Multimodal sensory control of motor performance by glycinergic interneurons of the mouse spinal cord deep dorsal horn.

dorsal horn glycinergic interneurons inhibition movement proprioception sensorimotor circuits spinal cord touch

Journal

Neuron
ISSN: 1097-4199
Titre abrégé: Neuron
Pays: United States
ID NLM: 8809320

Informations de publication

Date de publication:
17 Apr 2024
Historique:
received: 13 06 2023
revised: 31 10 2023
accepted: 26 01 2024
pubmed: 8 3 2024
medline: 8 3 2024
entrez: 7 3 2024
Statut: ppublish

Résumé

Sensory feedback is integral for contextually appropriate motor output, yet the neural circuits responsible remain elusive. Here, we pinpoint the medial deep dorsal horn of the mouse spinal cord as a convergence point for proprioceptive and cutaneous input. Within this region, we identify a population of tonically active glycinergic inhibitory neurons expressing parvalbumin. Using anatomy and electrophysiology, we demonstrate that deep dorsal horn parvalbumin-expressing interneuron (dPV) activity is shaped by convergent proprioceptive, cutaneous, and descending input. Selectively targeting spinal dPVs, we reveal their widespread ipsilateral inhibition onto pre-motor and motor networks and demonstrate their role in gating sensory-evoked muscle activity using electromyography (EMG) recordings. dPV ablation altered limb kinematics and step-cycle timing during treadmill locomotion and reduced the transitions between sub-movements during spontaneous behavior. These findings reveal a circuit basis by which sensory convergence onto dorsal horn inhibitory neurons modulates motor output to facilitate smooth movement and context-appropriate transitions.

Identifiants

DOI: 10.1016/j.neuron.2024.01.027 PMID: 38452762
pubmed: 38452762
pii: S0896-6273(24)00053-9
doi: 10.1016/j.neuron.2024.01.027
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1302-1327.e13

Informations de copyright

Copyright © 2024 Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Auteurs

Mark A Gradwell (MA)

Cell Biology and Neuroscience Department, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA; W.M. Keck Center for Collaborative Neuroscience, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA.

Nofar Ozeri-Engelhard (N)

Cell Biology and Neuroscience Department, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA; W.M. Keck Center for Collaborative Neuroscience, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA; Neuroscience PhD program, Rutgers Robert Wood Johnson Medical School, Piscataway, NJ, USA.

Jaclyn T Eisdorfer (JT)

Cell Biology and Neuroscience Department, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA; W.M. Keck Center for Collaborative Neuroscience, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA.

Olivier D Laflamme (OD)

Dalhousie PhD program, Dalhousie University, Halifax, NS, Canada; Department of Medical Neuroscience, Atlantic Mobility Action Project, Brain Repair Center, Dalhousie University, Halifax, NS, Canada.

Melissa Gonzalez (M)

Cell Biology and Neuroscience Department, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA; W.M. Keck Center for Collaborative Neuroscience, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA; Department of Biomedical Engineering, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA.

Aman Upadhyay (A)

Cell Biology and Neuroscience Department, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA; W.M. Keck Center for Collaborative Neuroscience, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA; Neuroscience PhD program, Rutgers Robert Wood Johnson Medical School, Piscataway, NJ, USA.

Laura Medlock (L)

Neurosciences & Mental Health, The Hospital for Sick Children, Toronto, ON, Canada; Institute of Biomedical Engineering, University of Toronto, Toronto, ON, Canada.

Tara Shrier (T)

Cell Biology and Neuroscience Department, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA; W.M. Keck Center for Collaborative Neuroscience, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA.

Komal R Patel (KR)

Cell Biology and Neuroscience Department, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA; W.M. Keck Center for Collaborative Neuroscience, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA.

Adin Aoki (A)

Cell Biology and Neuroscience Department, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA; W.M. Keck Center for Collaborative Neuroscience, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA.

Melissa Gandhi (M)

Cell Biology and Neuroscience Department, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA; W.M. Keck Center for Collaborative Neuroscience, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA.

Gloria Abbas-Zadeh (G)

Cell Biology and Neuroscience Department, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA; W.M. Keck Center for Collaborative Neuroscience, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA.

Olisemaka Oputa (O)

Cell Biology and Neuroscience Department, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA; W.M. Keck Center for Collaborative Neuroscience, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA.

Joshua K Thackray (JK)

Cell Biology and Neuroscience Department, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA; W.M. Keck Center for Collaborative Neuroscience, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA; Human Genetics Institute of New Jersey, Rutgers University, The State University of New Jersey, Piscataway, NJ, USA; Tourette International Collaborative Genetics Study (TIC Genetics).

Matthew Ricci (M)

School of Computer Science and Engineering, The Hebrew University of Jerusalem, Jerusalem, Israel.

Arlene George (A)

Cell Biology and Neuroscience Department, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA; W.M. Keck Center for Collaborative Neuroscience, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA.

Nusrath Yusuf (N)

Cell Biology and Neuroscience Department, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA; W.M. Keck Center for Collaborative Neuroscience, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA; Neuroscience PhD program, Rutgers Robert Wood Johnson Medical School, Piscataway, NJ, USA.

Jessica Keating (J)

Cell Biology and Neuroscience Department, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA; W.M. Keck Center for Collaborative Neuroscience, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA.

Zarghona Imtiaz (Z)

Cell Biology and Neuroscience Department, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA; W.M. Keck Center for Collaborative Neuroscience, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA.

Simona A Alomary (SA)

Cell Biology and Neuroscience Department, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA; W.M. Keck Center for Collaborative Neuroscience, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA.

Manon Bohic (M)

Cell Biology and Neuroscience Department, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA; W.M. Keck Center for Collaborative Neuroscience, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA.

Michael Haas (M)

Cell Biology and Neuroscience Department, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA; W.M. Keck Center for Collaborative Neuroscience, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA.

Yurdiana Hernandez (Y)

W.M. Keck Center for Collaborative Neuroscience, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA.

Steven A Prescott (SA)

Neurosciences & Mental Health, The Hospital for Sick Children, Toronto, ON, Canada; Department of Physiology, University of Toronto, Toronto, ON, Canada.

Turgay Akay (T)

Department of Medical Neuroscience, Atlantic Mobility Action Project, Brain Repair Center, Dalhousie University, Halifax, NS, Canada.

Victoria E Abraira (VE)

Cell Biology and Neuroscience Department, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA; W.M. Keck Center for Collaborative Neuroscience, Rutgers University, The State University of New Jersey, New Brunswick, NJ, USA. Electronic address: victoria.abraira@rutgers.edu.

Classifications MeSH