Social interactions impact on the dopaminergic system and drive individuality

Torquet, Nicolas; Marti, Fabio; Campart, Cynthia; Tolu, Stefania; Nguyen, Claire; Oberto, Virginie; Benallaoua, M.; Naudé, Jérémie; Didienne, Steve; Debray, N.; Jezequel, Soizic; Gouestre, L. Le; Hannesse, Bernadette; Mariani, Jean; Mourot, Alexandre; Fauré, Philippe

doi:10.1038/s41467-018-05526-5

Cited by 68 publications

(78 citation statements)

References 53 publications

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“…Similar experiments with a D1 receptor antagonist facilitated or did not modify social dominance in mice and monkeys (Yamaguchi et al 2017b) whereas local injection into the NAcc of an agonist increased dominance in rats (Van der Kooij 2018). Interestingly, changes in VTA dopamine cells activity is observed during the emergence of behavioral categories occurring within groups of dozens of mice living in complex semi-naturalistic environments (Torquet et al, 2018). It will be interesting to study social ranking between these categories using precedence test such as the tube test.…”

Section: Discussionmentioning

confidence: 99%

Dopamine and stress signalling interplay patterns social organization in mice

Battivelli

Vernochet

Nguyen

et al. 2019

Preprint

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The rules leading to the emergence of a social organization and the role of social ranking on normal and pathological behaviors remain elusive. Here we show that groups of four genetically identical male mice rapidly form enduring social ranking determined by precedence test and the sharing of beneficial resources. Highest ranked individuals are more anxious, more social and display increased spatial working memory. Whereas differences in anxiety between individuals appear after rank attainment, the higher sociability of top-ranked mice preexist. These behavioral differences correlate with physiological change. The highest ranked mice display indeed lower bursting activity of VTA dopamine neurons. The same animals are less responsive to preclinical models of stress behavioral disorders involving changes of dopamine system. They display lower locomotor sensitization to cocaine and are more resilient to repeated social defeat. The ablation of stress-elicited glucocorticoid receptor gene in dopaminoceptive neurons that affects the same pathological models, upwards the ranking status of mutant individuals. Altogether, these results support a role for social ranking in patterning interindividual VTA dopaminergic activity, behavioral responses and susceptibility to stressrelated psychopathologies.

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Section: Discussionmentioning

confidence: 99%

Dopamine and stress signalling interplay patterns social organization in mice

Battivelli

Vernochet

Nguyen

et al. 2019

Preprint

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“…Another hypothesis for the heterogeneity we observed in our animal model could be of epigenetic and/or environmental origin. It has been shown for example that phenotypic variability can emerge from variations in epigenetic regulation (59,(66)(67)(68).…”

Section: Discussionmentioning

confidence: 99%

“…As for OCD patients, we attempted to determine a similar heterogeneity in the KO mice. Indeed, some innovative studies have found evidence for inter-individual variability of cognitive traits in animal models (58,59), pointing out it is a necessary consideration for animal studies. To do so, we performed a two-step cluster analysis which identified two clusters within the KO mice with a silhouette measure of 0.6, indicating a good solution.…”

Section: Distinct Subgroups Of Ocd Patients and Ko Mice Exhibit A Behmentioning

confidence: 99%

A cross-species assessment of behavioral flexibility in compulsive disorders

Benzina

N’Diaye

Pélissolo

et al. 2019

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Short running title: Flexibility and compulsive behaviors in mice and menABSTRACT Background: Compulsive behaviors, one of the core symptoms of Obsessive-Compulsive Disorder (OCD), are defined as repetitive behaviors performed through rigid rituals. The lack of behavioral flexibility has been as being one of the primary causes of compulsions, but studies exploring this dimension have shown inconsistencies in different tasks performed in human and animal models of compulsive behavior. The aim of this study was so to assess the involvement of behavioral flexibility in compulsion, with a similar approach across different species sharing a common symptom of compulsivity.Methods: 40 OCD patients, 40 healthy individually matched control subjects, 26 C57BL/6J Sapap3 KO mice and 26 matched wildtype littermates were included in this study. A similar reversal learning task was designed to assess behavioral flexibility in parallel in these two species.Results: When considered as homogeneous groups, OCD patients and KO mice expressing compulsive behaviors did not significantly differ from their controls regarding behavioral flexibility. When clinical subtypes were considered, only patients exhibiting checking compulsions were impaired with more trials needed to reach the reversal criterion. In KO mice, a similarly impaired subgroup was identified. For both species, this impairment did not result in a greater perseveration after reversal, but in a greater lability in their responses in the reversal condition. Moreover, this impairment did not correlate with the severity of compulsive behaviors. Conclusions:In our cross-species study, we found no consistent link between compulsive behaviors and a lack of behavioral flexibility. However, we showed in both species that the compulsive group was heterogeneous in term of performance in our reversal learning task. Among the compulsive subjects, we identified a subgroup with impaired performance not due to perseverative and rigid behaviors as commonly hypothesized, but rather to an increase in response lability.

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“…Thus, our current results suggest that the strength of intrinsic hippocampal-cortical connectivity is a potential candidate for the modulation of goal-directed behavior in social groups. Social relationships can shape individual behavior and affect decision-making [38]. Although dominance hierarchy emerges from recurrent social interactions, it causally results from the synaptic efficacy of excitatory transmission in the mPFC [9].…”

Section: Discussionmentioning

confidence: 99%

Cortical dynamics underlying social behavior in dominance hierarchy and spatial navigation

Lara-Vásquez

Espinosa

Morales

et al. 2020

Preprint

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Rodents establish dominance hierarchy as a social ranking system in which one subject acts as dominant over all the other subordinate individuals. Dominance hierarchy regulates food access and mating opportunities, but little is known of its significance in collective behavior, for instance during navigation for foraging or migration. Here, we implemented a simplified goal-directed spatial navigation task in mice and found that the social context exerts significant influence on individual decision-making, even when efficient navigation rules leading to reward had been previously learned. Thus, decision-making and consequent task performance were strongly dependent on contingent social interactions arising during collective navigation, yet their influence on individual behavior was outlined by dominance hierarchy. Dominant animals did not behave as leaders during navigation; conversely, they were most sensitive to social context. Social ranking in turn was reflected in the neural activity and connectivity patterns of the prefrontal cortex and hippocampus, both in anesthetized and behaving mice. These results suggest that the interplay between contingent social interactions and dominance hierarchy can regulate behavioral performance, supported by the intrinsic matrix of coordinated activity in the hippocampal-prefrontal circuit. Significance StatementDecision-making is shaped by intrinsic features, such as memory-stored information, and external influences, such as social interactions, yet their interplay is not well understood. We studied decision-making during collective behavior and found that instead of prioritizing memory-based pertinent information, mice shifted their individual decisions according to contingent social interactions arising in the social context. Conversely, constitutive social interactions, such as dominance hierarchy, were relevant to outline the effect of the social environment on individual behavior. Our results suggest that intrinsic hippocampal-cortical activity and connectivity patterns define social interactions. Hence, intrinsic cortical dynamics underlie behavioral performance during social decision-making. Main text IntroductionSocial behavior is an adaptive response that has evolved to improve ecological fitness in many species [1]. Mammalian social behaviors occur in the context of extended groups; however, in laboratory settings, interactions such as fighting, chasing, courtship, and grooming, are typically investigated in pairs of individuals [2,3]. This approach of studying dyads, and treating the results as prototypical social behavior, has significant limitations because animal groups commonly rely on more complicated social structures. Indeed, recent experiments tracking mice in ethologically relevant environments have revealed strongly correlated social behaviors

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Social interactions impact on the dopaminergic system and drive individuality

Cited by 68 publications

References 53 publications

Dopamine and stress signalling interplay patterns social organization in mice

Dopamine and stress signalling interplay patterns social organization in mice

A cross-species assessment of behavioral flexibility in compulsive disorders

Cortical dynamics underlying social behavior in dominance hierarchy and spatial navigation

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