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 Drosophila 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.

Highlights

  • Mechanosensory neurons provide feedback essential for maintaining stable locomotion through unpredictable environments

  • Each hemilineage may be composed of many cell types (Harris et al, 2015; Lacin et al, 2020), and it remains an open question to what extent neurons within a hemilineage exhibit similar connectivity or function

  • We found that ventral nerve cord (VNC) neurons integrate mechanosensory signals from proprioceptor subtypes that encode distinct features of leg joint kinematics

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Summary

Introduction

Mechanosensory neurons provide feedback essential for maintaining stable locomotion through unpredictable environments. Sensory feedback from proprioceptors contributes to many behaviors, including regulation of body posture (Hasan and Stuart, 1988; Zill et al, 2004), coordination of goal-directed movement (Buschges, 2005; Lam and Pearson, 2002), locomotor adaptation (Bidaye et al, 2018; Dickinson et al, 2000), and motor learning (Isakov et al, 2016; Takeoka and Arber, 2019) In both invertebrates and vertebrates, proprioceptors encode diverse features of body kinematics (Tuthill and Azim, 2018).

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