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

Author

Listed:
  • Haohao Wu

    (Karolinska Institutet)

  • Charles Petitpré

    (Karolinska Institutet)

  • Paula Fontanet

    (Karolinska Institutet)

  • Anil Sharma

    (Karolinska Institutet)

  • Carmelo Bellardita

    (Karolinska Institutet
    University of Copenhagen)

  • Rolen M. Quadros

    (University of Nebraska Medical Center)

  • Paulo R. Jannig

    (Karolinska Institutet)

  • Yiqiao Wang

    (Karolinska Institutet)

  • J. Alexander Heimel

    (Netherlands Institute for Neuroscience)

  • Kylie K. Y. Cheung

    (Karolinska Institutet)

  • Simone Wanderoy

    (Karolinska Institutet)

  • Yang Xuan

    (Karolinska Institutet)

  • Konstantinos Meletis

    (Karolinska Institutet)

  • Jorge Ruas

    (Karolinska Institutet)

  • Channabasavaiah B. Gurumurthy

    (University of Nebraska Medical Center
    University of Nebraska Medical Center)

  • Ole Kiehn

    (Karolinska Institutet
    University of Copenhagen)

  • Saida Hadjab

    (Karolinska Institutet)

  • François Lallemend

    (Karolinska Institutet
    Ming Wai Lau Centre for Reparative Medicine, Stockholm Node, Karolinska Institutet)

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.

Suggested Citation

  • 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 , 2021. "Distinct subtypes of proprioceptive dorsal root ganglion neurons regulate adaptive proprioception in mice," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-21173-9
    DOI: 10.1038/s41467-021-21173-9
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    Cited by:

    1. Stephan Dietrich & Carlos Company & Kun Song & Elijah David Lowenstein & Levin Riedel & Carmen Birchmeier & Gaetano Gargiulo & Niccolò Zampieri, 2022. "Molecular identity of proprioceptor subtypes innervating different muscle groups in mice," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    2. Charles Petitpré & Louis Faure & Phoebe Uhl & Paula Fontanet & Iva Filova & Gabriela Pavlinkova & Igor Adameyko & Saida Hadjab & Francois Lallemend, 2022. "Single-cell RNA-sequencing analysis of the developing mouse inner ear identifies molecular logic of auditory neuron diversification," Nature Communications, Nature, vol. 13(1), pages 1-15, December.

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