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Published Online: 27 July 2022

Control of Forelimb and Hindlimb Movements and Their Coordination during Quadrupedal Locomotion across Speeds in Adult Spinal Cats

Publication: Journal of Neurotrauma
Volume 39, Issue Number 15-16

Abstract

Coordinating the four limbs is critical for terrestrial mammalian locomotion. Thoracic spinal transection abolishes neural communication between the brain and spinal networks controlling hindlimb/leg movements. Several studies have shown that animal models of spinal transection (spinalization), such as mice, rats, cats, and dogs recover hindlimb locomotion with the forelimbs stationary or suspended. We know less on the ability to generate quadrupedal locomotion after spinal transection, however. We collected kinematic and electromyography data in four adult cats during quadrupedal locomotion at five treadmill speeds before (intact cats) and after low-thoracic spinal transection (spinal cats). We show that adult spinal cats performed quadrupedal treadmill locomotion and modulated their speed from 0.4 m/sec to 0.8 m/sec but required perineal stimulation. During quadrupedal locomotion, several compensatory strategies occurred, such as postural adjustments of the head and neck and the appearance of new coordination patterns between the forelimbs and hindlimbs, where the hindlimbs took more steps than the forelimbs. We also observed temporal changes, such as shorter forelimb cycle/swing durations and shorter hindlimb cycle/stance durations in the spinal state. Forelimb double support periods occupied a greater proportion of the cycle in the spinal state, and hindlimb stride length was shorter. Coordination between the forelimbs and hindlimbs was weakened and more variable in the spinal state. Changes in muscle activity reflected spatiotemporal changes in the locomotor pattern. Despite important changes in the pattern, our results indicate that biomechanical properties of the musculoskeletal system play an important role in quadrupedal locomotion and offset some of the loss in neural communication between networks controlling the forelimbs and hindlimbs after spinal transection.

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Published In

cover image Journal of Neurotrauma
Journal of Neurotrauma
Volume 39Issue Number 15-16August 2022
Pages: 1113 - 1131
PubMed: 35343245

History

Published in print: August 2022
Published online: 27 July 2022
Published ahead of print: 6 May 2022
Published ahead of production: 27 March 2022

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    Authors

    Affiliations

    Johannie Audet**
    Department of Pharmacology-Physiology, Faculty of Medicine and Health Sciences, Centre de Recherche du CHUS, Université de Sherbrooke, Sherbrooke, Quebec, Canada.
    Jonathan Harnie**
    Department of Pharmacology-Physiology, Faculty of Medicine and Health Sciences, Centre de Recherche du CHUS, Université de Sherbrooke, Sherbrooke, Quebec, Canada.
    Charly G. Lecomte
    Department of Pharmacology-Physiology, Faculty of Medicine and Health Sciences, Centre de Recherche du CHUS, Université de Sherbrooke, Sherbrooke, Quebec, Canada.
    Stephen Mari
    Department of Pharmacology-Physiology, Faculty of Medicine and Health Sciences, Centre de Recherche du CHUS, Université de Sherbrooke, Sherbrooke, Quebec, Canada.
    Angèle N. Merlet
    Department of Pharmacology-Physiology, Faculty of Medicine and Health Sciences, Centre de Recherche du CHUS, Université de Sherbrooke, Sherbrooke, Quebec, Canada.
    Boris I. Prilutsky
    School of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia, USA.
    Ilya A. Rybak
    Department of Neurobiology and Anatomy, College of Medicine, Drexel University, Philadelphia, Pennsylvania, USA.
    Alain Frigon* [email protected]
    Department of Pharmacology-Physiology, Faculty of Medicine and Health Sciences, Centre de Recherche du CHUS, Université de Sherbrooke, Sherbrooke, Quebec, Canada.

    Notes

    **
    Both authors contributed equally to this article.
    *
    Address correspondence to : Alain Frigon, PhD, Department of Pharmacology-Physiology, Faculty of Medicine and Health Sciences, Université de Sherbrooke, 3001 12e Avenue Nord, Sherbrooke, Quebec J1H 5N4, Canada [email protected]

    Author Disclosure Statement

    No competing financial interests exist.

    Funding Information

    This work was supported by grants from the Natural Sciences and Engineering Research Council of Canada (NSERC RGPIN-2016-03790) to A.F., and the National Institutes of Health: R01 NS110550 to A.F, IAR and BIP. A.F. is a Fonds de Recherche-Santé Quebec (FRQS) Senior Research Scholar. J.H. and A.N.M. were supported by FRQS doctoral and postdoctoral scholarships, respectively. J.A. was supported by master's scholarships from NSERC and FRQS.

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