The rough-and-tumble play of rats as a natural behavior suitable for studying the social brain

Pellis, Vivien C.; Ham, Jackson R.; Achterberg, E. J. Marijke

doi:10.3389/fnbeh.2022.1033999

Cited by 22 publications

(24 citation statements)

References 52 publications

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“…During the juvenile and adolescent phases of life, when PFC development is in progress, most mammalians species, including rats and humans, display an abundance of a pleasurable and energetic form of social interaction, known as social play behavior (Panksepp et al, 1984; Vanderschuren et al, 1997; Pellis and Pellis, 2009; Manduca et al, 2014). One important characteristic of social play is that it allows animals to experiment with their own behavior and their interactions with others.…”

Section: Introductionmentioning

confidence: 99%

“…This experimentation during social play is thought to facilitate the development of a rich behavioral repertoire, that allows an individual to quickly adapt in a changeable world. In this way, social play may subserve the development of PFC-dependent skills such as flexibility, creativity, and decision-making (Špinka et al, 2001; Pellis and Pellis, 2009; Vanderschuren and Trezza, 2014). Indeed, during play the PFC is engaged (Van Kerkhof et al, 2014) and required (Bell et al, 2009; van Kerkhof et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

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Social play behavior shapes the development of prefrontal inhibition in a region-specific manner

Bijlsma

Vanderschuren

Wierenga

2023

Preprint

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Experience-dependent organization of neuronal connectivity is critical for brain development. We recently demonstrated the importance of social play behavior for the developmental fine-tuning of inhibitory synapses in the medial prefrontal cortex (mPFC) in rats. When these effects of play experience exactly occur and if this happens uniformly throughout the prefrontal cortex is currently unclear. Here we report important temporal and regional heterogeneity in the impact of social play on the development of excitatory and inhibitory neurotransmission in the mPFC and the orbitofrontal cortex (OFC). We recorded in layer 5 pyramidal neurons from juvenile (postnatal day (P)21), adolescent (P42) and adult (P85) rats after social play deprivation (SPD; between P21-P42). The development of these PFC subregions followed different trajectories. On P21, inhibitory and excitatory synaptic input was multiple times higher in the OFC than in the mPFC. SPD did not affect excitatory currents, but reduced inhibitory transmission in both mPFC and OFC. Intriguingly, the reduction occurred in the mPFC during SPD, while the reduction in the OFC only became manifested after SPD. These data reveal a complex interaction between social play experience and the specific developmental trajectories of prefrontal subregions.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Social play behavior shapes the development of prefrontal inhibition in a region-specific manner

Bijlsma

Vanderschuren

Wierenga

2023

Preprint

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“…There, the need to adjust does not exist, so children can be themselves (Winnicott, 2012). Play is crucial for children, as it is through play that they develop flexible responses to situations they create or encounter (Pellis & Pellis, 2009).…”

Section: Discussionmentioning

confidence: 99%

“When I sing—I exist”: A qualitative inquiry on posttraumatic growth in voicework groups with women coping with incest.

Riabzev¹,

Bensimon²

2023

Psychological Trauma: Theory, Research, Practice, and Policy

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“…Play behaviour is an intrinsically rewarding activity that is abundant among the young of humans and most other mammalian species (Pellis and Pellis, 2009; Graham and Burghardt, 2010). It is typically expressed under safe circumstances in which individuals can experiment with their behaviour and develop motor, social, cognitive and emotional skills necessary for optimal functioning later in life (Špinka et al, 2001; Pellis and Pellis, 2009; Gray, 2017; Nijhof et al, 2018; Sgro and Mychasiuk, 2020). Importantly, when exploring and experimenting with behaviour, playful situations may entail risks, such as the risk of rejection, injury or failure.…”

Section: Introductionmentioning

confidence: 99%

Opportunities for risk-taking during play alters cognitive performance and prefrontal inhibitory signalling in rats of both sexes

Bijlsma,

Birza,

Pimentel

et al. 2023

Preprint

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Social play behaviour is a rewarding activity that can entail risks, thus allowing young individuals to test the limits of their capacities and to train their cognitive and emotional adaptability to challenges. Here, we tested in rats how opportunities for risk-taking during play affect the development of cognitive and emotional capacities and medial prefrontal cortex (mPFC) function, a brain structure important for risk-based decision-making. Male and female rats were housed socially or social play-deprived (SPD) between postnatal day (P)21 and P42. During this period, half of both groups were daily exposed to a high-risk play environment. Around P85, all rats were tested for cognitive performance and emotional behaviour after which inhibitory currents were recorded in layer 5 pyramidal neurons in mPFC slices. We show that playing in a high-risk environment altered cognitive flexibility in both sexes, and improved behavioural inhibition in males. High-risk play altered anxiety-like behaviour in the elevated plus maze in males and in the open field in females, respectively. SPD affected cognitive flexibility in both sexes and decreased anxiety-like behaviour in the elevated plus maze in females. We found that synaptic inhibitory currents in the mPFC were increased in male, but not female, rats after high-risk play, while SPD lowered PFC synaptic inhibition in both sexes. Together, our data show that exposure to risks during play affects the development of cognition, emotional behaviour and inhibition in the mPFC. Furthermore, our study suggests that the opportunity to take risks during play cannot substitute for social play behaviour.

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The rough-and-tumble play of rats as a natural behavior suitable for studying the social brain

Abstract: October CITATIONPellis SM, Pellis VC, Ham JR and Achterberg EJM () The rough-and-tumble play of rats as a natural behavior suitable for studying the social brain.

Cited by 22 publications

References 52 publications

Social play behavior shapes the development of prefrontal inhibition in a region-specific manner

Social play behavior shapes the development of prefrontal inhibition in a region-specific manner

“When I sing—I exist”: A qualitative inquiry on posttraumatic growth in voicework groups with women coping with incest.

Opportunities for risk-taking during play alters cognitive performance and prefrontal inhibitory signalling in rats of both sexes

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