An asymmetric mechanical code ciphers curvature-dependent proprioceptor activity.

Area of Science:

• Neuroscience
• Biophysics
• Mechanobiology

Background:

• Locomotion relies on repetitive gait cycles, driven by mechanical feedback from proprioceptors.
• Proprioception adjusts motor programs, creating periodic orbits in low-dimensional spaces.
• Understanding mechanosensation's role in shaping these orbits is crucial.

Purpose of the Study:

• To investigate the mechanics, molecules, and neurons underlying proprioception in C. elegans.
• To elucidate how mechanosensation shapes locomotion's orbital trajectory.
• To challenge existing models of proprioceptive input.

Main Methods:

• Genome editing was employed to modify genetic components.
• Force spectroscopy was used to measure mechanical properties.
• Multiscale modeling provided a systems-level view of the mechanics.

Main Results:

• The spectrin network within proprioceptors encodes body posture via alternating tension and compression.
• TRP-4/NOMPC and TWK-16/TREK2 homologs of mechanosensitive ion channels are informed by this encoding.
• Proprioceptors were found to activate under compressive, not solely tensile, stresses in vivo and in vitro.

Conclusions:

• Proprioception in C. elegans is mediated by compressive forces acting on the spectrin network.
• This compressive sensing mechanism compartmentalizes neuronal activity within axons.
• The findings challenge the traditional model of proprioceptive stretch reception.