Descending networks transform command signals into population motor control

Abstract

To convert intentions into actions, movement instructions must pass from the brain to downstream motor circuits through descending neurons (DNs). These include small sets of command-like neurons that are sufficient to drive behaviours1—the circuit mechanisms for which remain unclear. Here we show that command-like DNs in Drosophila directly recruit networks of additional DNs to orchestrate behaviours that require the active control of numerous body parts. Specifically, we found that command-like DNs previously thought to drive behaviours alone2–4 in fact co-activate larger populations of DNs. Connectome analyses and experimental manipulations revealed that this functional recruitment can be explained by direct excitatory connections between command-like DNs and networks of interconnected DNs in the brain. Descending population recruitment is necessary for behavioural control: DNs with many downstream descending partners require network co-activation to drive complete behaviours and drive only simple stereotyped movements in their absence. These DN networks reside within behaviour-specific clusters that inhibit one another. These results support a mechanism for command-like descending control in which behaviours are generated through the recruitment of increasingly large DN networks that compose behaviours by combining multiple motor subroutines.

Comparative connectomics of the descending and ascending neurons of theDrosophilanervous system: stereotypy and sexual dimorphism

“…We have established a platform for systematic neuron typing based on light-level and cross- dataset identification, which we encourage the community to utilise for studying their specific circuits of interest. Early access to the proofread and annotated connectome data that we describe has already enabled and assisted a range of exciting work including studies of the circuit basis of locomotor behaviour and the organisational and functional logic of descending neurons (Braun et al, 2024; H. S. J. Cheong et al, 2024; Dallmann et al, 2024; Lee et al, 2024; Lesser et al, 2024; Sapkal et al, 2023; von Reyn et al, 2024 unpublished; Yang et al, 2023).…”

“…This extensive DN-DN interconnectivity in the brain suggests the possibility of coordinated action across DNs, an idea that has recently been investigated by combining our connectome data with elegant functional studies (Braun et al, 2024). Intriguingly, many of these DN-DN connections are axo-axonic; whether this can result in direct excitation or inhibition of the downstream neuron or rather gates the axonal output of this neuron is unclear although Braun et al (2024) were able to show that optogenetic activation of some DNs can propagate to others. The remaining DN output in the brain primarily targets central brain interneurons (45%), with functions likely including coordinating DN activity across the two sides of the brain.…”