Amyotrophic lateral sclerosis affects cortical and subcortical activity underlying motor inhibition and action monitoring

Mohammadi, Bahram; Kollewe, Katja; Cole, David M.; Fellbrich, Anja; Heldmann, Marcus; Samii, Amir; Dengler, Reinhard; Petri, Susanne; Münte, Thomas F.; Krämer, Ulrike M.

doi:10.1002/hbm.22814

Cited by 27 publications

(26 citation statements)

References 48 publications

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“…Given evidence for prefrontal control over posterior negativity amplitudes, these data might indicate a task-driven “sharpening” of visual processing (Rustamov et al, 2014 ), putatively in the service of functional compensation (Reuter-Lorenz and Cappell, 2008 ) and probably through additional mechanisms recruited in frontoparietal attention networks (Ptak, 2012 ; Vossel et al, 2014 ). If so, the present posterior negativity finding is in line with multiple neuroimaging studies that used various paradigms, and that demonstrated a diversity of patterns of enhanced cortical activity in ALS patients (Kew et al, 1993b ; Schoenfeld et al, 2005 ; Han and Ma, 2006 ; Stanton et al, 2006 ; Lulé et al, 2007 ; Dounaud et al, 2011 ; Goldstein et al, 2011 ; Mohammadi et al, 2011 , 2015 ; Cosottini et al, 2012 ; Witiuk et al, 2014 ; see Turner et al, 2012 , for review).…”

Section: Discussionsupporting

confidence: 85%

Executive Dysfunctions and Event-Related Brain Potentials in Patients with Amyotrophic Lateral Sclerosis

Seer

Fürkötter

Vogts

et al. 2015

Front. Aging Neurosci.

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A growing body of evidence implies psychological disturbances in amyotrophic lateral sclerosis (ALS). Specifically, executive dysfunctions occur in up to 50% of ALS patients. The recently shown presence of cytoplasmic aggregates (TDP-43) in ALS patients and in patients with behavioral variants of frontotemporal dementia suggests that these two disease entities form the extremes of a spectrum. The present study aimed at investigating behavioral and electrophysiological indices of conflict processing in patients with ALS. A non-verbal variant of the flanker task demanded two-choice responses to target stimuli that were surrounded by flanker stimuli which either primed the correct response or the alternative response (the latter case representing the conflict situation). Behavioral performance, event-related potentials (ERP), and lateralized readiness potentials (LRP) were analyzed in 21 ALS patients and 20 controls. In addition, relations between these measures and executive dysfunctions were examined. ALS patients performed the flanker task normally, indicating preserved conflict processing. In similar vein, ERP and LRP indices of conflict processing did not differ between groups. However, ALS patients showed enhanced posterior negative ERP waveform deflections, possibly indicating increased modulation of visual processing by frontoparietal networks in ALS. We also found that the presence of executive dysfunctions was associated with more error-prone behavior and enhanced LRP amplitudes in ALS patients, pointing to a prefrontal pathogenesis of executive dysfunctions and to a potential link between prefrontal and motor cortical functional dysregulation in ALS, respectively.

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Section: Discussionsupporting

confidence: 85%

Executive Dysfunctions and Event-Related Brain Potentials in Patients with Amyotrophic Lateral Sclerosis

Seer

Fürkötter

Vogts

et al. 2015

Front. Aging Neurosci.

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“…Although cognitively impaired ALS patients are predictably under‐represented in demanding functional neuroimaging tasks, comparatively reduced activation in the dorsolateral prefrontal cortex has been demonstrated [Witiuk et al, 2014], while other frontal regions reveal increased activation during inhibition of prepared manual movements [Mohammadi et al, 2015]. The present finding of abnormal beta power in AGCs during successful inhibition was limited to posterior cortical regions in the context of task‐induced inferior and pre‐frontal activity.…”

Section: Discussionmentioning

confidence: 50%

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

Proudfoot

Rohenkohl

Quinn

et al. 2016

Human Brain Mapping

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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.

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“…Inhibition was low [130]. Activation of the ipsilateral sensorimotor cortex was possibly linked to a compensatory mechanism in ALS [133].…”

Section: Resultsmentioning

confidence: 99%

The value of magnetic resonance imaging as a biomarker for amyotrophic lateral sclerosis: a systematic review

et al. 2016

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BackgroundAmyotrophic lateral sclerosis (ALS) is a fatal, rapidly progressive neurodegenerative disease that mainly affects the motor system. A number of potentially neuroprotective and neurorestorative disease-modifying drugs are currently in clinical development. At present, the evaluation of a drug’s clinical efficacy in ALS is based on the ALS Functional Rating Scale Revised, motor tests and survival. However, these endpoints are general, variable and late-stage measures of the ALS disease process and thus require the long-term assessment of large cohorts. Hence, there is a need for more sensitive radiological biomarkers. Various sequences for magnetic resonance imaging (MRI) of the brain and spinal cord have may have value as surrogate biomarkers for use in future clinical trials. Here, we review the MRI findings in ALS, their clinical correlations, and their limitations and potential role as biomarkers.MethodsThe PubMed database was screened to identify studies using MRI in ALS. We included general MRI studies with a control group and an ALS group and longitudinal studies even if a control group was lacking.ResultsA total of 116 studies were analysed with MRI data and clinical correlations. The most disease-sensitive MRI patterns are in motor regions but the brain is more broadly affected.ConclusionDespite the existing MRI biomarkers, there is a need for large cohorts with long term MRI and clinical follow-up. MRI assessment could be improved by standardized MRI protocols with multicentre studies.

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Amyotrophic lateral sclerosis affects cortical and subcortical activity underlying motor inhibition and action monitoring

Cited by 27 publications

References 48 publications

Executive Dysfunctions and Event-Related Brain Potentials in Patients with Amyotrophic Lateral Sclerosis

Executive Dysfunctions and Event-Related Brain Potentials in Patients with Amyotrophic Lateral Sclerosis

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

The value of magnetic resonance imaging as a biomarker for amyotrophic lateral sclerosis: a systematic review

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