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Dopaminergic mechanisms of dynamical social specialization in mouse microsocieties

Solie, C.; Nicolson, A.; Justo, R.; Layadi, Y.; Morin, B.; Batifol, C.; Reynolds, L. M.; le Borgne, T.; Fayad, S. L.; Gulmez, A.; Allegret--vautrot, J.; De Chaumont, F.; Viollet, C.; Didienne, S.; Debray, N.; Hardelin, J.-P.; Girard, B.; Mourot, A.; Naude, J.; Fabio, M.; Delord, B.; Faure, P.

2025-02-11 neuroscience
10.1101/2025.02.10.637303 bioRxiv
Show abstract

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.

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