Dopaminergic mechanisms of dynamical social specialization | Nature

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Subjects

- Dynamical systems

- Learning algorithms

- Neural circuits

- Reward

- Social behaviour

Abstract

Social organization and division of labour are fundamental to animal societies1,2,3, yet how these structures emerge from individual interactions and are shaped by neuromodulation remains unclear. Here, using behavioural tracking in a semi-natural environment, neural recordings and computational models that integrate reinforcement learning and social condition, we show that triads of isogenic mice develop specialized roles spontaneously while solving a foraging task under social constraints. Notably, despite minor intra-sex differences in behaviour when mice were tested alone, male triads formed stable worker–scrounger relationships driven by competition, whereas female triads adopted uniform, cooperative strategies. These sex-divergent roles were shaped by dopaminergic activity in the ventral tegmental area. Model analysis revealed how intra-sex and inter-sex parameter differences in resource exploitation, combined with contingent social interactions, drive behavioural specialization and division of labour. Most notably, it highlighted how contingency, amplified by competition, magnifies individual differences and shapes social profiles. The plastic, adaptive nature of social organization was apparent when sex mixing or reintroducing experienced individuals into naive groups reshaped role distribution. Furthermore, dopaminergic manipulations confirmed this plasticity, reshaping roles and altering group structure. Our findings support a multi-scale feedback loop whereby social context shapes neural states, which in turn reinforce behavioural specialization and stabilize social structures.

Main

Social animals interact and coordinate their behaviours to form social organizations—structured patterns of relationships and interactions that stabilize into collective forms (for example, division of labour and norms) and specialized roles3,4,5,6,7. A key challenge in behavioural science is deciphering how individual differences in behaviour emerge, how they contribute to collective actions and how they are linked to neural activity. While the broad effects of social organization on individual behaviour and specialization are well documented8,9,10,11,12, the underlying cognitive and neurophysiological mechanisms remain largely unexplored, mainly because of the difficulty of studying such mechanisms in controlled, artificial social settings that also allow neurobiological investigation.

In social groups, the production of and access to shared resources drive strategies such as competition or cooperation2,8,13. The producer–scrounger game illustrates this dynamic: some individuals produce resources, others exploit them1,2,14,15. Thus, foraging strategies span from independent food acquisition to exploiting others’ efforts, balancing effort, risk and reward under ecological and social constraints13. Evolutionary game theory16 predicts stable equilibria between such strategies, but typically assumes that behaviours are predetermined and stable17, overlooking the internal mechanisms that guide an individual’s behaviour, including the neural and cognitive processes that grant adaptative, learning-based flexible strategies17,18,19. Central to this adaptability is dopaminergic signalling, which reinforces rewarded actions by signalling when reward is larger than expected20,21,22,23, including social reward24,25. A second key process is the exploration–exploitation trade-off26,27,28,29, whereby individuals must choose between exploiting known options and exploring alternatives, a process in which dopamine has also been implicated30,31,32,33,34,35.

Here we hypothesize that social foraging strategies, including producer–scrounger dynamics, emerge flexibly through socially constrained reinforcement learning. In particular, we suggest that dopaminergic signalling shapes variability in learning and decision policies, thereby contributing to behavioural specialization. As social organizations forms, individuals adjust actions on the basis of expected payoffs, which in turn modify neural activity and learning rules, ultimately stabilizing social roles. Recent advances in continuous animal tracking and behaviour quantification in semi-naturalistic settings36,37,38,39,40 enable detailed measurements of how individuals interact and adapt their strategies over time. Using these approaches, we examined how foraging specialization emerges in small groups (n = 3) of isogenic mice housed in a controlled semi-natural environment.

Two foraging strategies in lone mice

We first assessed mice foraging behaviour and underlying neural mechanisms in a lone context. Female or male mice (n = 62) were placed alone in a 50 cm × 50 cm multi-compartment environment and tracked continuously for 5 days and 4 nights using the Live Mouse Tracker system36. This setup includes a lever on one side and a food dispenser with a beam