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

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. © 2016 Wiley Periodicals, Inc.

Aberrant interhemispheric homotopic functional and structural connectivity in amyotrophic lateral sclerosis

“…Additionally, neuropathological studies have shown prominent and consistent CC involvement in ALS, most abundant in the middle part 16 17. Neuroelectrophysiological studies such as TMS and MEG have also provided indirect evidence of impaired CC functioning by showing alterations of interhemispheric inhibition18 and cortical β-band oscillations 19. Based on these structural and functional alterations of CC, the present study complemented/extended these previous studies by showing a compromised interhemispheric neural connectivity.…”

Patterned functional network disruption in amyotrophic lateral sclerosis

“…The observed changes in spectral power are consistent with previously described θand α-band power decrease above the sensorimotor network (Bizovi car, Dreo, Koritnik, & Zidar, 2014;Nasseroleslami et al, 2019). Other studies in ALS have similarly identified decreased postmovement β-band power above motor cortices (Proudfoot et al, 2017;Riva et al, 2012), which is considered a reflection of idling and/or an active inhibition of the motor network (Cassim et al, 2001).…”

“…Note that the widespread patterns of increased co-modulation [amplitude envelope correlation (AEC)] are predominantly in the θand γ l -bands, while synchrony [imaginary coherence (iCoh)] patterns were predominantly in the δand β-bands. Other studies in ALS have similarly identified decreased postmovement β-band power above motor cortices (Proudfoot et al, 2017;Riva et al, 2012), which is considered a reflection of idling and/or an active inhibition of the motor network (Cassim et al, 2001). False discovery rate (FDR) was set to 10% (in each frequency band), yielding an estimated statistical power of 1-β = .96 and posterior probability of P 1 = .56 in the θ-band AEC and an estimated statistical power of 1-β = .89 and posterior probability of P 1 = .7 in the γ l -band AEC.…”

EEG functional network topology is associated with disability in patients with amyotrophic lateral sclerosis

“…Even though this latest finding seems in contrast with a recent MEG study30 that reported an intensified cortical beta desynchronization in ALS patients, other studies have not reported the same finding2831. Differences in protocol design, for example the use of different tasks, or resting-state data, or differences in characteristics of the patient population, may explain these differences across studies.…”