Parallel Processing of Two Mechanosensory Modalities by a Single Neuron in C. elegans

Abstract

Neurons convert synaptic or sensory inputs into cellular outputs. It is not well understood how a single neuron senses, processes multiple stimuli, and generates distinct neuronal outcomes. Here, we describe the mechanism by which the C. elegans PVD neurons sense two mechanical stimuli: external touch and proprioceptive body movement. These two stimuli are detected by distinct mechanosensitive DEG/ENaC/ASIC channels, which trigger distinct cellular outputs linked to mechanonociception and proprioception. Mechanonociception depends on DEGT-1 and activates PVD's downstream command interneurons through its axon, while proprioception depends on DEL-1, UNC-8, and MEC-10 to induce local dendritic Ca 2+ increase and dendritic release of a neuropeptide NLP-12. NLP-12 directly modulates neuromuscular junction activity through the cholecystokinin receptor homolog on motor axons, setting muscle tone and movement vigor. Thus, the same neuron simultaneously uses both its axon and dendrites as output apparatus to drive distinct sensorimotor outcomes.

Touch-induced mechanical strain in somatosensory neurons is independent of extracellular matrix mutations inCaenorhabditis elegans

“…, 2019 ) and that physical deformations are correlated with calcium transients. Similarly, movement induces localized calcium transients in the tertiary dendrites of the Caenorhabditis elegans PVD proprioceptors that depend on expression of a DEG/ENaC/ASIC protein ( Tao et al. , 2019 ).…”

Phase response analyses support a relaxation oscillator model of locomotor rhythm generation inCaenorhabditis elegans

“…The cell DVA has been shown to exhibit proprioceptive properties with a dependence on a mechanosensitive channel, TRP-4, which acts as a stretch receptor to regulate the body bend amplitude during locomotion (41). In the case of PVD, a recent study (42) has revealed that body stretches induce local dendritic calcium transients in PVD and dendritic release of a neuropeptide NLP-12 which appears to regulate the amplitude of sinusoidal body movements. However, whether these proprioceptive feedback systems contribute to locomotory rhythm generation remains unknown.…”

Neurite Branching Regulated by Neuronal Cell Surface Molecules in Caenorhabditis elegans

“…Together, the PVD and FLP neurons comprise a sensory network of the entire body that responds to harsh mechanical stimuli (Way and Chalfie, 1989). PVD and FLP neurons show some differences in function and morphology: PVD neurons sense hot and cold temperature, high osmolarity and play a role in proprioception, whereas FLP neurons sense noxious high temperatures and humidity (Chatzigeorgiou et al, 2010;Albeg et al, 2011;Mohammadi et al, 2013;Cohen et al, 2014;Tao et al, 2019). Also, PVD is morphologically unciliated while FLP is ciliated (Ward et al, 1975;Altun and Hall, 2011).…”