IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-45300-4.html
   My bibliography  Save this article

Functional plasticity of glutamatergic neurons of medullary reticular nuclei after spinal cord injury in mice

Author

Listed:
  • Maxime Lemieux

    (Centre de Recherche du CHU de Québec, CHUL-Neurosciences)

  • Narges Karimi

    (Centre de Recherche du CHU de Québec, CHUL-Neurosciences
    Université Laval)

  • Frederic Bretzner

    (Centre de Recherche du CHU de Québec, CHUL-Neurosciences
    Université Laval)

Abstract

Spinal cord injury disrupts the descending command from the brain and causes a range of motor deficits. Here, we use optogenetic tools to investigate the functional plasticity of the glutamatergic reticulospinal drive of the medullary reticular formation after a lateral thoracic hemisection in female mice. Sites evoking stronger excitatory descending drive in intact conditions are the most impaired after injury, whereas those associated with a weaker drive are potentiated. After lesion, pro- and anti-locomotor activities (that is, initiation/acceleration versus stop/deceleration) are overall preserved. Activating the descending reticulospinal drive improves stepping ability on a flat surface of chronically impaired injured mice, and its priming enhances recovery of skilled locomotion on a horizontal ladder. This study highlights the resilience and capacity for reorganization of the glutamatergic reticulospinal command after injury, along with its suitability as a therapeutical target to promote functional recovery.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45300-4
    DOI: 10.1038/s41467-024-45300-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-45300-4
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-45300-4?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. 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.
    2. Paolo Capelli & Chiara Pivetta & Maria Soledad Esposito & Silvia Arber, 2017. "Locomotor speed control circuits in the caudal brainstem," Nature, Nature, vol. 551(7680), pages 373-377, November.
    3. 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.
    4. Henri Lorach & Andrea Galvez & Valeria Spagnolo & Felix Martel & Serpil Karakas & Nadine Intering & Molywan Vat & Olivier Faivre & Cathal Harte & Salif Komi & Jimmy Ravier & Thibault Collin & Laure Co, 2023. "Walking naturally after spinal cord injury using a brain–spine interface," Nature, Nature, vol. 618(7963), pages 126-133, June.
    5. Fabien B. Wagner & Jean-Baptiste Mignardot & Camille G. Le Goff-Mignardot & Robin Demesmaeker & Salif Komi & Marco Capogrosso & Andreas Rowald & Ismael Seáñez & Miroslav Caban & Elvira Pirondini & Mol, 2018. "Targeted neurotechnology restores walking in humans with spinal cord injury," Nature, Nature, vol. 563(7729), pages 65-71, November.
    6. Gina G. Turrigiano & Kenneth R. Leslie & Niraj S. Desai & Lana C. Rutherford & Sacha B. Nelson, 1998. "Activity-dependent scaling of quantal amplitude in neocortical neurons," Nature, Nature, vol. 391(6670), pages 892-896, February.
    7. Marco Bonizzato & Galyna Pidpruzhnykova & Jack DiGiovanna & Polina Shkorbatova & Natalia Pavlova & Silvestro Micera & Grégoire Courtine, 2018. "Brain-controlled modulation of spinal circuits improves recovery from spinal cord injury," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    8. Claudia Kathe & Michael A. Skinnider & Thomas H. Hutson & Nicola Regazzi & Matthieu Gautier & Robin Demesmaeker & Salif Komi & Steven Ceto & Nicholas D. James & Newton Cho & Laetitia Baud & Katia Gala, 2022. "The neurons that restore walking after paralysis," Nature, Nature, vol. 611(7936), pages 540-547, November.
    9. Ralf D. Wimmer & L. Ian Schmitt & Thomas J. Davidson & Miho Nakajima & Karl Deisseroth & Michael M. Halassa, 2015. "Thalamic control of sensory selection in divided attention," Nature, Nature, vol. 526(7575), pages 705-709, October.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. 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.
    2. 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.
    3. 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.
    4. Kai Zhou & Wei Wei & Dan Yang & Hui Zhang & Wei Yang & Yunpeng Zhang & Yingnan Nie & Mingming Hao & Pengcheng Wang & Hang Ruan & Ting Zhang & Shouyan Wang & Yaobo Liu, 2024. "Dual electrical stimulation at spinal-muscular interface reconstructs spinal sensorimotor circuits after spinal cord injury," Nature Communications, Nature, vol. 15(1), pages 1-26, December.
    5. Lin Yang & Mengdi Zhang & Yuan Zhou & Dongxiao Jiang & Lilong Yu & Lingyu Xu & Fan Fei & Wenkai Lin & Yanrong Zheng & Jiannong Wu & Yi Wang & Zhong Chen, 2024. "Histamine-tuned subicular circuit mediates alert-driven accelerated locomotion in mice," Nature Communications, Nature, vol. 15(1), pages 1-16, 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.
    7. Matteo Saponati & Martin Vinck, 2023. "Sequence anticipation and spike-timing-dependent plasticity emerge from a predictive learning rule," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    8. Niranjan Chakravarthy & Shivkumar Sabesan & Kostas Tsakalis & Leon Iasemidis, 2009. "Controlling epileptic seizures in a neural mass model," Journal of Combinatorial Optimization, Springer, vol. 17(1), pages 98-116, January.
    9. Ashraf S. Gorgey & Robert Trainer & Tommy W. Sutor & Jacob A. Goldsmith & Ahmed Alazzam & Lance L. Goetz & Denise Lester & Timothy D. Lavis, 2023. "A case study of percutaneous epidural stimulation to enable motor control in two men after spinal cord injury," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    10. Sacha Jennifer van Albada & Moritz Helias & Markus Diesmann, 2015. "Scalability of Asynchronous Networks Is Limited by One-to-One Mapping between Effective Connectivity and Correlations," PLOS Computational Biology, Public Library of Science, vol. 11(9), pages 1-37, September.
    11. Dean J. Kareemo & Christina S. Winborn & Samantha S. Olah & Carley N. Miller & JungMin Kim & Chelsie A. Kadgien & Hannah S. Actor-Engel & Harrison J. Ramsay & Austin M. Ramsey & Jason Aoto & Matthew J, 2024. "Genetically encoded intrabody probes for labeling and manipulating AMPA-type glutamate receptors," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    12. Nikita Vladimirov & Fabian F. Voigt & Thomas Naert & Gabriela R. Araujo & Ruiyao Cai & Anna Maria Reuss & Shan Zhao & Patricia Schmid & Sven Hildebrand & Martina Schaettin & Dominik Groos & José María, 2024. "Benchtop mesoSPIM: a next-generation open-source light-sheet microscope for cleared samples," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    13. Christoph Hartmann & Andreea Lazar & Bernhard Nessler & Jochen Triesch, 2015. "Where’s the Noise? Key Features of Spontaneous Activity and Neural Variability Arise through Learning in a Deterministic Network," PLOS Computational Biology, Public Library of Science, vol. 11(12), pages 1-35, December.
    14. Gal Atlan & Noa Matosevich & Noa Peretz-Rivlin & Idit Marsh-Yvgi & Noam Zelinger & Eden Chen & Timna Kleinman & Noa Bleistein & Efrat Sheinbach & Maya Groysman & Yuval Nir & Ami Citri, 2024. "Claustrum neurons projecting to the anterior cingulate restrict engagement during sleep and behavior," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    15. Julijana Gjorgjieva & Taro Toyoizumi & Stephen J Eglen, 2009. "Burst-Time-Dependent Plasticity Robustly Guides ON/OFF Segregation in the Lateral Geniculate Nucleus," PLOS Computational Biology, Public Library of Science, vol. 5(12), pages 1-19, December.
    16. Aseel Shomar & Lukas Geyrhofer & Noam E Ziv & Naama Brenner, 2017. "Cooperative stochastic binding and unbinding explain synaptic size dynamics and statistics," PLOS Computational Biology, Public Library of Science, vol. 13(7), pages 1-24, July.
    17. Giacomo Valle & Natalija Katic Secerovic & Dominic Eggemann & Oleg Gorskii & Natalia Pavlova & Francesco M. Petrini & Paul Cvancara & Thomas Stieglitz & Pavel Musienko & Marko Bumbasirevic & Stanisa R, 2024. "Biomimetic computer-to-brain communication enhancing naturalistic touch sensations via peripheral nerve stimulation," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    18. Márton Albert Hajnal & Duy Tran & Michael Einstein & Mauricio Vallejo Martelo & Karen Safaryan & Pierre-Olivier Polack & Peyman Golshani & Gergő Orbán, 2023. "Continuous multiplexed population representations of task context in the mouse primary visual cortex," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    19. Dimitris Boufidis & Raghav Garg & Eugenia Angelopoulos & D. Kacy Cullen & Flavia Vitale, 2025. "Bio-inspired electronics: Soft, biohybrid, and “living” neural interfaces," Nature Communications, Nature, vol. 16(1), pages 1-17, December.
    20. Juan Prada & Manju Sasi & Corinna Martin & Sibylle Jablonka & Thomas Dandekar & Robert Blum, 2018. "An open source tool for automatic spatiotemporal assessment of calcium transients and local ‘signal-close-to-noise’ activity in calcium imaging data," PLOS Computational Biology, Public Library of Science, vol. 14(3), pages 1-34, March.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45300-4. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.