The effects of unilateral and bilateral cerebellar rTMS on human pharyngeal motor cortical activity and swallowing behavior

Ayodele Sasegbon,John Rothwell,Craig J Smith,Philip Bath,Shaheen Hamdy

doi:10.1007/s00221-020-05787-x

Abstract

The cerebellum is recognised to bilaterally modulate sensorimotor function and has recently been shown to play a role in swallowing. Unilateral cerebellar repetitive trans-cranial magnetic stimulation (rTMS) excites corticobulbar motor pathways to the pharynx but the effects of bilateral versus unilateral cerebellar rTMS on these pathways are unknown. In this three-part cross-over study, healthy participants (n = 13) were randomly allocated to receive unilateral or bilateral 10 Hz cerebellar rTMS. Participants were intubated with pharyngeal electromyography and/or manometry catheters for motor evoked potentials (MEPs) and pressure recordings. In part 1 of the study, single pulse TMS was used to measure baseline motor cortical pharyngeal MEP (PMEP) and hemispheric cerebellar MEP (CMEP) amplitudes, before cerebellar rTMS was administered. Repeat measures of PMEP amplitude were performed at 15-min intervals for an hour post unilateral and bilateral rTMS. Thereafter, in two further studies, a cortical ‘virtual lesion’ (V/L) was applied prior to cerebellar rTMS with pre and post PMEPs (part 2) and measurements of swallowing accuracy (part 3) using a behavioural task. Compared to baseline, unilateral and bilateral cerebellar rTMS provoked increases in pharyngeal cortical excitation (P = 0.028, 0.0005, respectively). Bilateral rTMS was significantly more effective than unilateral in causing cortical excitation (P = 0.0005) and in reversing the suppressive neurological (P = 0.0005) and behavioural (P = 0.0005) effects of a cortical V/L. Our findings suggest bilateral cerebellar rTMS has greater facilitatory effects on corticobulbar motor pathways to the pharynx than unilateral stimulation with the potential to be a more effective clinical therapy if its effects are reproduced in populations with neurogenic dysphagia.

Highlights

Despite the apparent simplicity of the process of deglutition, each swallow is a physiologically complex activity necessitating fine neurological control, healthy dentition and precisely coordinated contractions of muscles within the head and neck (Sasegbon and Hamdy 2017)
No adverse events arose during the course of the study with cortical or cerebellar single pulse TMS or repetitive trans-cranial magnetic stimulation (rTMS)
Our study shows both unilateral and bilateral cerebellar rTMS are able to cause pharyngeal cortical excitation when applied to an unconditioned swallowing motor system

Summary

Introduction

Despite the apparent simplicity of the process of deglutition, each swallow is a physiologically complex activity necessitating fine neurological control, healthy dentition and precisely coordinated contractions of muscles within the head and neck (Sasegbon and Hamdy 2017). The cerebellum—a region of the brain given over to the modulation of (sensori-)motor activity—shares some similarities with the cerebral motor cortices. It too is bi-hemispheric with its own motor homunculus topography (Roostaei et al 2014). Functional imaging studies have shown the cerebellum is activated during the process of swallowing (Harris et al 2005; Hamdy et al 1999b; Mosier et al 1999; Suzuki et al 2003). There has been some suggestion that the cerebellum displays asymmetry during swallowing in a similar manner to the cerebral motor cortex with the left hemisphere of the cerebellum displaying greater functional activity than the right (Malandraki et al 2009; Suzuki et al 2003).

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