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 coordinated 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, including walking and grooming. 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 using 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 actions.

Fine-grained descending control of steering in walkingDrosophila

“…Our results support a model where the speed and direction of locomotion are each influenced by the activity of multiple DNs, with some DNs contributing to both 27–30, 32, 46, 54 . Both parameters are also under feedback control, as sensory reafference continuously informs the brain about the body’s instantaneous forward velocity 70–72 and heading 73 .…”

A visual efference copy-based navigation algorithm inDrosophilafor complex visual environments

“…When these features enter the central brain, they are integrated across a large visual field by converging either to a small brain region or to a single cell (Mauss et al, 2015; Wu et al, 2016). These features are subsequently relayed to other central brain regions or descending neural circuits, which ultimately control action (Aymanns et al, 2022; Namiki et al, 2018). With recent advances in understanding the structural and functional principles of its visuomotor circuits, Drosophila presents a unique opportunity to reverse-engineer the entire visuomotor processes.…”

Neural mechanisms to incorporate visual counterevidence in self motion estimation

“…Unfortunately, the circuitry that translates the activity of LPTCs and other lobula neurons into the turning commands remains poorly understood. Recent functional studies have begun to uncover descending neurons that are involved in stimulus-driven turning, such as DNa02 (Aymanns et al, 2022; Rayshubskiy et al, 2020). It is of future interest to identify neurons that link LPTCs to these descending neurons, and look for where the signature of suppression by stationary patterns emerges.…”