Case Report: Event-Related Desynchronization Observed During Volitional Swallow by Electroencephalography Recordings in ALS Patients With Dysphagia

Dysphagia is a severe disability affecting daily life in patients with amyotrophic lateral sclerosis (ALS). It is caused by degeneration of both the bulbar motor neurons and cortical motoneurons projecting to the oropharyngeal areas. A previous report showed decreased event-related desynchronization (ERD) in the medial sensorimotor areas in ALS dysphagic patients. In the process of degeneration, brain reorganization may also be induced in other areas than the sensorimotor cortices. Furthermore, ALS patients with dysphagia often show a longer duration of swallowing. However, there have been no reports on brain activity in other cortical areas and the time course of brain activity during prolonged swallowing in these patients. In this case report, we investigated the distribution and the time course of ERD and corticomuscular coherence (CMC) in the beta (15–25 Hz) frequency band during volitional swallow using electroencephalography (EEG) in two patients with ALS. Case 1 (a 71-year-old man) was diagnosed 2 years before the evaluation. His first symptom was muscle weakness in the right hand; 5 months later, dysphagia developed and exacerbated. Since his dietary intake decreased, he was given an implantable venous access port. Case 2 (a 64-year-old woman) was diagnosed 1 year before the evaluation. Her first symptom was open-nasal voice and dysarthria; 3 months later, dysphagia developed and exacerbated. She was given a percutaneous endoscopic gastrostomy. EEG recordings were performed during volitional swallowing, and the ERD was calculated. The average swallow durations were 7.6 ± 3.0 s in Case 1 and 8.3 ± 2.9 s in Case 2. The significant ERD was localized in the prefrontal and premotor areas and lasted from a few seconds after the initiation of swallowing to the end in Case 1. The ERD was localized in the lateral sensorimotor areas only at the initiation of swallowing in Case 2. CMC was not observed in either case. These results suggest that compensatory processes for cortical motor outputs might depend on individual patients and that a new therapeutic approach using ERD should be developed according to the individuality of ALS patients with dysphagia.

[1]  T. Mima,et al.  Event-Related Desynchronization and Corticomuscular Coherence Observed During Volitional Swallow by Electroencephalography Recordings in Humans , 2021, Frontiers in Human Neuroscience.

[2]  Yun Qin,et al.  Enhancement of Event-Related Desynchronization in Motor Imagery Based on Transcranial Electrical Stimulation , 2021, Frontiers in Human Neuroscience.

[3]  Xiaokang Shu,et al.  Electroencephalography Mu Rhythm Changes and Decreased Spasticity After Repetitive Peripheral Magnetic Stimulation in Patients Following Stroke , 2020, Frontiers in Neurology.

[4]  F. Zappasodi,et al.  Pre-stimulus EEG Microstates Correlate With Anticipatory Alpha Desynchronization , 2020, Frontiers in Human Neuroscience.

[5]  J. Ranjeva,et al.  Structural Connectivity Alterations in Amyotrophic Lateral Sclerosis: A Graph Theory Based Imaging Study , 2019, Front. Neurosci..

[6]  Le Li,et al.  Combining Movement-Related Cortical Potentials and Event-Related Desynchronization to Study Movement Preparation and Execution , 2018, Front. Neurol..

[7]  Giles L. Colclough,et al.  Impaired corticomuscular and interhemispheric cortical beta oscillation coupling in amyotrophic lateral sclerosis , 2018, Clinical Neurophysiology.

[8]  James L. Coyle,et al.  Influence of attention and bolus volume on brain organization during swallowing , 2017, Brain Structure and Function.

[9]  C. Pantev,et al.  Randomized trial of transcranial direct current stimulation for poststroke dysphagia , 2018, Annals of neurology.

[10]  Kotoe Sakihara,et al.  Mu rhythm desynchronization by tongue thrust observation , 2015, Front. Hum. Neurosci..

[11]  Christo Pantev,et al.  Pharyngeal electrical stimulation can modulate swallowing in cortical processing and behavior — Magnetoencephalographic evidence , 2015, NeuroImage.

[12]  Akio Kimura,et al.  Brain-computer interface with somatosensory feedback improves functional recovery from severe hemiplegia due to chronic stroke , 2014, Front. Neuroeng..

[13]  C. Pantev,et al.  Altered Cortical Swallowing Processing in Patients with Functional Dysphagia: A Preliminary Study , 2014, PloS one.

[14]  L. Cohen,et al.  Brain–machine interface in chronic stroke rehabilitation: A controlled study , 2013, Annals of neurology.

[15]  Olaf Steinsträter,et al.  Cortical Processing of Swallowing in ALS Patients with Progressive Dysphagia – A Magnetoencephalographic Study , 2011, PloS one.

[16]  S. Lui,et al.  Functional magnetic resonance imaging study on dysphagia after unilateral hemispheric stroke: a preliminary study , 2009, Journal of Neurology, Neurosurgery & Psychiatry.

[17]  S. Hamdy,et al.  Cortical input in control of swallowing , 2009, Current opinion in otolaryngology & head and neck surgery.

[18]  Christo Pantev,et al.  Cortical compensation associated with dysphagia caused by selective degeneration of bulbar motor neurons , 2009, Human brain mapping.

[19]  Q. Gong,et al.  Structural and functional changes mapped in the brains of amyotrophic lateral sclerosis patients with/without dysphagia: A pilot study , 2009, Amyotrophic lateral sclerosis : official publication of the World Federation of Neurology Research Group on Motor Neuron Diseases.

[20]  David J Mikulis,et al.  Sensorimotor Cortical Plasticity During Recovery Following Spinal Cord Injury: A Longitudinal fMRI Study , 2007, Neurorehabilitation and neural repair.

[21]  M. Vaiman.  Standardization of surface electromyography utilized to evaluate patients with dysphagia , 2007, Head & face medicine.

[22]  Pavel Jurák,et al.  Intracerebral recording of cortical activity related to self-paced voluntary movements: a Bereitschaftspotential and event-related desynchronization/synchronization. SEEG study , 2006, Experimental Brain Research.

[23]  L. Cohen,et al.  Mechanisms underlying recovery of motor function after stroke , 2005, Postgraduate Medical Journal.

[24]  L. Cohen,et al.  Mechanisms underlying recovery of motor function after stroke. , 2004, Postgraduate medical journal.

[25]  Alan J Thompson,et al.  The influence of time after stroke on brain activations during a motor task , 2004, Annals of neurology.

[26]  Thomas Elbert,et al.  Reorganization of Human Cerebral Cortex: The Range of Changes Following Use and Injury , 2004, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[27]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[28]  I. Aydogdu,et al.  Neurophysiology of swallowing , 2003, Clinical Neurophysiology.

[29]  Bill Faw.  Pre-frontal executive committee for perception, working memory, attention, long-term memory, motor control, and thinking: A tutorial review , 2003, Consciousness and Cognition.

[30]  Erkki Oja,et al.  Independent component analysis: algorithms and applications , 2000, Neural Networks.

[31]  F. Smulders,et al.  Recording of Swallowing Events Using Electromyography as a Non-invasive Measurement of Salivation , 1999, Appetite.

[32]  F. L. D. Silva,et al.  Event-related EEG/MEG synchronization and desynchronization: basic principles , 1999, Clinical Neurophysiology.

[33]  M. Hallett,et al.  Electroencephalographic analysis of cortico-muscular coherence: reference effect, volume conduction and generator mechanism , 1999, Clinical Neurophysiology.

[34]  M. Hallett,et al.  Corticomuscular coherence: a review. , 1999, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[35]  J. Cedarbaum,et al.  The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function , 1999, Journal of the Neurological Sciences.

[36]  J C Rothwell,et al.  Recovery of swallowing after dysphagic stroke relates to functional reorganization in the intact motor cortex. , 1998, Gastroenterology.

[37]  Shigeru Sonoda,et al.  The Surface Electromyography on Suprahyoid Muscles during Swallowing , 1998 .

[38]  John C. Rothwell,et al.  The cortical topography of human swallowing musculature in health and disease , 1996, Nature Medicine.

[39]  B. Brooks,et al.  Clinical epidemiology of amyotrophic lateral sclerosis. , 1996, Neurologic clinics.

[40]  Mansi Pankaj Jani,et al.  Swallowing characteristics in Amyotrophic Lateral Sclerosis. , 2016, NeuroRehabilitation.

[41]  I. Rektor,et al.  Intracerebral ERD/ERS in voluntary movement and in cognitive visuomotor task. , 2006, Progress in brain research.

[42]  Charles R. Larson,et al.  Surface Electromyographic and Electroglottographic Studies in Normal Subjects Under Two Swallow Conditions: Normal and During the Mendelsohn Manuever , 2001, Dysphagia.

[43]  I. Aydogdu,et al.  Pathophysiological mechanisms of oropharyngeal dysphagia in amyotrophic lateral sclerosis. , 2000, Brain : a journal of neurology.

[44]  A M Amjad,et al.  A framework for the analysis of mixed time series/point process data--theory and application to the study of physiological tremor, single motor unit discharges and electromyograms. , 1995, Progress in biophysics and molecular biology.