A Connectome of the Male<i>Drosophila</i>Ventral Nerve Cord

Takemura, Shin-ya; Hayworth, Kenneth J.; Huang, Gary B.; Lǚ, Zhiyuan; Marin, Elizabeth C.; Preibisch, Stephan; Xu, Chengpei; Bogovic, John A.; Champion, Andrew; Cheong, Han S J; Costa, Marta; Eichler, Katharina; Katz, William T.; Knecht, Christopher J.; Li, Feng; Morris, Billy J.; Ordish, Christopher; Rivlin, Patricia K.; Schlegel, Philipp; Shinomiya, Kazunori; Stürner, Tomke; Zhao, Ting; Badalamente, Griffin; Bailey, Dennis A.; Brooks, Paul; Canino, Brandon S; Clements, Jody; Cook, Michael; Duclos, Octave; Dunne, Christopher R; Fairbanks, Kelli; Fang, Siqi; Finley, Samantha; Francis, Audrey; George, Reed A.; Gkantia, Marina; Harrington, Kyle; Hopkins, Gary Patrick; Hsu, Joseph; Hubbard, Philip M.; Javier, Alexandre; Kainmueller, Dagmar; Korff, Wyatt; Kovalyak, Julie; Krzemiński, Dominik; Lauchie, Shirley; Lohff, Alanna; Maldonado, Charli; Manley, Emily A; Mooney, Caroline; Neace, Erika; Nichols, Matthew; Ogundeyi, Omotara; Okeoma, Nneoma; Paterson, Tyler; Phillips, Elliott; Phillips, Emily M.; Ribeiro, Caitlin; Ryan, Sean M.; Rymer, Jon Thomson; Scott, Anne K; Scott, Ashley L; Shepherd, David; Shinomiya, Aya; Smith, Claire; Smith, Natalie L.; Suleiman, Alia; Takemura, Satoko; Talebi, Iris; Tamimi, Imaan F M; Trautman, Eric T.; Umayam, Lowell; Walsh, John J; Yang, Tansy; Rubin, Gerald M.; Scheffer, Louis K; Funke, Jan; Saalfeld, Stephan; Hess, Harald F.; Plaza, Stephen M.; Card, Gwyneth M; Jefferis, Gregory S.X.E.; Berg, Stuart

doi:10.1101/2023.06.05.543757

Cited by 46 publications

(52 citation statements)

References 26 publications

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“…In this regard, Drosophila offers unique advantages: it is the only limbed animal with a near-complete connectome [21][22][23][24][25] , and many Drosophila descending neurons (DNs) involved in walking control are uniquely identifiable as individual right-left cell pairs [26][27][28][29][30][31][32] . Moreover, new genetic tools 26,33 allow us to target single DNs for recording and perturbation during locomotion.…”

Section: Introductionmentioning

confidence: 99%

Fine-grained descending control of steering in walkingDrosophila

Yang,

Brezovec,

Serratosa Capdevila

et al. 2023

Preprint

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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.

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Section: Introductionmentioning

confidence: 99%

Fine-grained descending control of steering in walkingDrosophila

Yang,

Brezovec,

Serratosa Capdevila

et al. 2023

Preprint

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“…We could narrow the set of interesting lines to 11 drivers based on their locomotor phenotype and expression levels. Among the SEZ lines, we focused on 3 lines where we could unambiguously identify the neurons both in the light microscopy 27 as well as electron microscopy 5,31,32,72 datasets. Additionally, we found three Gal4 drivers that drove the strongest halting phenotypes.…”

Section: Methodsmentioning

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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“…Chen et al, 2018; Mamiya et al, 2018; Azevedo et al, 2020; Bidaye et al, 2020; Feng et al, 2020; Chockley et al, 2022; Hermans et al, 2022). Furthermore, ongoing work to map the entire connectome of the brain (Scheffer et al, 2020) and the ventral nerve cord (Phelps et al, 2021; Takemura et al, 2023) is aiding in unravelling the neuronal circuits involved in various aspects of motor control on the synaptic and circuit level.…”

Section: Introductionmentioning

confidence: 99%

A leg model based on anatomical landmarks to study 3D joint kinematics of walking inDrosophila melanogaster

Haustein,

Blanke,

Bockemühl

et al. 2024

Preprint

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Walking is the most common form of how animals move on land. The model organismDrosophila melanogasterhas become increasingly popular for studying how the nervous system controls behavior in general and walking in particular. Despite recent advances in tracking and modeling leg movements of walkingDrosophilain 3D, there are still gaps in knowledge about the biomechanics of leg joints due to the tiny size of fruit flies. For instance, the natural alignment of joint rotational axes was largely neglected in previous kinematic analyses. In this study we therefore present a detailed kinematic leg model in which not only the segment lengths but also the main rotational axes of the joints were derived from anatomical landmarks, namely the joint condyles. Our model with natural oblique joint axes is able to adapt to the 3D leg postures of straight and forward walking fruit flies with high accuracy. When we compared our model to an orthogonalized version, we observed that our model showed a smaller error as well as differences in the used range of motion (ROM), highlighting the advantages of modeling natural rotational axes alignment for the study of joint kinematics. We further found that the kinematic profiles of front, middle, and hind legs differed in the number of required degrees of freedom as well as their contributions to stepping, time courses of joint angles, and ROM. Our findings provide deeper insights into the joint kinematics of walking inDrosophila, and, additionally, help to develop dynamical, musculoskeletal, and neuromechanical simulations.

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A Connectome of the MaleDrosophilaVentral Nerve Cord

Cited by 46 publications

References 26 publications

Fine-grained descending control of steering in walkingDrosophila

Fine-grained descending control of steering in walkingDrosophila

Neural circuit mechanisms underlying context-specific halting inDrosophila

A leg model based on anatomical landmarks to study 3D joint kinematics of walking inDrosophila melanogaster

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