Abstract
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, ~ 200 ms/movement), flies clean with periodic leg sweeps and rubs. More surprisingly, transitions between bouts of head sweeping and leg rubbing are also periodic on a longer time scale (0.3-0.6 Hz, ~2 s/bout). 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 rhythms at the two time scales increase at the same rate, indicating that the nested CPGs may be linked. This relationship holds when sensory drive is held constant using optogenetic activation, but oscillations can decouple in spontaneously grooming flies, showing that alternative control modes are possible. Loss of sensory feedback does not disrupt periodicity but slow down the longer time scale alternation. Nested CPGs simplify the generation of complex but repetitive behaviors, and identifying them in Drosophila grooming presents an opportunity to map the neural circuits that constitute them.
Highlights
Animals combine simpler movements into complex routines, forming behaviors with organization across multiple time scales
When flies are covered in dust, they initially groom anterior body parts using their front legs (Seeds et al, 2014). They alternate between bouts of head sweeps, where the legs move synchronously, and bouts of leg rubbing, where the legs move in opposition to each other, scraping the dust off
We first count individual leg movements from raw videos as they are processed for our Automatic Behavior Recognition System (ABRS) pipeline and compute their frequencies
Summary
Animals combine simpler movements into complex routines, forming behaviors with organization across multiple time scales. We wondered how a complex behavior can be assembled from simpler movements in such a harmonious manner. Central pattern generators (CPGs) are neural circuits that produce rhythmic motor outputs in response to a trigger without requiring ongoing descending drive or patterned sensory inputs; CPGs control short stereotypic actions in cat walking, crayfish swimming, locust flight, leech heartbeat, and the stomatogastric and pyloric rhythms of crustaceans (reviewed in Berkowitz, 2019; Harris-Warrick and Ramirez, 2017 ; Grillner, 2006; Marder and Calabrese, 1996; Mulloney and Smarandache, 2010; Selverston, 2010). CPGs may contribute to control of more complex behaviors
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