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Midbrain circuits that set locomotor speed and gait selection

Author

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  • V. Caggiano

    (Mammalian Locomotor Laboratory, Karolinska Institutet
    IBM T.J. Watson Research Center)

  • R. Leiras

    (Mammalian Locomotor Laboratory, Karolinska Institutet
    University of Copenhagen)

  • H. Goñi-Erro

    (Mammalian Locomotor Laboratory, Karolinska Institutet
    University of Copenhagen)

  • D. Masini

    (Laboratory of Molecular Neuropharmacology)

  • C. Bellardita

    (Mammalian Locomotor Laboratory, Karolinska Institutet
    University of Copenhagen)

  • J. Bouvier

    (Mammalian Locomotor Laboratory, Karolinska Institutet
    CNRS and Université Paris-11)

  • V. Caldeira

    (Mammalian Locomotor Laboratory, Karolinska Institutet)

  • G. Fisone

    (Laboratory of Molecular Neuropharmacology)

  • O. Kiehn

    (Mammalian Locomotor Laboratory, Karolinska Institutet
    University of Copenhagen)

Abstract

Locomotion is a fundamental motor function common to the animal kingdom. It is implemented episodically and adapted to behavioural needs, including exploration, which requires slow locomotion, and escape behaviour, which necessitates faster speeds. The control of these functions originates in brainstem structures, although the neuronal substrate(s) that support them have not yet been elucidated. Here we show in mice that speed and gait selection are controlled by glutamatergic excitatory neurons (GlutNs) segregated in two distinct midbrain nuclei: the cuneiform nucleus (CnF) and the pedunculopontine nucleus (PPN). GlutNs in both of these regions contribute to the control of slower, alternating-gait locomotion, whereas only GlutNs in the CnF are able to elicit high-speed, synchronous-gait locomotion. Additionally, both the activation dynamics and the input and output connectivity matrices of GlutNs in the PPN and the CnF support explorative and escape locomotion, respectively. Our results identify two regions in the midbrain that act in conjunction to select context-dependent locomotor behaviours.

Suggested Citation

  • V. Caggiano & R. Leiras & H. Goñi-Erro & D. Masini & C. Bellardita & J. Bouvier & V. Caldeira & G. Fisone & O. Kiehn, 2018. "Midbrain circuits that set locomotor speed and gait selection," Nature, Nature, vol. 553(7689), pages 455-460, January.
    • Handle: RePEc:nat:nature:v:553:y:2018:i:7689:d:10.1038_nature25448
    DOI: 10.1038/nature25448
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    Cited by:

    1. Maxime Lemieux & Narges Karimi & Frederic Bretzner, 2024. "Functional plasticity of glutamatergic neurons of medullary reticular nuclei after spinal cord injury in mice," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. Satoshi Koba & Nao Kumada & Emi Narai & Naoya Kataoka & Kazuhiro Nakamura & Tatsuo Watanabe, 2022. "A brainstem monosynaptic excitatory pathway that drives locomotor activities and sympathetic cardiovascular responses," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    3. Sandeep Sharma & Cecilia A. Badenhorst & Donovan M. Ashby & Stephanie A. Vito & Michelle A. Tran & Zahra Ghavasieh & Gurleen K. Grewal & Cole R. Belway & Alexander McGirr & Patrick J. Whelan, 2024. "Inhibitory medial zona incerta pathway drives exploratory behavior by inhibiting glutamatergic cuneiform neurons," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    4. Li-Ju Hsu & Maëlle Bertho & Ole Kiehn, 2023. "Deconstructing the modular organization and real-time dynamics of mammalian spinal locomotor networks," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    5. Eric A. Kirk & Keenan T. Hope & Samuel J. Sober & Britton A. Sauerbrei, 2024. "An output-null signature of inertial load in motor cortex," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    6. Coralie Hérent & Séverine Diem & Giovanni Usseglio & Gilles Fortin & Julien Bouvier, 2023. "Upregulation of breathing rate during running exercise by central locomotor circuits in mice," Nature Communications, Nature, vol. 14(1), pages 1-17, December.

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