The motor pattern of rolling escape locomotion inDrosophilalarvae

Summary When undisturbed, Drosophila larvae move forward through their environment with sweeping waves of caudal to rostral muscle contraction [1, 2]. In stark contrast, nociceptive sensory stimuli (such as attacks by parasitoid wasps) trigger the larvae to roll across the substrate by corkscrewing around the long body axis [3, 4]. While studies have described the motor pattern of larval crawling [1, 2], the motor pattern of larval rolling escape locomotion remains unknown. Here, we have determined this pattern. To do so, we developed a high speed confocal time-lapse imaging preparation that allowed us to trigger rolling with optogenetics while simultaneously imaging a genetically encoded calcium sensor that was expressed in the muscles. Of the 30 muscles present in each larval abdominal hemisegment we find that only 11 muscles are consistently and specifically activated across segments during rolling. 8 additional muscles are more sparsely activated. Importantly, the sequential pattern of muscle recruitment during rolling is completely distinct from that of forward or reverse crawling. We discover that a roll involves a wave of muscle activation that propagates around the larval circumference (in the transverse plane of each segment) and involves four coactive muscle groups. A pattern of activation progresses from coactive ventral muscle groups to dorsal groups and then spreads across the midline to the contralateral dorsal muscle groups which then progresses back to the ventral groups. Finally, the direction of a roll (either clockwise or counterclockwise around the body) is determined by the clockwise or counterclockwise order of muscle group activation around the transverse plane.