VTA dopamine neuron activity encodes social interaction and promotes reinforcement learning through social prediction error
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Abstract
Social interactions are motivated behaviors that, in many species, facilitate learning. However, how the brain encodes the reinforcing properties of social interactions remains unclear. In this study, using in vivo recording in freely moving mice, we show that dopamine (DA) neurons of the ventral tegmental area (VTA) increase their activity during interactions with an unfamiliar conspecific and display heterogeneous responses. Using a social instrumental task, we then show that VTA DA neuron activity encodes social prediction error and drives social reinforcement learning. Thus, our findings suggest that VTA DA neurons are a neural substrate for a social learning signal that drives motivated behavior.
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VTA 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 Solié et al., 2022
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 Solié et al., 2022
VTA dopamine activity increased during lever pressing in a social instrumental operant task and optogenetic inhibition of VTA dopamine neurons impaired social reinforcement learning.
“Consistent with an involvement of DA in the reinforcing properties of a social interaction, VTA DA activity increased during lever pressing in a social instrumental operant task and optogenetic inhibition of VTA DA neurons impaired social reinforcement learning [57].”
From Neural circuits regulating prosocial behaviors (2023) · cites this paper as [57]
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 Solié et al., 2022
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Cites
A neural substrate of prediction and reward
Schultz, W., Dayan, P., & Montague, P. R. (1997) · Science · doi:10.1126/science.275.5306.1593 · Cited by 9,388 · see citing works
DeepLabCut: markerless pose estimation of user-defined body parts with deep learning
Mathis, A., Mamidanna, P., Cury, K. M., Abe, T., Murthy, V. N., Mathis, M. W., & Bethge, M. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0209-y · Cited by 5,187 · see citing works
Dopamine in motivational control: rewarding, aversive, and alerting
Bromberg-Martin, E. S., Matsumoto, M., & Hikosaka, O. (2010) · Neuron · doi:10.1016/j.neuron.2010.11.022 · Cited by 2,396 · see citing works
The social motivation theory of autism
Chevallier, C., Kohls, G., Troiani, V., Brodkin, E. S., & Schultz, R. T. (2012) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2012.02.007 · Cited by 2,072 · see citing works
The hippocampal-VTA loop: controlling the entry of information into long-term memory
Lisman, J. E., & Grace, A. A. (2005) · Neuron · doi:10.1016/j.neuron.2005.05.002 · Cited by 1,983 · see citing works
Natural neural projection dynamics underlying social behavior
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., et al. (2014) · Cell · doi:10.1016/j.cell.2014.05.017 · Cited by 1,389 · see citing works
The control of firing pattern in nigral dopamine neurons: burst firing
Grace, A., & Bunney, B. (1984) · Journal of Neuroscience · doi:10.1523/jneurosci.04-11-02877.1984 · Cited by 1,346 · see citing works
Neuron-type-specific signals for reward and punishment in the ventral tegmental area
Cohen, J. Y., Haesler, S., Vong, L., Lowell, B. B., & Uchida, N. (2012) · Nature · doi:10.1038/nature10754 · Cited by 1,318 · see citing works
Affective neuroscience of pleasure: reward in humans and animals
Berridge, K. C., & Kringelbach, M. L. (2008) · Psychopharmacology · doi:10.1007/s00213-008-1099-6 · Cited by 1,254 · see citing works
Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin
Dölen, G., Darvishzadeh, A., Huang, K. W., & Malenka, R. C. (2013) · Nature · doi:10.1038/nature12518 · Cited by 1,161 · see citing works
“Liking” and “wanting” food rewards: Brain substrates and roles in eating disorders
Berridge, K. C. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.02.044 · Cited by 1,147 · see citing works
Dopamine responses comply with basic assumptions of formal learning theory
Waelti, P., Dickinson, A., & Schultz, W. (2001) · Nature · doi:10.1038/35083500 · Cited by 1,018 · see citing works
Responses of monkey dopamine neurons during learning of behavioral reactions
Ljungberg, T., Apicella, P., & Schultz, W. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.67.1.145 · Cited by 987 · see citing works
Berke, J. D. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0152-y · Cited by 904 · see citing works
Processing of Social and Monetary Rewards in the Human Striatum
Izuma, K., Saito, D. N., & Sadato, N. (2008) · Neuron · doi:10.1016/j.neuron.2008.03.020 · Cited by 855 · see citing works
Roesch, M. R., Calu, D. J., & Schoenbaum, G. (2007) · Nature Neuroscience · doi:10.1038/nn2013 · Cited by 597 · see citing works
Gating of social reward by oxytocin in the ventral tegmental area
Hung, L. W., Neuner, S., Polepalli, J. S., Beier, K. T., Wright, M., Walsh, J. J., Lewis, E. M., Luo, L., Deisseroth, K., Dölen, G., et al. (2017) · Science · doi:10.1126/science.aan4994 · Cited by 578 · see citing works
Autism as a disorder of prediction
Sinha, P., Kjelgaard, M. M., Gandhi, T. K., Tsourides, K., Cardinaux, A. L., Pantazis, D., Diamond, S. P., & Held, R. M. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1416797111 · Cited by 563 · cited 5× · see citing works
“It has been suggested that impaired RPE relates to clinical phenotypes of psychiatric disorders and in particular of Autism Spectrum Disorders (ASD) 35 .”
InfluentialSpecialized coding of sensory, motor and cognitive variables in VTA dopamine neurons
Engelhard, B., Finkelstein, J., Cox, J., Fleming, W., Jang, H. J., Ornelas, S., Koay, S. A., Thiberge, S. Y., Daw, N. D., Tank, D. W., et al. (2019) · Nature · doi:10.1038/s41586-019-1261-9 · Cited by 544 · see citing works
Neural circuit mechanisms of social behavior
Chen, P., & Hong, W. (2018) · Neuron · doi:10.1016/j.neuron.2018.02.026 · Cited by 527 · see citing works
Absolute Coding of Stimulus Novelty in the Human Substantia Nigra/VTA
Bunzeck, N., & Düzel, E. (2006) · Neuron · doi:10.1016/j.neuron.2006.06.021 · Cited by 503 · see citing works
Arithmetic and local circuitry underlying dopamine prediction errors
Eshel, N., Bukwich, M., Rao, V., Hemmelder, V., Tian, J., & Uchida, N. (2015) · Nature · doi:10.1038/nature14855 · Cited by 386 · see citing works
Dopamine neurons projecting to the posterior striatum reinforce avoidance of threatening stimuli
Menegas, W., Akiti, K., Amo, R., Uchida, N., & Watabe‐Uchida, M. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0222-1 · Cited by 384 · see citing works
Volitional social interaction prevents drug addiction in rat models
Venniro, M., Zhang, M., Caprioli, D., Hoots, J. K., Golden, S. A., Heins, C., Morales, M., Epstein, D. H., & Shaham, Y. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0246-6 · Cited by 342 · see citing works
Social reward among juvenile mice
Panksepp, J. B., & Lahvis, G. P. (2007) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2006.00295.x · Cited by 248 · see citing works
Dopamine neurons respond to errors in the prediction of sensory features of expected rewards
Takahashi, Y. K., Batchelor, H. M., Liu, B., Khanna, A., Morales, M., & Schoenbaum, G. (2017) · Neuron · doi:10.1016/j.neuron.2017.08.025 · Cited by 200 · see citing works
Schultz, W. (2017) · Current Biology · doi:10.1016/j.cub.2017.02.064 · Cited by 177 · see citing works
An amygdala-to-hypothalamus circuit for social reward
Hu, R. K., Zuo, Y., Ly, T., Wang, J., Meera, P., Wu, Y. E., & Hong, W. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00828-2 · Cited by 174 · see citing works
Bariselli, S., Hörnberg, H., Prévost-Solié, C., Musardo, S., Hatstatt-Burklé, L., Scheiffele, P., & Bellone, C. (2018) · Nature Communications · doi:10.1038/s41467-018-05382-3 · Cited by 171 · see citing works
Self-citationHabenula Lesions Reveal that Multiple Mechanisms Underlie Dopamine Prediction Errors
Tian, J., & Uchida, N. (2015) · Neuron · doi:10.1016/j.neuron.2015.08.028 · Cited by 165 · see citing works
Feelings about food: the ventral tegmental area in food reward and emotional eating
Meye, F. J., & Adan, R. A. H. (2013) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2013.11.003 · Cited by 156 · see citing works
The medial prefrontal cortex shapes dopamine reward prediction errors under state uncertainty
Starkweather, C. K., Gershman, S. J., & Uchida, N. (2018) · Neuron · doi:10.1016/j.neuron.2018.03.036 · Cited by 136 · see citing works
Sharpe, M. J., Marchant, N. J., Ramsey, L. A., Richie, C. T., Zhang, Y. J., Campbell, E. J., Koivula, P. P., Necarsulmer, J., Mejías-Aponte, C. A., Morales, M., et al. (2017) · Current Biology · doi:10.1016/j.cub.2017.06.024 · Cited by 129 · see citing works
Alhadeff, A. L., Goldstein, N., Park, O., Klima, M. L., Vargas, A. P.-D., & Betley, J. N. (2019) · Neuron · doi:10.1016/j.neuron.2019.05.050 · Cited by 129 · see citing works
Enhancement of Vision by Monocular Deprivation in Adult Mice
Prusky, G. T., Alam, N. M., & Douglas, R. M. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3396-06.2006 · Cited by 112 · see citing works
Midbrain dopamine neurons signal aversion in a reward-context-dependent manner
Matsumoto, H., Tian, J., Uchida, N., & Watabe‐Uchida, M. (2016) · eLife · doi:10.7554/elife.17328 · Cited by 109 · see citing works
Social rewards: From basic social building blocks to complex social behavior
Tamir, D. I., & Hughes, B. L. (2018) · Perspectives on Psychological Science · doi:10.1177/1745691618776263 · Cited by 109 · see citing works
Recent advances in understanding the role of phasic dopamine activity
Schultz, W. (2019) · F1000Research · doi:10.12688/f1000research.19793.1 · Cited by 89 · see citing works
Dopamine transients do not act as model-free prediction errors during associative learning
Sharpe, M. J., Batchelor, H. M., Mueller, L. E., Chang, C. Y., Maes, E. J. P., Niv, Y., & Schoenbaum, G. M. (2020) · Nature Communications · doi:10.1038/s41467-019-13953-1 · Cited by 84 · see citing works
Midbrain circuits of novelty processing
Tapper, A. R., & Molas, S. (2020) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2020.107323 · Cited by 71 · see citing works
Impaired reward-related learning signals in remitted unmedicated patients with recurrent depression
Geugies, H., Mocking, R. J. T., Figueroa, C. A., Groot, P. F. C., Marsman, J.-B. C., Servaas, M. N., Steele, J. D., Schene, A. H., & Ruhé, H. G. (2019) · Brain · doi:10.1093/brain/awz167 · Cited by 67 · see citing works
Context-Dependent Multiplexing by Individual VTA Dopamine Neurons
Kremer, Y., Flakowski, J., Rohner, C., & Lüscher, C. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0502-20.2020 · Cited by 57 · see citing works
Kinard, J. L., Mosner, M. G., Greene, R. K., Addicott, M. A., Bizzell, J., Petty, C., Cernasov, P., Walsh, E. C., Eisenlohr-Moul, T. A., Carter, R. M., et al. (2020) · Autism Research · doi:10.1002/aur.2273 · Cited by 47 · see citing works
Quantifying Social Motivation in Mice Using Operant Conditioning
Martin, L. A., & Iceberg, E. (2015) · Journal of Visualized Experiments · doi:10.3791/53009 · Cited by 36 · see citing works
Bariselli, S., Contestabile, A., Tzanoulinou, S., Musardo, S., & Bellone, C. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00360 · Cited by 28 · see citing works
Self-citationNeural Mechanisms of Reward Prediction Error in Autism Spectrum Disorder
Mosner, M. G., McLaurin, R. E., Kinard, J. L., Hakimi, S., Parelman, J. M., Shah, J. S., Bizzell, J., Greene, R. K., Cernasov, P., Walsh, E. C., et al. (2019) · Autism Research and Treatment · doi:10.1155/2019/5469191 · Cited by 22 · see citing works
Nicotine Modifies Corticostriatal Plasticity and Amphetamine Rewarding Behaviors in Mice
Storey, G. P., Gonzalez-Fernandez, G., Bamford, I. J., Hur, M., McKinley, J. W., Heimbigner, L., Minasyan, A., Walwyn, W. M., & Bamford, N. S. (2016) · eNeuro · doi:10.1523/eneuro.0095-15.2015 · Cited by 21 · see citing works
Disrupted reinforcement learning during post-error slowing in ADHD
Chevrier, A., Bhaijiwala, M., Lipszyc, J., Cheyne, D., Graham, S., & Schachar, R. (2019) · PLOS ONE · doi:10.1371/journal.pone.0206780 · Cited by 21 · see citing works
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An amygdala-to-hypothalamus circuit for social reward
Hu, R. K., Zuo, Y., Ly, T., Wang, J., Meera, P., Wu, Y. E., & Hong, W. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00828-2 · Cited by 174 · see citing works
Emotional contagion and prosocial behavior in rodents
Keysers, C., Knapska, E., Moita, M. A. P., & Gazzola, V. (2022) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2022.05.005 · Cited by 123 · see citing works
Song, Q., Wei, A., Xu, H., Gu, Y., Jiang, Y. Q., Dong, N., Zheng, C., Wang, Q., Gao, M., Sun, S., et al. (2024) · Nature Neuroscience · doi:10.1038/s41593-023-01519-w · Cited by 128 · see citing works
Social isolation and the brain: effects and mechanisms
Xiong, Y., Hong, H., Liu, C., & Zhang, Y. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01835-w · Cited by 127 · see citing works
Detection, processing and reinforcement of social cues: regulation by the oxytocin system
Menon, R., & Neumann, I. D. (2023) · Nature Reviews Neuroscience · doi:10.1038/s41583-023-00759-w · Cited by 100 · see citing works
Explaining dopamine through prediction errors and beyond
Gershman, S. J., Assad, J. A., Datta, S. R., Linderman, S. W., Sabatini, B. L., Uchida, N., & Wilbrecht, L. (2024) · Nature Neuroscience · doi:10.1038/s41593-024-01705-4 · Cited by 101 · see citing works
Hypothalamic control of innate social behaviors
Mei, L., Osakada, T., & Lin, D. (2023) · Science · doi:10.1126/science.adh8489 · Cited by 83 · see citing works
Oxytocin neurons mediate the effect of social isolation via the VTA circuits
Musardo, S., Contestabile, A., Knoop, M., Baud, O., & Bellone, C. (2022) · eLife · doi:10.7554/elife.73421 · Cited by 77 · see citing works
Self-citationCharacterizing the mechanisms of social connection
Delgado, M. R., Fareri, D. S., & Chang, L. J. (2023) · Neuron · doi:10.1016/j.neuron.2023.09.012 · Cited by 81 · see citing works
Neural circuits regulating prosocial behaviors
Walsh, J. J., Christoffel, D. J., & Malenka, R. C. (2023) · Neuropsychopharmacology · doi:10.1038/s41386-022-01348-8 · Cited by 72 · see citing works
Therapeutic mechanisms of psychedelics and entactogens
Heifets, B. D., & Olson, D. E. (2023) · Neuropsychopharmacology · doi:10.1038/s41386-023-01666-5 · Cited by 67 · see citing works
Huzard, D., Martín, M., Maingret, F., Chemin, J., Jeanneteau, F. D., Méry, P., Fossat, P., Bourinet, E., & François, A. (2022) · Science Advances · doi:10.1126/sciadv.abo7566 · Cited by 61 · see citing works
A dopaminergic reward prediction error signal shapes maternal behavior in mice
Xie, Y., Huang, L., Corona, A., Pagliaro, A. H., & Shea, S. D. (2022) · Neuron · doi:10.1016/j.neuron.2022.11.019 · Cited by 51 · see citing works
Rappeneau, V., & Castillo Díaz, F. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105675 · Cited by 51 · see citing works
Batten, S. R., Bang, D., Kopell, B. H., Davis, A. N., Heflin, M., Fu, Q. X., Perl, O., Ziafat, K., Hashemi, A., Sáez, I., et al. (2024) · Nature Human Behaviour · doi:10.1038/s41562-024-01831-w · Cited by 48 · see citing works
Overlapping representations of food and social stimuli in mouse VTA dopamine neurons
Willmore, L., Minerva, A. R., Engelhard, B., Murugan, M., McMannon, B., Oak, N., Thiberge, S. Y., Peña, C. J., & Witten, I. B. (2023) · Neuron · doi:10.1016/j.neuron.2023.08.003 · Cited by 42 · see citing works
Bordes, J., Miranda, L., Müller‐Myhsok, B., & Schmidt, M. V. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105243 · Cited by 42 · see citing works
Bernardi, E., & Visioli, F. (2024) · Nutrition Research · doi:10.1016/j.nutres.2024.03.007 · Cited by 38 · see citing works
Vicarious Emotions of Fear and Pain in Rodents
Keysers, C., & Gazzola, V. (2023) · Affective Science · doi:10.1007/s42761-023-00198-x · Cited by 37 · see citing works
Deconstructing the contribution of sensory cues in social approach
Contestabile, A., Casarotto, G., Girard, B., Tzanoulinou, S., & Bellone, C. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15179 · Cited by 36 · see citing works
Self-citationIsaac, J., Karkare, S. C., Balasubramanian, H., Schappaugh, N., Javier, J. L., Rashid, M., & Murugan, M. (2024) · Nature Communications · doi:10.1038/s41467-024-52294-6 · Cited by 32 · see citing works
Dopaminergic error signals retune to social feedback during courtship
Roeser, A. C., Gadagkar, V., Das, A., Puzerey, P. A., Kardon, B., & Goldberg, J. H. (2023) · Nature · doi:10.1038/s41586-023-06580-w · Cited by 42 · see citing works
Sexually dimorphic dopaminergic circuits determine sex preference
Wei, A., Zhao, A., Zheng, C., Dong, N., Cheng, X., Duan, X., Zhong, S., Liu, X., Jian, J., Qin, Y., et al. (2025) · Science · doi:10.1126/science.adq7001 · Cited by 30 · see citing works
Dopamine control of social novelty preference is constrained by an interpeduncular-tegmentum circuit
Molas, S., Freels, T. G., Zhao-Shea, R., Lee, T., Giménez‐Gómez, P., Barbini, M., Martin, G. E., & Tapper, A. R. (2024) · Nature Communications · doi:10.1038/s41467-024-47255-y · Cited by 27 · see citing works
Oxytocin modulates neurocomputational mechanisms underlying prosocial reinforcement learning
Martins, D., Lockwood, P. L., Cutler, J., Moran, R., & Paloyelis, Y. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102253 · Cited by 28 · see citing works
Parasubthalamic calretinin neurons modulate wakefulness associated with exploration in male mice
Guo, H., Jiang, J.-B., Xu, W., Zhang, M.-T., Chen, H., Shi, H., Wang, L., He, M., Lazarus, M., Li, S., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-37797-y · Cited by 26 · see citing works
Monoaminergic Modulation of Learning and Cognitive Function in the Prefrontal Cortex
Boyle, N., Betts, S., & Lü, H. (2024) · Brain Sciences · doi:10.3390/brainsci14090902 · Cited by 29 · see citing works
Penalva-Tena, A., Bedke, J., Gaudin, A., Barrios, J. P., Bertram, E. P. L., & Douglass, A. D. (2018) · doi:10.1101/444026 · Cited by 41 · see citing works
Interconnected neural circuits mediating social reward
Isaac, J., & Murugan, M. (2024) · Trends in Neurosciences · doi:10.1016/j.tins.2024.10.004 · Cited by 25 · see citing works
Elum, J. E., Szelenyi, E. R., Juarez, B., Murry, A. D., Loginov, G. I., Zamorano, C. A., Gao, P., Wu, G., Ng-Evans, S., Yee, J. X., et al. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114668 · Cited by 25 · see citing works
Liu, X., Cui, Y., Zhang, Y., Guo, X., Meng, Y., Wang, X., Qiu, B., Li, X., Liu, W., & Zhang, D. (2022) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2022.113949 · Cited by 22 · see citing works
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Kim, N., Choo, H.-I., & Lee, Y. (2024) · Neuroscience · doi:10.1016/j.neuroscience.2024.07.018 · Cited by 20 · see citing works
Penalva-Tena, A., Bedke, J., Gaudin, A., Barrios, J. P., Bertram, E. P., & Douglass, A. D. (2024) · Current Biology · doi:10.1016/j.cub.2024.11.037 · Cited by 19 · see citing works
Zheng, C., Lei, W. I., Liu, B., Wang, Q., Huang, Y., Wang, S., Li, X., Gong, H., & Wang, Z. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112799 · Cited by 21 · see citing works
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Molas, S., Zhao-Shea, R., Freels, T. G., & Tapper, A. R. (2023) · eNeuro · doi:10.1523/eneuro.0282-22.2022 · Cited by 24 · see citing works
Pezzetta, R., Özkan, D. G., Era, V., Tieri, G., Zabberoni, S., Taglieri, S., da Costa, A. L. C., Peppe, A., Caltagirone, C., & Aglioti, S. M. (2023) · npj Parkinson s Disease · doi:10.1038/s41531-022-00441-5 · Cited by 18 · see citing works
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Self-citationHearing, touching, and multisensory integration during mate choice
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Establishing connectivity through microdissections of midbrain stimulation-related neural circuits
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Novak, G., & Seeman, M. (2022) · Healthcare · doi:10.3390/healthcare10091713 · Cited by 17 · see citing works
Chang, H.-T., Cheng, K., Hung, Y.-C., & Hsu, K. (2025) · Journal of Biomedical Science · doi:10.1186/s12929-025-01130-0 · Cited by 14 · see citing works
Pohl, T. T., & Hörnberg, H. (2022) · Neuronal Signaling · doi:10.1042/ns20210030 · Cited by 13 · see citing works
Dopamine dynamics underlying maternal motivation and reward
Day, K. R., & Shea, S. D. (2025) · Neuroscience Research · doi:10.1016/j.neures.2025.104928 · Cited by 13 · see citing works
Operant social self-administration in male CD1 mice
Lee, S. S., Vènniro, M., Shaham, Y., Hope, B. T., & Ramsey, L. A. (2024) · Psychopharmacology · doi:10.1007/s00213-024-06560-6 · Cited by 12 · see citing works
Zhao, X., Chae, Y. C., Smith, D., Chen, V., DeFelipe, D., Sokol, J. W., Sadangi, A., & Tschida, K. (2024) · eLife · doi:10.7554/elife.94924.3 · Cited by 13 · see citing works
Di, Y., Diao, Z., Zheng, Q., Li, J., Cheng, Q., Li, Z., Fang, S., Wang, H., Wei, C., Zheng, Q., et al. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.0623-22.2022 · Cited by 12 · see citing works
Glutamatergic Projection from the Ventral Tegmental Area to the Zona Incerta Regulates Fear Response
Wang, X.-Y., Zhang, H., Tong, K., Han, J. Y., Zhao, X.-Y., Song, Y., Hao, J., Sun, N., & Gao, C. (2024) · Neuroscience · doi:10.1016/j.neuroscience.2024.01.020 · Cited by 12 · see citing works
Raymond, J. S., Rehn, S., James, M. H., Everett, N. A., & Bowen, M. T. (2024) · Biology of Sex Differences · doi:10.1186/s13293-024-00612-4 · Cited by 12 · see citing works
How can ethology inform the neuroscience of fear, aggression and dominance?
Battivelli, D., Fan, Z., Hu, H., & Gross, C. T. (2024) · Nature reviews. Neuroscience · doi:10.1038/s41583-024-00858-2 · Cited by 11 · see citing works
Barbier, M., Rajamani, K. T., Netser, S., Wagner, S., & Harony‐Nicolas, H. (2025) · Advanced Science · doi:10.1002/advs.202414813 · Cited by 12 · see citing works
Navarrete, J. S., Schneider, K. N., Smith, B. M., Goodwin, N. L., Zhang, Y. Y., Salazar, A. S., Gonzalez, Y. E., Anumolu, P., Gross, E., Tsai, V. S., et al. (2024) · Biological Psychiatry · doi:10.1016/j.biopsych.2024.01.007 · Cited by 10 · see citing works
Adiletta, A., Pross, A., Taricco, N., & Sgadó, P. (2022) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2022.804881 · Cited by 9 · see citing works
Jansen, M., Lockwood, P. L., Cutler, J., & de Bruijn, E. R. A. (2023) · NeuroImage · doi:10.1016/j.neuroimage.2023.119983 · Cited by 7 · see citing works
Chow, J. J., Pitts, K. M., Schoenbaum, A., Costa, K. M., Schoenbaum, G. M., & Shaham, Y. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.1887-23.2024 · Cited by 9 · see citing works
Kitagawa, K., Takemoto, T., Seiriki, K., Kasai, A., Hashimoto, H., & Nakazawa, T. (2024) · Biochemical and Biophysical Research Communications - BBRC · doi:10.1016/j.bbrc.2024.150251 · Cited by 8 · see citing works
Rojek-Sito, K., Meyza, K. Z., Ziegart-Sadowska, K., Nazaruk, K., Puścian, A., Hamed, A., Kiełbiński, M., Solecki, W., & Knapska, E. (2023) · PLoS Biology · doi:10.1371/journal.pbio.3002343 · Cited by 9 · see citing works
Prairie voles as a model for adaptive reward remodeling following loss of a bonded partner
Sadino, J., & Donaldson, Z. (2024) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.15134 · Cited by 7 · see citing works
Emotions in multi-brain dynamics: A promising research frontier
Antonelli, F., Bernardi, F., Koul, A., Novembre, G., & Papaleo, F. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105965 · Cited by 8 · see citing works
Wang, Q., Wang, Y., Tian, Y., Li, Y., Han, J., Tai, F., & Jia, R. (2023) · Behavioural Brain Research · doi:10.1016/j.bbr.2023.114687 · Cited by 8 · see citing works
Kurdi, B., Sánchez, À., Dasgupta, N., & Banaji, M. R. (2023) · Journal of Personality and Social Psychology · doi:10.1037/pspa0000370 · Cited by 13 · see citing works
Roeser, A. C., Gadagkar, V., Das, A., Puzerey, P. A., Kardon, B., & Goldberg, J. H. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/822817 · Cited by 8 · see citing works
Borland, J. M. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105809 · Cited by 8 · see citing works
Socha, J., Grochecki, P., Smaga, I., Jastrzębska, J., Wronikowska‐Denysiuk, O., Marszałek‐Grabska, M., Słowik, T., Kotlinski, R., Filip, M., Lübec, G., et al. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25021041 · Cited by 7 · see citing works
How dopamine guides our social world
Padilla-Coreano, N., & Martínez-Rivera, F. J. (2025) · Pharmacological Reviews · doi:10.1016/j.pharmr.2025.100085 · Cited by 6 · see citing works
Age-specific regulation of sociability by hypothalamic Agrp neurons
İyilikci, O., Kim, L., Zimmer, M. R., Bober, J., Li, Y., Pelts, M., Santana, G. M. T., & Dietrich, M. O. (2025) · Current Biology · doi:10.1016/j.cub.2025.08.014 · Cited by 6 · see citing works
Pérez, A. D. A., Kautzmann, A. S., & Alvares, L. D. O. (2024) · Translational Psychiatry · doi:10.1038/s41398-024-02955-3 · Cited by 5 · see citing works
Sandoval, K. C., Rychlik, J., & Choe, K. Y. (2025) · eNeuro · doi:10.1523/eneuro.0196-24.2025 · Cited by 5 · see citing works
Establishing a social behavior paradigm for female mice
Xiao, H., Huang, C., Wu, Y. H., Wang, J. J., & Wang, H. (2025) · Frontiers in Neuroscience · doi:10.3389/fnins.2025.1630491 · Cited by 5 · see citing works
Johnston, M. P., & Wanat, M. J. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.1038236 · Cited by 6 · see citing works
Charting the neuroscience of interpersonal trust: A bibliographic literature review
Wu, Y. H., & Krüeger, F. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105930 · Cited by 6 · see citing works
Arakawa, H., Tokashiki, M., Higuchi, Y., & Konno, T. (2024) · Peptides · doi:10.1016/j.peptides.2024.171178 · Cited by 4 · see citing works
Overlapping representations of food and social stimuli in VTA dopamine neuronsPreprint
Willmore, L., Minerva, A. R., Engelhard, B., Murugan, M., McMannon, B., Oak, N., Thiberge, S. Y., Peña, C. J., & Witten, I. B. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.17.541104 · Cited by 5 · see citing works
Excess Neonatal Testosterone Causes Male-Specific Social and Fear Memory Deficits in Wild-Type Mice
Quiñones-Labernik, P., Blocklinger, K. L., Bruce, M. R., Hagan, E., Preuschl, D., Tesar, C., & Ferri, S. L. (2025) · eneuro · doi:10.1523/eneuro.0020-25.2025 · Cited by 4 · see citing works
“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).”
Tzanoulinou, S., Astori, S., Grandi, L. C., Gullo, F., Kalusivikako, R., Rai, S., Limorenko, G., Tafti, M., Becchetti, A., & Vassalli, A. (2026) · Biological Psychiatry · doi:10.1016/j.biopsych.2026.05.022 · Cited by 4 · see citing works
Social stress and affiliative touch: A tale of two affective states
Papantoniou, L. P., Vityk, O., & Tzanoulinou, S. (2026) · iScience · doi:10.1016/j.isci.2026.114833 · Cited by 4 · see citing works
EGCG attenuates METH self‐administration and reinstatement of METH seeking in mice
Si, Z., Wang, X., Yu, Z., Ruan, Y., Qian, L., Lin, S., Gong, X., Li, L., Huang, J., & Liu, Y. (2023) · Addiction Biology · doi:10.1111/adb.13307 · Cited by 4 · see citing works
VTA µ-Opioidergic Neurons Facilitate Low Sociability in Protracted Opioid Abstinence
Jo, A. Y., Xie, Y., Wooldridge, L. M., Rogers, S. A., Kimmey, B. A., Rodrigues, A., Ortega, R. A. S., Creasy, K. T., Beier, K. T., Blendy, J. A., et al. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.1154-24.2025 · Cited by 8 · see citing works
Organization of Brainwide Inputs to Discrete Lateral Septum Projection Populations
Isaac, J., Karkare, S. C., Balasubramanian, H., & Murugan, M. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.0797-25.2025 · Cited by 5 · see citing works
Era, V., Pesci, U. G., Moreau, Q., Pezzetta, R., Zabberoni, S., Peppe, A., da Costa, A. L. C., Taglieri, S., Candidi, M., & Aglioti, S. M. (2025) · Communications Biology · doi:10.1038/s42003-025-08638-z · Cited by 4 · see citing works
History, pharmacology and therapeutic mechanisms of 3,4‐methylenedioxymethamphetamine (MDMA)
Casey, A. B., & Heifets, B. D. (2025) · British Journal of Pharmacology · doi:10.1111/bph.70225 · Cited by 4 · see citing works
Araújo, A. C., Duarte, I. C., Sousa, T., Oliveira, J. M., Pereira, A. T., Macedo, A., & Castelo-Branco, M. S. (2024) · Scientific Reports · doi:10.1038/s41598-024-56161-8 · Cited by 4 · see citing works
Valence-dependent synaptic plasticity drives approach and avoidance behavior in social contextPreprint
Espinosa, P., Girard, B., Lucchini, M., Campanelli, F., Tiriticco, V., Mohrhauer, L., & Bellone, C. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.11.08.515650 · Cited by 4 · see citing works
Self-citationVTA μ–opioidergic neurons facilitate low sociability in protracted opioid withdrawalPreprint
Jo, A. Y., Xie, Y., Rodrigues, A., Ortega, R. A. S., Creasy, K. T., Beier, K. T., Blendy, J. A., & Corder, G. F. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.07.08.602522 · Cited by 4 · see citing works
BlueBerry: Closed-loop wireless optogenetic manipulation in freely moving animalsPreprint
Nourizonoz, A., Girard, B., Guyoton, M., Galiñanes, G. L., Thurnherr, R., Pellat, S., Bellone, C., & Huber, D. (2025) · eLife · doi:10.1101/2025.01.30.635697 · Cited by 5 · see citing works
Self-citationThe Ins and Outs of Dopamine Transporter Gene Manipulation: In Vivo Models of DAT Dysfunction
Stewart, A., & Blakely, R. (2025) · Advances in neurobiology · doi:10.1007/978-3-031-96364-3_10 · Cited by 3 · see citing works
Linking homeostasis to reinforcement learning: internal state control of motivated behavior
Yoshida, N., Sprekeler, H., & Gutkin, B. S. (2025) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2025.101611 · Cited by 3 · see citing works
A circuit-based framework for depression: Reshaping the pathological attractor
Yuan, Z., Quan, J., Cui, Y., & Luo, M. (2026) · Neuron · doi:10.1016/j.neuron.2026.04.009 · Cited by 4 · see citing works
From eye to AI: Studying rodent social behavior in the era of machine learning
Chindemi, G., Bellone, C., & Girard, B. J. T. (2026) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2026.106766 · Cited by 3 · see citing works
Self-citationMarcus, M. M., & Banks, M. L. (2025) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2025.106217 · Cited by 3 · see citing works
Contestabile, A., Casarotto, G., Girard, B., Righetti, B., Solié, C., Bellone, C., & Tzanoulinou, S. (2025) · European Journal of Neuroscience · doi:10.1111/ejn.70203 · Cited by 2 · see citing works
Self-citationРожкова, И. Н., Okotrub, S. V., Brusentsev, E. Y., Uldanova, K. E., Chuyko, E. А., Напримеров, В. А., Lipina, T. V., Amstislavskaya, T. G., & Amstislavsky, S. Y. (2023) · Vavilov Journal of Genetics and Breeding · doi:10.18699/vjgb-23-14 · Cited by 3 · see citing works
Fayad, S. L., Reynolds, L. M., Torquet, N., Tolu, S., Mondoloni, S., Nguyen, C., Siriphanh, A., Justo, R., Didienne, S., Debray, N., et al. (2024) · PLoS Biology · doi:10.1371/journal.pbio.3002850 · Cited by 2 · see citing works
Isaac, J., Balasubramanian, H., Karkare, S. C., Schappaugh, N., & Murugan, M. (2025) · STAR Protocols · doi:10.1016/j.xpro.2025.103788 · Cited by 2 · see citing works
Zheng, Q., Zhao, Y., Cheng, Q., Wang, H., Liu, F., Lai, J., Liu, Y., Zhang, X., Kang, Y., Li, Z., et al. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.0382-25.2025 · Cited by 2 · see citing works
Cheng, Q., Liu, W., Li, Y., Xu, S., Wei, C., Zheng, Q., Wu, M., Han, J., Liu, Z., Ren, W., et al. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2509072122 · Cited by 2 · see citing works
Wu, W., Mei, B., Wu, Y., Liu, L., Wang, Y., Lombardo, M., & Yang, H. (2026) · Food Research International · doi:10.1016/j.foodres.2026.118499 · Cited by 2 · see citing works
Dopaminergic mechanisms of dynamical social specialization
Solié, C., Nicolson, A., Justo, R., Layadi, Y., Morin, B., Batifol, C., Reynolds, L. M., Borgne, T. L., Fayad, S. L., Gulmez, A., et al. (2026) · Nature · doi:10.1038/s41586-026-10301-4 · Cited by 2 · see citing works
Self-citationSongbird mesostriatal dopamine pathways are spatially segregated before the onset of vocal learning
Ramarao, M., Roeser, A. C., Jones, C. D., & Goldberg, J. H. (2023) · PLoS ONE · doi:10.1371/journal.pone.0285652 · Cited by 2 · see citing works
- Authors
- Solié, C., Girard, B., Righetti, B., Tapparel, M., & Bellone, C.
- Affiliations
- University of Geneva (CH)
- Corresponding author
- Bellone, Camilla
- Venue
- Nature Neuroscience
- Published
- 2021-12-02
- Volume
- 25
- Issue
- 1
- Pages
- 86-97
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC7612196
- OpenAlex
- W3217059373
- Cited by
- 186
- References
- 48
- Citations by year
- 2026: 41 · 2025: 45 · 2024: 45 · 2023: 27 · 2022: 21 · 2021: 5 · 2019: 1 · 2018: 1
- FWCI
- 11.27
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature Neuroscience (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed (publishedVersion)
- Archive ouverte UNIGE (University of Geneva) (publishedVersion)
- PubMed Central (acceptedVersion)
- Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
- Funders
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (182326, 150704)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- ventral tegmental area, dopaminergic neurons, social interaction, social learning, neural coding, motivated behavior, conspecific interactions
- MeSH terms
- Social Interaction, Animals, Reinforcement, Psychology, Reward, Ventral Tegmental Area, Mice, Dopaminergic Neurons
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