Fine-grained descending control of steering in walkingDrosophila

Abstract

Locomotion involves rhythmic limb movement patterns that originate in circuits outside the brain. Purposeful locomotion requires descending commands from the brain, but we do not understand how these commands are structured. Here we investigate this issue, focusing on the control of steering in walking Drosophila. First, we describe different limb "gestures" associated with different steering maneuvers. Next, we identify a set of descending neurons whose activity predicts steering. Focusing on two descending cell types downstream from distinct brain networks, we show that they evoke specific limb gestures: one lengthens strides on the outside of a turn, while the other attenuates strides on the inside of a turn. Notably, a single descending neuron can have opposite effects during different locomotor rhythm phases, and we identify networks positioned to implement this phase-specific gating. Together, our results show how purposeful locomotion emerges from brain cells that drive specific, coordinated modulations of low-level patterns.

Transforming descending input into behavior: The organization of premotor circuits in theDrosophilaMale Adult Nerve Cord connectome

“…However, while DNa02 descends into the VNC on the ipsilateral side, DNg13 crosses in the brain and innervates the contralateral hemisegments in the VNC (Figure 16A). In the published literature, DNg13 is suggested to be involved in reaching movements (Cande et al, 2018), but the following circuit observations are consistent with both types having a role in turning, which has been confirmed by a recent study (Yang et al, 2023).…”

Inhibitory control of locomotor statistics in walkingDrosophila

“…We next sought to develop a physiologically-inspired conceptual model of locomotor control that could account for the statistics we observed experimentally— in particular the shifts in statistics that occur between baseline walking and search behavior, and the changes in odor-evoked run length with baseline ground speed state. As our starting point, we considered that (1) multiple DNs contribute to both forward and angular velocity (Rayshubskiy et al 2020, Yang et al 2023, Braun et al 2023), (2) different units make different contributions to forward versus angular velocity (Rayshubskiy et al 2020, Yang et al 2023, Bresovec et al 2024, Aymanns et al, 2022), (3) bilateral activity correlates with forward velocity while activity differences between hemispheres correlate with angular velocity, both in some single neurons (Bidaye et al 2020, Yang et al 2023), and in population imaging (Bresovec et al 2024, Aymanns et al 2022), and (4) distinct sets of DNs promote stopping (Lee and Doe 2021, Sapkal et al 2023). Based on these considerations, we developed a simple model of locomotor control (Fig.…”

“…3C). Connectomic analysis suggests that different DNs promoting turning receive input from largely non-overlapping upstream neurons (Yang et al 2023). Therefore, each unit in our model receives an independent Gaussian noise input, μ i .…”

“…In fruit flies, roughly 350 to 500 pairs of descending neurons (DNs) carry motor signals from the brain to the ventral nerve cord, the insect equivalent of the spinal cord (Hsu and Bhandawat, 2016, Namiki et al, 2018, Cheong et al 2024). Individual DNs have been identified that generate forward walking, turning, or both, when activated (Cande et al 2018, Rayshubsky et al 2020, Bidaye et al 2020, Yang et al 2023). Other DNs promote stopping behavior (Cande et al 2018, Carreira-Rosasrio et al 2018, Lee and Doe, 2021, Sapkal et al 2023).…”

Social state gates vision using three circuit mechanisms inDrosophila

“…The proportions of input from aIPg and the LCs vary (Figures 1b, e, g). The vast majority of cell types that receive LC10 input are interneurons in the AOTu, which then connect to descending pathways that drive motor action (38,51,52). These interneurons therefore may control distinct facets of aggressive behavior.…”