These studies have demonstrated that artificial activation of DN pairs is sufficient to drive complex behaviors including escape ( Lima and Miesenböck, 2005) (giant fiber neurons, 'GF'), antennal grooming ( Hampel et al., 2015)(antennal descending neurons, 'aDN'), backward walking ( Bidaye et al., 2014) (moonwalker descending neurons, 'MDN'), forward walking ( Bidaye et al., 2020) (DNp09), and landing ( Ache et al., 2019a) (DNp10 and DNp07). Until now, investigations of Drosophila have focused on individual or small sets of DNs. Thus, by building upon foundational work in other insects ( Heinrich, 2002 Kien, 1990 Böhm and Schildberger, 1992), studies in Drosophila can ultimately reveal how identified DNs work collectively to regulate complex behaviors. The functional properties of DNs can be understood within a circuit context using emerging connectomics datasets ( Zheng et al., 2018 Phelps et al., 2021). Sparse sets of these DNs can be experimentally targeted using transgenic driver lines ( Namiki et al., 2018) for functional recordings ( von Reyn et al., 2014 Schnell et al., 2017 Chen et al., 2018 Ache et al., 2019b Namiki et al., 2022) or physiological perturbations ( Cande, 2018 Zacarias et al., 2018 Ache et al., 2019a Namiki et al., 2022 Guo et al., 2022). Drosophila are thought to have between ~350 ( Namiki et al., 2018) and ~500 ( Hsu and Bhandawat, 2016) pairs of DNs. Flies are genetically-tractable, have a rich behavioral repertoire, and have a numerically small and compact nervous system ( Olsen and Wilson, 2008). The fruit fly, Drosophila melanogaster, is an excellent model for investigating how DNs regulate behavior. However, how the larger population of DNs coordinate their activities remains unknown. For some DNs, links between firing rate and behavioral features like walking speed have also been established ( Böhm and Schildberger, 1992). Through electrophysiological recordings in large insects, the activities of individual DNs have been linked to behaviors like walking and stridulation ( Heinrich, 2002). The information carried by individual DNs has long been a topic of interest ( Heinrich, 2002 Kien, 1990 Böhm and Schildberger, 1992). Because DNs make up only about 1% of brain neurons, DN population activity represents a critical information bottleneck: high-dimensional brain dynamics must be compressed into low-dimensional commands that efficiently interface with and are read out by motor circuits. There, DN axons impinge upon local circuits including central pattern generators (CPGs) that transform DN directives into specific limb or body part movements ( Bouvier et al., 2015 Capelli et al., 2017 Caggiano et al., 2018 Orger et al., 2008). To then drive behaviors, the brain conveys these decisions to motor circuits via a population of descending neurons (DNs) projecting to the spinal cord of vertebrates or ventral nerve cord (VNC) of invertebrates. For example, neurons or small networks may compete in a winner-take-all manner to select the next most appropriate motor action ( Cisek and Kalaska, 2010). The richness of animal behaviors depends on the coordinated actions of many individual neurons within a population. These results set the stage for a comprehensive, population-level understanding of how the brain’s descending signals regulate complex motor actions. Lastly, we illustrate how one can identify individual neurons from DN population recordings by using their spatial, functional, and morphological properties. Although odor context does not determine which behavior-encoding DNs are recruited, a few DNs encode odors rather than behaviors. A large fraction of walk-encoding DNs encode turning and far fewer weakly encode speed. We found that the largest fraction of recorded DNs encode walking while fewer are active during head grooming and resting. We evaluated these possibilities by recording populations of nearly 100 DNs in individual tethered flies while they generated limb-dependent behaviors, including walking and grooming. For example, they may modulate core behavioral commands or comprise parallel pathways that are engaged depending on sensory context. However, what additional role the larger population of DNs plays during natural behaviors remains largely unknown. Activating only a few DNs is known to be sufficient to drive complex behaviors like walking and grooming. In the fly, Drosophila melanogaster, this is coordinated by a population of ~ 1100 descending neurons (DNs). Deciphering how the brain regulates motor circuits to control complex behaviors is an important, long-standing challenge in neuroscience.
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