This study provides 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.
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 an elastic 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. The unique feature of multi-spectral, high-speed, volumetric SCAPE microscopy is capable of characterizing tissue and cellular dynamics in live behaving animals.
We have applied this imaging technology to characterize the dynamics of proprioceptive system in crawling Drosophila larvae with simultaneously tracking 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.