Behavioral evidence for nested central pattern generator control of Drosophila grooming

Central pattern generators (CPGs) are neurons or neural circuits that produce periodic output without requiring patterned input. More complex behaviors can be assembled from simpler subroutines, and nested CPGs have been proposed to coordinate their repetitive elements, organizing control over different time-scales. Here, we use behavioral experiments to establish that Drosophila grooming may be controlled by nested CPGs. On a short time-scale (5-7 Hz), flies execute periodic leg sweeps and rubs. More surprisingly, transitions between bouts of head cleaning and leg rubbing are also periodic on a longer time-scale (0.3 - 0.6 Hz). We examine grooming at a range of temperatures to show that the frequencies of both oscillations increase – a hallmark of CPG control – and also that the two time-scales increase at the same rate, indicating that the nested CPGs may be linked. This relationship also holds when sensory drive is held constant using optogenetic activation, but the rhythms can decouple in spontaneously grooming flies, showing that alternative control modes are possible. Loss of sensory feedback does not disrupt periodicity but slows the longer time-scale alternation. Nested CPGs simplify generation of complex but repetitive behaviors, and identifying them in Drosophila grooming presents an opportunity to map the neural circuits that constitute them.