The motor pattern of rolling escape locomotion in Drosophila larvae

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Abstract
When undisturbed, Drosophila larvae move forward through their environment with sweeping waves of caudal to rostral muscle contractions. In stark contrast, nociceptive sensory stimuli trigger the larvae to roll across the substrate by corkscrewing around the long body axis. Here, we have determined the detailed timing of muscle activation that generates the body rotation across abdominal segments. To do so, we developed a high-speed confocal time-lapse imaging preparation that allowed us to trigger rolling with nociceptor optogenetics while simultaneously imaging a genetically encoded calcium sensor expressed in the muscles. Of the 30 muscles present in each larval abdominal hemisegment, we found that only 11 muscles are consistently and specifically activated across segments during rolling. Eight 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. A roll involves a wave of muscle activation that propagates around the larval circumference (in the transverse plane of each segment) and involves four co-active muscle groups. A pattern of activation progresses from co-active ventral muscle groups to dorsal groups and then spreads across the midline to the contralateral dorsal muscle groups, then progresses back to the ventral groups. The direction of a roll is determined by the clockwise or counterclockwise order of muscle group activation around the transverse plane. Finally, an analysis of the connectivity of inputs to larval motor neurons revealed a ring-like network architecture that could support the sequence of activation of the rolling motor pattern.
Funding Information
  • National Institute of General Medical Sciences (5R01GM086458)
  • National Institute of General Medical Sciences (5R35GM148258)
  • Indiana University
  • Gill Institute for Neuroscience

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