Neural circuits for peristaltic wave propagation in crawling Drosophila larvae: analysis and modeling

Abstract

Drosophila larvae crawl by peristaltic waves of muscle contractions, which propagate along the animal body and involve the simultaneous contraction of the left and right side of each segment. Coordinated propagation of contraction does not require sensory input, suggesting that movement is generated by a central pattern generator (CPG). We characterized crawling behavior of newly hatched Drosophila larvae by quantifying timing and duration of segmental boundary contractions. We developed a CPG network model that recapitulates these patterns based on segmentally repeated units of excitatory and inhibitory (EI) neuronal populations coupled with immediate neighboring segments. A single network with symmetric coupling between neighboring segments succeeded in generating both forward and backward propagation of activity. The CPG network was robust to changes in amplitude and variability of connectivity strength. Introducing sensory feedback via "stretch-sensitive" neurons improved wave propagation properties such as speed of propagation and segmental contraction duration as observed experimentally. Sensory feedback also restored propagating activity patterns when an inappropriately tuned CPG network failed to generate waves. Finally, in a two-sided CPG model we demonstrated that two types of connectivity could synchronize the activity of two independent networks: connections from excitatory neurons on one side to excitatory contralateral neurons (E to E), and connections from inhibitory neurons on one side to excitatory contralateral neurons (I to E). To our knowledge, such I to E connectivity has not yet been found in any experimental system; however, it provides the most robust mechanism to synchronize activity between contralateral CPGs in our model. Our model provides a general framework for studying the conditions under which a single locally coupled network generates bilaterally synchronized and longitudinally propagating waves in either direction.