see citing works
Projection-specific modulation of dopamine neuron synapses by aversive and rewarding stimuli
Lammel, S., Ion, D. I., Roeper, J., & Malenka, R. C. (2011) · Neuron · doi:10.1016/j.neuron.2011.03.025 · Cited by 766 · see citing works
The rostromedial tegmental nucleus (RMTg), a GABAergic afferent to midbrain dopamine neurons, encodes aversive stimuli and inhibits motor responses.
Jhou, T. C., Fields, H. L., Baxter, M. G., Saper, C. B., & Holland, P. C. (2009) · Neuron · doi:10.1016/j.neuron.2009.02.001 · Cited by 696 · see citing works
Projections of the medial and lateral prefrontal cortices to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat
McDonald, A. J., Mascagni, F., & Guo, L. (1996) · Neuroscience · doi:10.1016/0306-4522(95)00417-3 · Cited by 689 · see citing works
The specificity of the ‘nonspecific’ midline and intralaminar thalamic nuclei
Groenewegen, H. J., & Berendse, H. W. (1994) · Trends in Neurosciences · doi:10.1016/0166-2236(94)90074-4 · Cited by 596 · 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
Self-citation
The mesopontine rostromedial tegmental nucleus: A structure targeted by the lateral habenula that projects to the ventral tegmental area of tsai and substantia nigra compacta
Jhou, T. C., Geisler, S., Marinelli, M., Degarmo, B. A., & Zahm, D. S. (2009) · Journal of Comparative Neurology · doi:10.1002/cne.21891 · Cited by 503 · see citing works
Measurement of Immediate‐Early Gene Activation‐ <i>c‐fos</i> and Beyond
Kovács, K. J. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01734.x · Cited by 493 · see citing works
Encoding predicted outcome and acquired value in orbitofrontal cortex during cue sampling depends upon input from basolateral amygdala.
Schoenbaum, G., Setlow, B., Saddoris, M. P., & Gallagher, M. (2003) · Neuron · doi:10.1016/s0896-6273(03)00474-4 · Cited by 484 · 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
Beyond the reward hypothesis: alternative functions of nucleus accumbens dopamine
Salamone, J. D., Correa, M., Mingote, S., & Weber, S. (2004) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2004.09.004 · Cited by 454 · see citing works
Basal ganglia and movement disorders: an update
Chesselet, M., & Delfs, J. M. (1996) · Trends in Neurosciences · doi:10.1016/0166-2236(96)10052-7 · Cited by 402 · see citing works
Negative Reward Signals from the Lateral Habenula to Dopamine Neurons Are Mediated by Rostromedial Tegmental Nucleus in Primates
Hong, S., Jhou, T. C., Smith, M., Saleem, K. S., & Hikosaka, O. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.1384-11.2011 · Cited by 390 · see citing works
Functional–anatomical implications of the nucleus accumbens core and shell subterritories
ZAHM, D. S. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb09264.x · Cited by 384 · see citing works
The pleasures of play: pharmacological insights into social reward mechanisms
Trezza, V., Baarendse, P. J. J., & Vanderschuren, L. J. M. J. (2010) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2010.06.008 · Cited by 372 · see citing works
Self-citation
The integrative function of the basal ganglia in instrumental conditioning
Balleine, B. W., Liljeholm, M., & Ostlund, S. B. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.10.034 · Cited by 356 · see citing works
Re-valuing the amygdala
Morrison, S. E., & Salzman, C. D. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.02.007 · Cited by 341 · see citing works
Extended Amygdala and Basal Forebrain
Alheid, G. F. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07082.x · Cited by 334 · see citing works
Disconnection of the anterior cingulate cortex and nucleus accumbens core impairs Pavlovian approach behavior: Further evidence for limbic cortical-ventral striatopallidal systems.
Parkinson, J. A., Willoughby, P. J., Robbins, T. W., & Everitt, B. J. (2000) · Behavioral Neuroscience · doi:10.1037//0735-7044.114.1.42 · Cited by 309 · see citing works
Prefrontal Cortical–Ventral Striatal Interactions Involved in Affective Modulation of Attentional Performance: Implications for Corticostriatal Circuit Function
Christakou, A., Robbins, T. W., & Everitt, B. J. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0949-03.2004 · Cited by 281 · see citing works
Laterodorsal tegmental stimulation elicits dopamine efflux in the rat nucleus accumbens by activation of acetylcholine and glutamate receptors in the ventral tegmental area
Forster, G. L., & Blaha, C. D. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00250.x · Cited by 271 · see citing works
Basal ganglia and movement disorders: an update
Chesselet, M. (1996) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)10052-7 · Cited by 266 · see citing works
A role for mesencephalic dopamine in activation: commentary on Berridge (2006)
Robbins, T. W., & Everitt, B. J. (2006) · Psychopharmacology · doi:10.1007/s00213-006-0528-7 · Cited by 265 · see citing works
Nucleus Accumbens μ-Opioid Receptors Mediate Social Reward
Trezza, V., Damsteegt, R., Achterberg, E. J. M., & Vanderschuren, L. J. M. J. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.5492-10.2011 · Cited by 263 · see citing works
Self-citation
Evaluating the rewarding nature of social interactions in laboratory animals
Trezza, V., Campolongo, P., & Vanderschuren, L. J. M. J. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.05.007 · Cited by 258 · see citing works
Self-citation
Social Play and Autistic Spectrum Disorders: A Perspective on Theory, Implications and Educational Approaches
Jordan, R. (2003) · Autism · doi:10.1177/1362361303007004002 · Cited by 248 · see citing works
Multiple Differences in the Play Fighting of Male and Female Rats. Implications for the Causes and Functions of Play
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
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
Amphetamine-Induced Behavior, Dopamine Release, and c-fosmRNA Expression: Modulation by Environmental Novelty
Badiani, A., Oates, M. M., Day, H. E. W., Watson, S. J., Akil, H., & Robinson, T. E. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-24-10579.1998 · Cited by 226 · see citing works
Rough-and-Tumble Play and the Development of the Social Brain
Pellis, S. M., & Pellis, V. C. (2007) · Current Directions in Psychological Science · doi:10.1111/j.1467-8721.2007.00483.x · Cited by 225 · see citing works
Involvement of opioid and dopaminergic systems in isolation-induced pinning and social grooming of young rats
Niesink, R. J. M., & Van Ree, J. M. (1989) · Neuropharmacology · doi:10.1016/0028-3908(89)90038-5 · Cited by 222 · 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
Modulation of dopamine efflux in the nucleus accumbens after cholinergic stimulation of the ventral tegmental area in intact, pedunculopontine tegmental nucleus-lesioned, and laterodorsal tegmental nucleus-lesioned rats
Blaha, C. D., Allen, L., Das, S., Inglis, W. L., LATIMER, M. L., Vincent, S., & Winn, P. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-02-00714.1996 · Cited by 216 · see citing works
Braking Dopamine Systems: A New GABA Master Structure for Mesolimbic and Nigrostriatal Functions
Barrot, M., Sesack, S. R., Georges, F. E., Pistis, M., Hong, S., & Jhou, T. C. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.3370-12.2012 · Cited by 215 · see citing works
Cortically Driven Immediate-Early Gene Expression Reflects Modular Influence of Sensorimotor Cortex on Identified Striatal Neurons in the Squirrel Monkey
Parthasarathy, H. B., & Graybiel, A. M. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-07-02477.1997 · Cited by 214 · 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
Self-citation
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
Neuropsychopharmacology
Rendleman, R. L., & Walkup, J. T. (2012) · Elsevier eBooks · doi:10.1016/b978-1-4377-0435-8.00049-4 · Cited by 197 · see citing works
Endocannabinoids in Amygdala and Nucleus Accumbens Mediate Social Play Reward in Adolescent Rats
Trezza, V., Damsteegt, R., Manduca, A., Petrosino, S., Van Kerkhof, L. W. M., Pasterkamp, R. J., Zhou, Y., Campolongo, P., Cuomo, V., Di Marzo, V., et al. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.0114-12.2012 · Cited by 190 · see citing works
Self-citation
The orbital cortex in rats topographically projects to central parts of the caudate-putamen complex
Schilman, E. A., Uylings, H. B. M., Graaf, Y. G.-D., Joel, D., & Groenewegen, H. J. (2008) · Neuroscience Letters · doi:10.1016/j.neulet.2007.12.024 · Cited by 187 · 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
Topography of projections from the medial prefrontal cortex to the amygdala in the rat.
Cassell, M., & Wright, D. J. (1986) · Brain Research Bulletin · doi:10.1016/0361-9230(86)90237-6 · Cited by 161 · see citing works
Deficient Social and Play Behavior in Juvenile and Adult Rats after Neonatal Cortical Lesion: Effects of Chronic Pubertal Cannabinoid Treatment
Schneider, M., & Koch, M. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300634 · Cited by 160 · see citing works
Attention, play, and social behavior in ADHD preschoolers
Alessandri, S. M. (1992) · Journal of Abnormal Child Psychology · doi:10.1007/bf00916693 · Cited by 157 · see citing works
Rough-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 150 · see citing works
Modulation of dopamine efflux in the striatum following cholinergic stimulation of the substantia nigra in intact and pedunculopontine tegmental nucleus-lesioned rats
Blaha, C. D., & Winn, P. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-03-01035.1993 · Cited by 146 · see citing works
Interactions between the prefrontal cortex and amygdala during delay discounting and reversal.
Churchwell, J. C., Morris, A. M., Heurtelou, N. M., & Kesner, R. P. (2009) · Behavioral Neuroscience · doi:10.1037/a0017734 · Cited by 141 · see citing works
Cannabinoid and opioid modulation of social play behavior in adolescent rats: Differential behavioral mechanisms
Trezza, V., & Vanderschuren, L. J. M. J. (2008) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2008.03.001 · Cited by 138 · see citing works
Self-citation
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
Influence of environmental factors on social play behavior of juvenile rats
Vanderschuren, L. (1995) · Physiology & Behavior · doi:10.1016/0031-9384(94)00385-i · Cited by 128 · see citing works
Self-citation
Sex-dependent effects of amygdaloid lesions on the social play of prepubertal rats.
Meaney, M. J., Dodge, A. M., & Beatty, W. W. (1981) · Physiology & Behavior · doi:10.1016/0031-9384(81)90175-x · Cited by 126 · see citing works
Handbook of Basal Ganglia Structure and Function
(2016) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-802206-1.00052-0 · Cited by 118 · 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
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
Effects of morphine on different aspects of social play in juvenile rats
Vanderschuren, L. J. M. J., Spruijt, B. M., Van Ree, J. M., & Niesink, R. J. M. (1995) · Psychopharmacology · doi:10.1007/bf02245191 · Cited by 115 · see citing works
Self-citation
Topography of cocaine‐induced gene regulation in the rat striatum: relationship to cortical inputs and role of behavioural context
Willuhn, I., Sun, W., & Steiner, H. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02525.x · Cited by 114 · 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
Acute and constitutive increases in central serotonin levels reduce social play behaviour in peri-adolescent rats
Homberg, J. R., Schiepers, O. J. G., Schoffelmeer, A. N. M., Cuppen, E. P. J. G., & Vanderschuren, L. J. M. J. (2007) · Psychopharmacology · doi:10.1007/s00213-007-0895-8 · Cited by 113 · see citing works
Self-citation
Environmental Novelty Differentially Affects c-fosmRNA Expression Induced by Amphetamine or Cocaine in Subregions of the Bed Nucleus of the Stria Terminalis and Amygdala
Day, H. E. W., Badiani, A., Uslaner, J. M., Oates, M. M., Vittoz, N. M., Robinson, T. E., Watson, S. J., & Akil, H. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-02-00732.2001 · Cited by 109 · see citing works
Methylphenidate Disrupts Social Play Behavior in Adolescent Rats
Vanderschuren, L. J. M. J., Trezza, V., Griffioen-Roose, S., Schiepers, O. J. G., Van Leeuwen, N., De Vries, T. J., & Schoffelmeer, A. N. M. (2008) · Neuropsychopharmacology · doi:10.1038/npp.2008.10 · Cited by 105 · see citing works
Self-citation
Expression of c-fos gene activation during rough and tumble play in juvenile rats
Gordon, N. S., Kollack-Walker, S., Akil, H., & Panksepp, J. (2002) · Brain Research Bulletin · doi:10.1016/s0361-9230(01)00762-6 · Cited by 103 · see citing works
Functional disconnection of a prefrontal cortical-dorsal striatal system disrupts choice reaction time performance: Implications for attentional function.
Christakou, A., Robbins, T. W., & Everitt, B. J. (2001) · Behavioral Neuroscience · doi:10.1037//0735-7044.115.4.812 · Cited by 103 · see citing works
The effects of neonatal lesions in the amygdala or ventral hippocampus on social behaviour later in life
Daenen, E. W. P. M., Wolterink, G., Gerrits, M. A. F. M., & van Ree, J. M. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00223-1 · Cited by 93 · see citing works
Suppression of play fighting by amphetamine: Effects of catecholamine antagonists, agonists and synthesis inhibitors
Beatty, W. W., Costello, K. B., & Berry, S. L. (1984) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(84)90194-1 · Cited by 85 · see citing works
Basal Ganglia
Gerfen, C. R. (2004) · The Rat Nervous System · doi:10.1016/b978-012547638-6/50019-5 · Cited by 85 · see citing works
Deep Brain Stimulation Reveals a Dissociation of Consummatory and Motivated Behaviour in the Medial and Lateral Nucleus Accumbens Shell of the Rat
Plasse, G., Schrama, R., van Seters, S., Vanderschuren, L. J. M. J., & Westenberg, H. G. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033455 · Cited by 78 · see citing works
Self-citation
Amygdala size and hypothalamus size predict social play frequency in nonhuman primates: A comparative analysis using independent contrasts.
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
Environmental context and drug history modulate amphetamine-induced c-fos mrna expression in the basal ganglia, central extended amygdala, and associated limbic forebrain
Ostrander, M. M., Badiani, A., Day, H. E. W., Norton, C. S., Watson, S. J., Akil, H., & Robinson, T. E. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00247-1 · Cited by 76 · see citing works
The rat orbital and agranular insular prefrontal cortical areas: a cytoarchitectonic and chemoarchitectonic study
Werd, H. J. J. M. V. D., & Uylings, H. B. M. (2008) · Brain Structure and Function · doi:10.1007/s00429-007-0164-y · Cited by 73 · see citing works
Neurofilament mRNA is reduced in Parkinson's disease substantia nigra pars compacta neurons
Hill, W., Arai, M., Cohen, J. A., & Trojanowski, J. Q. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903290304 · Cited by 71 · see citing works
Prosocial Effects of Nicotine and Ethanol in Adolescent Rats Through Partially Dissociable Neurobehavioral Mechanisms
Trezza, V., Baarendse, P. J. J., & Vanderschuren, L. J. M. J. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.85 · Cited by 71 · see citing works
Self-citation
Projections from the rat pedunculopontine and laterodorsal tegmental nuclei to the anterior thalamus and ventral tegmental area arise from largely separate populations of neurons
Holmstrand, E. C., & Sesack, S. R. (2011) · Brain Structure and Function · doi:10.1007/s00429-011-0320-2 · Cited by 70 · see citing works
The role of the striatum in organizing sequences of play fighting in neonatally dopamine-depleted rats
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
Untitled work
(2010) · American journal of play · Cited by 65 · see citing works
Self-citation
Thalamus
Groenewegen, H. J., & Witter, M. P. (2004) · Elsevier eBooks · doi:10.1016/b978-012547638-6/50018-3 · Cited by 61 · 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
The experience‐dependent maturation of prefronto‐limbic circuits and the origin of developmental psychopathology: implications for the pathogenesis and therapy of behavioural disorders
Braun, K., & Bock, J. (2011) · Developmental Medicine & Child Neurology · doi:10.1111/j.1469-8749.2011.04056.x · Cited by 54 · see citing works
D₂ dopamine receptor involvement in the rough-and-tumble play behavior of juvenile rats.
Siviy, S. M., Fleischhauer, A. E., Kerrigan, L. A., & Kuhlman, S. J. (1996) · Behavioral Neuroscience · doi:10.1037/0735-7044.110.5.1168 · Cited by 47 · see citing works
D-sub-2 dopamine receptor involvement in the rough-and-tumble play behavior of juvenile rats.
Siviy, S. M., Fleischhauer, A. E., Kerrigan, L. A., & Kuhlman, S. J. (1996) · Behavioral Neuroscience · doi:10.1037//0735-7044.110.5.1168 · Cited by 47 · see citing works
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
Expression of amphetamine sensitization is associated with recruitment of a reactive neuronal population in the nucleus accumbens core
Nordquist, R. E., Vanderschuren, L. J. M. J., Jonker, A. J., Bergsma, M., Vries, T. J. D., Pennartz, C. M. A., & Voorn, P. (2008) · Psychopharmacology · doi:10.1007/s00213-008-1100-4 · Cited by 41 · see citing works
Self-citation
The Role of High Level Play as a Predictor Social Functioning in Autism
Manning, M. M., & Wainwright, L. D. (2010) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-009-0899-9 · Cited by 41 · see citing works
Juvenile play in the rat: Thalamic and brain stem involvement
Siviy, S. M., & Panksepp, J. (1987) · Physiology & Behavior · doi:10.1016/0031-9384(87)90138-7 · Cited by 35 · see citing works
Habituation reduces novelty-induced FOS expression in the striatum and cingulate cortex
Struthers, W. M., DuPriest, A., & Runyan, J. D. (2005) · Experimental Brain Research · doi:10.1007/s00221-005-0061-7 · Cited by 35 · see citing works
Quantitative Non-radioactive In Situ Hybridization Study of GAP-43 and SCG10 mRNAs in the Cerebral Cortex of Adult and Infant Macaque Monkeys
Higo, N. (1999) · Cerebral Cortex · doi:10.1093/cercor/9.4.317 · Cited by 33 · see citing works
Organization of Prefrontal-Striatal Connections
Groenewegen, H. J., & Uylings, H. B. M. (2010) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-374767-9.00020-2 · Cited by 31 · see citing works
Sex-steroidal regulation of aromatase mRNA expression in adult male rat brain: a quantitative non-radioactive in situ hybridization study
Zhao, C., Fujinaga, R., Yanai, A., Kokubu, K., Takeshita, Y., Watanabe, Y., & Shinoda, K. (2008) · Cell and Tissue Research · doi:10.1007/s00441-008-0606-8 · Cited by 29 · see citing works
Quantitative non‐radioactive in situ hybridization of preproenkephalin mRNA with digoxigenin‐labeled cRNA probes
Robbins, E. M., Baldino, F., Roberts‐Lewis, J. M., Meyer, S. L., Grega, D. S., & Lewis, M. E. (1991) · The Anatomical Record · doi:10.1002/ar.1092310417 · Cited by 25 · see citing works
A Rapid and Highly Sensitive Method of Non Radioactive Colorimetric In Situ Hybridization for the Detection of mRNA on Tissue Sections
Stylianopoulou, E., Lykidis, D., Ypsilantis, P., Simopoulos, C. E., Skavdis, G., & Grigoriou, M. E. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033898 · Cited by 20 · see citing works
Serotonin, motivation, and playfulness in the juvenile rat
Siviy, S. M., Deron, L. M., & Kasten, C. R. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.07.002 · Cited by 18 · see citing works
Coincident stimulation of convergent cortical inputs enhances immediate early gene induction in the striatum
Miyachi, S., Hasegawa, Y. T., & Gerfen, C. R. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.02.051 · Cited by 14 · see citing works
Fosvergnügen The Excitement of Immediate‐Early Genes
Schilling, K., Curran, T., & MORGAN, J. I. (1991) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1991.tb25917.x · Cited by 12 · see citing works
Projections from Pallidum to Striatum
Voorn, P. (2010) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-374767-9.00014-7 · Cited by 11 · see citing works
Self-citation
Untitled work
(1999) · doi:10.1002/(sici)1098-2302(199903)34:2

Flagged first, then by citations

Research works printed but not linked: 2

Paxinos G Watson C The rat brain in sterotaxic coordinates 1998 Academic Press
Pellis SM Pellis VC The Playful Brain 2009 OneWorld Publications Oxford, UK

Sorted by citations

PV Interneurons: Critical Regulators of E/I Balance for Prefrontal Cortex-Dependent Behavior and Psychiatric Disorders
Ferguson, B. R., & Gao, W.-J. (2018) · Frontiers in Neural Circuits · doi:10.3389/fncir.2018.00037 · Cited by 594 · see citing works
The neurobiology of social play and its rewarding value in rats
Vanderschuren, L. J. M. J., Achterberg, E. J. M., & Trezza, V. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.07.025 · Cited by 329 · see citing works
Self-citation
Accumbal D1R Neurons Projecting to Lateral Hypothalamus Authorize Feeding
O’Connor, E. C., Kremer, Y., Lefort, S., Harada, M., Pascoli, V., Rohner, C., & Lüscher, C. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.038 · Cited by 308 · see citing works
What the Laboratory Rat has Taught us About Social Play Behavior: Role in Behavioral Development and Neural Mechanisms
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
Self-citation
Social Play Behavior in Adolescent Rats is Mediated by Functional Activity in Medial Prefrontal Cortex and Striatum
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
Self-citation
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
Self-citation
Autistic-Like Syndrome in Mu Opioid Receptor Null Mice is Relieved by Facilitated mGluR4 Activity
Becker, J. A. J., Clesse, D., Spiegelhalter, C., Schwab, Y., Merrer, J. L., & Kieffer, B. L. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.59 · Cited by 123 · see citing works
Deficits in mesolimbic reward pathway underlie social interaction impairments in children with autism
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
Distinct dynamics of social motivation drive differential social behavior in laboratory rat and mouse strains
Netser, S., Meyer, A., Magalnik, H., Zylbertal, A., Haskal, S., Briller, M., Bizer, A., Grinevich, V., & Wagner, S. (2020) · Nature Communications · doi:10.1038/s41467-020-19569-0 · Cited by 115 · see citing works
Emergence of social behavior deficit, blunted corticolimbic activity and adult depression-like behavior in a rodent model of maternal maltreatment
Rincón‐Cortés, M., & Sullivan, R. M. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.205 · Cited by 101 · see citing works
Network integrity of the parental brain in infancy supports the development of children’s social competencies
Abraham, E., Hendler, T., Zagoory‐Sharon, O., & Feldman, R. (2016) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsw090 · Cited by 90 · see citing works
Play fighting and the development of the social brain: The rat’s tale
Pellis, S. M., Pellis, V. C., Ham, J. R., & Stark, R. A. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105037 · Cited by 76 · see citing works
Interacting Cannabinoid and Opioid Receptors in the Nucleus Accumbens Core Control Adolescent Social Play
Manduca, 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
Self-citation
Methylphenidate and Atomoxetine Inhibit Social Play Behavior through Prefrontal and Subcortical Limbic Mechanisms in Rats
Achterberg, E. J. M., van Kerkhof, L. W. M., Damsteegt, R., Trezza, V., & Vanderschuren, L. J. M. J. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.2945-14.2015 · Cited by 58 · see citing works
Self-citation
Functional integrity of the habenula is necessary for social play behaviour in rats
van Kerkhof, L. W. M., Damsteegt, R., Trezza, V., Voorn, P., & Vanderschuren, L. J. M. J. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12353 · Cited by 56 · see citing works
Self-citation
Play, 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 · see citing works
Social Play Behavior Is Critical for the Development of Prefrontal Inhibitory Synapses and Cognitive Flexibility in Rats
Bijlsma, A., Omrani, A., Spoelder, M., Verharen, J. P. H., Bauer, L., Cornelis, C., de Zwart, B., van Dorland, R., Vanderschuren, L. J. M. J., & Wierenga, C. J. (2022) · The Journal of Neuroscience · doi:10.1523/jneurosci.0524-22.2022 · Cited by 54 · see citing works
Self-citation
Nutritional status and social behavior in preschool children: the mediating effects of neurocognitive functioning
Liu, J., & Raine, A. (2016) · Maternal and Child Nutrition · doi:10.1111/mcn.12321 · Cited by 44 · see citing works
Stable immediate early gene expression patterns in medial prefrontal cortex and striatum after long‐term cocaine self‐administration
Gao, P., Limpens, J. H. W., Spijker, S., Vanderschuren, L. J. M. J., & Voorn, P. (2015) · Addiction Biology · doi:10.1111/adb.12330 · Cited by 37 · see citing works
Self-citation
Peripubertal stress increases play fighting at adolescence and modulates nucleus accumbens CB1 receptor expression and mitochondrial function in the amygdala
Papilloud, A., Guillot de Suduiraut, I., Zanoletti, O., Grosse, J., & Sandi, C. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0215-6 · Cited by 38 · see citing works
The Role of the Medial Prefrontal Cortex in Regulating Social Familiarity-Induced Anxiolysis
Lungwitz, E. A., Stuber, G. D., Johnson, P. L., Dietrich, A. D., Schartz, N. D., Hanrahan, B., Shekhar, A., & Truitt, W. A. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.302 · Cited by 39 · 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
Maternal allergic inflammation in rats impacts the offspring perinatal neuroimmune milieu and the development of social play, locomotor behavior, and cognitive flexibility
Breach, M. R., Dye, C. N., Joshi, A., Platko, S., Gilfarb, R. A., Krug, A. R., Franceschelli, D. V., Galan, A., Dodson, C. M., & Lenz, K. M. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.03.025 · Cited by 35 · 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
“In support of this idea, play-induced activation patterns within many PFC regions correlate with activity in other connected regions within the striatum and amygdala (van Kerkhof et al., 2014).”
BackgroundMethod
Brain regional differences in social encounter-induced Fos expression in male and female rats after post-weaning social isolation
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
Male Long Evans rats reared with a Fischer-344 peer during the juvenile period show deficits in social competency: a role for play
Stark, R., & Pellis, S. M. (2020) · International Journal of Play · doi:10.1080/21594937.2020.1720142 · Cited by 32 · see citing works
Impact of enriched environment during adolescence on adult social behavior, hippocampal synaptic density and dopamine D2 receptor expression in rats
Gabriel, P., Mastracchio, T.-A., Bordner, K. A., & Jeffrey, R. (2020) · Physiology & Behavior · doi:10.1016/j.physbeh.2020.113133 · Cited by 34 · see citing works
Effects of social context on endocrine function and Zif268 expression in response to an acute stressor in adolescent and adult rats
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
Animal 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 · see citing works
Self-citation
Structure and function of the medial amygdala
(2020) · Handbook of Behavioral Neuroscience · doi:10.1016/b978-0-12-815134-1.00002-7 · Cited by 29 · 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
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
Prenatal alcohol exposure disrupts male adolescent social behavior and oxytocin receptor binding in rodents
Holman, P. J., Ellis, L. A., Morgan, E., & Weinberg, J. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2018.08.004 · Cited by 26 · see citing works
Activation patterns of vasopressinergic and oxytocinergic brain regions following social play exposure in juvenile male and female rats
Reppucci, C. J., Gergely, C. K., & Veenema, A. H. (2018) · Journal of Neuroendocrinology · doi:10.1111/jne.12582 · Cited by 26 · see citing works
Hyperactivation of the amygdala correlates with impaired social play behavior of prepubertal male rats in a maternal immune activation model
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
From adolescence to late aging: A comprehensive review of social behavior, alcohol, and neuroinflammation across the lifespan
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
Predictors of social instability stress effects on social interaction and anxiety in adolescent male rats
Hodges, T. E., Baumbach, J. L., & McCormick, C. M. (2018) · Developmental Psychobiology · doi:10.1002/dev.21626 · Cited by 22 · see citing works
Social reinstatement: a rat model of peer-induced relapse
Weiss, V. G., Yates, J. R., Beckmann, J. S., Hammerslag, L. R., & Bardo, M. T. (2018) · Psychopharmacology · doi:10.1007/s00213-018-5048-8 · Cited by 20 · see citing works
Social Instability Stress in Adolescence and Social Interaction in Female Rats
Asgari, P., McKinney, G., Hodges, T. E., & McCormick, C. M. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2021.09.022 · Cited by 19 · see citing works
Using the ‘stranger test’ to assess social competency in adult female Long Evans rats reared with a Fischer 344 partner
Stark, R. A., & Pellis, S. M. (2021) · Behavioural Processes · doi:10.1016/j.beproc.2021.104492 · 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
Self-citation
Towards an expanded neuroscientific understanding of social play
Kellman, J., & Radwan, K. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.11.005 · Cited by 16 · see citing works
Distinct Dynamics of Theta and Gamma Rhythmicity during Social Interaction Suggest Differential Mode of Action in the Medial Amygdala of Sprague Dawley Rats and C57BL/6J Mice
John, S. R., Dagash, W., Mohapatra, A. N., Netser, S., & Wagner, S. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.04.020 · Cited by 16 · see citing works
Differential epigenetic changes in the hippocampus and prefrontal cortex of female mice that had free access to cocaine
Ajonijebu, D. C., Abboussi, O., Mabandla, M. V., & Daniels, W. M. U. (2017) · Metabolic Brain Disease · doi:10.1007/s11011-017-0116-z · Cited by 16 · see citing works
Play and welfare in domestic cats: Current knowledge and future directions
Henning, J. S. L., Fernandez, E. J., Nielsen, T., & Hazel, S. J. (2022) · Animal Welfare · doi:10.7120/09627286.31.4.005 · Cited by 15 · see citing works
Sociability development in mice with cell-specific deletion of the NMDA receptor NR1 subunit gene
Ferri, S. L., Pallathra, A. A., Kim, H., Dow, H. C., Raje, P., McMullen, M., Bilker, W. B., Siegel, S. J., Abel, T., & Brodkin, E. S. (2020) · Genes, Brain and Behavior · doi:10.1111/gbb.12624 · Cited by 15 · see citing works
Social Interactions Increase Activation of Vasopressin-Responsive Neurons in the Dorsal Raphe
Patel, T. N., Caiola, H., Mallari, O. G., Blandino, K. L., Goldenthal, A. R., Dymecki, S. M., & Rood, B. D. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.05.032 · Cited by 12 · see citing works
Effects of prenatal alcohol exposure on social competence: Asymmetry in play partner preference among heterogeneous triads of male and female rats
Holman, P. J., Baglot, S. L., Morgan, E., & Weinberg, J. (2019) · Developmental Psychobiology · doi:10.1002/dev.21842 · Cited by 13 · see citing works
Learning through the ages: How the brain adapts to the social world across development
Nelson, E. E. (2017) · Cognitive Development · doi:10.1016/j.cogdev.2017.02.013 · Cited by 12 · 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
Sex Differences in the Structure and Function of the Vasopressin System in the Ventral Pallidum are Associated with the Sex-Specific Regulation of Social Play Behavior in Juvenile Rats
Lee, J., Reppucci, C. J., Bowden, S. M., Huez, E. D. M., Bredewold, R., & Veenema, A. H. (2021) · Hormones and Behavior · doi:10.1016/j.yhbeh.2024.105563 · Cited by 10 · see citing works
The lateral habenula integrates age and experience to promote social transitions in developing rats
Cobb-Lewis, D. E., George, A., Hu, S., Packard, K., Song, M., Nikitah, I., Nguyen-Lopez, O., Tesone, E., Rowden, J., Wang, J., et al. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114556 · Cited by 11 · see citing works
The medial preoptic area and its projections to the ventral tegmental area and the periaqueductal gray are activated in response to social play behavior in juvenile rats.
Zhao, C., & Riters, L. V. (2023) · Behavioral Neuroscience · doi:10.1037/bne0000555 · Cited by 11 · see citing works
Reward-related dynamical coupling between basolateral amygdala and nucleus accumbens
Hsu, C.-C., Madsen, T. E., O’Gorman, E., Gourley, S. L., & Rainnie, D. G. (2020) · Brain Structure and Function · doi:10.1007/s00429-020-02099-2 · Cited by 9 · see citing works
A neuronal activation correlate in striatum and prefrontal cortex of prolonged cocaine intake
Gao, P., de Munck, J. C., Limpens, J. H. W., Vanderschuren, L. J. M. J., & Voorn, P. (2017) · Brain Structure and Function · doi:10.1007/s00429-017-1412-4 · Cited by 8 · see citing works
Self-citation
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
Chronic modafinil administration to preadolescent rats impairs social play behavior and dopaminergic system
Cid-Jofré, V., Gárate-Pérez, M. F., Clark, P. J., Valero-Jara, V., España, R. A., Sotomayor‐Zárate, R., Cruz, G., & Renard, G. M. (2020) · Neuropharmacology · doi:10.1016/j.neuropharm.2020.108404 · Cited by 8 · see citing works
The effects of different types of social interactions on the electrophysiology of neurons in the nucleus accumbens in rodents
Borland, J. M. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105809 · Cited by 8 · see citing works
Immediate early gene expression reveals interactions between social and nicotine rewards on brain activity in adolescent male rats
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
Communal nesting shapes the sex-dependent glutamatergic response to early life stress in the rat prefrontal cortex
Mottarlini, F., Rizzi, B., Targa, G., Buzzelli, V., Trapano, M. D., Rullo, L., Candeletti, S., Ciccocioppo, R., Fattore, L., Romualdi, P., et al. (2024) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2024.1406687 · Cited by 6 · see citing works
Self-citation
Adversity in early adolescence promotes an enduring anxious phenotype and increases serotonergic innervation of the infralimbic medial prefrontal cortex
Tao, C. S., Dhamija, P., Booij, L., & Menard, J. L. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.09.004 · Cited by 6 · see citing works
From curiosity to play: re‐evaluating the evolutionary origins of play
Iki, S. (2025) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.70009 · Cited by 6 · see citing works
Psychostimulants and social behaviors
Cid-Jofré, V., Bahamondes, T., Correa, A. Z., Arias, I. A., Reyes-Parada, M. I., & Renard, G. M. (2024) · Frontiers in Pharmacology · doi:10.3389/fphar.2024.1364630 · Cited by 5 · see citing works
Patterns of neuronal activation following ethanol-induced social facilitation and social inhibition in adolescent cFos-LacZ male and female rats
Towner, T. T., Applegate, D. T., Coleman, H. J., Papastrat, K. M., Varlinskaya, E. I., & Werner, D. F. (2024) · Behavioural Brain Research · doi:10.1016/j.bbr.2024.115118 · Cited by 5 · see citing works
Animal Models to Investigate Social Support Induced Anxiety Reductions
Majumdar, S., Lungwitz, E. A., Andrews, K. D., Chambers, J. E., & Truitt, W. A. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-813693-5.00012-5 · Cited by 5 · see citing works
Modulating the Activity of the VMPFC With tDCS Alters the Social Framing Effect
Chen, Y., Lu, X., Yu, P., Zeng, L., Ye, H., Shi, Q., & Guo, W. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.677006 · Cited by 5 · see citing works
Social play is critical for the development of prefrontal inhibitory synapses and cognitive flexibility in ratsPreprint
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
Self-citation
Social circuits under developmental threat: Bridging rodent and human neuroscience
Murgueitio, N., Propper, C. B., & Sheridan, M. A. (2025) · Developmental Review · doi:10.1016/j.dr.2025.101228 · Cited by 4 · see citing works
The role of play-derived experiences on the development of the medial prefrontal cortex and adult social behavior
Stark, R. (2021) · Cited by 3 · see citing works
Social behavior and neuronal activation in adolescent female Fos-LacZ transgenic rats: Impact of acute ethanol challenge and baseline levels of social preference
Hosová-Kennedy, D., Varlinskaya, E. I., & Werner, D. F. (2023) · Alcohol · doi:10.1016/j.alcohol.2023.10.039 · Cited by 2 · see citing works
Exploring the brain-behaviour interface: The role of juvenile play experiences
Himmler, B. T. (2015) · Open ULeth Scholarship (OPUS) (University of Lethbridge) · Cited by 2 · see citing works
Polymodal Sensory Thalamic Inputs to the Rat Lateral Amygdala are Facilitated by Chronic Ethanol Exposure and Regulate Withdrawal-associated AnxietyPreprint
Morales, M., McGinnis, M. M., Chappell, A. M., Parrish, B. C., & McCool, B. A. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/557256 · Cited by 1 · see citing works
Social Play Behavior
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
Self-citation
Rat Anterior Insula Symmetrically Represents Tickling-Induced Playful EmotionsPreprint
Dagher, S., & Ishiyama, S. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.04.02.587725 · Cited by 1 · see citing works
Computer Vision for Lesser Egyptian Jerboa ( Jaculus jaculus ) Behavioral Analysis and Animal Care RefinementPreprint
Boulanger, M. D., Miyamae, J. A., Martin, T. L., Hish, G., & Moore, T. Y. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.07.30.667603 · 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)
Prosocial Influences on Nicotine Reinforcement, Reward, and Neural Signaling in Rodent Models
Peartree, N. A. (2015)
Patterns of Endocrine, Behavioural, and Neural Function Underlying Social Deficits after Social Instability Stress in Adolescent Rats
Hodges, T. E. (2018) · Brock University Digital Repository (Brock University)
How social play experience shapes development of higher brain function
Bijlsma, A. (2023) · doi:10.33540/1927
The nucleus accumbens to ventral pallidum pathway regulates social play behavior via sex-specific mechanisms in juvenile rats
Lee, J., Anderson, D., Orsucci, I. C., Bowden, S., & Veenema, A. H. (2026) · Brain Structure and Function · doi:10.1007/s00429-026-03100-0

Social Play Behavior in Adolescent Rats is Mediated by Functional Activity in Medial Prefrontal Cortex and Striatum
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
Self-citation
Expression of c-fos gene activation during rough and tumble play in juvenile rats
Gordon, N. S., Kollack-Walker, S., Akil, H., & Panksepp, J. (2002) · Brain Research Bulletin · doi:10.1016/s0361-9230(01)00762-6 · Cited by 103 · see citing works
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
What the Laboratory Rat has Taught us About Social Play Behavior: Role in Behavioral Development and Neural Mechanisms
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
Self-citation
How social play experience shapes development of higher brain function: From synapses to behaviour
Bijlsma, A., Diergeneeskunde, F., Vanderschuren, L. J. M. J., & Wierenga, C. J. (2023) · Utrecht University Repository (Utrecht University)
Self-citation

Authors: van Kerkhof, L. W. M., Trezza, V., Mulder, T., Gao, P., Voorn, P., & Vanderschuren, L. J. M. J.
Affiliations: Roma Tre University (IT)
University Medical Center Utrecht (NL)
Amsterdam Neuroscience (NL)
Utrecht University (NL)
Corresponding author: Vanderschuren, Louk J. M. J.
ORCID: Trezza, Viviana
Mulder, Tessa
Voorn, Pieter
Vanderschuren, Louk J. M. J.
Venue: Brain Structure and Function
Publisher: Springer Science and Business Media LLC
Published: 2013-05-14
Volume: 219
Issue: 4
Pages: 1181-211
ISSN: 1863-2653 (ISSN-L)
1863-2661
DOI: 10.1007/s00429-013-0558-y
PMC: PMC3770763
OpenAlex: W2076156575
Cited by: 83
References: 127
Citations by year: 2026: 1 · 2025: 3 · 2024: 7 · 2023: 7 · 2022: 4 · 2021: 8 · 2020: 11 · 2019: 5 · 2018: 9 · 2017: 5 · 2016: 9 · 2015: 7 · 2014: 3 · 2013: 4
FWCI: 11.51
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Brain Structure and Function (publishedVersion)
PubMed (publishedVersion)
Pure Amsterdam UMC (publishedVersion)
Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
Iris (Roma Tre University) (submittedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion)
Funders: National Institute on Drug Abuse (R01DA022628)
Topics: Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: limbic system, c-fos, neural circuits, medial prefrontal cortex, orbitofrontal cortex, dorsal striatum, nucleus accumbens, lateral amygdala, thalamus, dorsal raphe nucleus, pedunculopontine nucleus, topographic organization, reward, motivation, cognitive control
MeSH terms: Animals, Behavior, Animal, Limbic System, Male, Neural Pathways, Play and Playthings, Social Behavior, Tyrosine 3-Monooxygenase, Proto-Oncogene Proteins c-fos, Rats, Wistar, 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

Cellular activation in limbic brain systems during social play behaviour in rats

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks