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Changes in the Excitability of Corticobulbar Projections Due to Intraoral Cooling with Ice

  • Michiyuki KawakamiEmail author
  • Sara Simeoni
  • Sara Tremblay
  • Ricci Hannah
  • Toshiyuki Fujiwara
  • John C. Rothwell
Original Article


The aim of this study was to assess the effects of ice applied to the oral cavity on the excitability of corticobulbar projections to the swallowing muscles. The subjects were 8 healthy adult volunteers (mean age 29.0 ± 4.9 years). Motor-evoked potentials (MEPs) were recorded from the suprahyoid muscle complex using surface electrodes. Two blocks of 20 MEPs with a test stimulus intensity of 120% of the resting motor threshold were recorded at rest (baseline). Subjects then underwent 5-min thermal stimulation by either of 3 different types: (1) “ice-stick inside mouth,” (2) “ice-stick on neck,” and (3) “room temperature inside mouth.” Blocks of 20 MEPs were then recorded immediately and at 5-min intervals for the following 15 min. There was a significant difference in the effects of the 3 interventions on the amplitude of the MEPs following stimulation (two-way ANOVA: INTERVENTION × TIME; F8,84 = 3.76, p < 0.01). One-way ANOVA was used to evaluate the changes over time for each intervention type. Only “ice-stick inside mouth” caused an increase in the MEPs (one-way ANOVA main effect of TIME: F4,28 = 4.04, p = 0.010) with significant differences between baseline and P10 (mean difference 0.050; confidence interval (CI) 95% 0.019–0.079; p = 0.004). There were no significant effects of either “ice-stick on neck” or “room temperature inside mouth” (F4,28 = 1.13, p = 0.36; F4,28 = 1.36, p = 0.27, respectively). Ice stimulation within the oral cavity increases the excitability of the cortical swallowing motor pathway.


Swallowing Temperature Reaction time task Motor-evoked potential Deglutition Deglutition disorders 


Author Contribution

MK and JCR contributed to the conception and study design, data acquisition, analysis and interpretation, and drafting of the manuscript. SS and RH contributed to data acquisition and analysis. ST and TF contributed to data acquisition, analysis and drafting of the manuscript. All authors revised the article critically and approved the final version for publication.

Compliance with Ethical Standards


JCR and RH were supported by a Medical Research Council Grant (MR/K01384X/1). The other authors declare no conflicts of interest.

Informed Consent

Informed consent was obtained from all participants.


  1. 1.
    Miller AJ. Deglutition. Physiol Rev. 1982;62:129–84.CrossRefGoogle Scholar
  2. 2.
    Thexton AJ. Mastication and swallowing: an overview. Br Dent J. 1992;173:197–206.CrossRefGoogle Scholar
  3. 3.
    Jean A, Car A. Inputs to the swallowing medullary neurons from the peripheral afferent fibers and the swallowing cortical area. Brain Res. 1979;178:567–72.CrossRefGoogle Scholar
  4. 4.
    Ertekin C, Kiylioglu N, Tarlaci S, Keskin A, Aydogdu I. Effect of mucosal anaesthesia on oropharyngeal swallowing. Neurogastroenterol Motil. 2000;12:567–72.CrossRefGoogle Scholar
  5. 5.
    Mansson I, Sandberg N. Effects of surface anesthesia on deglutition in man. Laryngoscope. 1974;84:427–37.CrossRefGoogle Scholar
  6. 6.
    Hamdy S, Aziz Q, Rothwell JC, Singh K, Barlow J, Hughes D, Tallis RC, Thompson DG. The cortical topography of human swallowing musculature in health and disease. Nat Med. 1996;2:1217–24.CrossRefGoogle Scholar
  7. 7.
    Hamdy S, Aziz Q, Rothwell JC, Hobson A, Thompson DG. Sensorimotor modulation of human cortical swallowing pathways. J Physiol. 1998;506:857–66.CrossRefGoogle Scholar
  8. 8.
    Fraser C, Rothwell JC, Power M, Hobson A, Thompson D, Hamdy S. Differential changes in human pharyngoesophageal motor excitability induced by swallowing, pharyngeal stimulation, and anesthesia. Am J Physiol Gastrointest Liver Physiol. 2003;285:137–44.CrossRefGoogle Scholar
  9. 9.
    Mistry S, Rothwell JC, Thompson DG, Hamdy S. Modulation of human cortical swallowing motor pathways after pleasant and aversive taste stimuli. Am J Physiol Gastrointest Liver Physiol. 2006;291:666–71.CrossRefGoogle Scholar
  10. 10.
    Selçuk B, Uysal H, Aydogdu I, Akyuz M, Ertekin C. Effect of temperature on electrophysiological parameters of swallowing. J Rehabil Res Dev. 2007;44:373–80.CrossRefGoogle Scholar
  11. 11.
    Michou E, Mastan A, Ahmed S, Mistry S, Hamdy S. Examining the role of carbonation and temperature on water swallowing performance: a swallowing reaction-time study. Chem Senses. 2012;37:799–807.CrossRefGoogle Scholar
  12. 12.
    Logemann JA. The dysphagia diagnostic procedure as a treatment efficacy trial. Clin Commun Disord. 1993;3:1–10.Google Scholar
  13. 13.
    Lazzara G, Lazarus C, Logemann JA. Impact of thermal stimulation on the triggering of the swallowing reflex. Dysphagia. 1986;1:73–7.CrossRefGoogle Scholar
  14. 14.
    Ali GN, Laundl TM, Wallace KL, DeCarle DJ, Cook IJ. Influence of cold stimulation on the normal pharyngeal swallow response. Dysphagia. 1996;11:2–8.CrossRefGoogle Scholar
  15. 15.
    Sciortino K, Liss JM, Case JL, Gerritsen KG, Katz RC. Effects of mechanical, cold, gustatory, and combined stimulation to the human anterior faucial pillars. Dysphagia. 2003;18:16–26.CrossRefGoogle Scholar
  16. 16.
    Rossi S, Hallett M, Rossini PM, Pascual-Leone A, Safety of TMS Consensus Group. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol. 2009;120:2008–39.CrossRefGoogle Scholar
  17. 17.
    Nakamura T, Fujishima I. Usefulness of ice massage in triggering the swallow reflex. J Stroke Cerebrovasc Dis. 2013;22:378–82.CrossRefGoogle Scholar
  18. 18.
    Plowman-Prine EK, Triggs WJ, Malcolm MP, Rosenbek JC. Reliability of transcranial magnetic stimulation for mapping swallowing musculature in the human motor cortex. Clin Neurophysiol. 2008;119:2298–303.CrossRefGoogle Scholar
  19. 19.
    Magara J, Watanabe M, Tsujimura T, Hamdy S, Inoue M. Cold thermal oral stimulation produces immediate excitability in human pharyngeal motor cortex. Neurogastroenterol Motil. 2018;30:e13384. Scholar
  20. 20.
    Bisch EM, Logemann JA, Rademaker AW, Kahrilas PJ, Lazarus CL. Pharyngeal effects of bolus volume, viscosity, and temperature in patients with dysphagia resulting from neurologic impairment and in normal subjects. J Speech Hear Res. 1994;37:1041–59.CrossRefGoogle Scholar
  21. 21.
    Rosenbek JC, Robbins J, Fishback B, Levine RL. Effects of thermal application on dysphagia after stroke. J Speech Hear Res. 1991;34:1257–68.CrossRefGoogle Scholar
  22. 22.
    Helfrich-Miller KR, Rector KL, Straka JA. Dysphagia: its treatment in the profoundly retarded patient with cerebral palsy. Arch Phys Med Rehabil. 1986;67:520–5.Google Scholar
  23. 23.
    Jean A. Brainstem control of swallowing: localisation and organisation of central pattern generator for swallowing. In: Taylor A, editor. Neurophysiology of the jaws and teeth, vol. 1. London: MacMillan Press; 1990. p. 294–321.CrossRefGoogle Scholar
  24. 24.
    Al-Toubi AK, Abu-Hijleh A, Huckabee ML, Macrae P, Doeltgen SH. Effects of repeated volitional swallowing on the excitability of submental corticobulbar motor pathways. Dysphagia. 2011;26:311–7.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Sobell Department of Motor Neuroscience and Movement DisordersUCL Institute of NeurologyLondonUK
  2. 2.Department of Rehabilitation MedicineKeio University School of MedicineTokyoJapan
  3. 3.Department of Physical Medicine and RehabilitationJuntendo University Graduate School of MedicineTokyoJapan

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