Initiation and modulation of locomotor circuitry output with multisite transcutaneous electrical stimulation of the spinal cord in noninjured humans.
The mammalian lumbar spinal cord has the capability to generate locomotor activity in the absence of input from the brain. Previously, we reported that transcutaneous electrical stimulation of the spinal cord at vertebral level T11 can activate the locomotor circuitry in noninjured subjects when their legs are placed in a gravity-neutral position (Gorodnichev RM, Pivovarova EA, Pukhov A, Moiseev SA, Savokhin AA, Moshonkina TR, Shcherbakova NA, Kilimnik VA, Selionov VA, Kozlovskaia IB, Edgerton VR, Gerasimenko IU. Fiziol Cheloveka 38: 46-56, 2012). In the present study we hypothesized that stimulating multiple spinal sites and therefore unique combinations of networks converging on postural and locomotor lumbosacral networks would be more effective in inducing more robust locomotor behavior and more selective control than stimulation of more restricted networks. We demonstrate that simultaneous stimulation at the cervical, thoracic, and lumbar levels induced coordinated stepping movements with a greater range of motion at multiple joints in five of six noninjured subjects. We show that the addition of stimulation at L1 and/or at C5 to stimulation at T11 immediately resulted in enhancing the kinematics and interlimb coordination as well as the EMG patterns in proximal and distal leg muscles. Sequential cessation of stimulation at C5 and then at L1 resulted in a progressive degradation of the stepping pattern. The synergistic and interactive effects of transcutaneous stimulation suggest a multisegmental convergence of descending and ascending, and most likely propriospinal, influences on the spinal neuronal circuitries associated with locomotor activity. The potential impact of using multisite spinal cord stimulation as a strategy to neuromodulate the spinal circuitry has significant implications in furthering our understanding of the mechanisms controlling posture and locomotion and for regaining significant sensorimotor function even after a severe spinal cord injury.
Pavlov Institute of Physiology, St. Petersburg, Russia; Integrative Biology and Physiology, University of California, Los Angeles, California; and yuryg@ucla.edu.
Yury
Y
Gerasimenko
Velikie Luky State Academy of Physical Education and Sport, Velikie Luky, Russia;
Ruslan
R
Gorodnichev
Velikie Luky State Academy of Physical Education and Sport, Velikie Luky, Russia;
Aleksandr
A
Puhov
Pavlov Institute of Physiology, St. Petersburg, Russia;
Tatiana
T
Moshonkina
Pavlov Institute of Physiology, St. Petersburg, Russia;
Aleksandr
A
Savochin
Institute for Information Transmission Problems, Russian Academy of Science, Moscow, Russia;
Victor
V
Selionov
Integrative Biology and Physiology, University of California, Los Angeles, California; and Brain Research Institute, University of California, Los Angeles, California.
Roland R
RR
Roy
Departments of Neurosurgery University of California, Los Angeles, California;
Daniel C
DC
Lu
Departments of Neurosurgery University of California, Los Angeles, California; Integrative Biology and Physiology, University of California, Los Angeles, California; and Brain Research Institute, University of California, Los Angeles, California.
V Reggie
VR
Edgerton
D001696:Biomechanical Phenomena; D005121:Extremities / Q000294:innervation / Q000502:physiology; D006801:Humans; D008297:Male; D004856:Postural Balance; D013116:Spinal Cord / Q000502:physiology*; D004561:Transcutaneous Electric Nerve Stimulation; D016138:Walking; D055815:Young Adult
locomotor neuronal circuitry; multisite transcutaneous spinal cord stimulation; noninjured subjects; stepping movements