VTA dopamine neuron activity encodes social interaction and promotes reinforcement learning through social prediction error

Prévost-Solié, Clément; Girard, Benoı̂t; Righetti, Beatrice; Tapparel, Malika; Bellone, Camilla

doi:10.1038/s41593-021-00972-9

Cited by 91 publications

(77 citation statements)

References 43 publications

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“…Compared to previous studies on PD (Seer et al, 2017), our patients in 'off' condition had a long withdrawal phase (~ 18 h) from their dopaminergic medication, which might have allowed to better highlight the contribution of dopamine in performance monitoring, when compared with their ordinary pharmacological treatment. Tellingly, no differential errorrelated theta activity was found in HCs and PD 'on', further hinting at the central role of dopamine in performance monitoring-related mid-frontal theta and in regulating the precision of information during predictive processes, triggered by salient and unexpected events (Friston & Kiebel, 2009), as recently found also in social context (Moreau et al 2022;Solié et al, 2022).…”

Section: Dopamine Does Influence Error-related Mid-frontal Theta Acti...mentioning

confidence: 67%

Selective influence of dopamine on electrocortical signatures of error monitoring: a combined EEG and immersive virtual reality study in Parkinson’s disease

Pezzetta

Ozkan

Era

et al. 2022

Preprint

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The saliency of detecting errors in one's own and other's actions is likely linked to the discrepancy between intended or expected and produced or observed output. Salient events seem related to dopamine, the balance of which is profoundly altered in Parkinson's disease (PD). EEG studies in healthy participants indicate that the occurrence of errors in observed actions triggers a variety of electrocortical indices (like mid-frontal theta activity and the Error Positivity, oPe), that seem to map different aspects of error detection and performance monitoring. Whether these indices are differently modulated by dopamine in the same individual has never been investigated. To explore this issue, we recorded EEG markers of error detection by asking healthy controls (HCs) and PD patients to observe ecological reach-to-grasp a glass actions performed by a virtual arm seen in first person perspective. PD patients were tested under their dopaminergic medication ('on-condition'), and after dopaminergic withdrawal ('off-condition'). HCs showed a clear oPe and an increase of theta power during the observation of erroneous vs. correct actions. In PD patients, oPe responses were always preserved. Crucially, however, an error-related increase of theta power was found in 'on' but not in 'off' state PD patients. Thus, different EEG error signatures may index the activity of independent systems and error-related theta power is selectively modulated by dopamine depletion. Our findings may pave the way to the discovery of dopamine-related biomarkers of higher-order motor cognition dysfunctions that may have crucial theoretical and applied implications.

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Section: Dopamine Does Influence Error-related Mid-frontal Theta Acti...mentioning

confidence: 67%

Selective influence of dopamine on electrocortical signatures of error monitoring: a combined EEG and immersive virtual reality study in Parkinson’s disease

Pezzetta

Ozkan

Era

et al. 2022

Preprint

View full text Add to dashboard Cite

show abstract

“…The dopaminergic system has been shown to influence key aspects of social and affiliative behavior in humans and other vertebrates ( Opendak et al, 2021 ; Solié et al, 2022 ), and to cooperate in modulating key components of the social brain network ( Gunaydin and Deisseroth, 2014 ). In addition, accumulating evidence point to an involvement of DA neurotransmission in atypical social development in children with ASD ( Scott-Van Zeeland et al, 2010 ; Supekar et al, 2018 ; Zürcher et al, 2021 ).…”

Section: Discussionmentioning

confidence: 99%

Embryonic Valproate Exposure Alters Mesencephalic Dopaminergic Neurons Distribution and Septal Dopaminergic Gene Expression in Domestic Chicks

Adiletta

Pross

Taricco

et al. 2022

Front. Integr. Neurosci.

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In recent years, the role of the dopaminergic system in the regulation of social behavior is being progressively outlined, and dysfunctions of the dopaminergic system are increasingly associated with neurodevelopmental disorders, including autism spectrum disorder (ASD). To study the role of the dopaminergic (DA) system in an animal model of ASD, we investigated the effects of embryonic exposure to valproic acid (VPA) on the postnatal development of the mesencephalic DA system in the domestic chick. We found that VPA affected the rostro-caudal distribution of DA neurons, without changing the expression levels of several dopaminergic markers in the mesencephalon. We also investigated a potential consequence of this altered DA neuronal distribution in the septum, a social brain area previously associated to social behavior in several vertebrate species, describing alterations in the expression of genes linked to DA neurotransmission. These findings support the emerging hypothesis of a role of DA dysfunction in ASD pathogenesis. Together with previous studies showing impairments of early social orienting behavior, these data also support the use of the domestic chick model to investigate the neurobiological mechanisms potentially involved in early ASD symptoms.

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“…Active (reciprocal and unilateral) and passive interaction definition. Similarly to published work (54), we defined active (reciprocal and unilateral) and passive social interactions based on the localization of the social contact on the body of the two mice interacting. We used the automatically annotated event extracted by the LMT and considered all contacts associated with nose-to-nose contacts and side-by-side contacts as reciprocal interaction.…”

Section: Live Mouse Trackermentioning

confidence: 99%

The impact of C-tactile low-threshold mechanoreceptors on affective touch and social interactions in mice

et al. 2022

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Affective touch is necessary for proper neurodevelopment and sociability. However, it remains unclear how the neurons innervating the skin detect affective and social behaviors. The C low-threshold mechanoreceptors (C-LTMRs), a specific population of somatosensory neurons in mice, appear particularly well suited, physiologically and anatomically, to perceive affective and social touch. However, their contribution to sociability has not been resolved yet. Our observations revealed that C-LTMR functional deficiency induced social isolation and reduced tactile interactions in adulthood. Conversely, transient increase in C-LTMR excitability in adults, using chemogenetics, was rewarding, promoted touch-seeking behaviors, and had prosocial influences on group dynamics. This work provides the first empirical evidence that specific peripheral inputs alone can drive complex social behaviors. It demonstrates the existence of a specialized neuronal circuit, originating in the skin, wired to promote interactions with other individuals.

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VTA dopamine neuron activity encodes social interaction and promotes reinforcement learning through social prediction error

Cited by 91 publications

References 43 publications

Selective influence of dopamine on electrocortical signatures of error monitoring: a combined EEG and immersive virtual reality study in Parkinson’s disease

Selective influence of dopamine on electrocortical signatures of error monitoring: a combined EEG and immersive virtual reality study in Parkinson’s disease

Embryonic Valproate Exposure Alters Mesencephalic Dopaminergic Neurons Distribution and Septal Dopaminergic Gene Expression in Domestic Chicks

The impact of C-tactile low-threshold mechanoreceptors on affective touch and social interactions in mice

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