Networks of descending neurons transform command-like signals into population-based behavioral control

Abstract

To transform 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 behaviors--the circuit mechanisms for which remain unclear. Here, we show that command-like DNs in Drosophila directly recruit networks of additional DNs to orchestrate flexible behaviors. Specifically, we found that optogenetic activation of command-like DNs previously thought to drive behaviors alone in fact co-activate larger populations of DNs. Connectome analysis revealed that this functional recruitment can be explained by direct excitatory connections between command-like DNs and networks of interconnected DNs in the brain. The size of downstream DN networks is predictive of whether descending population recruitment is necessary to generate a complete behavior: DNs with many downstream descending partners require network recruitment to drive flexible behaviors, while neurons with fewer partners can alone drive stereotyped behaviors and simple movements. Finally, DN networks reside within behavior-specific clusters that inhibit one another. These results support a mechanism for command-like descending control whereby a continuum of stereotyped to flexible behaviors are generated through the recruitment of increasingly large DN networks which likely construct a complete behavior by combining multiple motor subroutines.