Segmental motor recovery after cervical spinal cord injury relates to density and integrity of corticospinal tract projections

Balbinot, Gustavo; Li, Guijin; Kalsi-Ryan, Sukhvinder; Abel, Rainer; Maier, Doris; Kalke, Yorck-Bernhard; Weidner, Norbert; Rupp, Rüdiger; Schubert, Martin; Curt, Armin; Zariffa, José

doi:10.1038/s41467-023-36390-7

Cited by 15 publications

(14 citation statements)

References 92 publications

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“…Findings revealed that single session ( Benavides et al, 2020 ) or multiple sessions ( Murray and Knikou, 2017 ) of AC-TSCS without carrier frequency can increase the MEPs amplitudes associated with upper extremity muscles along with improvement in voluntary muscle strength and upper limb motor function ( Murray and Knikou, 2017 ; Benavides et al, 2020 ). We believe that further understanding of the corticospinal mechanisms associated with recovery of upper limb motor function following TSCS intervention specifically targeted at the cervical enlargement is of significant importance after SCI as cervical spinal motorneurons receive extensive inputs from corticospinal tracts ( Balbinot et al, 2023 ). Emerging evidence also suggests that the neuroplasticity induced by spinal cord stimulation also depends on the number of residual supraspinal inputs survived, thereby limiting the effects of TSCS in situations involving a substantial loss of supraspinal axons ( Balaguer et al, 2023 ).…”

Section: Discussionmentioning

confidence: 99%

Modulations in neural pathways excitability post transcutaneous spinal cord stimulation among individuals with spinal cord injury: a systematic review

Tajali,

Balbinot,

Pakosh

et al. 2024

Front. Neurosci.

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IntroductionTranscutaneous spinal cord stimulation (TSCS), a non-invasive form of spinal cord stimulation, has been shown to improve motor function in individuals living with spinal cord injury (SCI). However, the effects of different types of TSCS currents including direct current (DC-TSCS), alternating current (AC-TSCS), and spinal paired stimulation on the excitability of neural pathways have not been systematically investigated. The objective of this systematic review was to determine the effects of TSCS on the excitability of neural pathways in adults with non-progressive SCI at any level.MethodsThe following databases were searched from their inception until June 2022: MEDLINE ALL, Embase, Web of Science, Cochrane Library, and clinical trials. A total of 4,431 abstracts were screened, and 23 articles were included.ResultsNineteen studies used TSCS at the thoracolumbar enlargement for lower limb rehabilitation (gait & balance) and four studies used cervical TSCS for upper limb rehabilitation. Sixteen studies measured spinal excitability by reporting different outcomes including Hoffmann reflex (H-reflex), flexion reflex excitability, spinal motor evoked potentials (SMEPs), cervicomedullay evoked potentials (CMEPs), and cutaneous-input-evoked muscle response. Seven studies measured corticospinal excitability using motor evoked potentials (MEPs) induced by transcranial magnetic stimulation (TMS), and one study measured somatosensory evoked potentials (SSEPs) following TSCS. Our findings indicated a decrease in the amplitude of H-reflex and long latency flexion reflex following AC-TSCS, alongside an increase in the amplitudes of SMEPs and CMEPs. Moreover, the application of the TSCS-TMS paired associative technique resulted in spinal reflex inhibition, manifested by reduced amplitudes in both the H-reflex and flexion reflex arc. In terms of corticospinal excitability, findings from 5 studies demonstrated an increase in the amplitude of MEPs linked to lower limb muscles following DC-TSCS, in addition to paired associative stimulation involving repetitive TMS on the brain and DC-TSCS on the spine. There was an observed improvement in the latency of SSEPs in a single study. Notably, the overall quality of evidence, assessed by the modified Downs and Black Quality assessment, was deemed poor.DiscussionThis review unveils the systematic evidence supporting the potential of TSCS in reshaping both spinal and supraspinal neuronal circuitries post-SCI. Yet, it underscores the critical necessity for more rigorous, high-quality investigations.

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Section: Discussionmentioning

confidence: 99%

Modulations in neural pathways excitability post transcutaneous spinal cord stimulation among individuals with spinal cord injury: a systematic review

Tajali,

Balbinot,

Pakosh

et al. 2024

Front. Neurosci.

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“…Rehabilitation following SCI is primarily composed of repetitive movements over long periods to facilitate motor recovery. Such training has been proved to be related to corticospinal tract projections [ 44 ] and neural adaptations in secondary tracts [ 45 ]. Despite the cortical effort required, the increased muscle activity in SCI patients may be supported by subcortical structures including the reticulospinal and rubrospinal tracts.…”

Section: Discussionmentioning

confidence: 99%

Characteristics of corticomuscular coupling during wheelchair Tai Chi in patients with spinal cord injury

Chen

et al. 2023

J NeuroEngineering Rehabil

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Background Wheelchair Tai Chi (WCTC) has been proved to have benefits for the brain and motor system of spinal cord injury (SCI) patients. However, the characteristics of corticomuscular coupling during WCTC are scarcely known. We aimed to investigate changes following SCI on corticomuscular coupling, and further compare the coupling characteristics of WCTC with aerobic exercise in SCI patients. Methods A total of 15 SCI patients and 25 healthy controls were recruited. The patients had to perform aerobic exercise and WCTC, while healthy controls needed to complete a set of WCTC. The participants accomplished the test following the tutorial video in a sitting position. The upper limb muscle activation was measured from upper trapezius, medial deltoid, biceps brachii and triceps brachii with surface electromyography. Cortical activity in the prefrontal cortex, premotor cortex, supplementary motor area and primary motor cortex was simultaneously collected by functional near-infrared spectroscopy. The functional connectivity, phase synchronization index and coherence values were then calculated and statistically analyzed. Results Compared to healthy controls, changes in functional connectivity and higher muscle activation were observed in the SCI group. There was no significant difference in phase synchronization between groups. Among patients, significantly higher coherence values between the left biceps brachii as well as the right triceps brachii and contralateral regions of interest were found during WCTC than during aerobic exercise. Conclusion The patients may compensate for the lack of corticomuscular coupling by enhancing muscle activation. This study demonstrated the potential and advantages of WCTC in eliciting corticomuscular coupling, which may optimize rehabilitation following SCI.

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“…Anatomical studies have long reported some continuity across the injured segment in at least half of the examined clinically motor complete SCI cases [5,6]. A recent retrospective analysis using the European Multicenter Study about Spinal Cord Injury dataset reported that about 14% of individuals with present motor evoked potentials (indicating preserved connections traversing the injury zone) were sensorimotor complete cases [7].…”

Section: Introductionmentioning

confidence: 99%

A computational model of surface electromyography signal alterations after spinal cord injury

Li,

Balbinot,

Furlan

et al. 2023

J. Neural Eng.

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Spinal cord injury (SCI) can cause significant impairment and disability with an impact on the quality of life for individuals with SCI and their caregivers. Surface electromyography (sEMG) is a sensitive and non-invasive technique to measure muscle activity and has demonstrated great potential in capturing neuromuscular changes resulting from SCI. The mechanisms of the sEMG signal characteristic changes due to SCI are multi-faceted and difficult to study in vivo. In this study, we utilized well-established computational models to characterize changes in sEMG signal after SCI and identify sEMG features that are sensitive and specific to different aspects of the SCI. Starting from existing models for motor neuron pool organization and motor unit action potential generation for healthy neuromuscular systems, we implemented scenarios to model damages to upper motor neurons, lower motor neurons, and the number of muscle fibers within each motor unit. After simulating sEMG signals from each scenario, we extracted time and frequency domain features and investigated the impact of SCI disruptions on sEMG features using the Kendall Rank Correlation analysis. The results indicate that commonly used amplitude-based sEMG features (such as mean absolute values and root mean square) cannot differentiate between injury scenarios, but a broader set of features (including autoregression and cepstrum coefficients) provides greater specificity to the type of damage present. We introduce a novel approach to mechanistically relate sEMG features (often underused in SCI research) to different types of neuromuscular alterations that may occur after SCI. This work contributes to the further understanding and utilization of sEMG in clinical applications, which will ultimately improve patient outcomes after SCI.

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Segmental motor recovery after cervical spinal cord injury relates to density and integrity of corticospinal tract projections

Cited by 15 publications

References 92 publications

Modulations in neural pathways excitability post transcutaneous spinal cord stimulation among individuals with spinal cord injury: a systematic review

Modulations in neural pathways excitability post transcutaneous spinal cord stimulation among individuals with spinal cord injury: a systematic review

Characteristics of corticomuscular coupling during wheelchair Tai Chi in patients with spinal cord injury

A computational model of surface electromyography signal alterations after spinal cord injury

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