Biomechanical origins of proprioceptor feature selectivity and topographic maps in the Drosophila leg

• DOI: 10.1016/j.neuron.2023.07.009
• Publication Date: 2023-08-09T14:38:06Z
• 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
• Keywords: Medical Sciences; Sensory Receptor Cells; Cell Phenomena; Life Sciences; 500; Genetics and Genomics; Proprioception; Ion Channels; Biomedical Informatics; Medical Molecular Biology; Medical Specialties; Medicine and Health Sciences; and Immunity; Animals; Drosophila Proteins; Drosophila; Medical Genetics; Biological Phenomena

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.