Characterization of Proprioceptive System Dynamics in Behaving Drosophila Larvae Using High-Speed Volumetric Microscopy
Year: 2019
Type: article
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 neuron's 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.
Source: Current Biology
Language: English
Subfield: Cellular and Molecular Neuroscience
Field: Neuroscience
Domain: Life Sciences
Open Access status: hybrid
Estimated APC paid: $5,200
Funders: National Science Foundation, U.S. Department of Defense, Simons Foundation, McKnight Foundation, National Institutes of Health, Multidisciplinary University Research Initiative, National Institute of Neurological Disorders and Stroke, Eunice Kennedy Shriver National Institute of Child Health and Human Development
Awards: G1242600127, G2111327958, G3116301191, G4890566774, G6092025276, SCAPE microscopy for high-speed in-vivo volumetric microscopy in behaving organisms, Neurobiology and Behavior Research Training Grant, SCAPE microscopy for high-speed 3D imaging of cellular function in behaving animals: Continued innovation, optimization, and dissemination, G9000268851
OpenAlex ID: W2952067902