A neural circuit basis for context-modulation of individual locomotor behavior

Defying the cliche that biological variation arises from differences in nature or nurture, genetically identical animals reared in the same environment exhibit striking differences in their behaviors. Innate behaviors can be surprisingly flexible, for example by exhibiting context-dependence. The intersection of behavioral individuality and context-dependence is largely unexplored, particularly at the neural circuit level. Here, we show that individual flies’ tendencies to turn left or right (locomotor handedness) changes when ambient illumination changes. This change is itself a stable individual behavioral characteristic. Silencing output neurons of the central complex (a premotor area that mediates goal-directed navigation) blocks this change. These neurons respond to light with idiosyncratic changes to their baseline calcium levels, and idiosyncratic morphological variation in their presynaptic arbors correlates with idiosyncratic sensory-context-specific turn biases. These findings provide a circuit mechanism by which individual locomotor biases arise and are modulated by sensory context.