UC Santa Barbara

Complex behaviors are assembled from simpler movements executed in sequence. However, how each component is controlled and how their combination is coordinated is not well understood. Here, we used fly grooming as an advantageous system to investigate two fundamental questions of motor control in sequential behavior.1) How are different actions coordinated within a sequence? Descending neurons, which connect the brain to the nerve cord, are a key bottleneck in the sensorimotor circuits and are therefore idea to address this question. For anterior grooming behavior in fly, we find that its subroutines, head sweeps and leg rubs, can be initiated separately, or as a set, by different descending neurons. Moreover, through genetic manipulation, behavioral assays, and connectomic analysis, we show that both the circuits in the brain and ventral nerve cord participate in coordinating the alternation of these two movements. We propose that the existence of redundant regulation strategies can provide backup plan for an important behavior. It ensures the behavior can be executed the best way under different scenarios and ensure the sequence to be executed without confusion. 2) How is each action coordinated? Flies rub their legs in response to the light touch which is location-dependent: the stimulated leg becomes the target. Depending on the segment, leg rubbing involves either contralateral legs or the neighboring ipsilateral, intersegmental legs. Here, we are interested in how sensory inputs from different body regions are processed to generate proper motor outputs. We identified a class of segmentally repeated command-like interneurons whose activation exhibits segment-specific leg rubbing responses. We uncovered a local sensorimotor circuit present in all segments that we propose reinforces the selection of the target leg. We also found segmental differences in the pre-motor wring that explains which leg are recruited for leg rubbings. These anatomical and behavioral results demonstrate how neuron wiring coordinates the segmentally different leg rubbing in grooming. In conclusion, our studies on fly grooming shed light on the neural circuits and coordination rules underlying this complex behavior, offering valuable insights into broader principles of motor control.