Aylin Gulmez

Social organization and division of labour are fundamental to animal societies^1,2,3, 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.

The mechanisms underlying social organization in mice have predominantly been studied in male colonies, where sociability predicts higher rank and high-ranked individuals show greater anxiety. Here, we demonstrate that groups of isogenic female mice also form stable social hierarchies. Our data indicate that females destined for high rank already exhibit greater sociability and possibly higher anxiety before group formation, and these traits remain consistent afterwards. We further investigated the influence of sex by creating mixed-sex colonies, which revealed a similar hierarchical structure, with both males and females having equal chances of becoming high- or low-ranked. We previously found reduced dopamine neuron activity in high-ranked males; in contrast, high-ranked females show the opposite pattern. Furthermore, while glucocorticoid receptor signaling in dopaminoceptive neurons restricts high rank in males, this effect is absent in females. Overall, these results highlight sex-specific mechanisms that contribute to social ranking and related behavioral traits in mice.

Summary: Social organization and division of labor are fundamental to animal societies, but how do these structures emerge from individual interactions, and what role does neuromodulation play in shaping them? Using behavioral tracking in a semi-natural environment, neural recordings, and computational models integrating reinforcement and social learning, we show that groups of three isogenic mice spontaneously develop specialized roles while solving a foraging task requiring individual decisions under social constraints. Moreover, these roles are shaped by dopaminergic activity in the ventral tegmental area. Strikingly, despite minor sex-differences in behavior when mice were tested alone, male triads formed stable worker-scrounger relationships driven by competition, whereas female triads adopted uniform, cooperative strategies. Model analysis revealed how intra- and inter-sex parameter differences in resource exploitation, combined with contingent and dynamic social interactions, drive behavioral specialization and labor division. Most notably, it highlighted how contingency, amplified by competition, magnifies individual differences and shapes social profiles. The plastic, adaptive nature of social organization within triads was confirmed by manipulating dopaminergic cell activity, which reshaped social roles and altered group structure. Our findings support a feedback loop where social context shapes neural states, which in turn reinforce behavioral specialization and stabilize social structures.

Flexible decision-making requires not only updating values, but redefining which features constitute an action in a given context. We recorded nucleus accumbens (NAc) dopamine release while mice navigated a three-target intracranial self-stimulation foraging task in which outcomes were evaluated under three distinct reward delivery rules. Despite a constant motor repertoire, dopamine transients reorganized across contingencies and generalized linear models revealed context-dependent dopamine signal reflecting action direction, recent outcome-history, or target identity. Reinforcement-learning model comparison showed that these signatures are best explained by distinct reward prediction errors (RPEs) defined over different state–action representations, rather than a single fixed model-free scheme. A single deep reinforcement-learning agent trained by temporal-difference learning, recapitulated both the rule-specific policies and the corresponding dopamine signature. These results identify NAc dopamine as a dynamic readout of representation learning, remapping prediction errors onto the task features that define successful action as contingencies change.