A suppression hierarchy among competing motor programs drives sequential grooming in Drosophila

Abstract

Motor sequences are formed through the serial execution of different movements, but how nervous systems implement this process remains largely unknown. We determined the organizational principles governing how dirty fruit flies groom their bodies with sequential movements. Using genetically targeted activation of neural subsets, we drove distinct motor programs that clean individual body parts. This enabled competition experiments revealing that the motor programs are organized into a suppression hierarchy; motor programs that occur first suppress those that occur later. Cleaning one body part reduces the sensory drive to its motor program, which relieves suppression of the next movement, allowing the grooming sequence to progress down the hierarchy. A model featuring independently evoked cleaning movements activated in parallel, but selected serially through hierarchical suppression, was successful in reproducing the grooming sequence. This provides the first example of an innate motor sequence implemented by the prevailing model for generating human action sequences.DOI: http://dx.doi.org/10.7554/eLife.02951.001

Targeted manipulation of neuronal activity in behaving adult flies

“…Scale bar, 100 μm. Images are published in the following references (Seeds et al 2014;Hampel et al 2015). (c) Thermogenetic activation of neurons within each pattern using dTrpA1 can elicit grooming of the head (left, R18C11-GAL4) or wing (right, R53A06-GAL4).…”

“…For example, higher temperatures may increase grooming behavior or reduce mating (Seeds et al 2014;Vaughan et al 2014). Similarly, optogenetic activation can introduce confounding behavioral artifacts.…”

“…The different systems used for warming or cooling flies include temperature-controlled rooms or chambers, water baths, heating blocks or pads, or peltier plates (Marella et al 2012;Mann et al 2013;Flood et al 2013;Seeds et al 2014;Sun et al 2014;Hampel et al 2015). Chambers that house the flies have been designed with features that facilitate rapid warming such as mesh floors, or heat-conducting floors that are in direct contact with a heating element (Seeds et al 2014;Harris et al 2015). Alternatively, the flies and/ or chambers can be pre-warmed prior to an experiment (Keleman et entire body to temperature induction that typically occurs over a time frame of seconds to minutes.…”

“…For example, a male fly will spend less time courting a female in a large chamber than in a small chamber wherein the male is always in proximity to the female (Ewing and Ewing 1984;Zawistowski and Richmond 1987;Griffith and Ejima 2009). Chambers with low ceilings restrict flies to the floor for studying non-flight behaviors such as locomotion or grooming (Seeds et al 2014;Triphan et al 2016). Of note, chamber heights that are too low restrict the performance of behaviors that involve a raised posture, such as copulation or aggression (Hotta and Benzer 1976;Simon and Dickinson 2010).…”

“…Although the behaviors of flies can be measured without directly observing their movements (Mendes et al 2013;Itskov et al 2014;Seeds et al 2014;Albin et al 2015;Egnor and Branson 2016), here we focus on video recording and annotating the movements of flies. Chambers should not only allow flies to perform the behavior of interest, but their design must also facilitate the recording of fly movements such that specific features of the movements can be annotated.…”