Abstract
When placed on a temperature gradient, a Drosophila larva navigates away from excessive cold or heat by regulating the size, frequency, and direction of reorientation maneuvers between successive periods of forward movement. Forward movement is driven by peristalsis waves that travel from tail to head. During each reorientation maneuver, the larva pauses and sweeps its head from side to side until it picks a new direction for forward movement. Here, we characterized the motor programs that underlie the initiation, execution, and completion of reorientation maneuvers by measuring body segment dynamics of freely moving larvae with fluorescent muscle fibers as they were exposed to temporal changes in temperature. We find that reorientation maneuvers are characterized by highly stereotyped spatiotemporal patterns of segment dynamics. Reorientation maneuvers are initiated with head sweeping movement driven by asymmetric contraction of a portion of anterior body segments. The larva attains a new direction for forward movement after head sweeping movement by using peristalsis waves that gradually push posterior body segments out of alignment with the tail (i.e., the previous direction of forward movement) into alignment with the head. Thus, reorientation maneuvers during thermotaxis are carried out by two alternating motor programs: (1) peristalsis for driving forward movement and (2) asymmetric contraction of anterior body segments for driving head sweeping movement.
Highlights
Systems neuroscience strives to connect animal behavior to the structure and dynamics of the nervous system
Forward movement of the Drosophila larva, as in other Diptera species, is driven by waves of peristalsis that travel from tail to head [11]
We used the direct visualization of segment dynamics with highresolution fluorescence microscopy to characterize the motor programs that drive thermotaxis in transgenic Drosophila larvae with fluorescently labeled muscle fibers
Summary
Systems neuroscience strives to connect animal behavior to the structure and dynamics of the nervous system. By studying brain and behavior in the Drosophila larva, a genetically tractable model organism with a small nervous system and simple body plan, it might be possible to characterize the pathways that encode complex behaviors all the way from sensory input to motor output. To reach this goal, we must develop tools to interrogate all layers of neuronal and muscle dynamics that occur during behavior. A larva’s crawling trajectory can be characterized as a sequence of periods of persistent forward movement (runs) that are interrupted at random by reorientation maneuvers. The larva biases the size, frequency, and direction of these reorientation maneuvers to enhance the likelihood that its overall trajectory trends towards favorable temperatures [4]
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