Altered cortical beta-band oscillations reflect motor system degeneration in amyotrophic lateral sclerosis

Malcolm Proudfoot, Gustavo Rohenkohl, Andrew Quinn, Giles L. Colclough, Joanne Wuu, Kevin Talbot, Mark W. Woolrich, Michael G Benatar, Anna C. Nobre, Martin R. Turner

Research output: Contribution to journalArticle

19 Citations (Scopus)

Abstract

Continuous rhythmic neuronal oscillations underpin local and regional cortical communication. The impact of the motor system neurodegenerative syndrome amyotrophic lateral sclerosis (ALS) on the neuronal oscillations subserving movement might therefore serve as a sensitive marker of disease activity. Movement preparation and execution are consistently associated with modulations to neuronal oscillation beta (15–30 Hz) power. Cortical beta-band oscillations were measured using magnetoencephalography (MEG) during preparation for, execution, and completion of a visually cued, lateralized motor task that included movement inhibition trials. Eleven “classical” ALS patients, 9 with the primary lateral sclerosis (PLS) phenotype, and 12 asymptomatic carriers of ALS-associated gene mutations were compared with age-similar healthy control groups. Augmented beta desynchronization was observed in both contra- and ipsilateral motor cortices of ALS patients during motor preparation. Movement execution coincided with excess beta desynchronization in asymptomatic mutation carriers. Movement completion was followed by a slowed rebound of beta power in all symptomatic patients, further reflected in delayed hemispheric lateralization for beta rebound in the PLS group. This may correspond to the particular involvement of interhemispheric fibers of the corpus callosum previously demonstrated in diffusion tensor imaging studies. We conclude that the ALS spectrum is characterized by intensified cortical beta desynchronization followed by delayed rebound, concordant with a broader concept of cortical hyperexcitability, possibly through loss of inhibitory interneuronal influences. MEG may potentially detect cortical dysfunction prior to the development of overt symptoms, and thus be able to contribute to the assessment of future neuroprotective strategies. Hum Brain Mapp 38:237–254, 2017.

Original languageEnglish (US)
Pages (from-to)237-254
Number of pages18
JournalHuman Brain Mapping
Volume38
Issue number1
DOIs
StatePublished - Jan 1 2017

Fingerprint

Amyotrophic Lateral Sclerosis
Magnetoencephalography
Motor Neuron Disease
Cortical Synchronization
Mutation
Diffusion Tensor Imaging
Corpus Callosum
Motor Cortex
Communication
Phenotype
Control Groups
Brain
Genes
Power (Psychology)

Keywords

  • biomarker
  • inhibition
  • magnetoencephalography
  • motor neurone disease
  • neuroimaging
  • neurophysiology

ASJC Scopus subject areas

  • Anatomy
  • Radiological and Ultrasound Technology
  • Radiology Nuclear Medicine and imaging
  • Neurology
  • Clinical Neurology

Cite this

Proudfoot, M., Rohenkohl, G., Quinn, A., Colclough, G. L., Wuu, J., Talbot, K., ... Turner, M. R. (2017). Altered cortical beta-band oscillations reflect motor system degeneration in amyotrophic lateral sclerosis. Human Brain Mapping, 38(1), 237-254. https://doi.org/10.1002/hbm.23357

Altered cortical beta-band oscillations reflect motor system degeneration in amyotrophic lateral sclerosis. / Proudfoot, Malcolm; Rohenkohl, Gustavo; Quinn, Andrew; Colclough, Giles L.; Wuu, Joanne; Talbot, Kevin; Woolrich, Mark W.; Benatar, Michael G; Nobre, Anna C.; Turner, Martin R.

In: Human Brain Mapping, Vol. 38, No. 1, 01.01.2017, p. 237-254.

Research output: Contribution to journalArticle

Proudfoot, M, Rohenkohl, G, Quinn, A, Colclough, GL, Wuu, J, Talbot, K, Woolrich, MW, Benatar, MG, Nobre, AC & Turner, MR 2017, 'Altered cortical beta-band oscillations reflect motor system degeneration in amyotrophic lateral sclerosis', Human Brain Mapping, vol. 38, no. 1, pp. 237-254. https://doi.org/10.1002/hbm.23357
Proudfoot, Malcolm ; Rohenkohl, Gustavo ; Quinn, Andrew ; Colclough, Giles L. ; Wuu, Joanne ; Talbot, Kevin ; Woolrich, Mark W. ; Benatar, Michael G ; Nobre, Anna C. ; Turner, Martin R. / Altered cortical beta-band oscillations reflect motor system degeneration in amyotrophic lateral sclerosis. In: Human Brain Mapping. 2017 ; Vol. 38, No. 1. pp. 237-254.
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