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Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin

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  • Gül Dölen

    (Nancy Pritzker Laboratory, Stanford University School of Medicine, 265 Campus Drive
    Present address: Department of Neuroscience, Johns Hopkins University, 855 North Wolfe Street, Baltimore, Maryland 21205, USA.)

  • Ayeh Darvishzadeh

    (Nancy Pritzker Laboratory, Stanford University School of Medicine, 265 Campus Drive)

  • Kee Wui Huang

    (Nancy Pritzker Laboratory, Stanford University School of Medicine, 265 Campus Drive)

  • Robert C. Malenka

    (Nancy Pritzker Laboratory, Stanford University School of Medicine, 265 Campus Drive)

Abstract

Social behaviours in species as diverse as honey bees and humans promote group survival but often come at some cost to the individual. Although reinforcement of adaptive social interactions is ostensibly required for the evolutionary persistence of these behaviours, the neural mechanisms by which social reward is encoded by the brain are largely unknown. Here we demonstrate that in mice oxytocin acts as a social reinforcement signal within the nucleus accumbens core, where it elicits a presynaptically expressed long-term depression of excitatory synaptic transmission in medium spiny neurons. Although the nucleus accumbens receives oxytocin-receptor-containing inputs from several brain regions, genetic deletion of these receptors specifically from dorsal raphe nucleus, which provides serotonergic (5-hydroxytryptamine; 5-HT) innervation to the nucleus accumbens, abolishes the reinforcing properties of social interaction. Furthermore, oxytocin-induced synaptic plasticity requires activation of nucleus accumbens 5-HT1B receptors, the blockade of which prevents social reward. These results demonstrate that the rewarding properties of social interaction in mice require the coordinated activity of oxytocin and 5-HT in the nucleus accumbens, a mechanistic insight with implications for understanding the pathogenesis of social dysfunction in neuropsychiatric disorders such as autism.

Suggested Citation

  • Gül Dölen & Ayeh Darvishzadeh & Kee Wui Huang & Robert C. Malenka, 2013. "Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin," Nature, Nature, vol. 501(7466), pages 179-184, September.
  • Handle: RePEc:nat:nature:v:501:y:2013:i:7466:d:10.1038_nature12518
    DOI: 10.1038/nature12518
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    Cited by:

    1. Henry W. Kietzman & Gracy Trinoskey-Rice & Sarah A. Blumenthal & Jidong D. Guo & Shannon L. Gourley, 2022. "Social incentivization of instrumental choice in mice requires amygdala-prelimbic cortex-nucleus accumbens connectivity," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    2. Nihaad Paraouty & Justin D. Yao & Léo Varnet & Chi-Ning Chou & SueYeon Chung & Dan H. Sanes, 2023. "Sensory cortex plasticity supports auditory social learning," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. M. E. Flanigan & O. J. Hon & S. D’Ambrosio & K. M. Boyt & L. Hassanein & M. Castle & H. L. Haun & M. M. Pina & T. L. Kash, 2023. "Subcortical serotonin 5HT2c receptor-containing neurons sex-specifically regulate binge-like alcohol consumption, social, and arousal behaviors in mice," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    4. Jennifer Isaac & Sonia Corbett Karkare & Hymavathy Balasubramanian & Nicholas Schappaugh & Jarildy Larimar Javier & Maha Rashid & Malavika Murugan, 2024. "Sex differences in neural representations of social and nonsocial reward in the medial prefrontal cortex," Nature Communications, Nature, vol. 15(1), pages 1-27, December.
    5. Masafumi Tsurutani & Teppei Goto & Mitsue Hagihara & Satsuki Irie & Kazunari Miyamichi, 2024. "Selective vulnerability of parvocellular oxytocin neurons in social dysfunction," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    6. David Wolf & Renée Hartig & Yi Zhuo & Max F. Scheller & Mirko Articus & Marcel Moor & Valery Grinevich & Christiane Linster & Eleonora Russo & Wolfgang Weber-Fahr & Jonathan R. Reinwald & Wolfgang Kel, 2024. "Oxytocin induces the formation of distinctive cortical representations and cognitions biased toward familiar mice," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    7. Andrea Bonassi & Ilaria Cataldo & Giulio Gabrieli & Moses Tandiono & Jia Nee Foo & Bruno Lepri & Gianluca Esposito, 2022. "The Interaction between Serotonin Transporter Allelic Variation and Maternal Care Modulates Instagram Sociability in a Sample of Singaporean Users," IJERPH, MDPI, vol. 19(9), pages 1-15, April.
    8. Ashim Gupta & Abdalla Bowirrat & Luis Llanos Gomez & David Baron & Igor Elman & John Giordano & Rehan Jalali & Rajendra D. Badgaiyan & Edward J. Modestino & Mark S. Gold & Eric R. Braverman & Anish Ba, 2022. "Hypothesizing in the Face of the Opioid Crisis Coupling Genetic Addiction Risk Severity (GARS) Testing with Electrotherapeutic Nonopioid Modalities Such as H-Wave Could Attenuate Both Pain and Hedonic," IJERPH, MDPI, vol. 19(1), pages 1-12, January.
    9. Kansai Fukumitsu & Misato Kaneko & Teppo Maruyama & Chihiro Yoshihara & Arthur J. Huang & Thomas J. McHugh & Shigeyoshi Itohara & Minoru Tanaka & Kumi O. Kuroda, 2022. "Amylin-Calcitonin receptor signaling in the medial preoptic area mediates affiliative social behaviors in female mice," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    10. Hyosang Kim & Doyoun Kim & Yisul Cho & Kyungdeok Kim & Junyeop Daniel Roh & Yangsik Kim & Esther Yang & Seong Soon Kim & Sunjoo Ahn & Hyun Kim & Hyojin Kang & Yongchul Bae & Eunjoon Kim, 2022. "Early postnatal serotonin modulation prevents adult-stage deficits in Arid1b-deficient mice through synaptic transcriptional reprogramming," Nature Communications, Nature, vol. 13(1), pages 1-19, December.

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