The neurobiology of social play behaviour: Past, present and future

Achterberg, E. J. Marijke; Vanderschuren, Louk J. M. J.

doi:10.1016/j.neubiorev.2023.105319

Cited by 19 publications

(7 citation statements)

References 228 publications

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“…Most of what we know about the neurobiology and endocrinology of play has come from studying the play fighting of laboratory rats (Achterberg and Vanderschuren, 2023;McCarthy, 2023). Beginning with crude lists of which brain areas and which neurotransmitters do and do not affect play (Panksepp et al, 1984;Thor and Holloway, 1984a;Vanderschuren et al, 1997), we now have a broad outline of the neural circuitry involved.…”

Section: The Mechanisms Underlying Play Fightingmentioning

confidence: 99%

“…Moreover, new insights about the contribution of previously unsuspected neural structures are being steadily revealed (Gloveli et al, 2023;Zhao and Riters, 2023). However, while some have argued for the existence of a distinct play brain circuit (Panksepp, 1998;Siviy and Panksepp, 2011), the nodes and connections identified so far are common to those important for social behavior in general, especially affinitive social behavior (Chen and Hong, 2018;Luo, 2018;Achterberg and Vanderschuren, 2023). Even so, comparing these brain areas between the sexes and across rat strains indicate that some of those neural circuits influence specific aspects of play (Siviy, 2020;VanRyzin et al, 2020), suggesting that, with advances in mapping dynamic brain circuits showing patterns of activation and communication (Bermudez-Contreras et al, 2018), a distinctive "play circuit" may eventually be characterized in terms of how these widely used areas function together when producing play relative to other affinitive social behavior.…”

Section: The Mechanisms Underlying Play Fightingmentioning

confidence: 99%

“…In rats, while some age-related changes in play fighting may involve the masculinizing effects of androgens, some of the changes in females involve the active role of ovarian hormones (Pellis, 2002b). For the progress made to date in mapping the neural circuits involved in play and some of the endocrinological influences on the development of those circuits, we direct readers to some recent reviews (e.g., VanRyzin et al, 2020;Achterberg and Vanderschuren, 2023;McCarthy, 2023). While the comparative data are not yet available to be certain as to what may constitute the general mechanisms at the neurobiological level, they are sufficient to shed new light on two unresolved issues related to the motivational mechanisms that have been thought to regulate play behavior.…”

Section: The Mechanisms Underlying Play Fightingmentioning

confidence: 99%

“…Even in their pure forms, the content of each category can be diverse, for example, social play can involve behavior typically associated with sex, maternal activities, predation, or conspecific aggression (Pellis, 1988;Pellis and Pellis, 2009). The form of social play that appears to simulate conspecific aggression, often referred to as play fighting, is one of the most often reported and most intensely studied forms of play (Pellis and Pellis, 1998a;Pellis and Pellis, 2017a), and has provided some of our deepest insights into the mechanisms and functions of play (for extensive reviews, see Pellis et al, 2010a;Pellis et al, 2014;Vanderschuren and Trezza, 2014;Siviy, 2016;Vanderschuren et al, 2016;Palagi, 2018;Sharpe, 2019;VanRyzin et al, 2020;Achterberg and Vanderschuren, 2023;Cooper et al, 2023;Nunes and Montemayor, 2023;Palagi, 2023;Pellis et al, 2023a). To gain a feel for the phenomenon, consider Mbundi and Ntondo, two captive, three-year-old male lowland gorillas (Gorilla gorilla gorilla) charging, grappling, and wrestling each other (Pellis and Pellis, 2016a).…”

Section: Introductionmentioning

confidence: 99%

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Play fighting revisited: its design features and how they shape our understanding of its mechanisms and functions

Pellis,

Ham

2024

Front. Ethol.

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Play fighting has been one of the most intensely studied forms of play and so has provided some of our deepest insights into the understanding of play in general. As the label implies, this behavior resembles serious fighting, in that the animals compete for an advantage over one another, but unlike true aggression, for play fighting to remain playful, it also incorporates a degree of cooperation and reciprocity – restrained competition seems to be its hallmark. Despite these common features, it should be noted that both the advantage competed over and the mechanisms by which restraint is achieved varies across species. Such variation mitigates simple generalities. For example, how empirical support for a proposed adaptive function in one species not being replicated in another, is to be interpreted. What has emerged over the past few decades is that play fighting is diverse, varying across several dimensions, some superficial, some fundamental, making choosing species to compare a challenge. In this paper, we explore various design features that constitute play fighting and the ways these can be modified across different species and lineages of species. Given that a major pillar of ethology is that description precedes explanation, having a good grasp of the behavioral diversity of play fighting is an essential starting point for detailed analyses of the mechanisms and functions of play. We show that commonalities across species likely involve different mechanisms than do species idiosyncrasies, and that different styles of play fighting likely afford different adaptive opportunities.

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Section: The Mechanisms Underlying Play Fightingmentioning

confidence: 99%

Section: The Mechanisms Underlying Play Fightingmentioning

confidence: 99%

Section: The Mechanisms Underlying Play Fightingmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Play fighting revisited: its design features and how they shape our understanding of its mechanisms and functions

Pellis,

Ham

2024

Front. Ethol.

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“…Social play behavior is a fundamental aspect of animal behavior, serving crucial roles in social development, learning, and synapse formation [1][2][3][4][5][6]. Numerous studies have highlighted several brain regions important in play behavior, including the habenula, prefrontal cortex, nucleus accumbens, periaqueductal gray, and striatum [7][8][9][10].…”

Section: Introductionmentioning

confidence: 99%

Rat Anterior Insula Symmetrically Represents Tickling-Induced Playful Emotions

Dagher,

Ishiyama

2024

Preprint

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Social play, an integral aspect of animal behavior, is inherently associated with positive emotions, yet the neuronal underpinnings of these playful states remain inadequately explored. We examined the anterior insula's involvement in processing tickle-induced playful emotions in rats. Our findings revealed diverse patterns of insular activity during tickling, with 20% of the recorded units displaying strong activation, and another 20% exhibiting inhibition. These units responded similarly to other playful contexts, such as gentle touch and hand chase, but not to neutral locomotion. Tickle-activated units demonstrated a positive correlation of firing rates with appetitive vocalization rates, whereas tickle-inhibited units showed a negative correlation. Distinct spike waveforms were associated with the tickle response patterns, suggesting potential cell-type dependencies. However, pharmacological manipulation of the global anterior insula did not yield observable effects on play behavior in rats. Anterograde tracing revealed extensive insular projections to areas including the amygdala and nucleus accumbens. Taken together, our findings suggest that the anterior insula symmetrically represents tickle-induced playful emotional states.

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Neurexin1α knockout in rats causes aberrant social behaviour: relevance for autism and schizophrenia

Achterberg,

Biemans,

Vanderschuren

2024

Psychopharmacology

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Rationale Genetic and environmental factors cause neuropsychiatric disorders through complex interactions that are far from understood. Loss-of-function mutations in synaptic proteins like neurexin1α have been linked to autism spectrum disorders (ASD) and schizophrenia (SCZ), both characterised by problems in social behaviour. Childhood social play behaviour is thought to facilitate social development, and lack of social play may precipitate or exacerbate ASD and SCZ. Objective To test the hypothesis that an environmental insult acts on top of genetic vulnerability to precipitate psychiatric-like phenotypes. To that aim, social behaviour in neurexin1α knockout rats was assessed, with or without deprivation of juvenile social play. We also tested drugs prescribed in ASD or SCZ to assess the relevance of this dual-hit model for these disorders. Results Neurexin1α knockout rats showed an aberrant social phenotype, with high amounts of social play, increased motivation to play, age-inappropriate sexual mounting, and an increase in general activity. Play deprivation subtly altered later social behaviour, but did not affect the phenotype of neurexin1α knockout rats. Risperidone and methylphenidate decreased play behaviour in both wild-type and knockout rats. Amphetamine-induced hyperactivity was exaggerated in neurexin1α knockout rats. Conclusion Deletion of the neurexin1α gene in rats causes exaggerated social play, which is not modified by social play deprivation. This phenotype therefore resembles disinhibited behaviour rather than the social withdrawal seen in ASD and SCZ. The neurexin1α knockout rat could be a model for inappropriate or disinhibited social behaviour seen in childhood mental disorders.

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The neurobiology of social play behaviour: Past, present and future

Cited by 19 publications

References 228 publications

Play fighting revisited: its design features and how they shape our understanding of its mechanisms and functions

Play fighting revisited: its design features and how they shape our understanding of its mechanisms and functions

Rat Anterior Insula Symmetrically Represents Tickling-Induced Playful Emotions

Neurexin1α knockout in rats causes aberrant social behaviour: relevance for autism and schizophrenia

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