Behavioural choice emerges from nonlinear all-to-all interactions between drives

Under the right conditions any drive can overcome nearly any other, yet studies of behavioural selection predominantly focus on only one, or occasionally two behaviours. We present an experimental and computational framework that captures and explains the resolution of conflicts between several competing motivations. We characterize neurons that integrate information from all rival drives to generate an aggregate signal that urges male Drosophila to transition out of mating. Experimental investigation of these Drive Integrating Neurons (DINs) revealed time-varying, supralinear interactions among competing drives that stimulate the DINs and induce a change in behaviour. Extending these findings to model the interactions between all of an animals motivations led to the surprising prediction that, under many conditions, all-to-all interactions actually buffer the dominant drive against challengers. We experimentally validated this prediction, showing that weak drives for a variety of tertiary goals can have a profound stabilizing effect on the ongoing behaviour. These results emerge only if non-linear integration of other motivations occurs for each of an animals drives, suggesting the potential universality of this mechanism. Our findings emphasize the interconnectedness of motivational systems and the consequent importance of considering the full motivational state of an animal to understand its behaviour.