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Origins of proprioceptor feature selectivity and topographic maps in theDrosophilaleg

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 Year :
2022
Publisher :
Cold Spring Harbor Laboratory, 2022.

Abstract

Our ability to sense and move our bodies relies on proprioceptors, sensory neurons that detect mechanical forces within the body. Proprioceptors are diverse: different subtypes detect different features of joint kinematics, such as position, directional movement, and vibration. However, because they are located within complex and dynamic peripheral tissues, the underlying mechanisms of proprioceptor feature selectivity remain poorly understood. Here, we investigate molecular and biomechanical contributions to proprioceptor diversity in theDrosophilaleg. Using single-nucleus RNA sequencing, we found that different proprioceptor subtypes express similar complements of mechanosensory and other ion channels. However, anatomical reconstruction of the proprioceptive organ and connected tendons revealed major biomechanical differences between proprioceptor subtypes. We constructed a computational model of the proprioceptors and tendons, which identified a putative biomechanical mechanism for joint angle selectivity. The model also predicted the existence of a goniotopic map of joint angle among position-tuned proprioceptors, which we confirmed using calcium imaging. Our findings suggest that biomechanical specialization is a key determinant of proprioceptor feature selectivity inDrosophila. More broadly, our discovery of proprioceptive maps in the fly leg reveals common organizational principles between proprioception and other topographically organized sensory systems.

Details

Database :
OpenAIRE
Accession number :
edsair.doi...........a56a4d746e96227473e6a861d7319478
Full Text :
https://doi.org/10.1101/2022.08.08.503192