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Spatiotemporal neuromodulation therapies engaging muscle synergies improve motor control after spinal cord injury.

ABSTRACT: Electrical neuromodulation of lumbar segments improves motor control after spinal cord injury in animal models and humans. However, the physiological principles underlying the effect of this intervention remain poorly understood, which has limited the therapeutic approach to continuous stimulation applied to restricted spinal cord locations. Here we developed stimulation protocols that reproduce the natural dynamics of motoneuron activation during locomotion. For this, we computed the spatiotemporal activation pattern of muscle synergies during locomotion in healthy rats. Computer simulations identified optimal electrode locations to target each synergy through the recruitment of proprioceptive feedback circuits. This framework steered the design of spatially selective spinal implants and real-time control software that modulate extensor and flexor synergies with precise temporal resolution. Spatiotemporal neuromodulation therapies improved gait quality, weight-bearing capacity, endurance and skilled locomotion in several rodent models of spinal cord injury. These new concepts are directly translatable to strategies to improve motor control in humans.

SUBMITTER: Wenger N

PROVIDER: S-EPMC5061079 | biostudies-literature | 2016 Feb

REPOSITORIES: biostudies-literature

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Spatiotemporal neuromodulation therapies engaging muscle synergies improve motor control after spinal cord injury.

Wenger Nikolaus N Moraud Eduardo Martin EM Gandar Jerome J Musienko Pavel P Capogrosso Marco M Baud Laetitia L Le Goff Camille G CG Barraud Quentin Q Pavlova Natalia N Dominici Nadia N Minev Ivan R IR Asboth Leonie L Hirsch Arthur A Duis Simone S Kreider Julie J Mortera Andrea A Haverbeck Oliver O Kraus Silvio S Schmitz Felix F DiGiovanna Jack J van den Brand Rubia R Bloch Jocelyne J Detemple Peter P Lacour Stéphanie P SP Bézard Erwan E Micera Silvestro S Courtine Grégoire G

Nature medicine 20160118 2

Electrical neuromodulation of lumbar segments improves motor control after spinal cord injury in animal models and humans. However, the physiological principles underlying the effect of this intervention remain poorly understood, which has limited the therapeutic approach to continuous stimulation applied to restricted spinal cord locations. Here we developed stimulation protocols that reproduce the natural dynamics of motoneuron activation during locomotion. For this, we computed the spatiotemp ...[more]

PMID: 26779815

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Project description:An important strategy for promoting voluntary movements after motor system injury is to harness activity-dependent corticospinal tract (CST) plasticity. We combine forelimb motor cortex (M1) activation with co-activation of its cervical spinal targets in rats to promote CST sprouting and skilled limb movement after pyramidal tract lesion (PTX). We used a two-step experimental design in which we first established the optimal combined stimulation protocol in intact rats and then used the optimal protocol in injured animals to promote CST repair and motor recovery. M1 was activated epidurally using an electrical analog of intermittent theta burst stimulation (iTBS). The cervical spinal cord was co-activated by trans-spinal direct current stimulation (tsDCS) that was targeted to the cervical enlargement, simulated from finite element method. In intact rats, forelimb motor evoked potentials (MEPs) were strongly facilitated during iTBS and for 10 min after cessation of stimulation. Cathodal, not anodal, tsDCS alone facilitated MEPs and also produced a facilitatory aftereffect that peaked at 10 min. Combined iTBS and cathodal tsDCS (c-tsDCS) produced further MEP enhancement during stimulation, but without further aftereffect enhancement. Correlations between forelimb M1 local field potentials and forelimb electromyogram (EMG) during locomotion increased after electrical iTBS alone and further increased with combined stimulation (iTBS+c-tsDCS). This optimized combined stimulation was then used to promote function after PTX because it enhanced functional connections between M1 and spinal circuits and greater M1 engagement in muscle contraction than either stimulation alone. Daily application of combined M1 iTBS on the intact side and c-tsDCS after PTX (10 days, 27 min/day) significantly restored skilled movements during horizontal ladder walking. Stimulation produced a 5.4-fold increase in spared ipsilateral CST terminations. Combined neuromodulation achieves optimal motor recovery and substantial CST outgrowth with only 27 min of daily stimulation compared with 6h, as in our prior study, making it a potential therapy for humans with spinal cord injury.

Project description:"Yips" are involuntary movements that interfere with the automatic execution of sports movements. However, how the coordination among the various muscles necessary for sports movements is impaired in athletes with yips remains to be fully understood. This study aimed to assess whether muscle synergy analysis through non-negative matrix factorization (NMF) could identify impaired spatiotemporal muscle coordination in baseball players with throwing yips. Twenty-two college baseball players, including 12 with and 10 without yips symptoms participated in the study. Electromyographic activity was recorded from 13 ipsilateral upper extremity muscles during full-effort throwing. Muscle synergies were extracted through NMF. Cluster analysis was conducted to identify any common spatiotemporal patterns of muscle synergies in players with yips. Whether individual players with yips showed deviations in spatiotemporal patterns of muscle synergies compared with control players was also investigated. Four muscle synergies were extracted for each player, but none were specific to the yips group. However, a more detailed analysis of individual players revealed that two of the three players who presented dystonic symptoms during the experiment exhibited specific patterns that differed from those in control players. By contrast, each player whose symptoms were not reproduced during the experiment presented spatiotemporal patterns of muscle synergies similar to those of the control group. The results of this study indicate no common spatiotemporal pattern of muscle synergies specific to the yips group. Furthermore, these results suggest that the spatiotemporal pattern of muscle synergies in baseball throwing motion is not impaired in situations where symptoms are not reproduced even if the players have yips symptoms. However, muscle synergy analysis can identify the characteristics of muscle coordination of players who exhibit dystonic movements. These findings can be useful in developing personalized therapeutic strategies based on individual characteristics of yips symptoms.

Dataset Information

Spatiotemporal neuromodulation therapies engaging muscle synergies improve motor control after spinal cord injury.

Publications

Spatiotemporal neuromodulation therapies engaging muscle synergies improve motor control after spinal cord injury.

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