Descending neuron population dynamics during odor-evoked and spontaneous limb-dependent behaviors

Abstract

Deciphering how the brain regulates motor circuits to control complex behaviors is an important, long-standing challenge in neuroscience. In the fly, Drosophila melanogaster, this is accomplished by a population of ∼ 1100 descending neurons (DNs). Activating only a few DNs is known to be sufficient to drive complex behaviors like walking and grooming. However, what additional role the larger population of DNs plays during natural behaviors remains largely unknown. For example, they may modulate core behavioral commands, or comprise parallel pathways that are engaged depending on sensory context. We evaluated these possibilities by recording populations of nearly 100 DNs in individual tethered flies while they generated limb-dependent behaviors. We found that the largest fraction of recorded DNs encode walking while fewer are active during head grooming and resting. A large fraction of walk-encoding DNs encode turning and far fewer weakly encode speed. Although odor context does not determine which behavior-encoding DNs are recruited, a few DNs encode odors rather than behaviors. Lastly, we illustrate how one can identify individual neurons from DN population recordings by analyzing their spatial, functional, and morphological properties. These results set the stage for a comprehensive, population-level understanding of how the brain’s descending signals regulate complex motor behaviors.

Tools for connectomic reconstruction and analysis of a femaleDrosophilaventral nerve cord

“…The FANC connectome will have many uses beyond the study of limb motor control. For example, it will enable the identification and analysis of neural circuits for descending modulation (Aymanns et al, 2022; Namiki et al, 2018), ascending communication with the brain (Chen et al, 2022), and sensory organs distributed across the fly limbs, thorax, and abdomen (Tuthill and Wilson, 2016). By creating a bridge between the VNC connectome and the body, the MN projectome will facilitate development and analysis of neuromechanical models for flexible motor control (Lobato-Rios et al, 2022).…”