TY - JOUR

T1 - Comparison of operation of spinal locomotor networks activated by supraspinal commands and by epidural stimulation of the spinal cord in cats

AU - Musienko, Pavel E.

AU - Lyalka, Vladimir F.

AU - Gorskii, Oleg V.

AU - Merkulyeva, Natalia

AU - Gerasimenko, Yuri P.

AU - Deliagina, Tatiana G.

AU - Zelenin, Pavel V.

N1 - Funding Information: This work was supported by grants from the Russian Science Foundation (No 14‐15‐00788) and by the Russian Foundation for Basic Research (No 16‐04‐01791) to PEM; by a grant from the NIH (R01 NS‐100928) to TGD and PEM; by grants from the Swedish Research Council to TGD (2017‐02944) and to PVZ (No. 21076). Publisher Copyright: © 2020 The Authors. The Journal of Physiology © 2020 The Physiological Society Copyright: Copyright 2020 Elsevier B.V., All rights reserved.

PY - 2020/8/1

Y1 - 2020/8/1

N2 - Key points: Epidural electrical stimulation (ES) of the spinal cord restores/improves locomotion in patients. ES-evoked locomotor movements differ to some extent from the normal ones. Operation of the locomotor network during ES is unknown. We compared the activity of individual spinal neurons during locomotion initiated by signals from the brainstem and by ES. We demonstrated that the spinal network generating locomotion under each of the two conditions is formed by the same neurons. A part of this network operates similarly under the two conditions, suggesting that it is essential for generation of locomotion under both conditions. Another part of this network operates differently under the two conditions, suggesting that it is responsible for differences in the movement kinematics observed under the two conditions. Abstract: Locomotion is a vital motor function for both animals and humans. Epidural electrical stimulation (ES) of the spinal cord is used to restore/improve locomotor movements in patients. However, operation of locomotor networks during ES has never been studied. Here we compared the activity of individual spinal neurons recorded in decerebrate cats of either sex during locomotion initiated by supraspinal commands (caused by stimulation of the mesencephalic locomotor region, MLR) and by ES. We found that under both conditions, the same neurons had modulation of their activity related to the locomotor rhythm, suggesting that the network generating locomotion under the two conditions is formed by the same neurons. About 40% of these neurons had stable modulation (i.e. small dispersion of their activity phase in sequential cycles), as well as a similar phase and shape of activity burst in MLR- and ES-evoked locomotor cycles. We suggest that these neurons form a part of the locomotor network that operates similarly under the two conditions, and are critical for generation of locomotion. About 23% of the modulated neurons had stable modulation only during MLR-evoked locomotion. We suggest that these neurons are responsible for some differences in kinematics of MLR- and ES-evoked locomotor movements. Finally, 25% of the modulated neurons had unstable modulation during both MLR- and ES-evoked locomotion. One can assume that these neurons contribute to maintenance of the excitability level of locomotor networks necessary for generation of stepping, or belong to postural networks, activated simultaneously with locomotor networks by both MLR stimulation and ES.

AB - Key points: Epidural electrical stimulation (ES) of the spinal cord restores/improves locomotion in patients. ES-evoked locomotor movements differ to some extent from the normal ones. Operation of the locomotor network during ES is unknown. We compared the activity of individual spinal neurons during locomotion initiated by signals from the brainstem and by ES. We demonstrated that the spinal network generating locomotion under each of the two conditions is formed by the same neurons. A part of this network operates similarly under the two conditions, suggesting that it is essential for generation of locomotion under both conditions. Another part of this network operates differently under the two conditions, suggesting that it is responsible for differences in the movement kinematics observed under the two conditions. Abstract: Locomotion is a vital motor function for both animals and humans. Epidural electrical stimulation (ES) of the spinal cord is used to restore/improve locomotor movements in patients. However, operation of locomotor networks during ES has never been studied. Here we compared the activity of individual spinal neurons recorded in decerebrate cats of either sex during locomotion initiated by supraspinal commands (caused by stimulation of the mesencephalic locomotor region, MLR) and by ES. We found that under both conditions, the same neurons had modulation of their activity related to the locomotor rhythm, suggesting that the network generating locomotion under the two conditions is formed by the same neurons. About 40% of these neurons had stable modulation (i.e. small dispersion of their activity phase in sequential cycles), as well as a similar phase and shape of activity burst in MLR- and ES-evoked locomotor cycles. We suggest that these neurons form a part of the locomotor network that operates similarly under the two conditions, and are critical for generation of locomotion. About 23% of the modulated neurons had stable modulation only during MLR-evoked locomotion. We suggest that these neurons are responsible for some differences in kinematics of MLR- and ES-evoked locomotor movements. Finally, 25% of the modulated neurons had unstable modulation during both MLR- and ES-evoked locomotion. One can assume that these neurons contribute to maintenance of the excitability level of locomotor networks necessary for generation of stepping, or belong to postural networks, activated simultaneously with locomotor networks by both MLR stimulation and ES.

KW - decerebrate cat

KW - epidural stimulation

KW - locomotion

KW - mesencephalic locomotor region

KW - sensory feedback

KW - spinal neurons

KW - CENTRAL PATTERN GENERATOR

KW - MECHANISMS

KW - LUMBAR

KW - ORGANIZATION

KW - CIRCUITS

KW - ELECTRICAL-STIMULATION

KW - EXTENSOR MUSCLES

KW - HINDLIMB

KW - INTERNEURONS

KW - MOTONEURONS

UR - http://www.scopus.com/inward/record.url?scp=85086231988&partnerID=8YFLogxK

U2 - 10.1113/JP279460

DO - 10.1113/JP279460

M3 - Article

C2 - 32445488

AN - SCOPUS:85086231988

VL - 598

SP - 3459

EP - 3483

JO - Journal of Physiology

JF - Journal of Physiology

SN - 0022-3751

IS - 16

ER -