Divergent neural circuits for proprioceptive and exteroceptive sensing of theDrosophilaleg

Abstract

Somatosensory neurons provide the nervous system with information about mechanical forces originating inside and outside the body. Here, we use connectomics to reconstruct and analyze neural circuits downstream of the largest somatosensory organ in theDrosophilaleg, the femoral chordotonal organ (FeCO). The FeCO has been proposed to support both proprioceptive sensing of the fly's femur-tibia joint and exteroceptive sensing of substrate vibrations, but it remains unknown which sensory neurons and central circuits contribute to each of these functions. We found that different subtypes of FeCO sensory neurons feed into distinct proprioceptive and exteroceptive pathways. Position- and movement-encoding FeCO neurons connect to local leg motor control circuits in the ventral nerve cord (VNC), indicating a proprioceptive function. In contrast, signals from the vibration-encoding FeCO neurons are integrated across legs and transmitted to auditory regions in the brain, indicating an exteroceptive function. Overall, our analyses reveal the structure of specialized circuits for processing proprioceptive and exteroceptive signals from the fly leg. They also demonstrate how analyzing patterns of synaptic connectivity can distill organizing principles from complex sensorimotor circuits.

Inhibitory circuits generate rhythms for leg movements during Drosophila grooming

“…Claw extension sensing neurons connect to two 13A neurons that inhibit tibia extensor MNs. These neurons also directly connect to tibia flexor MNs 23 . Together, extension-sensing proprioceptors activate flexor MNs and 13A neurons that inhibit extensor MNs, possibly inducing a switch from extension to flexion.…”

“…Thus, flexion position-sensing proprioceptors activate 13As that inhibit medial joint flexion. Recent connectomics analysis showed that flexion sensing proprioceptors send direct excitatory feedback to tibia extensor MNs and indirect inhibitory feedback to tibia flexor MNs 23 . Together, flexion sensing proprioceptors directly activate the extensor MNs, and inhibit the tibia flexor MNs by activating primary 13A neurons.…”

“…Furthermore, analysis of the descending neuron to motor pathway identified interactions between various premotor GABAergic neurons and between glutamatergic neurons from multiple lineages, which are hypothesized to be involved in limb coordination during walking. These central circuits also receive sensory feedback from proprioceptors in the leg [20][21][22][23] . Recent connectome mapping and genetic tools to manipulate specific neurons have opened up the possibility to test the role of the central and peripheral signals in limb coordination.…”

Comparative connectomics of the descending and ascending neurons of theDrosophilanervous system: stereotypy and sexual dimorphism

“…Early access to the proofread and annotated connectome data that we describe has already enabled and assisted a range of exciting work including studies of the circuit basis of locomotor behaviour and the organisational and functional logic of descending neurons (Braun et al, 2024; H. S. J. Dallmann et al, 2024;Lee et al, 2024;Lesser et al, 2024;Sapkal et al, 2023;von Reyn et al, 2024 unpublished;Yang et al, 2023). The sensorimotor reconstructions presented enable us to infer the circuit basis of behaviours, including sexually dimorphic patterns, allowing us to formulate new hypotheses regarding numerous circuit components.…”

“…We have established a platform for systematic neuron typing based on light-level and cross-dataset identification, which we encourage the community to utilise for studying their specific circuits of interest. Pre-publication access to our work has already benefited a number of publications ( Braun et al, 2023 ; H. S. J. Cheong et al, 2024 ; Dallmann et al, 2024 ; Lee et al, 2024 ; Lesser et al, 2024 ; Sapkal et al, 2023 ; Yang et al, 2023 ).…”