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Cerebellar repetitive transcranial magnetic stimulation restores pharyngeal brain activity and swallowing behaviour after disruption by a cortical virtual lesion.
J Physiol. 2019 05; 597(9):2533-2546.JP

Abstract

KEY POINTS

Despite evidence that the human cerebellum has an important role in swallowing neurophysiology, the effects of cerebellar stimulation on swallowing in the disrupted brain have not been explored. In this study, for the first time, the application of cerebellar neurostimulation is characterized in a human model of disrupted swallowing (using a cortical virtual lesion). It is demonstrated that cerebellar stimulation can reverse the suppressed activity in the cortical swallowing system and restore swallowing function in a challenging behavioural task, suggesting the findings may have important therapeutic implications.

ABSTRACT

Repetitive transcranial magnetic stimulation (rTMS) can alter neuronal activity within the brain with therapeutic potential. Low frequency stimulation to the 'dominant' cortical swallowing projection induces a 'virtual-lesion' transiently suppressing cortical excitability and disrupting swallowing behaviour. Here, we compared the ability of ipsi-lesional, contra-lesional and sham cerebellar rTMS to reverse the effects of a 'virtual-lesion' in health. Two groups of healthy participants (n = 15/group) were intubated with pharyngeal catheters. Baseline pharyngeal motor evoked potentials (PMEPs) and swallowing performance (reaction task) were measured. Participants received 10 min of 1 Hz rTMS to the pharyngeal motor cortex which elicited the largest PMEPs to suppress cortical activity and disrupt swallowing behaviour. Over six visits, participants were randomized to receive 250 pulses of 10 Hz cerebellar rTMS to the ipsi-lesional side, contra-lesional side or sham while assessing PMEP amplitude or swallowing performance for an hour afterwards. Compared to sham, active cerebellar rTMS, whether administered ipsi-lesionally (P = 0.011) or contra-lesionally (P = 0.005), reversed the inhibitory effects of the cortical 'virtual-lesion' on PMEPs and swallowing accuracy (ipsi-lesional, P < 0.001, contra-lesional, P < 0.001). Cerebellar rTMS was able to reverse the disruptive effects of a 'virtual lesion'. These findings provide evidence for developing cerebellar rTMS into a treatment for post-stroke dysphagia.

Authors+Show Affiliations

Gastrointestinal (GI) Sciences, Division of Diabetes, Endocrinology and Gastroenterology, School of Medical Sciences, University of Manchester, Salford Royal Hospital (part of the Manchester Academic Health Sciences Center (MAHSC)), Salford, UK.Gastrointestinal (GI) Sciences, Division of Diabetes, Endocrinology and Gastroenterology, School of Medical Sciences, University of Manchester, Salford Royal Hospital (part of the Manchester Academic Health Sciences Center (MAHSC)), Salford, UK. Division of Dysphagia Rehabilitation, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan.Gastrointestinal (GI) Sciences, Division of Diabetes, Endocrinology and Gastroenterology, School of Medical Sciences, University of Manchester, Salford Royal Hospital (part of the Manchester Academic Health Sciences Center (MAHSC)), Salford, UK.Gastrointestinal (GI) Sciences, Division of Diabetes, Endocrinology and Gastroenterology, School of Medical Sciences, University of Manchester, Salford Royal Hospital (part of the Manchester Academic Health Sciences Center (MAHSC)), Salford, UK. Department of Speech and Language Therapy, Technological Educational Institute of Western Greece, Patras, Greece.Gastrointestinal (GI) Sciences, Division of Diabetes, Endocrinology and Gastroenterology, School of Medical Sciences, University of Manchester, Salford Royal Hospital (part of the Manchester Academic Health Sciences Center (MAHSC)), Salford, UK. Manchester University Foundation Trust, Neurogastroenterology, Wythenshawe Hospital, Manchester, UK.Division of Dysphagia Rehabilitation, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan.Stroke, Division of Clinical Neuroscience, University of Nottingham, Nottingham, UK.Sobell Department of Motor Neuroscience and Movement Disorders, University College London, London, UK.Division of Dysphagia Rehabilitation, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan.Gastrointestinal (GI) Sciences, Division of Diabetes, Endocrinology and Gastroenterology, School of Medical Sciences, University of Manchester, Salford Royal Hospital (part of the Manchester Academic Health Sciences Center (MAHSC)), Salford, UK.

Pub Type(s)

Journal Article
Randomized Controlled Trial
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

30907429

Citation

Sasegbon, Ayodele, et al. "Cerebellar Repetitive Transcranial Magnetic Stimulation Restores Pharyngeal Brain Activity and Swallowing Behaviour After Disruption By a Cortical Virtual Lesion." The Journal of Physiology, vol. 597, no. 9, 2019, pp. 2533-2546.
Sasegbon A, Watanabe M, Simons A, et al. Cerebellar repetitive transcranial magnetic stimulation restores pharyngeal brain activity and swallowing behaviour after disruption by a cortical virtual lesion. J Physiol. 2019;597(9):2533-2546.
Sasegbon, A., Watanabe, M., Simons, A., Michou, E., Vasant, D. H., Magara, J., Bath, P. M., Rothwell, J., Inoue, M., & Hamdy, S. (2019). Cerebellar repetitive transcranial magnetic stimulation restores pharyngeal brain activity and swallowing behaviour after disruption by a cortical virtual lesion. The Journal of Physiology, 597(9), 2533-2546. https://doi.org/10.1113/JP277545
Sasegbon A, et al. Cerebellar Repetitive Transcranial Magnetic Stimulation Restores Pharyngeal Brain Activity and Swallowing Behaviour After Disruption By a Cortical Virtual Lesion. J Physiol. 2019;597(9):2533-2546. PubMed PMID: 30907429.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Cerebellar repetitive transcranial magnetic stimulation restores pharyngeal brain activity and swallowing behaviour after disruption by a cortical virtual lesion. AU - Sasegbon,Ayodele, AU - Watanabe,Masahiro, AU - Simons,Andre, AU - Michou,Emilia, AU - Vasant,Dipesh H, AU - Magara,Jin, AU - Bath,Philip M, AU - Rothwell,John, AU - Inoue,Makoto, AU - Hamdy,Shaheen, Y1 - 2019/04/03/ PY - 2018/12/07/received PY - 2019/03/21/accepted PY - 2019/3/26/pubmed PY - 2020/7/15/medline PY - 2019/3/26/entrez SP - 2533 EP - 2546 JF - The Journal of physiology JO - J Physiol VL - 597 IS - 9 N2 - KEY POINTS: Despite evidence that the human cerebellum has an important role in swallowing neurophysiology, the effects of cerebellar stimulation on swallowing in the disrupted brain have not been explored. In this study, for the first time, the application of cerebellar neurostimulation is characterized in a human model of disrupted swallowing (using a cortical virtual lesion). It is demonstrated that cerebellar stimulation can reverse the suppressed activity in the cortical swallowing system and restore swallowing function in a challenging behavioural task, suggesting the findings may have important therapeutic implications. ABSTRACT: Repetitive transcranial magnetic stimulation (rTMS) can alter neuronal activity within the brain with therapeutic potential. Low frequency stimulation to the 'dominant' cortical swallowing projection induces a 'virtual-lesion' transiently suppressing cortical excitability and disrupting swallowing behaviour. Here, we compared the ability of ipsi-lesional, contra-lesional and sham cerebellar rTMS to reverse the effects of a 'virtual-lesion' in health. Two groups of healthy participants (n = 15/group) were intubated with pharyngeal catheters. Baseline pharyngeal motor evoked potentials (PMEPs) and swallowing performance (reaction task) were measured. Participants received 10 min of 1 Hz rTMS to the pharyngeal motor cortex which elicited the largest PMEPs to suppress cortical activity and disrupt swallowing behaviour. Over six visits, participants were randomized to receive 250 pulses of 10 Hz cerebellar rTMS to the ipsi-lesional side, contra-lesional side or sham while assessing PMEP amplitude or swallowing performance for an hour afterwards. Compared to sham, active cerebellar rTMS, whether administered ipsi-lesionally (P = 0.011) or contra-lesionally (P = 0.005), reversed the inhibitory effects of the cortical 'virtual-lesion' on PMEPs and swallowing accuracy (ipsi-lesional, P < 0.001, contra-lesional, P < 0.001). Cerebellar rTMS was able to reverse the disruptive effects of a 'virtual lesion'. These findings provide evidence for developing cerebellar rTMS into a treatment for post-stroke dysphagia. SN - 1469-7793 UR - https://www.unboundmedicine.com/medline/citation/30907429/Cerebellar_repetitive_transcranial_magnetic_stimulation_restores_pharyngeal_brain_activity_and_swallowing_behaviour_after_disruption_by_a_cortical_virtual_lesion_ L2 - https://doi.org/10.1113/JP277545 DB - PRIME DP - Unbound Medicine ER -