A critical role for Piezo2 channels in the mechanotransduction of mouse proprioceptive neurons

Danny Florez-Paz,Rohini Kuner,Kiran Kumar Bali,Ana Gomis

doi:10.1038/srep25923

Abstract

Proprioceptors are responsible for the conscious sensation of limb position and movement, muscle tension or force, and balance. Recent evidence suggests that Piezo2 is a low threshold mechanosensory receptor in the peripheral nervous system, acting as a transducer for touch sensation and proprioception. Thus, we characterized proprioceptive neurons in the mesencephalic trigeminal nucleus that are involved in processing proprioceptive information from the face and oral cavity. This is a specific population of neurons that produce rapidly adapting mechanically-activated currents that are fully dependent on Piezo2. As such, we analyzed the deficits in balance and coordination caused by the selective deletion of the channel in proprioceptors (conditional knockout). The data clearly shows that Piezo2 fulfills a critical role in a defined homogeneous population of proprioceptor neurons that innervate the head muscles, demonstrating that this ion channel is essential for mammalian proprioceptive mechanotransduction.

Highlights

Proprioceptors are responsible for the conscious sensation of limb position and movement, muscle tension or force, and balance
Two mouse Cre lines (Pvalb-Cre and HoxB8-Cre) were used to target a population of sensory neurons that included proprioceptive neurons and a subset of cutaneous mechanoreceptors[2]. Mechanical stimulation of these peripheral neurons evoked non-selective, cationic, rapidly adapting (RA) currents that were dependent on Piezo[2] expression, as well as intermediately adapting (IA) currents that were independent of Piezo[2]
Our results define mesencephalic trigeminal nucleus (MTN) neurons as a unique, homogenous population of proprioceptive neurons that have morphological and functional properties typically associated to low threshold mechanoreceptors: a large soma, Figure 2

Summary

Introduction

Proprioceptors are responsible for the conscious sensation of limb position and movement, muscle tension or force, and balance. We characterized proprioceptive neurons in the mesencephalic trigeminal nucleus that are involved in processing proprioceptive information from the face and oral cavity This is a specific population of neurons that produce rapidly adapting mechanically-activated currents that are fully dependent on Piezo[2]. The homogeneous population of neurons in this nucleus represents a much cleaner system to analyze proprioception than the peripheral sensory ganglia that contain mixed populations of sensory neurons, including proprioceptors, touch receptors, nociceptors and thermoreceptors[7,8,9,10,11] These functionally homogeneous trigeminal mechanosensory neurons extend axons that selectively innervate the muscle spindles of the jaw-closing muscles, mediating the stretch reflex and the activity of the periodontal ligaments[12,13]. We found that Piezo[2] is essential for mechanotransduction in these central proprioceptive neurons and in proprioception per se

Methods

Results

Conclusion