Distributed control of motor circuits for backward walking inDrosophila

Abstract

How do descending inputs from the brain control leg motor circuits to change the way an animal walks? Conceptually, descending neurons are thought to function either as command-type neurons, in which a single type of descending neuron exerts a high-level control to elicit a coordinated change in motor output, or through a more distributed population coding mechanism, whereby a group of neurons, each with local effects, act in combination to elicit a global motor response. The Drosophila Moonwalker Descending Neurons (MDNs), which alter leg motor circuit dynamics so that the fly walks backwards, exemplify the command-type mechanism. Here, we identify several dozen MDN target neurons within the leg motor circuits, and show that two of them mediate distinct and highly-specific changes in leg muscle activity during backward walking: LIN156 neurons provide the hindleg power stroke during stance phase; LIN128 neurons lift the legs at the end of stance to initiate swing. Through these two effector neurons, MDN directly controls both the stance and swing phases of the backward stepping cycle. MDN exerts these changes only upon the hindlegs; the fore- and midlegs follow passively through ground contact. These findings suggest that command-type descending neurons can also operate through the distributed control of local motor circuits.

LiftPose3D, a deep learning-based approach for transforming 2D to 3D pose in laboratory animals

“…During walking, 2D tracking of the tarsal claws traced out stereotypical trajectories in the x-y plane (Figure 3D, top) [50] which corresponded to circular movements in the unmeasured x-z plane (Figure 3D, bottom). These predicted x-z cycles were of largest amplitude for the front, prothoracic legs, consistent with real kinematic measurements during forward walking[51].…”

“…Remarkably, we found that the network could predict physiologically realistic 3D poses in this new dataset using only ventral 2D poses ( Figure 3G and Video 8 ). During walking, 2D tracking of the tarsal claws traced out stereotypical trajectories in the x-y plane ( Figure 3H , top) [54] and circular movements in the unmeasured x-z plane ( Figure 3H , bottom) whose amplitudes were consistent with real kinematic measurements during forward walking [55].…”

A connectome of theDrosophilacentral complex reveals network motifs suitable for flexible navigation and context-dependent action selection

“…DNg and DNa01 are in circuits targeted only by the PFL3 neurons and not PFL2 neurons. PFL2 and PFL3 neurons also reach the moonwalker neuron MDN (Bidaye et al, 2014;Feng et al, 2020), which has a bilateral innervation pattern and is known to drive backward walking. This connection is almost exclusively contralateral (Figure 63-figure supplement 1A,B), a suggestion that the MDN could also be involved in asymmetric behaviors.…”

Behavioral evidence for nested central pattern generator control ofDrosophilagrooming

“…This high-level, overarching, CPG can control the alternations between leg rubs and sweeps that are themselves governed by faster, low-level CPGs. The idea that multiple CPGs coordinate movements is not new: CPGs may control each leg joint, regulating the interaction between flexor and extensor muscles, governing the way coxa-trochanter and femur-tibia joints are coordinated to produce forward or backward walking, or mediating interactions among limbs (Feng et al, 2020;Mantziaris, Bockemuhl, & Buschges, 2020). In the vertebrate spinal cord, inhibitory and excitatory commissural neurons can cause the CPGs controlling the legs to synchronize for a hopping gait or operate out-of-phase for walking (Kiehn, 2016).…”