Journal Article

Distinct subtypes of proprioceptive dorsal root ganglion neurons regulate adaptive proprioception in mice

Heimel, J. Alexander, Kiehn, Ole, Jannig, Paulo R., Petitpré, Charles, Bellardita, Carmelo, Fontanet, Paula, Wu, Haohao, Lallemend, François, Meletis, Konstantinos, Hadjab, Saida, Gurumurthy, Channabasavaiah B., Cheung, Kylie K. Y., Quadros, Rolen M., Wang, Yiqiao, Xuan, Yang, Ruas, Jorge, Sharma, Anil, Wanderoy, Simone

2021

Overview

Proprioceptive neurons (PNs) are essential for the proper execution of all our movements by providing muscle sensory feedback to the central motor network. Here, using deep single cell RNAseq of adult PNs coupled with virus and genetic tracings, we molecularly identify three main types of PNs (Ia, Ib and II) and find that they segregate into eight distinct subgroups. Our data unveil a highly sophisticated organization of PNs into discrete sensory input channels with distinct spatial distribution, innervation patterns and molecular profiles. Altogether, these features contribute to finely regulate proprioception during complex motor behavior. Moreover, while Ib- and II-PN subtypes are specified around birth, Ia-PN subtypes diversify later in life along with increased motor activity. We also show Ia-PNs plasticity following exercise training, suggesting Ia-PNs are important players in adaptive proprioceptive function in adult mice. Molecular diversity of proprioceptive neuron types (Ia, Ib and II PNs) is unclear. Here, the authors characterized the functional organization and development of eight subtypes of PNs in mice. Importantly, Ia subtypes are plastic, suggesting a role in adaptive proprioception during motor behavior.

• Publisher: Nature Publishing Group UK,Nature Publishing Group,Nature Portfolio
• Subject: 13 / 13/51 / 38 / 38/32 / 38/91 / 631/337/2019 / 631/378/2571/2573 / 631/378/3917 / 631/378/87 / 64 / 64/60 / Animals / Calbindin 1 - genetics / Calbindin 1 - metabolism / Calcium-Binding Proteins - genetics / Calcium-Binding Proteins - metabolism / Co-Repressor Proteins - genetics / Co-Repressor Proteins - metabolism / Core Binding Factor Alpha 2 Subunit - genetics / Core Binding Factor Alpha 2 Subunit - metabolism / Core Binding Factor Alpha 3 Subunit - genetics / Core Binding Factor Alpha 3 Subunit - metabolism / Dorsal root ganglia / Feedback, Sensory - physiology / Fitness training programs / Functional morphology / Ganglia, Spinal - cytology / Ganglia, Spinal - metabolism / Gene Expression / Genes / Humanities and Social Sciences / Innervation / Lectins, C-Type - genetics / Lectins, C-Type - metabolism / LIM Domain Proteins - genetics / LIM Domain Proteins - metabolism / Male / Mice / Mice, Inbred C57BL / Mice, Transgenic / Motor activity / Motor Neurons - classification / Motor Neurons - cytology / Motor Neurons - metabolism / multidisciplinary / Muscles / Nerve Tissue Proteins - genetics / Nerve Tissue Proteins - metabolism / Neurons / Neurosciences / Pharmacology / Physical Conditioning, Animal / Physical training / Proprioception / Proprioception - physiology / Science / Science (multidisciplinary) / Sensory feedback / Sensory Receptor Cells - classification / Sensory Receptor Cells - cytology / Sensory Receptor Cells - metabolism / Single-Cell Analysis / Spatial distribution / Spinal cord / Spinal Cord - cytology / Spinal Cord - metabolism / Subgroups