Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin
Open accessAbstract
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.
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Oxytocin induced LTD in nucleus accumbens medium spiny neurons, as presynaptic oxytocin receptors on serotoninergic terminals lead to increased serotonin release onto medium spiny neurons and consequent LTD.
“Oxytocin induced LTD in nucleus accumbens medium spiny neurons (Figure 4b), as presynaptic oxytocin receptors on serotoninergic terminals lead to increased serotonin release onto medium spiny neurons and consequent LTD”
From Oxytocin, Neural Plasticity, and Social Behavior (2021) · cites this paper as Dölen et al. 2013
PVN oxytocin fibers innervate mouse nucleus accumbens, where oxytocin release was important for social-conditioned place preference and serotonin-dependent long-term depression (LTD).
“Dölen et al. (2013) observed PVN oxytocin fibers innervating mouse nucleus accumbens, where oxytocin release was important for social-conditioned place preference and serotonin-dependent long-term depression (LTD).”
From Oxytocin, Neural Plasticity, and Social Behavior (2021) · cites this paper as Dölen et al. 2013
Increased activity in VTA dopaminergic neurons promotes social reinforcement learning.
“Specifically, research has demonstrated that VTA dopaminergic neurons become activated in rodents engaged in conspecific interactions, and increased activity in these neurons promotes social reinforcement learning (Bariselli et al., 2018; D ¨ olen et al., 2013; Soli ´ e et al., 2022).”
From Convergence of oxytocin and dopamine signalling in neuronal circuits: Insights into the neurobiology of social interactions across species (2024) · cites this paper as Dölen et al., 2013
The Abstract reports that oxytocin and serotonin activity in the nucleus accumbens is required for social reward in mice. The Concluding remarks say that future studies of dopamine’s role in social reward would be informative; our copy does not report that increased VTA dopaminergic-neuron activity promotes social reinforcement learning (searched: VTA dopaminergic neurons, ventral tegmental area). (LLM, conf=0.74)
Experimental — accuracy not yet measuredVTA dopaminergic neurons become activated in rodents engaged in conspecific interactions.
“Specifically, research has demonstrated that VTA dopaminergic neurons become activated in rodents engaged in conspecific interactions, and increased activity in these neurons promotes social reinforcement learning (Bariselli et al., 2018; D ¨ olen et al., 2013; Soli ´ e et al., 2022).”
From Convergence of oxytocin and dopamine signalling in neuronal circuits: Insights into the neurobiology of social interactions across species (2024) · cites this paper as Dölen et al., 2013
The Concluding remarks discuss oxytocin- and serotonin-dependent social reward in the nucleus accumbens and say that dopamine’s role in social reward warrants future study. Our copy does not report activation of VTA dopaminergic neurons during conspecific interactions or show that increased activity in those neurons promotes social reinforcement learning (searched: VTA dopaminergic activation; ventral tegmental area dopamine and social reward). (LLM, conf=0.77)
Experimental — accuracy not yet measuredIn mice, formation of social reward requires coordinated activity of oxytocin and serotonin within the NAcc.
“In mice, formation of social reward requires coordinated activity of oxytocin and serotonin within the NAcc (Dölen et al., 2013).”
From Social functioning in major depressive disorder (2016) · cites this paper as Dölen et al., 2013
In mice, oxytocin works with the serotonin system in the nucleus accumbens to modulate the rewarding aspects of social interaction.
“Recent research in mice has now shown that OT works in concert with the serotonin system in the NAcc of mice to modulate the rewarding aspects of social interaction (25).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [25]
Oxytocin receptor signaling influences several social behaviors in animals, including maternal care and bonding, social reward and gregariousness, social recognition, and pair bonding in monogamous species.
“OXTR affects a range of social behaviors in animals including maternal nurturing and bonding (1, 2), social reward and gregariousness (3, 4), social recognition (5), and pair bonding in monogamous species (6–8).”
From Variation in the Oxytocin Receptor Gene Predicts Brain Region–Specific Expression and Social Attachment (2016) · cites this paper as [3]
Preclinical studies have found that oxytocin may regulate social-emotional functioning.
“Preclinical studies have found that the neuropeptide, oxytocin, may regulate socialemotional functioning (Dölen et al., 2013;Hicks et al., 2012;Lim and Young, 2006;Lukas et al., 2011;Onaka et al., 2012).”
From Meta-analysis of the effects of intranasal oxytocin on interpretation and expression of emotions (2017) · cites this paper as Dölen et al., 2013
Social interactions can be rewarding and recruit components of the brain's reward circuitry, including VTA DA neurons and the NAc.
“Social interactions can be rewarding and thereby recruit components of the brain’s reward circuitry, including the ventral tegmental area (VTA) dopamine (DA) neurons and the nucleus accumbens (NAc) (Dölen et al., 2013, Gunaydin et al., 2014, Robinson et al., 2002).”
From Dorsal raphe dopamine neurons represent the experience of social isolation (2016) · cites this paper as Dölen et al., 2013
In mice, both pharmacologic blockade and molecular ablation of presynaptic oxytocin receptors in the nucleus accumbens impaired social reward processing, as assayed by social conditioned place preference.
“In mice, both pharmacologic blockade and molecular ablation of presynaptic OXT receptors in the NAc impaired social reward processing, as assayed by social CPP [41].”
From Neural circuits regulating prosocial behaviors (2023) · cites this paper as [41]
Modifications in the conditioned place preference assay have expanded its use to investigate the rewarding properties of prosocial interactions.
“More recently, modifications in the CPP assay have been made to expand its use to investigate the rewarding properties of prosocial interactions [40,41].”
From Neural circuits regulating prosocial behaviors (2023) · cites this paper as [41]
Oxytocin induces serotonin release from dorsal raphe inputs in the nucleus accumbens, which acts on presynaptic 5-HT1b receptors that are also required for social reward.
“Additional experimental manipulations suggested that OXT induces 5-HT release from dorsal raphe (DR) inputs in the NAc, which acts on presynaptic 5-HT1b receptors that are also required for social reward [41].”
From Neural circuits regulating prosocial behaviors (2023) · cites this paper as [41]
This 5-HT1b receptor-triggered synaptic plasticity was subsequently found to be generated by bath application of oxytocin or MDMA.
“This simple form of 5-HT1b receptor-triggered synaptic plasticity was subsequently found to be generated by bath application of OXT or MDMA [41,51], results consistent with the 5-HT releasing properties of these agents.”
From Neural circuits regulating prosocial behaviors (2023) · cites this paper as [41]
Oxytocin enhances social reward.
“Oxytocin promotes maternal nurturing and bonding, enhances social reward, and increases the salience of social stimuli.”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [80]
Paraventricular oxytocin and dorsal raphe serotonin projections to the nucleus accumbens are required for social reward in mice.
“For example, Dölen et al (80), using elegant circuit manipulations, demonstrated that PVN OXT and DR serotonin projections to the nucleus accumbens (NAcc) are required for social reward in mice.”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [80]
Oxytocin mediates a broad spectrum of prosocial behaviors such as empathy, pair bonding, mating and social reward.
“Oxytocin mediates a broad spectrum of prosocial behaviors such as empathy, pair bonding, mating and social reward (Dölen et al., 2013; L. W. Hung et al., 2017; Insel and Young, 2001; Nakajima et al., 2014; Rogers-Carter et al., 2018).”
From Neuromodulation of maternal circuits by oxytocin (2019) · cites this paper as Dölen et al., 2013
NAc, dRph, and VTA receive direct or indirect projections from hypothalamic OT neurons.
“the nucleus accumbens (NAc), dorsal raphe nucleus (dRph), and ventral tegmental area (VTA) receive direct or indirect projections from hypothalamic OT neurons (Beier et al., 2015; Dölen et al., 2013; Hung et al., 2017; Nardou et al., 2019)”
From Parallel social information processing circuits are differentially impacted in autism (2020) · cites this paper as Dölen et al., 2013
Hippocampus projects back to basolateral amygdala and NAc, where oxytocinergic, dopaminergic, and serotonergic innervation from the hypothalamic paraventricular nucleus, ventral tegmental area, and dorsal raphe nucleus are necessary for social reward learning.
“The hippocampus projects back to basolateral amygdala and nucleus accumbens (NAc), where oxytocinergic, dopaminergic, and serotonergic innervation from the hypothalamic paraventricular nucleus, ventral tegmental area, and dorsal raphe nucleus, respectively, are necessary for social reward learning [21,22].”
From Translational opportunities for circuit-based social neuroscience: advancing 21st century psychiatry (2021) · cites this paper as [22]
Changes in locomotor activity are unlikely to account for differences in sCPP across a variety of experimental manipulations.
“Previously, we have shown that changes in locomotor activity are unlikely to account for differences in sCPP across a variety of experimental manipulations (Dölen et al., 2013; Nardou et al., 2019)”
From Parallel social information processing circuits are differentially impacted in autism (2020) · cites this paper as Dölen et al., 2013
Prior investigations in rodents and primates have provided evidence for neurons that encode information about other individuals, demonstrating changes in activity when animals observe another's appetitive or aversive experiences.
“Prior investigations in rodents and primates, for example, have provided evidence for the presence of neurons that encode information about other individuals, demonstrating changes in activity when the animals observe another’s appetitive or aversive experiences 1–11.”
From Reduced sociability and social agency encoding in adult Shank3-mutant mice are restored through gene re-expression in real time (2021) · cites this paper as [3]
Previous investigations have provided insight into how discrete aspects of another animal's experience, such as receipt of reward, may be encoded by cells.
“Previous investigations have provided insight into how discrete aspects of another animal’s experience, such as receipt of reward, may be encoded by cells 1–7,9.”
From Reduced sociability and social agency encoding in adult Shank3-mutant mice are restored through gene re-expression in real time (2021) · cites this paper as [3]
The use of microdialysis to measure regionally-specific neuronal release of neuropeptides has provided important mechanistic insights into neuropeptide modulation in a variety of species and social contexts.
“The use of microdialysis to measure regionally-specific neuronal release of neuropeptides has provided important mechanistic insights into neuropeptide modulation in a variety of species and a host of social contexts, including maternal behavior, social recognition, social preference, social reward, social memory, and social buffering (Bosch and Neumann, 2012; Dölen et al., 2013; Dumais et al., 20”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Dölen et al., 2013
Mice form a preference for social bedding compared to isolated bedding.
“In an elegant study, authors showed that mice form a preference for social bedding compared to the isolated bedding (Dolen et al. 2013).”
From A precision medicine approach to oxytocin trials (2017) · cites this paper as Dolen et al. 2013
Mice treated with an OT antagonist within the NAcc did not form this preference.
“Moreover, mice treated with an OT antagonist within the NAcc did not form this preference.”
From A precision medicine approach to oxytocin trials (2017) · cites this paper as Dolen et al. 2013
Oxytocin is crucial in many aspects of social behavior, including affiliation and reward.
“This neuropeptide is crucial in many aspects of social behavior, including affiliation6 and reward.7”
From Enhancement of anandamide-mediated endocannabinoid signaling corrects autism-related social impairment (2016) · cites this paper as [7]
OT regulates neuronal activities in multiple neural circuits, such as sensory cortices, nucleus accumbens, and prefrontal cortex.
“OT regulates neuronal activities in multiple neural circuits, such as sensory cortices (Marlin et al., 2015), nucleus accumbens (Dölen et al., 2013), and prefrontal cortex (Nakajima et al., 2014).”
From Neuronal Representation of Social Information in the Medial Amygdala of Awake Behaving Mice (2017) · cites this paper as Dölen et al., 2013
Brain regions responding to naturally rewarding stimuli, including the VTA and NAc, are crucially involved in social behaviors.
“Brain regions responding to naturally rewarding stimuli, including the ventral tegmental area (VTA) and the nucleus accumbens (NAc), are crucially involved in social behaviors (Dolen et al., 2013; Gunaydin et al., 2014; Huang and Hessler, 2008).”
From Mechanisms underlying microbial-mediated changes in social behavior in mouse models of autism spectrum disorder (2019) · cites this paper as Dolen et al., 2013
5-HT and oxytocin interplay in the nucleus accumbens significantly mediates the rewarding aspects of social behavior.
“There are also signs of support for the view that 5-HT and oxytocin interplay in the nucleus accumbens significantly mediate the rewarding aspects of social behavior (Dolen et al., 2013).”
From The oxytocin receptor represents a key hub in the GPCR heteroreceptor network: Potential relevance for brain and behavior (2022) · cites this paper as Dolen et al., 2013
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- Authors
- Dölen, G., Darvishzadeh, A., Huang, K. W., & Malenka, R. C.
- Affiliations
- Stanford Medicine (US)
- Corresponding author
- Malenka, Robert C.
- Venue
- Nature
- Published
- 2013-09
- Volume
- 501
- Issue
- 7466
- Pages
- 179-184
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC4091761
- OpenAlex
- W2099168883
- Cited by
- 1,161
- References
- 49
- Citations by year
- 2026: 72 · 2025: 107 · 2024: 86 · 2023: 87 · 2022: 124 · 2021: 118 · 2020: 119 · 2019: 77 · 2018: 95 · 2017: 75 · 2016: 84 · 2015: 62 · 2014: 45 · 2013: 9
- FWCI
- 100.07
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Institute on Drug Abuse (R21DA032955, P01DA008227)
- National Institute of Neurological Disorders and Stroke (NS069375, P30NS069375)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- social reward, oxytocin, serotonin, nucleus accumbens core, dorsal raphe nucleus, 5-HT1B receptor, medium spiny neurons, social reinforcement, synaptic plasticity, autism spectrum disorder, social dysfunction
- MeSH terms
- Animals, Autistic Disorder, Conditioning, Psychological, Female, Male, Mice, Inbred C57BL, Mice, Transgenic, Synaptic Transmission, Neurons, Nucleus Accumbens, Oxytocin, Raphe Nuclei, Reward, Serotonin, Social Behavior, Gene Deletion, Presynaptic Terminals, Receptors, Oxytocin, Mice, Knockout, Long-Term Synaptic Depression, Receptor, Serotonin, 5-HT1B, Mice
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 ›
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