Correction: The manifold structure of limb coordination in walking Drosophila

DeAngelis, Brian D; Zavatone-Veth, Jacob A.; Clark, Damon A.

doi:10.7554/elife.65214

Cited by 5 publications

(3 citation statements)

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“…Our analysis identifies a relatively small number of strong candidate cell types controlling inter-leg coordination that should be the target of future experiments. However, we observed that the majority of these interconnections are cholinergic, in contrast with previous models which hypothesize that leg locomotor CPGs controlling individual legs are inter-coupled by inhibitory interconnections (DeAngelis et al, 2020; Grillner and Kozlov, 2021; Hiraoka, 2021). However, we propose that this contradiction can be resolved if excitatory interconnections target inhibitory pre-motor neurons (see Discussion and Figure 21B).…”

Section: Resultscontrasting

confidence: 99%

“…The morphology and connectivity of these sequential neurons strongly suggests that they coordinate legs across segments. However five out of five groups projecting posteriorly and three of five groups projecting anteriorly are cholinergic in contrast to previous predictions of inhibitory interconnections (DeAngelis et al, 2020;Grillner and Kozlov, 2021;Hiraoka, 2021).…”

Section: Inter-leg Coordination Is Not Purely Inhibitorycontrasting

confidence: 99%

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

Cheong

Eichler

Stuerner

et al. 2023

Preprint

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In most animals, a relatively small number of descending neurons (DNs) connect higher brain centers in the animal's head to motor neurons (MNs) in the nerve cord of the animal's body that effect movement of the limbs. To understand how brain signals generate behavior, it is critical to understand how these descending pathways are organized onto the body MNs. In the fly, Drosophila melanogaster, MNs controlling muscles in the leg, wing, and other motor systems reside in a ventral nerve cord (VNC), analogous to the mammalian spinal cord. In companion papers, we introduced a densely-reconstructed connectome of the Drosophila Male Adult Nerve Cord (MANC, Takemura et al., 2023), including cell type and developmental lineage annotation (Marin et al., 2023), which provides complete VNC connectivity at synaptic resolution. Here, we present a first look at the organization of the VNC networks connecting DNs to MNs based on this new connectome information. We proofread and curated all DNs and MNs to ensure accuracy and reliability, then systematically matched DN axon terminals and MN dendrites with light microscopy data to link their VNC morphology with their brain inputs or muscle targets. We report both broad organizational patterns of the entire network and fine-scale analysis of selected circuits of interest. We discover that direct DN-MN connections are infrequent and identify communities of intrinsic neurons linked to control of different motor systems, including putative ventral circuits for walking, dorsal circuits for flight steering and power generation, and intermediate circuits in the lower tectulum for coordinated action of wings and legs. Our analysis generates hypotheses for future functional experiments and, together with the MANC connectome, empowers others to investigate these and other circuits of the Drosophila ventral nerve cord in richer mechanistic detail.

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Section: Resultscontrasting

confidence: 99%

Section: Inter-leg Coordination Is Not Purely Inhibitorycontrasting

confidence: 99%

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

Cheong

Eichler

Stuerner

et al. 2023

Preprint

View full text Add to dashboard Cite

show abstract

“…Pivots were defined as time periods with high angular velocity (>2r/s) and low translational velocity (<5mm/s) after smoothing with 0.5s window. These pivot thresholds are set based on empirical observation as well as previous literature [75][76][77] indicating values for slow walking and high turning.…”

Section: Optogenetic Activation In Untethered Animalsmentioning

confidence: 99%

Neural circuit mechanisms underlying context-specific halting inDrosophila

Sapkal,

Mancini,

Kumar

et al. 2023

Preprint

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Walking is a complex motor program involving coordinated and distributed activity across the brain and the spinal cord. Halting appropriately at the correct time is a critical but often overlooked component of walking control. While recent studies have delineated specific genetically defined neuronal populations in the mouse brainstem that drive different types of halting1–3, the underlying neural circuit mechanisms responsible for overruling the competing walking-state neural activity to generate context-appropriate halting, remain unclear. Here, we elucidate two fundamental mechanisms by whichDrosophilaimplement context-appropriate halting. The first mechanism (“walk-OFF” mechanism) relies on GABAergic neurons that inhibit specific descending walking commands in the brain, while the second mechanism (“brake” mechanism) relies on excitatory cholinergic neurons in the nerve-cord that lead to an active arrest of stepping movements. Using connectome-informed models4–6and functional studies, we show that two neuronal types that deploy the “walk-OFF” mechanism inhibit distinct populations of walking-promotion neurons, leading to differential halting of forward-walking or steering. The “brake” neurons on the other hand, override all walking commands by simultaneously inhibiting descending walking promoting pathways and increasing the resistance at the leg-joints leading to an arrest of leg movements in the stance phase of walking. We characterized two ethologically relevant behavioral contexts in which the distinct halting mechanisms were used by the animal in a mutually exclusive manner: the “walk-OFF” pathway was engaged for halting during feeding, and the “brake” pathway was engaged for halting during grooming. Furthermore, this knowledge of the neural targets and mechanisms for halting, allowed us to use connectomics to predict novel halting pathways that could be relevant in other behavioral contexts.

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Neural circuit mechanisms underlying context-specific halting in Drosophila

Sapkal,

Mancini,

Kumar

et al. 2024

Nature

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Walking is a complex motor programme involving coordinated and distributed activity across the brain and the spinal cord. Halting appropriately at the correct time is a critical component of walking control. Despite progress in identifying neurons driving halting1–6, the underlying neural circuit mechanisms responsible for overruling the competing walking state remain unclear. Here, using connectome-informed models7–9 and functional studies, we explain two fundamental mechanisms by which Drosophila implement context-appropriate halting. The first mechanism (‘walk-OFF’) relies on GABAergic neurons that inhibit specific descending walking commands in the brain, whereas the second mechanism (‘brake’) relies on excitatory cholinergic neurons in the nerve cord that lead to an active arrest of stepping movements. We show that two neurons that deploy the walk-OFF mechanism inhibit distinct populations of walking-promotion neurons, leading to differential halting of forward walking or turning. The brake neurons, by constrast, override all walking commands by simultaneously inhibiting descending walking-promotion neurons and increasing the resistance at the leg joints. We characterized two behavioural contexts in which the distinct halting mechanisms were used by the animal in a mutually exclusive manner: the walk-OFF mechanism was engaged for halting during feeding and the brake mechanism was engaged for halting and stability during grooming.

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Correction: The manifold structure of limb coordination in walking Drosophila

Cited by 5 publications

References 0 publications

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

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

Neural circuit mechanisms underlying context-specific halting inDrosophila

Neural circuit mechanisms underlying context-specific halting in Drosophila

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