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

doi:10.1016/j.clinph.2018.03.019

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

Psychology

Research output: Contribution to journal › Article › peer-review

22 Citations (Scopus)

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 language	English
Pages (from-to)	1479-1489
Number of pages	11
Journal	Clinical Neurophysiology
Volume	129
Issue number	7
DOIs	https://doi.org/10.1016/j.clinph.2018.03.019
Publication status	Published - Jul 2018

Bibliographical note

Funding Information:
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.

Publisher Copyright:
© 2018 International Federation of Clinical Neurophysiology

Keywords

ALS
Biomarker
Coherence
MEG

ASJC Scopus subject areas

Sensory Systems
Neurology
Clinical Neurology
Physiology (medical)

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10.1016/j.clinph.2018.03.019

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title = "Impaired corticomuscular and interhemispheric cortical beta oscillation coupling in amyotrophic lateral sclerosis",

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.",

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author = "Malcolm Proudfoot and {van Ede}, Freek and Andrew Quinn and Colclough, {Giles L.} and Joanne Wuu and Kevin Talbot and Michael Benatar and Woolrich, {Mark W.} and Nobre, {Anna C.} and Turner, {Martin R.}",

note = "Funding Information: MP was supported by a Wellcome Trust Research Training Fellowship (104369/Z/14/Z). FvE was supported by a Marie Sk{\l}odowska-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. Publisher Copyright: {\textcopyright} 2018 International Federation of Clinical Neurophysiology",

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AU - Proudfoot, Malcolm

AU - van Ede, Freek

AU - Quinn, Andrew

AU - Colclough, Giles L.

AU - Wuu, Joanne

AU - Talbot, Kevin

AU - Benatar, Michael

AU - Woolrich, Mark W.

AU - Nobre, Anna C.

AU - Turner, Martin R.

N1 - Funding Information: 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. Publisher Copyright: © 2018 International Federation of Clinical Neurophysiology

PY - 2018/7

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N2 - 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.

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

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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