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Preconditioning human pharyngeal motor cortex enhances directional metaplasticity induced by repetitive transcranial magnetic stimulation.
J Physiol. 2020 11; 598(22):5213-5230.JP

Abstract

KEY POINTS

Recent studies have proposed therapeutic potential for repetitive transcranial magnetic stimulation (rTMS) in swallowing rehabilitation, yet its outcomes vary across individuals and studies. Such variability may be related to the brain state before stimulation. Metaplasticity is a higher order plasticity which regulates cortical response to plasticity changes. Studies have shown that preconditioning of the hand motor cortex could increase cortical capacity for neuroplastic change and enhance rTMS outcomes. We investigated, for the first time, the directional metaplastic properties in human pharyngeal motor cortex using preconditioned rTMS. We found that preconditioned rTMS with specific time intervals between preconditioning and conditioning rTMS had stronger stimulation effects in both swallowing neurophysiology and behaviour than that without preconditioning. Our results provide evidence for enhanced directional metaplasticity in pharyngeal motor cortex and new insights into its clinical application for dysphagia.

ABSTRACT

Despite growing evidence that repetitive transcranial magnetic stimulation (rTMS) can be used as a treatment for dysphagia, its efficacy varies across individuals. Such variability may relate to the pre-stimulation state of neuronal activation. Previous studies found that preconditioning the hand motor cortex before rTMS could enhance stimulation outcomes through metaplasticity. No studies have investigated such mechanisms in human pharyngeal motor cortex. Therefore, we investigated the preconditioning effects of rTMS on swallowing neurophysiology and behaviour. Healthy adults were recruited for swallowing neurophysiological (n = 14) and behavioural (n = 14) experiments. They were first given eight different preconditioned (1 and 5 Hz) rTMS interventions with varying inter-rTMS intervals. Motor evoked potentials (MEPs) were measured before and for 60 min post-rTMS. Based on the changes in pharyngeal MEPs, the optimal preconditioned 1 Hz and 5 Hz rTMS protocols were then applied as interventions while assessing swallowing performance using a reaction time task. We found that 5 Hz rTMS preconditioned with 1 Hz rTMS with 30 min inter-rTMS interval induced the greatest increase on pharyngeal cortical excitability (F1,13  = 21.244; P < 0.001). By comparison, 1 Hz rTMS preconditioned with 5 Hz rTMS with 90 min inter-rTMS interval was most optimal for suppressing pharyngeal motor cortex (F1,13  = 13.547; P = 0.003). Behaviourally, swallowing accuracy was improved after preconditioned 5 Hz rTMS (F1,13  = 10.109, P = 0.007) and reduced after preconditioned 1 Hz rTMS (F1,13  = 14.108, P = 0.009) compared to sham. Thus, two optimal protocols for inducing functional metaplasticity in human pharyngeal motor cortex have been identified. These protocols appear superior to conventional rTMS and may be relevant to future clinical application in neurogenic dysphagia.

Authors+Show Affiliations

Centre for Gastrointestinal Sciences, Division of Diabetes, Endocrinology and Gastroenterology, School of Medical Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, UK.Division of Neuroscience & Experimental Psychology, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, UK.Centre for Gastrointestinal Sciences, Division of Diabetes, Endocrinology and Gastroenterology, School of Medical Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, UK. Department of Rehabilitation Medicine, The Third Affiliated Hospital, Sun Yat-sen University, Guangzhou, China.Centre for Gastrointestinal Sciences, Division of Diabetes, Endocrinology and Gastroenterology, School of Medical Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, UK.

Pub Type(s)

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

Language

eng

PubMed ID

32804405

Citation

Cheng, Ivy, et al. "Preconditioning Human Pharyngeal Motor Cortex Enhances Directional Metaplasticity Induced By Repetitive Transcranial Magnetic Stimulation." The Journal of Physiology, vol. 598, no. 22, 2020, pp. 5213-5230.
Cheng I, Scarlett H, Zhang M, et al. Preconditioning human pharyngeal motor cortex enhances directional metaplasticity induced by repetitive transcranial magnetic stimulation. J Physiol. 2020;598(22):5213-5230.
Cheng, I., Scarlett, H., Zhang, M., & Hamdy, S. (2020). Preconditioning human pharyngeal motor cortex enhances directional metaplasticity induced by repetitive transcranial magnetic stimulation. The Journal of Physiology, 598(22), 5213-5230. https://doi.org/10.1113/JP279977
Cheng I, et al. Preconditioning Human Pharyngeal Motor Cortex Enhances Directional Metaplasticity Induced By Repetitive Transcranial Magnetic Stimulation. J Physiol. 2020;598(22):5213-5230. PubMed PMID: 32804405.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Preconditioning human pharyngeal motor cortex enhances directional metaplasticity induced by repetitive transcranial magnetic stimulation. AU - Cheng,Ivy, AU - Scarlett,Honor, AU - Zhang,Mengqing, AU - Hamdy,Shaheen, Y1 - 2020/09/03/ PY - 2020/04/15/received PY - 2020/08/11/accepted PY - 2020/8/18/pubmed PY - 2021/3/2/medline PY - 2020/8/18/entrez KW - brain KW - magnetic stimulation KW - neuromodulation KW - neurophysiology KW - swallowing KW - transcranial magnetic stimulation SP - 5213 EP - 5230 JF - The Journal of physiology JO - J Physiol VL - 598 IS - 22 N2 - KEY POINTS: Recent studies have proposed therapeutic potential for repetitive transcranial magnetic stimulation (rTMS) in swallowing rehabilitation, yet its outcomes vary across individuals and studies. Such variability may be related to the brain state before stimulation. Metaplasticity is a higher order plasticity which regulates cortical response to plasticity changes. Studies have shown that preconditioning of the hand motor cortex could increase cortical capacity for neuroplastic change and enhance rTMS outcomes. We investigated, for the first time, the directional metaplastic properties in human pharyngeal motor cortex using preconditioned rTMS. We found that preconditioned rTMS with specific time intervals between preconditioning and conditioning rTMS had stronger stimulation effects in both swallowing neurophysiology and behaviour than that without preconditioning. Our results provide evidence for enhanced directional metaplasticity in pharyngeal motor cortex and new insights into its clinical application for dysphagia. ABSTRACT: Despite growing evidence that repetitive transcranial magnetic stimulation (rTMS) can be used as a treatment for dysphagia, its efficacy varies across individuals. Such variability may relate to the pre-stimulation state of neuronal activation. Previous studies found that preconditioning the hand motor cortex before rTMS could enhance stimulation outcomes through metaplasticity. No studies have investigated such mechanisms in human pharyngeal motor cortex. Therefore, we investigated the preconditioning effects of rTMS on swallowing neurophysiology and behaviour. Healthy adults were recruited for swallowing neurophysiological (n = 14) and behavioural (n = 14) experiments. They were first given eight different preconditioned (1 and 5 Hz) rTMS interventions with varying inter-rTMS intervals. Motor evoked potentials (MEPs) were measured before and for 60 min post-rTMS. Based on the changes in pharyngeal MEPs, the optimal preconditioned 1 Hz and 5 Hz rTMS protocols were then applied as interventions while assessing swallowing performance using a reaction time task. We found that 5 Hz rTMS preconditioned with 1 Hz rTMS with 30 min inter-rTMS interval induced the greatest increase on pharyngeal cortical excitability (F1,13  = 21.244; P < 0.001). By comparison, 1 Hz rTMS preconditioned with 5 Hz rTMS with 90 min inter-rTMS interval was most optimal for suppressing pharyngeal motor cortex (F1,13  = 13.547; P = 0.003). Behaviourally, swallowing accuracy was improved after preconditioned 5 Hz rTMS (F1,13  = 10.109, P = 0.007) and reduced after preconditioned 1 Hz rTMS (F1,13  = 14.108, P = 0.009) compared to sham. Thus, two optimal protocols for inducing functional metaplasticity in human pharyngeal motor cortex have been identified. These protocols appear superior to conventional rTMS and may be relevant to future clinical application in neurogenic dysphagia. SN - 1469-7793 UR - https://www.unboundmedicine.com/medline/citation/32804405/Preconditioning_human_pharyngeal_motor_cortex_enhances_directional_metaplasticity_induced_by_repetitive_transcranial_magnetic_stimulation_ L2 - https://doi.org/10.1113/JP279977 DB - PRIME DP - Unbound Medicine ER -