Synaptic architecture of leg and wing premotor control networks inDrosophila

Abstract

Animal movement is controlled by motor neurons (MNs), which project out of the central nervous system to activate muscles. Because individual muscles may be used in many different behaviors, MN activity must be flexibly coordinated by dedicated premotor circuitry, the organization of which remains largely unknown. Here, we use comprehensive reconstruction of neuron anatomy and synaptic connectivity from volumetric electron microscopy (i.e., connectomics) to analyze the wiring logic of motor circuits controlling theDrosophilaleg and wing. We find that both leg and wing premotor networks are organized into modules that link MNs innervating muscles with related functions. However, the connectivity patterns within leg and wing motor modules are distinct. Leg premotor neurons exhibit proportional gradients of synaptic input onto MNs within each module, revealing a novel circuit basis for hierarchical MN recruitment. In comparison, wing premotor neurons lack proportional synaptic connectivity, which may allow muscles to be recruited in different combinations or with different relative timing. By comparing the architecture of distinct limb motor control systems within the same animal, we identify common principles of premotor network organization and specializations that reflect the unique biomechanical constraints and evolutionary origins of leg and wing motor control.

Whole-body simulation of realistic fruit fly locomotion with deep reinforcement learning

“…This NeuroAI approach is enabled with unprecedented spatial and temporal detail by our body model and imitation learning framework. Future work can leverage the connectomic mapping of the entire fruit fly nervous system , Lesser et al, 2023, Azevedo et al, 2022, Takemura et al, 2023 to more realistically model neural circuits underlying sensorimotor behavior. In the short term, our body model and imitation learning framework can enable the model-based investigation of the neural underpinnings of sensory-motor behaviors such as escape invoked by looming stimuli [Card, 2012], gaze-stabilization [Cruz and Chiappe, 2023], the control of movement by the ventral nerve cord [Lesser et al, 2023, Azevedo et al, 2022, Takemura et al, 2023.…”

“…For instance, new imaging of musculature and sensory systems can improve biomechanical fidelity of actuation and sensory feedback. The black-box artificial neural network controllers we trained using imitation learning can be made more realistic by introducing connectome constraints [Lappalainen et al, 2023] based on recent measurements of connectivity of the brain and ventral nerve cord [Lesser et al, 2023, Azevedo et al, 2022, Takemura et al, 2023, as well as neural activity , Pacheco et al, 2021, Aimon et al, 2023. Thus our present work serves as a platform to enable future studies of embodied cognition [Zador et al, 2023], modeling the neural and biomechanical basis of sensorimotor behavior in unprecedented detail.…”

Nested neural circuits generate distinct acoustic signals during Drosophila courtship

“…At present, connectomic analysis is also typically limited to very small sample sizes, usually just one, and so we cannot address variability both within and between species. These limitations will eventually be overcome through advances in electron (Cheong et al, 2023;Dorkenwald et al;Lesser et al, 2023;Marin et al, 2023;Phelps et al, 2021b;Scheffer et al, 2020;Schlegel et al, 2023a) and light (Lillvis et al, 2022) microscopy to provide molecular detail and to allow study of much larger sample sizes.…”

“…Split-GAL4 enhancer combinations identified in D. melanogaster have been used to target pIP10 in D. yakuba (Ding et al, 2019), suggesting that the split-GAL4 reagents we have identified may be useful for studying homologous circuits across Drosophila species. Testing anatomical hypotheses will require comparative connectomics, which should be facilitated by recent advances in EM (Dorkenwald et al;Lesser et al, 2023;Marin et al, 2023;Phelps et al, 2021a;Scheffer et al, 2020;Schlegel et al, 2023aSchlegel et al, , 2023bSheridan et al, 2022;Xu et al, 2017) and in expansion microscopy (Lillvis et al, 2022).…”

“…Split-GAL4 enhancer combinations identified in D. melanogaster have been used to target pIP10 in D. yakuba 50 , suggesting that the split-GAL4 reagents we have identified may be useful for studying homologous circuits across Drosophila species. Testing anatomical hypotheses will require comparative connectomics, which should be facilitated by recent advances in EM 40,[65][66][67][68][69][70][71][72] and in expansion microscopy 30 .…”