Contrasting Roles of Dopamine and Noradrenaline in the Motivational Properties of Social Play Behavior in Rats
Open accessAbstract
Social play behavior, abundant in the young of most mammalian species, is thought to be important for social and cognitive development. Social play is highly rewarding, and as such, the expression of social play depends on its pleasurable and motivational properties. Since the motivational properties of social play have only sporadically been investigated, we developed a setup in which rats responded for social play under a progressive ratio schedule of reinforcement. Dopaminergic neurotransmission plays a key role in incentive motivational processes, and both dopamine and noradrenaline have been implicated in the modulation of social play behavior. Therefore, we investigated the role of dopamine and noradrenaline in the motivation for social play. Treatment with the psychostimulant drugs methylphenidate and cocaine increased responding for social play, but suppressed its expression during reinforced play periods. The dopamine reuptake inhibitor GBR-12909 increased responding for social play, but did not affect its expression, whereas the noradrenaline reuptake inhibitor atomoxetine decreased responding for social play as well as its expression. The effects of methylphenidate and cocaine on responding for social play, but not their play-suppressant effects, were blocked by pretreatment with the dopamine receptor antagonist α-flupenthixol. In contrast, pretreatment with the α2-adrenoceptor antagonist RX821002 prevented the play-suppressant effect of methylphenidate, but left its effect on responding for social play unaltered. In sum, the present study introduces a novel method to study the incentive motivational properties of social play behavior in rats. Using this paradigm, we demonstrate dissociable roles for dopamine and noradrenaline in social play behavior: dopamine stimulates the motivation for social play, whereas noradrenaline negatively modulates the motivation for social play behavior and its expression.
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
Cites
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?
Mesolimbic dopamine activity affects not just the launching of nape attacks but also the motivation to engage in play.
“That mesolimbic dopamine activity does not just affect the launching of nape attacks, but also the motivation to engage in play, has been shown by operant conditioning methods”
From The rough-and-tumble play of rats as a natural behavior suitable for studying the social brain (2022) · cites this paper as Achterberg et al., 2016
The ‘Dissociable Roles of Dopamine and Noradrenaline in Social Play Motivation and Expression’ section reports that dopamine-enhancing drugs increased operant responding for social play, supporting an effect on motivation. The ‘Operant Conditioning’ section identifies pouncing as an attempt to contact a partner’s nape, and the study measures it separately. But the drugs were not targeted to the mesolimbic pathway, so the study does not directly establish the claim’s regional specificity. (LLM, conf=0.82)
Experimental — accuracy not yet measuredSystemic administration of the norepinephrine reuptake inhibitor atomoxetine decreases responding for social play and decreases the expression of social play.
“systemic administration of the NE reuptake inhibitor atomoxetine decreased responding for social play and decreased the expression of social play [9].”
From Involvement of dopamine, but not norepinephrine, in the sex-specific regulation of juvenile socially rewarding behavior by vasopressin (2018) · cites this paper as [9]
Systemic administration of drugs enhancing dopamine signaling increases reinforcement responding for social play, and these effects are blocked by non-specific dopamine receptor antagonists.
“systemic administration of drugs enhancing DA signaling increased reinforcement responding for social play, and these effects were blocked by administration of non-specific DA receptor antagonists [9].”
From Involvement of dopamine, but not norepinephrine, in the sex-specific regulation of juvenile socially rewarding behavior by vasopressin (2018) · cites this paper as [9]
Dopamine manipulations affect how hard rats will work for the reward of access to a playmate.
“in which dopamine manipulations affect how hard rats will work for the reward of access to a playmate (Achterberg et al., 2016).”
From The rough-and-tumble play of rats as a natural behavior suitable for studying the social brain (2022) · cites this paper as Achterberg et al., 2016
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Dissecting components of reward: ‘liking’, ‘wanting’, and learning
Berridge, K. C., Robinson, T. E., & Aldridge, J. W. (2009) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2008.12.014 · Cited by 1,942 · 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
Thompson, M. R., Callaghan, P. D., Hunt, G. E., Cornish, J. L., & McGregor, I. S. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.02.032 · Cited by 237 · 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
Self-citationThiel, K. J., Okun, A. C., & Neisewander, J. L. (2008) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2008.02.013 · Cited by 164 · see citing works
Peartree, N. A., Hood, L. E., Thiel, K. J., Sanabria, F., Pentkowski, N. S., Chandler, K. N., & Neisewander, J. L. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.10.001 · Cited by 90 · see citing works
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-citationD₂ 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
Flagged first, then by citations
Research works printed but not linked: 1
- Pellis SM, Pellis VC (2009). The Playful Brain. OneWorld Publications: Oxford, UK.
Cited by
Sorted by citations
Salamone, J. D., Yohn, S. E., López-Cruz, L., San Miguel, N., & Correa, M. (2016) · Brain · doi:10.1093/brain/aww050 · Cited by 350 · 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-citationNeural mechanisms of social homeostasis
Matthews, G. A., & Tye, K. M. (2019) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.14016 · Cited by 273 · see citing works
The neurobiology of social play behaviour: Past, present and future
Achterberg, E. J. M., & Vanderschuren, L. J. M. J. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105319 · Cited by 56 · 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
Self-citationA novel operant task to assess social reward and motivation in rodents
Borland, J. M., Frantz, K. J., Aiani, L. M., Grantham, K. N., Song, Z., & Albers, H. E. (2017) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2017.06.003 · Cited by 40 · see citing works
Bredewold, R., Nascimento, N. F., Ro, G. S., Cieslewski, S. E., Reppucci, C. J., & Veenema, A. H. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0100-2 · Cited by 31 · see citing works
The rough-and-tumble play of rats as a natural behavior suitable for studying the social brain
Pellis, S. M., Pellis, V. C., Ham, J. R., & Achterberg, E. J. M. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.1033999 · Cited by 29 · see citing works
“That mesolimbic dopamine activity does not just affect the launching of nape attacks, but also the motivation to engage in play, has been shown by operant conditioning methods, in which dopamine manipulations affect how hard rats will work for the reward of access to a playmate (Achterberg et al., 2016).”
BackgroundSelf-citationWho’s laughing? Play, tickling and ultrasonic vocalizations in rats.
Burke, C. J., Pellis, S. M., & Achterberg, E. J. M. (2022) · Philosophical Transactions of the Royal Society B · doi:10.1098/rstb.2021.0184 · Cited by 23 · see citing works
Self-citationBredewold, R., Washington, C., & Veenema, A. H. (2025) · Neuropsychopharmacology · doi:10.1038/s41386-024-01987-z · Cited by 13 · see citing works
“Future studies could test this by using operant conditioning, which has been successfully used to separate the motivational and pleasurable aspects of social play behavior [9, 67, 68].”
Neurexin1α knockout in rats causes aberrant social behaviour: relevance for autism and schizophrenia
Achterberg, E. J. M., Biemans, B., & Vanderschuren, L. J. M. J. (2025) · Psychopharmacology · doi:10.1007/s00213-024-06559-z · Cited by 9 · see citing works
“…findings that methylphenidate reduces social play through both prefrontal and subcortical limbic structures implies that alongside increased – prefrontal – inhibition, methylphenidate may also alter the – subcortically mediated – emotional properties of social play (Achterberg et al. 2015).”
Self-citation
- Authors
- Achterberg, E. J. M., van Kerkhof, L. W. M., Servadio, M., van Swieten, M. M. H., Houwing, D. J., Aalderink, M., Driel, N. V., Trezza, V., & Vanderschuren, L. J. M. J.
- Affiliations
- Utrecht University (NL)
- University Medical Center Utrecht (NL)
- Roma Tre University (IT)
- Corresponding author
- Vanderschuren, Louk J M J
- ORCID
- Venue
- Neuropsychopharmacology
- Published
- 2015-07-15
- Volume
- 41
- Issue
- 3
- Pages
- 858-868
- ISSN
- 0893-133X (ISSN-L)
- 1740-634X
- PMC
- PMC4707831
- OpenAlex
- W1548490952
- Cited by
- 103
- References
- 8
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 13 · 2023: 11 · 2022: 12 · 2021: 11 · 2020: 11 · 2019: 9 · 2018: 12 · 2017: 5 · 2016: 9
- FWCI
- 4.04
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Neuropsychopharmacology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- Iris (Roma Tre University) (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Funders
- European Commission (293589)
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek
- National Institute on Drug Abuse (R01DA022628)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- social play, dopamine, norepinephrine, incentive motivation, reward, methylphenidate, cocaine, GBR 12909, atomoxetine, dopamine uptake inhibition, norepinephrine reuptake inhibition, alpha-flupenthixol, alpha2-adrenoceptor antagonists, progressive ratio schedule, rats
- MeSH terms
- Atomoxetine Hydrochloride, Animals, Cocaine, Conditioning, Operant, Dopamine, Flupenthixol, Male, Methylphenidate, Motivation, Neuropsychological Tests, Norepinephrine, Piperazines, Random Allocation, Receptors, Dopamine, Social Behavior, Rats, Wistar, Receptors, Adrenergic, alpha-2, Dopamine Antagonists, Adrenergic Uptake Inhibitors, Dopamine Uptake Inhibitors, Idazoxan, Adrenergic alpha-2 Receptor Antagonists
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
