Walking strides direct rapid and flexible recruitment of visual circuits for course control in Drosophila

Flexible mapping between activity in sensory systems and movement parameters is a hallmark of motor control. This flexibility depends on the continuous comparison of short-term postural dynamics and the longer-term goals of an animal, thereby necessitating neural mechanisms that can operate across multiple timescales. To understand how such body-brain interactions emerge across timescales to control movement, we performed whole-cell patch recordings from visual neurons involved in course control in Drosophila. We show that the activity of leg mechanosensory cells, propagating via specific ascending neurons, is critical for stride-by-stride steering adjustments driven by the visual circuit, and, at longer timescales, it provides information about the moving body’s state to flexibly recruit the visual circuit for course control. Thus, our findings demonstrate the presence of an elegant stride-based mechanism operating at multiple timescales for context-dependent course control. We propose that this mechanism functions as a general basis for the adaptive control of locomotion. •HS cells receive stride-coupled signals via ascending neurons•The stride-coupled signals reflect an internal motor context•Motor context modulates HS cells at multiple timescales•HS cells drive rapid steering depending on motor context Fujiwara et al. show that HS cells, self-motion sensitive neurons in Drosophila, are modulated at different timescales by walking strides. The modulation recruits HS cells to adjust heading only during fast walking. This study provides a mechanistic link between body state and brain activity for the flexible control of locomotion.