Opioid modulation of social play reward in juvenile rats

Achterberg, E. J. Marijke; Swieten, M.M.H. van; Houwing, Danielle J.; Trezza, Viviana; Vanderschuren, Louk J. M. J.

doi:10.1016/j.neuropharm.2018.09.007

Cited by 39 publications

(23 citation statements)

References 71 publications

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“…Consistent, we have previously shown that the widely reported social play-enhancing effect of morphine (e.g. Trezza & Vanderschuren, 2008b;Vanderschuren et al, 1995a) could only be observed in our operant set-up when both animals in a test pair were treated (Achterberg et al, 2019). Furthermore, the effect was solely found after 24 h but not 2 h of social isolation prior to testing.…”

Section: Effects Of Nicotine On the Motivational And Pleasurable Propsupporting

confidence: 90%

“…In the present study, we therefore directly investigated whether treatment with nicotine and alcohol affected the motivational and pleasurable properties of social play behaviour. To measure the motivational aspects of social play behaviour, we used an operant conditioning task, in which rats pressed a lever for access to a playful partner under a progressive ratio schedule of reinforcement (Achterberg et al, 2019;Achterberg, Van Kerkhof, et al, 2016;. Place conditioning was used to gauge whether pleasurable aspects of social play behaviour were affected by treatment with nicotine and alcohol (Achterberg et al, 2019;Bardo & Bevins, 2000;Calcagnetti & Schechter, 1992;Douglas, Varlinskaya, & Spear, 2004;Tzschentke, 2007;Vanderschuren et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

“…To measure the motivational aspects of social play behaviour, we used an operant conditioning task, in which rats pressed a lever for access to a playful partner under a progressive ratio schedule of reinforcement (Achterberg et al, 2019;Achterberg, Van Kerkhof, et al, 2016;. Place conditioning was used to gauge whether pleasurable aspects of social play behaviour were affected by treatment with nicotine and alcohol (Achterberg et al, 2019;Bardo & Bevins, 2000;Calcagnetti & Schechter, 1992;Douglas, Varlinskaya, & Spear, 2004;Tzschentke, 2007;Vanderschuren et al, 2016). Since both alcohol and nicotine enhance the expression of social play behaviour at least partly via dopamine signalling (Trezza, Baarendse, et al, 2009) and dopamine neurotransmission has been implicated in the motivation for social play (Achterberg, Van Kerkhof, et al, 2016), we predicted that alcohol and nicotine increase the motivation to play.…”

Section: Introductionmentioning

confidence: 99%

“…Since both alcohol and nicotine enhance the expression of social play behaviour at least partly via dopamine signalling (Trezza, Baarendse, et al, 2009) and dopamine neurotransmission has been implicated in the motivation for social play (Achterberg, Van Kerkhof, et al, 2016), we predicted that alcohol and nicotine increase the motivation to play. Secondly, opioid and cannabinoid neurotransmission, also implicated in the social play-enhancing effects of nicotine and alcohol (Trezza, Baarendse, et al, 2009;, act on the pleasurable but not necessarily the motivational aspects of social play behaviour Achterberg et al, 2019). Therefore we predicted that the pleasurable aspects of social play are also enhanced by treatment with these substances.…”

Section: Introductionmentioning

confidence: 99%

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Treatment with low doses of nicotine but not alcohol affects social play reward in rats

Achterberg

Vanderschuren

2020

International Journal of Play

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Social play behaviour is a vigorous, highly rewarding activity in young animals. It is thought to facilitate social, cognitive and emotional development, but its underlying neural mechanisms are incompletely understood. Previously, we found that low doses of alcohol and nicotine enhanced social play behaviour in young rats. Using place and operant conditioning setups to assess the pleasurable and motivational aspects of social play, we investigated how treatment with nicotine and alcohol affects social play reward. Nicotine-treatment increased the incentive motivational properties of social play as well as the expression of social play itself. Moreover, while nicotine by itself evoked conditioned place preference (CPP), it reduced social play-induced CPP. Alcohol-treatment did not affect the motivation for and expression of social play, nor did it affect social play-induced CPP. The finding that nicotine but not alcohol modulates social play reward increases our understanding of the neural underpinnings of this developmentally important behaviour.

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Section: Effects Of Nicotine On the Motivational And Pleasurable Propsupporting

confidence: 90%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Treatment with low doses of nicotine but not alcohol affects social play reward in rats

Achterberg

Vanderschuren

2020

International Journal of Play

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“…Mu opioid receptor activation facilitates reward derived from social interaction and other natural experiences, as well as the abuse liability of exogenous opiate narcotics [1][2][3]. Agonists with high mu opioid receptor affinity increase visual attention to faces in humans, and enhance social play behavior in juvenile rodents as well as marmosets, while pharmacological blockade of opioid receptors causes deficits in these behaviors [4][5][6]. Mu opioid receptor availability in the human nucleus accumbens is regulated by a variety of social circumstances [7,8], and intra-accumbal manipulations of mu opioid receptor activation can bidirectionally modulate social behavior in rodents [9][10][11].…”

Section: Introductionmentioning

confidence: 99%

Mu Opioid Receptor Gene Dosage Influences Reciprocal Social Behaviors and Nucleus Accumbens Microcircuitry

Toddes

Lefevre

Brandner

et al. 2020

Preprint

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The mu opioid receptor regulates reward derived from both drug use and natural experiences, including social interaction. Homozygous genetic knockout of the mu opioid receptor (Oprm1-/-) causes social deficits in mice, whereas partial dysregulation of mu opioid signaling has been documented in several human neuropsychiatric disorders. Here, we investigated the social behavior of male and female mice with heterozygous genetic knockout of the mu opioid receptor (Oprm1+/-), modeling partial reduction of mu opioid signaling. Reciprocal social interaction and social conditioned place preference were diminished in Oprm1+/- and Oprm1-/- mutants of both sexes. Interaction with Oprm1 mutants also altered the social behavior of genotypical test partners. We corroborated this latter result using a social preference task, in which genotypical mice preferred interactions with another typical mouse over Oprm1 mutants. We also analyzed inhibitory synapses in the nucleus accumbens, a key brain region for mu opioid regulation of social behavior, using methods that differentiate between medium spiny neurons (MSNs) expressing the D1 or D2 dopamine receptor. Inhibitory synaptic transmission was increased in D2-MSNs of male mutants, but not female mutants, while the density of inhibitory synaptic puncta at the cell body of D2-MSNs was increased in both male and female mutants. These changes in nucleus accumbens microcircuitry were more robust in Oprm1+/- mutants than Oprm1-/- mutants, demonstrating that partial reductions of mu opioid signaling can have large effects on brain function and behavior. Our results support a role for partial dysregulation of mu opioid signaling in social deficits associated with neuropsychiatric conditions.

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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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Opioid modulation of social play reward in juvenile rats

Cited by 39 publications

References 71 publications

Treatment with low doses of nicotine but not alcohol affects social play reward in rats

Treatment with low doses of nicotine but not alcohol affects social play reward in rats

Mu Opioid Receptor Gene Dosage Influences Reciprocal Social Behaviors and Nucleus Accumbens Microcircuitry

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

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