Natural neural projection dynamics underlying social behavior
Open accessAbstract
Social interaction is a complex behavior essential for many species and is impaired in major neuropsychiatric disorders. Pharmacological studies have implicated certain neurotransmitter systems in social behavior, but circuit-level understanding of endogenous neural activity during social interaction is lacking. We therefore developed and applied a new methodology, termed fiber photometry, to optically record natural neural activity in genetically and connectivity-defined projections to elucidate the real-time role of specified pathways in mammalian behavior. Fiber photometry revealed that activity dynamics of a ventral tegmental area (VTA)-to-nucleus accumbens (NAc) projection could encode and predict key features of social, but not novel object, interaction. Consistent with this observation, optogenetic control of cells specifically contributing to this projection was sufficient to modulate social behavior, which was mediated by type 1 dopamine receptor signaling downstream in the NAc. Direct observation of deep projection-specific activity in this way captures a fundamental and previously inaccessible dimension of mammalian circuit dynamics.
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VTA-DA neurons play a central role in modulating the pleasurable and aversive aspects of social interactions.
“Dopaminergic neurons, arising from both the ventral tegmental area (VTA) and substantia nigra (SN), have attracted significant scientific interest regarding social behaviour, particularly VTA-DA neurons, owing to their central role in modulating the pleasurable and aversive aspects of social interactions (Gunaydin et al., 2014; Ilango et al., 2014; Merrer et al., 2024; 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 Gunaydin et al., 2014
The Results section reports that VTA-DA activity predicts social interaction and that activating a VTA projection increases social interaction in mice. It also reports anxiety-like effects and conditioned place aversion from a different VTA projection, but does not establish modulation of aversive aspects of social interactions. Page numbers are unavailable in our copy. (LLM, conf=0.88)
Experimental — accuracy not yet measuredDopaminergic neurons of the VTA that project to the NAc play a pivotal role in regulating both social cues and reward processing in both humans and rodents.
“Dopaminergic neurons of the VTA, which extend their projections to the nucleus accumbens (NAc), play a pivotal role in regulating both social cues and reward processing in both humans and rodents (Bariselli et al., 2018; Gunaydin et al., 2014, 2014; Kawamichi et al., 2016).”
From Convergence of oxytocin and dopamine signalling in neuronal circuits: Insights into the neurobiology of social interactions across species (2024) · cites this paper as Gunaydin et al., 2014
The Results section (page unavailable) reports that activating VTA-to-NAc projections increased social interaction in mice. The Introduction and Discussion connect this circuitry to reward-related behavior, but the paper does not establish that these neurons regulate reward processing in humans; its direct findings concern mice. (LLM, conf=0.87)
Experimental — accuracy not yet measuredSocial 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 Gunaydin et al., 2014
VTA DA neurons are thought to play a causal role in social reward.
“However, since optogenetic activation of VTA DA neurons increases social interaction (Gunaydin et al., 2014) and supports positive reinforcement (Tsai et al., 2009, Witten et al., 2011), they are thought to play a causal role in social reward.”
From Dorsal raphe dopamine neurons represent the experience of social isolation (2016) · cites this paper as Gunaydin et al., 2014
Optogenetic activation of nucleus accumbens-projecting dopamine neurons can influence prosocial behaviors.
“This is a surprising result, which deserves further exploration, given that optogenetic activation of NAc-projecting DA neurons can influence prosocial behaviors [52].”
From Neural circuits regulating prosocial behaviors (2023) · cites this paper as [52]
Dopamine neurons of the ventral tegmental area are necessary and sufficient to promote social interaction.
“Recent studies have highlighted the necessity and sufficiency of dopamine (DA) neurons of the ventral tegmental area (VTA) to promote social interaction (Gunaydin et al., 2014; Solié et al., 2022).”
From Oxytocin neurons mediate the effect of social isolation via the VTA circuits (2022) · cites this paper as Gunaydin et al., 2014
DA neurons in the VTA play a role in social behavior.
“Previous studies have indicated the role of DA neurons in the VTA in social behavior (Gunaydin et al., 2014; Bariselli et al., 2018; Bariselli et al., 2016b) and shown that chronic isolation alters DA levels in the NAc (Hall et al., 1998; ).”
From Oxytocin neurons mediate the effect of social isolation via the VTA circuits (2022) · cites this paper as Gunaydin et al., 2014
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 Gunaydin et al., 2014
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“The ventral tegmental area, nucleus accumbens, and cerebellum have also been implicated in the regulation of social behavior (Gunaydin et al., 2014; Carta et al., 2019; Porcelli et al., 2019; Musardo et al., 2022; Solié et al., 2022).”
- Authors
- Gunaydin, L. A., Grosenick, L., Finkelstein, J. C., Kauvar, I. V., Fenno, L. E., Adhikari, A., Lammel, S., Mirzabekov, J. J., Airan, R. D., Zalocusky, K. A., Tye, K. M., Anikeeva, P., Malenka, R. C., & Deisseroth, K.
- Affiliations
- Stanford University (US)
- Stanford Medicine (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Deisseroth, Karl
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2014-06
- Volume
- 157
- Issue
- 7
- Pages
- 1535-1551
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC4123133
- OpenAlex
- W1977514547
- Cited by
- 1,389
- References
- 59
- Citations by year
- 2026: 80 · 2025: 107 · 2024: 131 · 2023: 170 · 2022: 135 · 2021: 131 · 2020: 125 · 2019: 128 · 2018: 118 · 2017: 101 · 2016: 98 · 2015: 51 · 2014: 11 · 2012: 1
- FWCI
- 39.74
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institute of Mental Health (R01MH086373)
- National Institute on Drug Abuse (R01DA020794, R37DA035377)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- social behavior, ventral tegmental area, nucleus accumbens, dopamine, neural activity dynamics, fiber photometry, optogenetics, social interaction, neuropsychiatric disorders, neural circuits
- MeSH terms
- Animals, Female, Neural Pathways, Nucleus Accumbens, Photometry, Receptors, Dopamine, Reward, Rhodopsin, Social Behavior, Ventral Tegmental Area, Calcium Signaling, Mice
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