Impaired corticomuscular and interhemispheric cortical beta oscillation coupling in amyotrophic lateral sclerosis

Malcolm Proudfoot, Freek van Ede, Andrew Quinn, Giles L. Colclough, Joanne Wuu, Kevin Talbot, Michael Benatar, Mark W. Woolrich, Anna C. Nobre*, Martin R. Turner

*Corresponding author for this work

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

Objectives: The neural activity of the primary motor cortex is variably synchronised with contralateral peripheral electromyographic signals, which is thought to facilitate long-range communication through the motor system. Such corticomuscular coherence (CMC) is typically observed in the beta-band (15–30 Hz) range during steady force production. We aimed to measure pathological alteration to CMC resulting from ALS. Methods: CMC was appraised during a forearm grip task in 17 ALS patients contrasted against age-matched healthy controls. An exploratory comparison with a group of asymptomatic ALS gene carriers and neuropathy disease mimics was also undertaken. Neural signals were acquired by whole-head magnetoencephalography and localised via structural MRI to the motor cortices. Results: During light voluntary muscular contraction, beta-band CMC was significantly reduced in ALS patients compared to healthy controls. Propagation of motoric beta rhythms across the cortical hemispheres was also shown to be impaired in ALS patients. CMC was preserved in the asymptomatic gene carrier and did not distinguish ALS patients from neuropathy mimics. Conclusion: Functional connectivity metrics reveal an ALS-related decrease in both corticomuscular and interhemispheric communication during bilateral grip force production. Significance: MEG-derived beta oscillation coupling may be a potential biomarker of motor system dysfunction in ALS, against which to measure future therapeutic efficacy.

Original languageEnglish
Pages (from-to)1479-1489
Number of pages11
JournalClinical Neurophysiology
Volume129
Issue number7
DOIs
Publication statusPublished - Jul 2018
Externally publishedYes

Funding

MP was supported by a Wellcome Trust Research Training Fellowship (104369/Z/14/Z). FvE was supported by a Marie Skłodowska-Curie Individual Fellowship from the European Commission (ACCESS2WM). GLC was supported by the Research Councils UK Digital Economy Programme (EP/G036861/1). ACN was supported by a Wellcome Trust Senior Investigator Award (104571/ Z/14/Z). MWW and AQ were supported by the Medical Research Council UK MEG Partnership Grant (MR/K005464/1). MRT was supported by a Medical Research Council and Motor Neurone Disease Association Lady Edith Wolfson Senior Clinical Fellowship (MR/K01014X/1). MB and JW were supported by the Muscular Dystrophy Association (4365 and 172123), ALS Association (2015), Kimmelman Estate and ALS Recovery Fund. Further support for the study was received from the National Institute for Health Research Oxford Biomedical Research Centre based at Oxford University Hospitals NHS Foundation Trust.

FundersFunder number
Marie Skłodowska-Curie
Medical Research Council UK MEGMR/K005464/1
Motor Neurone Disease Association Lady Edith Wolfson Senior Clinical Fellowship
National Institute for Health Research Oxford Biomedical Research Centre
Research Councils UK Digital Economy Programme104571/ Z/14/Z, EP/G036861/1
Amyotrophic Lateral Sclerosis Association
Muscular Dystrophy Association172123
Wellcome Trust104369/Z/14/Z
Horizon 2020 Framework Programme655374
Medical Research CouncilMR/K01014X/1
European CommissionACCESS2WM

    Keywords

    • ALS
    • Biomarker
    • Coherence
    • MEG

    Fingerprint

    Dive into the research topics of 'Impaired corticomuscular and interhemispheric cortical beta oscillation coupling in amyotrophic lateral sclerosis'. Together they form a unique fingerprint.

    Cite this