Altered cortical beta-band oscillations reflect motor system degeneration in amyotrophic lateral sclerosis.
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. © 2016 Wiley Periodicals, Inc.
Nuffield Department of Clinical Neurosciences, University of Oxford, United Kingdom.|Oxford Centre for Human Brain Activity, Department of Psychiatry, University of Oxford, United Kingdom.
Malcolm
0000-0002-0774-4366
M
Proudfoot
Oxford Centre for Human Brain Activity, Department of Psychiatry, University of Oxford, United Kingdom.
Gustavo
G
Rohenkohl
Oxford Centre for Human Brain Activity, Department of Psychiatry, University of Oxford, United Kingdom.
Andrew
A
Quinn
Oxford Centre for Human Brain Activity, Department of Psychiatry, University of Oxford, United Kingdom.
Giles L
0000-0003-1074-7186
GL
Colclough
Department of Neurology, Miller School of Medicine, University of Miami, Florida.
Joanne
J
Wuu
Nuffield Department of Clinical Neurosciences, University of Oxford, United Kingdom.
Kevin
K
Talbot
Oxford Centre for Human Brain Activity, Department of Psychiatry, University of Oxford, United Kingdom.
Mark W
MW
Woolrich
Department of Neurology, Miller School of Medicine, University of Miami, Florida.
Michael
M
Benatar
Oxford Centre for Human Brain Activity, Department of Psychiatry, University of Oxford, United Kingdom.
Anna C
AC
Nobre
Nuffield Department of Clinical Neurosciences, University of Oxford, United Kingdom.
Martin R
MR
Turner
D000368:Aged; D000690:Amyotrophic Lateral Sclerosis / Q000473:pathology* / Q000503:physiopathology*; D001611:Beta Rhythm / Q000502:physiology*; D001931:Brain Mapping; D003657:Decision Making; D005260:Female; D007839:Functional Laterality / Q000502:physiology; D006801:Humans; D007266:Inhibition, Psychological; D015225:Magnetoencephalography; D008297:Male; D008875:Middle Aged; D009043:Motor Activity / Q000502:physiology*; D009044:Motor Cortex / Q000503:physiopathology*; D016472:Motor Neuron Disease / Q000473:pathology / Q000503:physiopathology; D009483:Neuropsychological Tests; D011930:Reaction Time; D012720:Severity of Illness Index
biomarker; inhibition; magnetoencephalography; motor neurone disease; neuroimaging; neurophysiology