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Abstract
Drosophila Transmembrane channel-like (Tmc) is a protein that functions in larval
proprioception. The closely related TMC1 protein is required for mammalian hearing
and is a pore-forming subunit of the hair cell mechanotransduction channel. In hair
cells, TMC1 is gated by small deflections of microvilli that produce tension on extracellular
tip-links that connect adjacent villi. How Tmc might be gated in larval proprioceptors,
which are neurons having a morphology that is completely distinct from hair cells,
is unknown. Here, we have used high-speed confocal microscopy both to measure displacements
of proprioceptive sensory dendrites during larval movement and to optically measure
neural activity of the moving proprioceptors. Unexpectedly, the pattern of dendrite
deformation for distinct neurons was unique and differed depending on the direction
of locomotion: ddaE neuron dendrites were strongly curved by forward locomotion, while
the dendrites of ddaD were more strongly deformed by backward locomotion. Furthermore,
GCaMP6f calcium signals recorded in the proprioceptive neurons during locomotion indicated
tuning to the direction of movement. ddaE showed strong activation during forward
locomotion, while ddaD showed responses that were strongest during backward locomotion.
Peripheral proprioceptive neurons in animals mutant for Tmc showed a near-complete
loss of movement related calcium signals. As the strength of the responses of wild-type
animals was correlated with dendrite curvature, we propose that Tmc channels may be
activated by membrane curvature in dendrites that are exposed to strain. Our findings
begin to explain how distinct cellular systems rely on a common molecular pathway
for mechanosensory responses. He et al. use high-speed confocal imaging to visualize
the dynamic morphology of proprioceptive sensory neurons through the transparent skin
of crawling Drosophila larvae. They use machine vision to create 3D models that
describe how the neurons change during locomotion. They investigate the activity of
the cells and the role of Tmc channels.