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

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

doi:10.1038/s41467-021-21173-9

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

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

Research output: Contribution to journal › Article › peer-review

46 Scopus citations

Abstract

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.

Original language	English (US)
Article number	1026
Journal	Nature communications
Volume	12
Issue number	1
DOIs	https://doi.org/10.1038/s41467-021-21173-9
State	Published - Dec 1 2021

ASJC Scopus subject areas

General Chemistry
General Biochemistry, Genetics and Molecular Biology
General Physics and Astronomy

Access to Document

10.1038/s41467-021-21173-9

Cite this

Wu, H., Petitpré, C., Fontanet, P., Sharma, A., Bellardita, C., Quadros, R. M., Jannig, P. R., Wang, Y., Heimel, J. A., Cheung, K. K. Y., Wanderoy, S., Xuan, Y., Meletis, K., Ruas, J., Gurumurthy, C. B., Kiehn, O., Hadjab, S., & Lallemend, F. (2021). Distinct subtypes of proprioceptive dorsal root ganglion neurons regulate adaptive proprioception in mice. Nature communications, 12(1), Article 1026. https://doi.org/10.1038/s41467-021-21173-9

Wu, H, Petitpré, C, Fontanet, P, Sharma, A, Bellardita, C, Quadros, RM, Jannig, PR, Wang, Y, Heimel, JA, Cheung, KKY, Wanderoy, S, Xuan, Y, Meletis, K, Ruas, J, Gurumurthy, CB, Kiehn, O, Hadjab, S & Lallemend, F 2021, 'Distinct subtypes of proprioceptive dorsal root ganglion neurons regulate adaptive proprioception in mice', Nature communications, vol. 12, no. 1, 1026. https://doi.org/10.1038/s41467-021-21173-9

@article{f2c7eddbfef0402e91bd4e9a9a573525,

title = "Distinct subtypes of proprioceptive dorsal root ganglion neurons regulate adaptive proprioception in mice",

abstract = "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.",

author = "Haohao Wu and Charles Petitpr{\'e} and Paula Fontanet and Anil Sharma and Carmelo Bellardita and Quadros, {Rolen M.} and Jannig, {Paulo R.} and Yiqiao Wang and Heimel, {J. Alexander} and Cheung, {Kylie K.Y.} and Simone Wanderoy and Yang Xuan and Konstantinos Meletis and Jorge Ruas and Gurumurthy, {Channabasavaiah B.} and Ole Kiehn and Saida Hadjab and Fran{\c c}ois Lallemend",

note = "Publisher Copyright: {\textcopyright} 2021, The Author(s).",

year = "2021",

month = dec,

day = "1",

doi = "10.1038/s41467-021-21173-9",

language = "English (US)",

volume = "12",

journal = "Nature communications",

issn = "2041-1723",

publisher = "Nature Research",

number = "1",

}

TY - JOUR

T1 - Distinct subtypes of proprioceptive dorsal root ganglion neurons regulate adaptive proprioception in mice

AU - Wu, Haohao

AU - Petitpré, Charles

AU - Fontanet, Paula

AU - Sharma, Anil

AU - Bellardita, Carmelo

AU - Quadros, Rolen M.

AU - Jannig, Paulo R.

AU - Wang, Yiqiao

AU - Heimel, J. Alexander

AU - Cheung, Kylie K.Y.

AU - Wanderoy, Simone

AU - Xuan, Yang

AU - Meletis, Konstantinos

AU - Ruas, Jorge

AU - Gurumurthy, Channabasavaiah B.

AU - Kiehn, Ole

AU - Hadjab, Saida

AU - Lallemend, François

PY - 2021/12/1

Y1 - 2021/12/1

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=85101451990&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85101451990&partnerID=8YFLogxK

U2 - 10.1038/s41467-021-21173-9

DO - 10.1038/s41467-021-21173-9

M3 - Article

C2 - 33589589

AN - SCOPUS:85101451990

SN - 2041-1723

VL - 12

JO - Nature communications

JF - Nature communications

IS - 1

M1 - 1026

ER -

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

Abstract

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Cite this