Characterization of Proprioceptive System Dynamics in Behaving Drosophila Larvae Using High-Speed Volumetric Microscopy

Abstract

Proprioceptors provide feedback about body position that is essential for coordinated movement. Proprioceptive sensing of the position of rigid joints has been described in detail in several systems; however, it is not known how animals with a flexible skeleton encode their body positions. Understanding how diverse larval body positions are dynamically encoded requires knowledge of proprioceptor activity patterns in vivo during natural movement. Here we used high-speed volumetric swept confocally aligned planar excitation (SCAPE) microscopy in crawling Drosophila larvae to simultaneously track the position, deformation, and intracellular calcium activity of their multidendritic proprioceptors. Most proprioceptive neurons were found to activate during segment contraction, although one subtype was activated by extension. During cycles of segment contraction and extension, different proprioceptor types exhibited sequential activity, providing a continuum of position encoding during all phases of crawling. This sequential activity was related to the dynamics of each neurons terminal processes, and could endow each proprioceptor with a specific role in monitoring different aspects of body-wall deformation. We demonstrate this deformation encoding both during progression of contraction waves during locomotion as well as during less stereotyped, asymmetric exploration behavior. Our results provide powerful new insights into the body-wide neuronal dynamics of the proprioceptive system in crawling Drosophila, and demonstrate the utility of our SCAPE microscopy approach for characterization of neural encoding throughout the nervous system of a freely behaving animal.

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Document Details

Document Type
Technical Report
Publication Date
Mar 07, 2019
Accession Number
AD1069055

Entities

People

  • Aditi Singhania
  • Elizabeth M.c. Hillman
  • Rebecca D. Vaadia
  • Venkatakaushik Voleti
  • Wenze Li
  • Wesley B. Grueber

Organizations

  • Columbia University

Tags

Communities of Interest

  • Air Platforms
  • Biomedical

DTIC Thesaurus Topics

  • Acquisition
  • Amplitude
  • Animals
  • Biology
  • Brain
  • Cells
  • Central Nervous System
  • Coding
  • Confocal Microscopy
  • Microscopy
  • Nervous System
  • Neurons
  • New York
  • Physical Properties
  • Square Roots
  • Statistical Analysis
  • Wave Propagation

Fields of Study

  • Biology

Readers

  • Neuroscience
  • Robotics and Automation.