Biomechanical Origins of Proprioceptor Feature Selectivity and Topographic Maps in the Drosophila Leg

Authors

Akira Mamiya
Anne Sustar
Igor Siwanowicz
Yanyan Qi
Tzu-Chiao Lu
Pralaksha Gurung
Chenghao Chen
Jasper S Phelps
Aaron T Kuan
Alexandra Pacureanu
Wei-Chung Allen Lee
Hongjie Li
Natasha Mhatre
John C Tuthill

Publication Date

10-18-2023

Journal

Neuron

DOI

10.1016/j.neuron.2023.07.009

PMID

37562405

PMCID

PMC10644877

PubMedCentral® Posted Date

10-18-2024

PubMedCentral® Full Text Version

Author MSS

Published Open-Access

yes

Keywords

Animals, Drosophila, Sensory Receptor Cells, Proprioception, Drosophila Proteins, Ion Channels

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.