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Nature Medicine 2018 Gill ML.Pdf LETTERS https://doi.org/10.1038/s41591-018-0175-7 Corrected: Publisher correction Neuromodulation of lumbosacral spinal networks enables independent stepping after complete paraplegia Megan L. Gill1,10, Peter J. Grahn2,10, Jonathan S. Calvert 3, Margaux B. Linde1, Igor A. Lavrov2,4,5, Jeffrey A. Strommen1, Lisa A. Beck1, Dimitry G. Sayenko6,7, Meegan G. Van Straaten1, Dina I. Drubach2, Daniel D. Veith1, Andrew R. Thoreson1, Cesar Lopez1, Yury P. Gerasimenko6,8, V. Reggie Edgerton6, Kendall H. Lee1,2,9,11* and Kristin D. Zhao1,9,11* Spinal sensorimotor networks that are functionally discon- Previously, we reported a case of complete loss of function below nected from the brain because of spinal cord injury (SCI) the sixth thoracic spinal segment due to SCI that occurred 3 years can be facilitated via epidural electrical stimulation (EES) to before study enrollment. During 22 weeks of locomotor training restore robust, coordinated motor activity in humans with (LT), before implantation of the EES system, evidence of discom- paralysis1–3. Previously, we reported a clinical case of com- plete SCI was observed. The LT approach to functional recovery plete sensorimotor paralysis of the lower extremities in which has been shown to improve walking speed in humans with par- EES restored the ability to stand and the ability to control tially retained motor functions after SCI23,24, but LT has not enabled step-like activity while side-lying or suspended vertically in recovery of stepping in those with complete loss of motor function a body-weight support system (BWS)4. Since then, dynamic in the lower extremity25,26. task-specific training in the presence of EES, termed multi- After initial outcomes of standing and intentional control of modal rehabilitation (MMR), was performed for 43 weeks and step-like leg movement using EES were observed, we set out to resulted in bilateral stepping on a treadmill, independent from determine whether the same subject could achieve independent trainer assistance or BWS. Additionally, MMR enabled inde- weight-bearing stepping during 43 weeks of MMR. MMR sessions pendent stepping over ground while using a front-wheeled were comprised of subject-driven attempts to perform EES-enabled walker with trainer assistance at the hips to maintain bal- activities while supine, side-lying, seated, standing, and stepping ance. Furthermore, MMR engaged sensorimotor networks to with trainer assistance and with BWS provided as needed. achieve dynamic performance of standing and stepping. To Clinical evaluations, performed at several time points through- our knowledge, this is the first report of independent stepping out the study with EES turned off, indicated no change in func- enabled by task-specific training in the presence of EES by a tion (Supplementary Fig. 1a,b). Transcranial magnetic stimulation human with complete loss of lower extremity sensorimotor (TMS) over the scalp elicited motor evoked potentials (MEPs) of function due to SCI. normal latencies in muscles innervated from above the SCI; how- Scientific evidence has shown that EES of lumbosacral spinal ever, MEPs were not present below the SCI (Supplementary Fig. 1c). circuitry can generate tonic and rhythmic patterns of motor activ- Tibial somatosensory evoked potentials (SSEPs) were not present in ity in spinalized animals5–11 and humans diagnosed with complete recordings over the scalp (Supplementary Fig. 1c). Over the course SCI12–15. More recently, EES in humans with complete loss of motor of the study, changes in the Modified Ashworth scale of spasticity function after SCI enabled volitional control of flexion and exten- were unremarkable (Supplementary Fig. 1d). Magnetic resonance sion leg movements, as well as standing1,2. However, EES-enabled imaging (MRI) of the spine showed intact tissue within the SCI site stepping after complete loss of lower extremity function due to SCI (Supplementary Fig. 2). Prolonged attempts to maximally contract has not been reported. muscles, with intention focused on increasing activity in either the Despite a clinical diagnosis of complete loss of sensorimotor left or right leg, resulted in bursts of muscle activity across agonist function after traumatic SCI, subfunctional neural connections and antagonist leg muscles that increased in amplitude and leg selec- likely remain intact across the injury (that is, discomplete SCI pro- tivity over time; however, functional movement was not achieved file)16–18. Spared connections across a discomplete SCI are not robust (Supplementary Fig. 3). Together, these results indicate a function- enough to generate clinically observable functions. However, they ally complete SCI with evidence of a discomplete SCI profile. are capable of modulating excitability of sublesional spinal senso- The use of a single program of active electrodes and stimula- rimotor networks19–22. tion parameters (voltage, pulse width, and frequency) enabled the 1Rehabilitation Medicine Research Center, Department of Physical Medicine and Rehabilitation, Mayo Clinic, Rochester, MN, USA. 2Department of Neurologic Surgery, Mayo Clinic, Rochester, MN, USA. 3Mayo Clinic Graduate School of Biomedical Sciences, Mayo Clinic, Rochester, MN, USA. 4Department of Biomedical Engineering, Mayo Clinic, Rochester, Minnesota, USA. 5Institute of Fundamental Medicine and Biology, Kazan Federal University, Kazan, Russia. 6Department of Integrative Biology and Physiology, University of California Los Angeles, Los Angeles, CA, USA. 7Department of Neurosurgery, Center for Neuroregeneration, Houston Methodist Research Institute, Houston, TX, USA. 8Pavlov Institute of Physiology, Russian Academy of Sciences, St. Petersburg, Russia. 9Department of Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN, USA. 10These authors contributed equally: Megan L. Gill, Peter J. Grahn.11These authors jointly directed: Kendall H. Lee, Kristin D. Zhao *e-mail: [email protected]; [email protected] NatURE MEDICINE | www.nature.com/naturemedicine LETTERS NATURE MEDICINE a beWeek 4 (MMR session 11) Week 43 (MMR session 112) Single-program EES Treadmill speed Interleaved EES Treadmill speed 0.35 m/s (40 Hz combined) 0.22 m/s 210 µs 30% BWS No BWS No trainer assist 210 s Trainer hip µ assist Trainer stance Arms on 25 Hz 210 µs 210 µs 25 Hz Trainer swing assist support bars for 5 V assist 20 Hz 20 Hz balance 3.3 V 3.7 V cfFiltered EMG RMS envelopes Filtered EMG RMS envelopes 1 s n = 10 steps 1 s n = 10 steps Two-program interleaved EES RF 100 µV RF 200 V RF 50 V RF 20 µV µ µ Left 210 s MH 200 µV Left MH MH µ MH 50 µV 200 µV 50 µV vGRF 450 N Stance Swing vGRF 450 N Stance Swing 1 s n = 10 steps 1 s n = 10 steps 20 Hz RF 100 V µ RF 20 µV RF 200 µV RF 50 µV Right MH 200 µV Right MH 50 µV MH 200 µV MH 25 µV vGRF 450 N Stance Swing vGRF 225 N Stance Swing dg Step cycle phase–specific muscle activity RF Step cycle phase–specific muscle activity RF 210 µs Left leg Right leg MH Left leg Right leg *** MH 2 n = 10 steps 2 n = 10 steps 2 n = 10 steps 2 n.s. *** n = 10 steps *** *** *** 20 Hz *** *** *** *** *** 1 1 1 1 *** Arbitrary units Arbitrary units Arbitrary units Arbitrary units 0 0 0 0 Stance Early Late Stance Early Late Stance Early Late Stance Early Late swing swing swing swing swing swing swing swing Fig. 1 | Progression of EES-enabled stepping performance on a treadmill. a, Schematic depicting single-program EES used during week 4 of MMR and two-program interleaved EES used during week 43 to enable stepping on a treadmill. Anodes, red squares; cathodes, black squares. b,e, EES settings and exemplary image from week 4 (b) and week 43 (e) depicting trainer assistance and BWS needed to achieve stepping. c,f, Filtered EMG and averaged RMS envelopes from the RF and MH synchronized to vGRF recordings under each foot at week 4 (c) and week 43 (f). vGRF, vertical ground reaction force. d,g, Differences in RF and MH activity during stance, early (first 50%) swing phase, and late (last 50%) swing phase are shown as means ( ± s.d) at week 4 (d) and week 43 (g). RMS envelopes and means were generated from 10 steps of each leg at week 4 and week 43. n.s., not significant; ***P < 0.001, two-tailed Mann–Whitney test. subject to control function in one leg at a voltage intensity that state of cocontraction (P =​ 0.14) and thereby impairing the ability was suboptimal for enabling function in the contralateral leg to independently extend the leg for stance phase load acceptance. (Fig. 1a). Over the course of MMR, we discovered that two inter- By week 43 of MMR, the use of two interleaved EES programs leaved EES programs enabled bilateral control of leg functions via improved the subject’s ability to control each leg in order to achieve independent adjustment of active electrodes and voltage intensities independent stepping on the treadmill at a speed of 0.22 m/s with- within each program. out trainer assistance or BWS (Fig. 1e). The subject maintained During treadmill stepping at week 4 of MMR, single-program upper body balance via hand placement on support bars to facilitate EES was applied while the subject attempted to step on a treadmill anterolateral weight shifting during gait (Fig. 1e and Supplementary moving at 0.35 m/s (Fig. 1b). In order to achieve EES-enabled tread- Video 1). For both legs, EMG showed bursts of RF activity during mill stepping, 30% BWS and trainer assistance at the hip, knee, and the stance phase, with inhibition occurring during the early part of ankle of each leg were required (Fig. 1b). Rectus femoris (RF) and the swing phase (Fig. 1f and Supplementary Fig. 5). MH activity was medial gastrocnemius (MG) activity, recorded by skin surface elec- characterized by tonic activation during stance and bursting activity tromyography (EMG), was characterized by bursts of activity dur- during swing phase with reciprocal inhibition of RF activity.
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