@article {69949, title = {Proprioceptive limit detectors mediate sensorimotor control of the Drosophila leg}, journal = {bioRxiv}, year = {2025}, month = {2025 May 15}, abstract = {

Many animals possess mechanosensory neurons that fire when a limb nears the limit of its physical range, but the function of these proprioceptive limit detectors remains poorly understood. Here, we investigate a class of proprioceptors on the Drosophila leg called hair plates. Using calcium imaging in behaving flies, we find that a hair plate on the fly coxa (CxHP8) detects the limits of anterior leg movement. Reconstructing CxHP8 axons in the connectome, we found that they are wired to excite posterior leg movement and inhibit anterior leg movement. Consistent with this connectivity, optogenetic activation of CxHP8 neurons elicited posterior postural reflexes, while silencing altered the swing-to-stance transition during walking. Finally, we use comprehensive reconstruction of peripheral morphology and downstream connectivity to predict the function of other hair plates distributed across the fly leg. Our results suggest that each hair plate is specialized to control specific sensorimotor reflexes that are matched to the joint limit it detects. They also illustrate the feasibility of predicting sensorimotor reflexes from a connectome with identified proprioceptive inputs and motor outputs.

}, doi = {10.1101/2025.05.15.654260}, url = {https://www.biorxiv.org/content/early/2025/05/19/2025.05.15.654260}, author = {Pratt, Brandon G. and Dallmann, Chris J. and Chou, Grant M. and Siwanowicz, Igor and Walling-Bell, Sarah and Cook, Andrew and Sustar, Anne and Azevedo, Anthony and Tuthill, John C.} } @article {68933, title = {Biomechanical origins of proprioceptor feature selectivity and topographic maps in the Drosophila leg.}, journal = {Neuron}, year = {2023}, month = {2023 Aug 04}, abstract = {

Our ability to sense and move our bodies relies on proprioceptors, sensory neurons that detect mechanical forces within the body. Different subtypes of proprioceptors detect different kinematic features, such as joint position, movement, and vibration, but the mechanisms that underlie proprioceptor feature selectivity remain poorly understood. Using single-nucleus RNA sequencing (RNA-seq), we found that proprioceptor subtypes in the Drosophila leg lack differential expression of mechanosensitive ion channels. However, anatomical reconstruction of the proprioceptors and connected tendons revealed major biomechanical differences between subtypes. We built a model of the proprioceptors and tendons that identified a biomechanical mechanism for joint angle selectivity and predicted the existence of a topographic map of joint angle, which we confirmed using calcium imaging. Our findings suggest that biomechanical specialization is a key determinant of proprioceptor feature selectivity in Drosophila. More broadly, the discovery of proprioceptive maps reveals common organizational principles between proprioception and other topographically organized sensory systems.

}, issn = {1097-4199}, doi = {10.1016/j.neuron.2023.07.009}, author = {Mamiya, Akira and Sustar, Anne and Siwanowicz, Igor and Qi, Yanyan and Lu, Tzu-Chiao and Gurung, Pralaksha and Chen, Chenghao and Phelps, Jasper S and Kuan, Aaron T and Pacureanu, Alexandra and Lee, Wei-Chung Allen and Li, Hongjie and Mhatre, Natasha and Tuthill, John C} } @article {67751, title = {Functional architecture of neural circuits for leg proprioception in Drosophila.}, journal = {Current Biology}, volume = {31}, year = {2021}, month = {2021 Dec 06}, pages = {5163}, abstract = {

To effectively control their bodies, animals rely on feedback from proprioceptive mechanosensory neurons. In the Drosophila leg, different proprioceptor subtypes monitor joint position, movement direction, and vibration. Here, we investigate how these diverse sensory signals are integrated by central proprioceptive circuits. We find that signals for leg joint position and directional movement converge in second-order neurons, revealing pathways for local feedback control of leg posture. Distinct populations of second-order neurons integrate tibia vibration signals across pairs of legs, suggesting a role in detecting external substrate vibration. In each pathway, the flow of sensory information is dynamically gated and sculpted by inhibition. Overall, our results reveal parallel pathways for processing of internal and external mechanosensory signals, which we propose mediate feedback control of leg movement and vibration sensing, respectively. The existence of a functional connectivity map also provides a resource for interpreting connectomic reconstruction of neural circuits for leg proprioception.

}, issn = {1879-0445}, doi = {10.1016/j.cub.2021.09.035}, author = {Chen, Chenghao and Agrawal, Sweta and Mark, Brandon and Mamiya, Akira and Sustar, Anne and Phelps, Jasper S and Lee, Wei-Chung Allen and Dickson, Barry J and Card, Gwyneth M and Tuthill, John C} } @article {65860, title = {Central processing of leg proprioception in Drosophila.}, journal = {eLife}, volume = {9}, year = {2020}, month = {2020 Dec 02}, abstract = {

Proprioception, the sense of self-movement and position, is mediated by mechanosensory neurons that detect diverse features of body kinematics. Although proprioceptive feedback is crucial for accurate motor control, little is known about how downstream circuits transform limb sensory information to guide motor output. Here, we investigate neural circuits in that process proprioceptive information from the fly leg. We identify three cell-types from distinct developmental lineages that are positioned to receive input from proprioceptor subtypes encoding tibia position, movement, and vibration. 13Bα neurons encode femur-tibia joint angle and mediate postural changes in tibia position. 9Aα neurons also drive changes in leg posture, but encode a combination of directional movement, high frequency vibration, and joint angle. Activating 10Bα neurons, which encode tibia vibration at specific joint angles, elicits pausing in walking flies. Altogether, our results reveal that central circuits integrate information across proprioceptor subtypes to construct complex sensorimotor representations that mediate diverse behaviors, including reflexive control of limb posture and detection of leg vibration.

}, issn = {2050-084X}, doi = {10.7554/eLife.60299}, author = {Agrawal, Sweta and Dickinson, Evyn S and Sustar, Anne and Gurung, Pralaksha and Shepherd, David and Truman, James W and Tuthill, John C} }