Role of VTA dopamine neurons and neuroligin 3 in sociability traits related to nonfamiliar conspecific interaction

Bariselli, Sebastiano; Hörnberg, Hanna; Prévost-Solié, Clément; Musardo, Stefano; Hatstatt-Burklé, Laetitia; Scheiffele, Peter; Bellone, Camilla

doi:10.1038/s41467-018-05382-3

Cited by 143 publications

(172 citation statements)

References 59 publications

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“…2A). As previously shown, (16) time sniffing the social stimulus habituated within and between the 3 trials ( Fig. 2B, C).…”

Section: Main Textsupporting

confidence: 81%

“…Within the VTA, a subset of DA neurons encodes the novelty of the rewards more than its value (15). Moreover, we have previously shown a progressive decrease in interaction during exposure time and following repeated exposure to the social stimulus (16). Therefore, we asked whether VTA DA neuron can differentially encode the value and the novelty associated with social interaction.…”

Section: Main Textmentioning

confidence: 99%

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Dopamine neurons of the VTA encode active conspecific interaction and promote social learning through social reward prediction error

Prévost-Solié

Girard

Righetti

et al. 2020

Preprint

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Social interactions motivate behavior in many species, facilitating learning, foraging and cooperative behavior. However, how the brain encodes the reinforcing properties of social interactions remains elusive. Here using in vivo recording in freely moving mice, we show that Dopamine (DA) neurons of the Ventral Tegmental Area (VTA) increase their activity during active interactions with unfamiliar conspecific. Using a social instrumental task, we then show that VTA DA neuron activity signals social reward prediction error and drives social reinforcement learning. Thereby, our findings propose that VTA DA neurons are a neural substrate for a social learning signal driving motivated behavior.the lever zone and in the interaction zone. Friedman test (χ 2 (49) = 61.27, P < 0.0001) followed by Bonferroni-Holm correction.

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“…2A). As previously shown, (16) time sniffing the social stimulus habituated within and between the 3 trials ( Fig. 2B, C).…”

Section: Main Textsupporting

confidence: 81%

Section: Main Textmentioning

confidence: 99%

Dopamine neurons of the VTA encode active conspecific interaction and promote social learning through social reward prediction error

Prévost-Solié

Girard

Righetti

et al. 2020

Preprint

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“…Altered VTA connectivity and impaired VTA dopamine neurons activity were demonstrated in ASD patients 40 and in ASD models 19,20,[41][42][43][44] respectively. We used whole-cell patch-clamp to record VTA dopamine neurons in acute brain slices from control and p-Cresol-treated animals ( Figure 1P-W).…”

Section: P-cresol Impairs Dopamine Neurons Excitability In the Vta Anmentioning

confidence: 99%

The microbial metabolitep-Cresol induces autistic-like behaviors in mice by remodeling the gut microbiota

Bermudez-Martin

Becker

Caramello

et al. 2020

Preprint

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Background: Perturbations of the microbiota-gut-brain axis have been identified in autism spectrum disorders (ASD), suggesting that the microbiota could be involved in the development or maintenance of abnormal social and stereotyped behaviors in ASD patients.Yet, the underlying mediators and mechanisms remain unclear. We hypothesized that microbial metabolites produced by the gut microbiota contribute to behavioral deficits in ASD.We focused on p-Cresol, a microbial metabolite previously described as abnormally elevated in ASD patients. Methods:Wild-type mice were chronically treated with p-Cresol in drinking water to mimic intestinal exposure. We combined behavioral phenotyping, electrophysiology, microbiota 16S sequencing and fecal microbiota transplantations to decipher the consequences of p-Cresol exposure. Results:We showed that p-Cresol selectively induced behavioral alterations reminiscent of ASD core symptoms: social behavior deficits, stereotypies and perseverative behaviors, but no changes in anxiety, locomotion or cognition. We further showed that p-Cresol decreases the activity of dopamine neurons in the ventral tegmental area (VTA), a key brain region for social reward processing. In addition, we reveal that p-Cresol remodels the intestinal microbiome, impacting specific bacterial taxa associated with social behavior deficits and stereotypies. We further demonstrated that social behavior deficits are transferred to control mice after transplantation of microbiota from p-Cresol-treated mice. Finally, both social interactions and VTA dopamine neurons activity were normalized in p-Cresol treated mice after transplant of microbiota from control mice. Conclusions:Our study suggests that the microbial metabolite p-Cresol could be involved in the development of autistic behaviors through remodeling of the gut microbiota.

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“…Social interaction is a complex behavior that critically relies on the integrity of midbrain DA ventral tegmental area (VTA) neurons [64][65][66] . The dissection of neural circuits regulating social interaction indicate that several neural pathways converging onto different VTA DA neurons may regulate distinct components of social behaviors.…”

Section: Discussionmentioning

confidence: 99%

Cerebellar dopamine D2 receptors regulate preference for social novelty

Cutando

Puighermanal

Castell

et al. 2019

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The cerebellum, a primary center involved in the control of sensorimotor tasks, also contributes to higher cognitive functions including reward, emotion and social interaction. The regulation of these behaviors has been largely ascribed to the monoaminergic system in limbic regions.However, the contribution of cerebellar dopamine signaling in the modulation of these functions remains largely unknown due to the lack of precise characterization of cerebellar dopaminoceptive neurons. By combining cell type-specific transcriptomic and histological analyses, 3D imaging and electrophysiology we demonstrate that cerebellar dopamine D2 receptors (D2R) in mice are preferentially expressed in Purkinje cells (PCs). While activation of D2R regulate synaptic efficacy onto PCs, their deletion or overexpression in PCs bidirectionally controls preference for social novelty without affecting motor functions.Altogether, these findings demonstrate novel D2R's roles in PC function and causally link cerebellar D2R levels of expression to social behaviors.

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Role of VTA dopamine neurons and neuroligin 3 in sociability traits related to nonfamiliar conspecific interaction

Cited by 143 publications

References 59 publications

Dopamine neurons of the VTA encode active conspecific interaction and promote social learning through social reward prediction error

Dopamine neurons of the VTA encode active conspecific interaction and promote social learning through social reward prediction error

The microbial metabolitep-Cresol induces autistic-like behaviors in mice by remodeling the gut microbiota

Cerebellar dopamine D2 receptors regulate preference for social novelty

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