Electrical spinal cord stimulation must preserve proprioception to enable locomotion in humans with spinal cord injury

Emanuele Formento, Karen Minassian, Fabien Wagner, Jean Baptiste Mignardot, Camille G. Le Goff-Mignardot, Andreas Rowald, Jocelyne Bloch, Silvestro Micera, Marco Capogrosso, Gregoire Courtine
Nat Neurosci. 2018-10-31; 21(12): 1728-1741
DOI: 10.1038/s41593-018-0262-6

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1. Nat Neurosci. 2018 Dec;21(12):1728-1741. doi: 10.1038/s41593-018-0262-6. Epub
2018 Oct 31.

Electrical spinal cord stimulation must preserve proprioception to enable
locomotion in humans with spinal cord injury.

Formento E(1)(2), Minassian K(2), Wagner F(2), Mignardot JB(2), Le Goff-Mignardot
CG(2), Rowald A(2)(3), Bloch J(4), Micera S(1)(5), Capogrosso M(3), Courtine
G(6)(7).

Author information:
(1)Bertarelli Foundation Chair in Translational NeuroEngineering, Institute of
Bioengineering, Swiss Federal Institute of Technology (EPFL), Lausanne,
Switzerland.
(2)Center for Neuroprosthetics and Brain Mind Institute, School of Life Sciences,
Swiss Federal Institute of Technology (EPFL), Lausanne, Switzerland.
(3)Department of Medicine, Faculty of Sciences, University of Fribourg, Fribourg,
Switzerland.
(4)Department of Neurosurgery, University Hospital of Lausanne (CHUV), Lausanne,
Switzerland.
(5)Neural Engineering Area, Institute of Biorobotics, Scuola Superiore Sant’Anna,
Pisa, Italy.
(6)Center for Neuroprosthetics and Brain Mind Institute, School of Life Sciences,
Swiss Federal Institute of Technology (EPFL), Lausanne, Switzerland.
.
(7)Department of Neurosurgery, University Hospital of Lausanne (CHUV), Lausanne,
Switzerland. .

Comment in
Nat Neurosci. 2018 Dec;21(12):1647-1648.
Nat Rev Neurosci. 2019 Jan;20(1):1.

Epidural electrical stimulation (EES) of the spinal cord restores locomotion in
animal models of spinal cord injury but is less effective in humans. Here we
hypothesized that this interspecies discrepancy is due to interference between
EES and proprioceptive information in humans. Computational simulations and
preclinical and clinical experiments reveal that EES blocks a significant amount
of proprioceptive input in humans, but not in rats. This transient
deafferentation prevents modulation of reciprocal inhibitory networks involved in
locomotion and reduces or abolishes the conscious perception of leg position.
Consequently, continuous EES can only facilitate locomotion within a narrow range
of stimulation parameters and is unable to provide meaningful locomotor
improvements in humans without rehabilitation. Simulations showed that burst
stimulation and spatiotemporal stimulation profiles mitigate the cancellation of
proprioceptive information, enabling robust control over motor neuron activity.
This demonstrates the importance of stimulation protocols that preserve
proprioceptive information to facilitate walking with EES.

DOI: 10.1038/s41593-018-0262-6
PMCID: PMC6268129
PMID: 30382196 [Indexed for MEDLINE]


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