Abstract
Swallowing problems (dysphagia) are common after brain injury and can affect as many as 50% of patients in the period immediately after stroke. In some cases this can lead to serious morbidity, in particular malnutrition and pulmonary aspiration. Despite this, swallowing therapies remain controversial, with limited evidence base and few objective outcome measures that would provide scientific support for the observed changes. Moreover, swallowing can recover in some patients to a safe level within weeks, introducing stroke as an interesting model for understanding brain recovery and compensation. A better understanding of these adaptive processes, seen during the spontaneous recovery phase, may help in developing therapeutic interventions capable of driving brain changes and encouraging the recovery process and is therefore a key goal for clinical neuroscience research warranting systematic investigation. In this chapter, we will review current knowledge and discuss some of the pioneering work conducted by researchers in the field of human swallowing neuromodulation over the last decade. The chapter will provide insights as to how the cerebral control of swallowing can be studied non-invasively in the human brain using neuroimaging tools and neurostimulation techniques. In addition, it will describe how both using these neurostimulation techniques to manipulate the brain’s natural capacity to re-organise (cortical plasticity) after injury or in response to new stimuli and studying brain capacity to re-organise help in the development of novel therapies for the treatment of dysphagia and other motor disorders in humans.
References
Ahn YH et al (2017) Effect of bihemispheric anodal transcranial direct current stimulation for dysphagia in chronic stroke patients: a randomized clinical trial. J Rehabil Med 49(1):30–35
Ali GN et al (1996) Influence of cold stimulation on the normal pharyngeal swallow response. Dysphagia 11(1):2–8
Amarasena J et al (2003) Effect of cortical masticatory area stimulation on swallowing in anesthetized rabbits. Brain Res 965(1-2):222–238
Arima T et al (2011) Corticomotor plasticity induced by tongue-task training in humans: a longitudinal fMRI study. Exp Brain Res 212(2):199–212
Baijens LW et al (2012) The effect of surface electrical stimulation on swallowing in dysphagic Parkinson patients. Dysphagia 27(4):528–537
Bailey CJ, Karhu J, Ilmoniemi RJ (2001) Transcranial magnetic stimulation as a tool for cognitive studies. Scand J Psychol 42(3):297–305. [Review] [51 refs]
Baranyi A, Feher O (1981) Synaptic facilitation requires paired activation of convergent pathways in the neocortex. Nature 290(5805):413–415
Barer DH (1989) The natural history and functional consequences of dysphagia after hemispheric stroke. J Neurol Neurosurg Psychiatry 52(2):236–241
Barikroo A, Lam PM (2011) Comparing the effects of rehabilitation swallowing therapy vs. functional neuromuscular electrical stimulation therapy in an encephalitis patient: a case study. Dysphagia 26(4):418–423
Bastian HC (1898) A treatise on aphasia and other speech defects. Lewis, London
Bath PM et al (2016) Pharyngeal electrical stimulation for treatment of dysphagia in subacute stroke a randomized controlled trial. Stroke 47(6):1562–U399
Beom J, Kim SJ, Han TR (2011) Electrical stimulation of the suprahyoid muscles in brain-injured patients with dysphagia: a pilot study. Ann Rehabil Med 35(3):322–327
Bulow M, Olsson R, Ekberg O (2003) Videoradiographic analysis of how carbonated thin liquids and thickened liquids affect the physiology of swallowing in subjects with aspiration on thin liquids. Acta Radiol 44(4):366–372
Bulow M et al (2008) Neuromuscular electrical stimulation (NMES) in stroke patients with oral and pharyngeal dysfunction. Dysphagia 23(3):302–309
Cabre M et al (2010) Prevalence and prognostic implications of dysphagia in elderly patients with pneumonia. Age Ageing 39(1):39–45
Calautti C et al (2001) Dynamics of motor network overactivation after striatocapsular stroke: a longitudinal PET study using a fixed-performance paradigm. Stroke 32(11):2534–2542
Carnaby-Mann GD, Crary MA (2007) Examining the evidence on neuromuscular electrical stimulation for swallowing: a meta-analysis. Arch Otolaryngol Head Neck Surg 133(6):564–571
Chee C et al (2005) The influence of chemical gustatory stimuli and oral anaesthesia on healthy human pharyngeal swallowing. Chem Senses 30(5):393–400
Cheeran B et al (2009) The future of restorative neurosciences in stroke: driving the translational research pipeline from basic science to rehabilitation of people after stroke. Neurorehabil Neural Repair 23(2):97–107
Chen YW et al (2016) The effects of surface neuromuscular electrical stimulation on post-stroke dysphagia: a systemic review and meta-analysis. Clin Rehabil 30(1):24–35
Cheng IK et al (2015) Preliminary evidence of the effects of high-frequency repetitive transcranial magnetic stimulation (rTMS) on swallowing functions in post-stroke individuals with chronic dysphagia. Int J Lang Commun Disord 50(3):389–396
Cheng IKY et al (2017) Neuronavigated high-frequency repetitive transcranial magnetic stimulation for chronic post-stroke dysphagia: a randomized controlled study. J Rehabil Med 49(6):475–481
Chervyakov AV et al (2015) Possible mechanisms underlying the therapeutic effects of transcranial magnetic stimulation. Front Hum Neurosci 9:303
Christiaanse ME et al (2011) Neuromuscular electrical stimulation is no more effective than usual care for the treatment of primary dysphagia in children. Pediatr Pulmonol 46(6):559–565
Cola MG et al (2010) Relevance of subcortical stroke in dysphagia. Stroke 41(3):482–486
Colombel C, Lalonde R, Caston J (2002) The effects of unilateral removal of the cerebellar hemispheres on motor functions and weight gain in rats. Brain Res 950(1-2):231–238
Cramer SC et al (1997) A functional MRI study of subjects recovered from hemiparetic stroke. Stroke 28(12):2518–2527
Cruikshank SJ, Weinberger NM (1996) Evidence for the Hebbian hypothesis in experience-dependent physiological plasticity of neocortex: a critical review. Brain Res Rev 22(3):191–228
Dan Y, Poo M-M (2006) Spike timing-dependent plasticity: from synapse to perception. Physiol Rev 86(3):1033–1048
Daniels SK, Foundas AL (1999) Lesion localization in acute stroke patients with risk of aspiration. J Neuroimaging 9(2):91–98
Dennis MS et al (2005a) Effect of timing and method of enteral tube feeding for dysphagic stroke patients (FOOD): a multicentre randomised controlled trial. Lancet 365(9461):764–772
Dennis MS, Lewis SC, Warlow C (2005b) Routine oral nutritional supplementation for stroke patients in hospital (FOOD): a multicentre randomised controlled trial. Lancet 365(9461):755–763
DePippo KL et al (1994) Dysphagia therapy following stroke: a controlled trial. Neurology 44(9):1655–1660
Doty RW (1951) Influence of stimulus pattern on reflex deglutition. Am J Physiol 166(1):142–158
Du J et al (2016) Repetitive transcranial magnetic stimulation for rehabilitation of poststroke dysphagia: a randomized, double-blind clinical trial. Clin Neurophysiol 127(3):1907–1913
Dziewas R et al (2017) Design and implementation of Pharyngeal electrical Stimulation for early de-cannulation in TRACheotomized (PHAST-TRAC) stroke patients with neurogenic dysphagia: a prospective randomized single-blinded interventional study. Int J Stroke 12(4):430–437
Ebihara S et al (2011) Sensory stimulation to improve swallowing reflex and prevent aspiration pneumonia in elderly dysphagic people. J Pharmacol Sci 115(2):99–104
Essa H et al (2017) The BDNF polymorphism Val66Met may be predictive of swallowing improvement post pharyngeal electrical stimulation in dysphagic stroke patients. Neurogastroenterol Motil 29(8). https://doi.org/10.1111/nmo.13062
Falsetti P et al (2009) Oropharyngeal dysphagia after stroke: incidence, diagnosis, and clinical predictors in patients admitted to a neurorehabilitation unit. J Stroke Cerebrovasc Dis 18(5):329–335
Foley NC et al (2009) A review of the relationship between dysphagia and malnutrition following stroke. J Rehabil Med 41(9):707–713
Fraser C et al (2002) Driving plasticity in human adult motor cortex is associated with improved motor function after brain injury. Neuron 34(5):831–840
Fraser C et al (2003) Differential changes in human pharyngoesophageal motor excitability induced by swallowing, pharyngeal stimulation, and anesthesia. Am J Physiol Gastrointest Liver Physiol 285(1):G137–G144
Freed ML et al (2001) Electrical stimulation for swallowing disorders caused by stroke. Respir Care 46(5):466–474
Fregni Fa et al (2005) Transcranial direct current stimulation of the unaffected hemisphere in stroke patients. Neuroreport 16(14):1551–1555
Gallas S et al (2010) Sensory transcutaneous electrical stimulation improves post-stroke dysphagic patients. Dysphagia 25(4):291–297
Gandiga PC, Hummel FC, Cohen LG (2006) Transcranial DC stimulation (tDCS): a tool for double-blind sham-controlled clinical studies in brain stimulation. Clin Neurophysiol 117(4):845–850
Geeganage C et al (2012) Interventions for dysphagia and nutritional support in acute and subacute stroke. Cochrane Database Syst Rev 10:CD000323
Ghelichi L et al (2016) A single-subject study to evaluate the inhibitory repetitive transcranial magnetic stimulation combined with traditional dysphagia therapy in patients with post-stroke dysphagia. Iran J Neurol 15(3):140–145
Gisel E (2008) Interventions and outcomes for children with dysphagia. Dev Disabil Res Rev 14(2):165–173
Goldberg LJ, Chandler SH, Tal M (1982) Relationship between jaw movements and trigeminal motoneuron membrane-potential fluctuations during cortically induced rhythmical jaw movements in the guinea pig. J Neurophysiol 48(1):110–138
Gonzalez-Fernandez M et al (2008) Supratentorial regions of acute ischemia associated with clinically important swallowing disorders: a pilot study. Stroke 39(11):3022–3028
Gow D et al (2004) Induction of long-term plasticity in human swallowing motor cortex following repetitive cortical stimulation. Clin Neurophysiol 115(5):1044–1051
Grelot L et al (1992) Membrane potential changes of phrenic motoneurons during fictive vomiting, coughing, and swallowing in the decerebrate cat. J Neurophysiol 68(6):2110–2119
Ha L, Hauge T (2003) Percutaneous endoscopic gastrostomy (PEG) for enteral nutrition in patients with stroke. Scand J Gastroenterol 38(9):962–966
ten Hallers EJ et al (2004) Animal models for tracheal research. Biomaterials 25(9):1533–1543
Hamamoto T et al (2009) Localization of transient receptor potential vanilloid (TRPV) in the human larynx. Acta Otolaryngol 129(5):560–568
Hamdy S et al (1996) The cortical topography of human swallowing musculature in health and disease. Nat Med 2(11):1217–1224
Hamdy S et al (1998a) Recovery of swallowing after dysphagic stroke relates to functional reorganization in the intact motor cortex. Gastroenterology 115(5):1104–1112
Hamdy S et al (1998b) Long-term reorganization of human motor cortex driven by short-term sensory stimulation. Nat Neurosci 1(1):64–68
Hamdy S et al (1999a) Cortical activation during human volitional swallowing: an event-related fMRI study. Am J Physiol 277(1 Pt 1):G219–G225
Hamdy S et al (1999b) Identification of the cerebral loci processing human swallowing with H2(15)O PET activation. J Neurophysiol 81(4):1917–1926
Hamdy S et al (2001) Induction of cortical swallowing activity by transcranial magnetic stimulation in the anaesthetized cat. Neurogastroenterol Motil 13(1):65–72
Hamdy S et al (2003) Modulation of human swallowing behaviour by thermal and chemical stimulation in health and after brain injury. Neurogastroenterol Motil 15(1):69–77
Heijnen BJ et al (2012) Neuromuscular electrical stimulation versus traditional therapy in patients with Parkinson’s disease and oropharyngeal dysphagia: effects on quality of life. Dysphagia 27(3):336–345
Hess G, Donoghue JP (1994) Long-term potentiation of horizontal connections provides a mechanism to reorganize cortical motor maps. J Neurophysiol 71(6):2543–2547
Hooker D (1954) Early human fetal behavior, with a preliminary note on double simultaneous fetal stimulation. Res Publ Assoc Res Nerv Ment Dis 33:98–113
van Hooren MR et al (2014) Treatment effects for dysphagia in Parkinson’s disease: a systematic review. Parkinsonism Relat Disord 20(8):800–807
Huang CS et al (1988) Organization of the primate face motor cortex as revealed by intracortical microstimulation and electrophysiological identification of afferent inputs and corticobulbar projections. J Neurophysiol 59(3):796–818
Huang CS et al (1989) Topographical distribution and functional properties of cortically induced rhythmical jaw movements in the monkey (Macaca fascicularis). J Neurophysiol 61(3):635–650
Humbert IA, Joel S (2012) Tactile, gustatory, and visual biofeedback stimuli modulate neural substrates of deglutition. Neuroimage 59(2):1485–1490
Hummel F et al (2005) Effects of non-invasive cortical stimulation on skilled motor function in chronic stroke. Brain 128(3):490–499. [Article]
Issa FG (1994) Gustatory stimulation of the oropharynx fails to induce swallowing in the sleeping dog. Gastroenterology 107(3):650–656
Jayasekeran V et al (2010) Adjunctive functional pharyngeal electrical stimulation reverses swallowing disability after brain lesions. Gastroenterology 138(5):1737–1746
Jayasekeran V, Rothwell J, Hamdy S (2011a) Non-invasive magnetic stimulation of the human cerebellum facilitates cortico-bulbar projections in the swallowing motor system. Neurogastroenterol Motil 23(9):831–e341
Jayasekeran V et al (2011b) Val66Met in brain-derived neurotrophic factor affects stimulus-induced plasticity in the human pharyngeal motor cortex. Gastroenterology 141(3):827–836. e1-3
Jean A (2001) Brain stem control of swallowing: neuronal network and cellular mechanisms. Physiol Rev 81(2):929–969
Jefferson S et al (2009a) Reversal of a virtual lesion in human pharyngeal motor cortex by high frequency contralesional brain stimulation. Gastroenterology 137(3):841–849. 849 e1
Jefferson S et al (2009b) Characterizing the application of transcranial direct current stimulation in human pharyngeal motor cortex. Am J Physiol Gastrointest Liver Physiol 297(6):G1035–G1040
Johnson ER, McKenzie SW, Sievers A (1993) Aspiration pneumonia in stroke. Arch Phys Med Rehabil 74(9):973–976
Kaas J (1997) Functional plasticity in adult cortex. In: Seminars in neuroscience. Academic Press, Orlando, Florida
Kandler R (1990) Safety of transcranial magnetic stimulation. Lancet 335(8687):469–470
Katzan IL et al (2003) The effect of pneumonia on mortality among patients hospitalized for acute stroke. Neurology 60(4):620–625
Kelso SR, Ganong AH, Brown TH (1986) Hebbian synapses in hippocampus. Proc Natl Acad Sci U S A 83(14):5326–5330
Khedr EM, Abo-Elfetoh N (2010) Therapeutic role of rTMS on recovery of dysphagia in patients with lateral medullary syndrome and brainstem infarction. J Neurol Neurosurg Psychiatry 81(5):495–499
Khedr EM et al (2008) Dysphagia and hemispheric stroke: a transcranial magnetic study. Neurophysiol Clin 38(4):235–242
Khedr EM, Abo-Elfetoh N, Rothwell JC (2009) Treatment of post-stroke dysphagia with repetitive transcranial magnetic stimulation. Acta Neurol Scand 119(3):155–161
Kidd D et al (1995) The natural history and clinical consequences of aspiration in acute stroke. QJM 88(6):409–413
Kim L et al (2011) Effect of repetitive transcranial magnetic stimulation on patients with brain injury and Dysphagia. Ann Rehabil Med 35(6):765–771
Kim SY et al (2014) Differences in videofluoroscopic swallowing study (VFSS) findings according to the vascular territory involved in stroke. Dysphagia 29(4):444–449
Kitagawa J et al (2002) Pharyngeal branch of the glossopharyngeal nerve plays a major role in reflex swallowing from the pharynx. Am J Physiol Regul Integr Comp Physiol 282(5):R1342–R1347
Ko JH et al (2008) Repetitive transcranial magnetic stimulation of dorsolateral prefrontal cortex affects performance of the Wisconsin card sorting task during provision of feedback. Int J Biomed Imaging 2008:143238
Kobayashi M, Pascual-Leone A (2003) Transcranial magnetic stimulation in neurology. Lancet Neurol 2(3):145–156
Kumar S et al (2011) Noninvasive brain stimulation may improve stroke-related dysphagia: a pilot study. Stroke 42(4):1035–1040
Kushner DS et al (2013) Neuromuscular electrical stimulation efficacy in acute stroke feeding tube-dependent dysphagia during inpatient rehabilitation. Am J Phys Med Rehabil 92(6):486–495
Kwon M, Lee JH, Kim JS (2005) Dysphagia in unilateral medullary infarction: lateral vs medial lesions. Neurology 65(5):714–718
de Lama Lazzara G, Lazarus C, Logemann J (1986) Impact of thermal stimulation on the triggering of the swallowing reflex. Dysphagia 1(2):73–77
Lamkadem M et al (1999) Stimulation of the chewing area of the cerebral cortex induces inhibitory effects upon swallowing in sheep. Brain Res 832(1-2):97–111
Lamm NC, De Felice A, Cargan A (2005) Effect of tactile stimulation on lingual motor function in pediatric lingual dysphagia. Dysphagia 20(4):311–324
Lazzara G, Lazarus C, Logemann J (1986) Impact of thermal stimulation on the triggering of the swallowing reflex. Dysphagia 1(2):73–77
Lee SY et al (2012) Neuromuscular electrical stimulation therapy for dysphagia caused by Wilson’s disease. Ann Rehabil Med 36(3):409–413
Lee JH et al (2015) Effect of repetitive transcranial magnetic stimulation according to the stimulation site in stroke patients with dysphagia. Ann Rehabil Med 39(3):432–439
Lefaucheur JP et al (2014) Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS). Clin Neurophysiol 125(11):2150–2206
Li S et al (2009) Functional magnetic resonance imaging study on dysphagia after unilateral hemispheric stroke: a preliminary study. J Neurol Neurosurg Psychiatry 80(12):1320–1329
Lim KB et al (2014) Effect of low-frequency rTMS and NMES on subacute unilateral hemispheric stroke with dysphagia. Ann Rehabil Med 38(5):592–602
Lin PH et al (2011) Effects of functional electrical stimulation on dysphagia caused by radiation therapy in patients with nasopharyngeal carcinoma. Support Care Cancer 19(1):91–99
Lowell SY et al (2008) Sensory stimulation activates both motor and sensory components of the swallowing system. Neuroimage 42(1):285–295
Maeda F et al (2000) Interindividual variability of the modulatory effects of repetitive transcranial magnetic stimulation on cortical excitability. Exp Brain Res 133(4):425–430
Magara J et al (2016) Exploring the effects of synchronous pharyngeal electrical stimulation with swallowing carbonated water on cortical excitability in the human pharyngeal motor system. Neurogastroenterol Motil 28(9):1391–1400
Malandraki GA et al (2009) Neural activation of swallowing and swallowing-related tasks in healthy young adults: an attempt to separate the components of deglutition. Hum Brain Mapp 30(10):3209–3226
Mann G, Hankey GJ, Cameron D (1999) Swallowing function after stroke: prognosis and prognostic factors at 6 months. Stroke 30(4):744–748
Marshall RS et al (2000) Evolution of cortical activation during recovery from corticospinal tract infarction. Stroke 31(3):656–661
Martin RE (2009) Neuroplasticity and swallowing. Dysphagia 24(2):218–229
Martin RE et al (1997) Functional properties of neurons in the primate tongue primary motor cortex during swallowing. J Neurophysiol 78(3):1516–1530
Martin RE et al (1999) Features of cortically evoked swallowing in the awake primate (Macaca fascicularis). J Neurophysiol 82(3):1529–1541
Martino R et al (2005) Dysphagia after stroke: incidence, diagnosis, and pulmonary complications. Stroke 36(12):2756–2763
McFarland DH, Lund JP (1993) An investigation of the coupling between respiration, mastication, and swallowing in the awake rabbit. J Neurophysiol 69(1):95–108
McKay DR et al (2002) Induction of persistent changes in the organisation of the human motor cortex. Exp Brain Res 143(3):342–349
Michou E, Hamdy S (2009) Cortical input in control of swallowing. Curr Opin Otolaryngol Head Neck Surg 17(3):166–171
Michou E et al (2009) Reversibility in human swallowing motor cortex by paired cortical and peripheral stimulation to a unilateral virtual lesion: evidence for targetting the contralesional cortex. Gastroenterology 136(5):A-17–A-18
Michou E et al (2012a) Examining the role of carbonation and temperature on water swallowing performance: a swallowing reaction-time study. Chem Senses 37(9):799–807
Michou E et al (2012b) Targeting unlesioned pharyngeal motor cortex improves swallowing in healthy individuals and after dysphagic stroke. Gastroenterology 142(1):29–38
Michou E et al (2013) Priming pharyngeal motor cortex by repeated paired associative stimulation: implications for dysphagia neurorehabilitation. Neurorehabil Neural Repair 27(4):355–362
Michou E et al (2014) Characterizing the mechanisms of central and peripheral forms of neurostimulation in chronic dysphagic stroke patients. Brain Stimul 7(1):66–73
Michou E et al (2015) fMRI and MRS measures of neuroplasticity in the pharyngeal motor cortex. Neuroimage 117:1–10
Michou E et al (2016) Repetitive transcranial magnetic stimulation: a novel approach for treating oropharyngeal dysphagia. Curr Gastroenterol Rep 18(2):10
Mihai PG, von Bohlen Und Halbach O, Lotze M (2013) Differentiation of cerebral representation of occlusion and swallowing with fMRI. Am J Physiol Gastrointest Liver Physiol 304(10):G847–G854
Mihai PG et al (2014) Sequential evolution of cortical activity and effective connectivity of swallowing using fMRI. Hum Brain Mapp 35(12):5962–5973
Mihai PG et al (2016) Brain imaging correlates of recovered swallowing after dysphagic stroke: a fMRI and DWI study. Neuroimage Clinical 12:1013–1021
Miller FR (1920) The cortical paths for mastication and deglutition. J Physiol 53(6):473–478
Miller AJ (1972) Characteristics of the swallowing reflex induced by peripheral nerve and brain stem stimulation. Exp Neurol 34(2):210–222
Miller AJ (2008) The neurobiology of swallowing and dysphagia. Dev Disabil Res Rev 14(2):77–86
Miller FR, Sherrington CS (1916) Some observations on the buccopharyngeal stage of reflex deglutition in the cat. Q. J Exp Physiol. 9:147–186
Mistry S et al (2006) Modulation of human cortical swallowing motor pathways after pleasant and aversive taste stimuli. Am J Physiol Gastrointest Liver Physiol 291(4):G666–G671
Mistry S et al (2007) Unilateral suppression of pharyngeal motor cortex to repetitive transcranial magnetic stimulation reveals functional asymmetry in the hemispheric projections to human swallowing. J Physiol 585(Pt 2):525–538
Momosaki R, Abo M, Kakuda W (2014) Bilateral repetitive transcranial magnetic stimulation combined with intensive swallowing rehabilitation for chronic stroke Dysphagia: a case series study. Case Rep Neurol 6(1):60–67
Momosaki R et al (2016a) Influence of repetitive peripheral magnetic stimulation on neural plasticity in the motor cortex related to swallowing. Int J Rehabil Res 39(3):263–266
Momosaki R et al (2016b) Noninvasive brain stimulation for dysphagia after acquired brain injury: a systematic review. J Med Invest 63(3-4):153–158
Mosier K, Bereznaya I (2001) Parallel cortical networks for volitional control of swallowing in humans. Exp Brain Res 140(3):280–289
Mosier K et al (1999) Cortical representation of swallowing in normal adults: functional implications. Laryngoscope 109(9):1417–1423
Mostafeezur RM et al (2012) Cannabinoids facilitate the swallowing reflex elicited by the superior laryngeal nerve stimulation in rats. PLoS One 7(11):e50703
Murphy TH, Corbett D (2009) Plasticity during stroke recovery: from synapse to behaviour. Nat Rev Neurosci 10(12):861–872
Mussen AT (1930) The cerebellum. A new classification of the lobes based on their reactions to stimulation. Arch Neurol Psychiatr. 23:411–461
Nakato R et al (2017) Effects of capsaicin on older patients with oropharyngeal dysphagia: a double-blind, placebo-controlled, crossover study. Digestion 95(3):210–220
Narita N et al (1999) Effects of functional disruption of lateral pericentral cerebral cortex on primate swallowing. Brain Res 824(1):140–145
Nitsche MA, Paulus W (2000) Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol 527(Pt 3):633–639
Nitsche MAMD, Paulus WMD (2001) Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology 57:1899–1901
Norton B et al (1996) A randomised prospective comparison of percutaneous endoscopic gastrostomy and nasogastric tube feeding after acute dysphagic stroke. BMJ 312(7022):13–16
O’Neil KH et al (1999) The dysphagia outcome and severity scale. Dysphagia 14(3):139–145
Ootani S et al (1995) Convergence of afferents from the SLN and GPN in cat medullary swallowing neurons. Brain Res Bull 37(4):397–404
Ortega O et al (2016) A comparative study between two sensory stimulation strategies after two weeks treatment on older patients with oropharyngeal dysphagia. Dysphagia 31(5):706–716
Paciaroni M et al (2004) Dysphagia following stroke. Eur Neurol 51(3):162–167
Park CL, O’Neill PA, Martin DF (1997) A pilot exploratory study of oral electrical stimulation on swallow function following stroke: an innovative technique. Dysphagia 12(3):161–166
Park JW et al (2012) Effortful swallowing training combined with electrical stimulation in post-stroke dysphagia: a randomized controlled study. Dysphagia 27(4):521–527
Park JW et al (2013) The effect of 5Hz high-frequency rTMS over contralesional pharyngeal motor cortex in post-stroke oropharyngeal dysphagia: a randomized controlled study. Neurogastroenterol Motil 25(4):324–e250
Park E et al (2017) Effects of bilateral repetitive transcranial magnetic stimulation on post-stroke dysphagia. Brain Stimulation 10(1):75–82
Pascual-Leone A et al (2005) The plastic human brain cortex. Annu Rev Neurosci 28:377–401
Peck KK et al (2010) Cortical activation during swallowing rehabilitation maneuvers: a functional MRI study of healthy controls. Laryngoscope 120(11):2153–2159
Penfield WaEB (1937) Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 60:389–443
Pisegna JM et al (2016) Effects of non-invasive brain stimulation on post-stroke dysphagia: a systematic review and meta-analysis of randomized controlled trials. Clin Neurophysiol 127(1):956–968
Power M et al (2004) Changes in pharyngeal corticobulbar excitability and swallowing behavior after oral stimulation. Am J Physiol Gastrointest Liver Physiol 286(1):G45–G50
Power ML et al (2006) Evaluating oral stimulation as a treatment for dysphagia after stroke. Dysphagia 21(1):49–55
Pyndt HS, Ridding MC (2004) Modification of the human motor cortex by associative stimulation. Exp Brain Res 159(1):123–128
Raginis-Zborowska A et al (2016a) Variable responsivity in the human pharyngeal motor cortex following excitatory/inhibitory non-invasive brain stimulation paradigms. Gastroenterology 150(4):S859–S859
Raginis-Zborowska A et al (2016b) Exploring the association between genetic polymorphisms and swallowing motor cortex excitability induced by repetitive transcranial magnetic stimulation: is response predicted by genetic predisposition? Gut 65:A113–A113
Reis DJ, Doba N, Nathan MA (1973) Predatory attack, grooming, and consummatory behaviors evoked by electrical stimulation of cat cerebellar nuclei. Science 182:845–847
Ridding MC, Rothwell JC (2007) Is there a future for therapeutic use of transcranial magnetic stimulation? Nat Rev Neurosci 8(7):559
Ridding MC, Taylor JL (2001) Mechanisms of motor-evoked potential facilitation following prolonged dual peripheral and central stimulation in humans. J Physiol 537(2):623–631
Rofes L et al (2013) Natural capsaicinoids improve swallow response in older patients with oropharyngeal dysphagia. Gut 62(9):1280–1287
Rosenbek JC et al (1996) Thermal application reduces the duration of stage transition in dysphagia after stroke. Dysphagia 11(4):225–233
Rosenbek JC et al (1998) Comparing treatment intensities of tactile-thermal application. Dysphagia 13(1):1–9
Rossi S et al (2009) Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 120(12):2008–2039
Sanes JN, Donoghue JP (2000) Plasticity and primary motor cortex. Annu Rev Neurosci 23:393–415
Schabitz WR et al (2004) Effect of brain-derived neurotrophic factor treatment and forced arm use on functional motor recovery after small cortical ischemia. Stroke 35(4):992–997
Sciortino K et al (2003) Effects of mechanical, cold, gustatory, and combined stimulation to the human anterior faucial pillars. Dysphagia 18(1):16–26
Scutt P et al (2015) Pharyngeal electrical stimulation for treatment of poststroke dysphagia: individual patient data meta-analysis of randomised controlled trials. Stroke Res Treat 2015:429053
Sdravou K, Walshe M, Dagdilelis L (2012) Effects of carbonated liquids on oropharyngeal swallowing measures in people with neurogenic dysphagia. Dysphagia 27(2):240–250
Sessle BJ, Kenny DJ (1973) Control of tongue and facial motility: neural mechanisms that may contribute to movements such as swallowing and sucking. Symp Oral Sens Percept 4:222–231
Shaker R et al (2002) Rehabilitation of swallowing by exercise in tube-fed patients with pharyngeal dysphagia secondary to abnormal UES opening. Gastroenterology 122(5):1314–1321
Shigematsu T, Fujishima I, Ohno K (2013) Transcranial direct current stimulation improves swallowing function in stroke patients. Neurorehabil Neural Repair 27(4):363–369
Siebner HR, Rothwell J (2003) Transcranial magnetic stimulation: new insights into representational cortical plasticity. Exp Brain Res 148(1):1–16
Singh S, Hamdy S (2006) Dysphagia in stroke patients. Postgrad Med J 82(968):383–391
Singh S et al (2009) A magnetic resonance spectroscopy study of brain glutamate in a model of plasticity in human pharyngeal motor cortex. Gastroenterology 136(2):417–424
Smithard DG et al (1996) Complications and outcome after acute stroke. Does dysphagia matter? Stroke 27(7):1200–1204
Smithard DG, Smeeton NC, Wolfe CD (2007) Long-term outcome after stroke: does dysphagia matter? Age Ageing 36(1):90–94
Soros P et al (2008) Functional MRI of oropharyngeal air-pulse stimulation. Neuroscience 153(4):1300–1308
Soros P, Inamoto Y, Martin RE (2009) Functional brain imaging of swallowing: an activation likelihood estimation meta-analysis. Hum Brain Mapp 30(8):2426–2439
Speyer R et al (2010) Effects of therapy in oropharyngeal dysphagia by speech and language therapists: a systematic review. Dysphagia 25(1):40–65
Stefan K et al (2000) Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 123(Pt 3):572–584
Stefan K et al (2002) Mechanisms of enhancement of human motor cortex excitability induced by interventional paired associative stimulation. J Physiol 543(Pt 2):699–708
Steinhagen V et al (2009) Swallowing disturbance pattern relates to brain lesion location in acute stroke patients. Stroke 40(5):1903–1906
Strafella AP et al (2001) Repetitive transcranial magnetic stimulation of the human prefrontal cortex induces dopamine release in the caudate nucleus. J Neurosci 21(15):RC157
Sumi T (1969) Some properties of cortically-evoked swallowing and chewing in rabbits. Brain Res 15(1):107–120
Sumi T (1972) Reticular ascending activation of frontal cortical neurons in rabbits, with special reference to the regulation of deglutition. Brain Res 46:43–54
Sun SF et al (2013) Combined neuromuscular electrical stimulation (NMES) with fiberoptic endoscopic evaluation of swallowing (FEES) and traditional swallowing rehabilitation in the treatment of stroke-related dysphagia. Dysphagia 28(4):557–566
Suntrup S et al (2013) Magnetoencephalographic evidence for the modulation of cortical swallowing processing by transcranial direct current stimulation. Neuroimage 83:346–354
Suntrup S et al (2015a) The impact of lesion location on dysphagia incidence, pattern and complications in acute stroke. Part 1: dysphagia incidence, severity and aspiration. Eur J Neurol 22(5):832–838
Suntrup S et al (2015b) Pharyngeal electrical stimulation can modulate swallowing in cortical processing and behavior—magnetoencephalographic evidence. Neuroimage 104:117–124
Suntrup S et al (2015c) Electrical pharyngeal stimulation for dysphagia treatment in tracheotomized stroke patients: a randomized controlled trial. Intensive Care Med 41(9):1629–1637
Suntrup-Krueger et al (2016) Electrical pharyngeal stimulation increases substance P level in saliva. Neurogastroenterol Motil. 28(6):855–60. doi: 10.1111/nmo.12783. Epub 2016 Feb 12. https://www.ncbi.nlm.nih.gov/pubmed/26871730
Suzuki M et al (2003) Activation of cerebellum and basal ganglia on volitional swallowing detected by functional magnetic resonance imaging. Dysphagia 18(2):71–77
Takeuchi NMD et al (2005) Repetitive transcranial magnetic stimulation of contralesional primary motor cortex improves hand function after stroke. Stroke 36(12):2681–2686. [Article]
Tan C et al (2013) Transcutaneous neuromuscular electrical stimulation can improve swallowing function in patients with dysphagia caused by non-stroke diseases: a meta-analysis. J Oral Rehabil 40(6):472–480
Teismann IK et al (2009) Tactile thermal oral stimulation increases the cortical representation of swallowing. BMC Neurosci 10:71
Terre R, Mearin F (2006) Oropharyngeal dysphagia after the acute phase of stroke: predictors of aspiration. Neurogastroenterol Motil 18(3):200–205
Theurer JA et al (2005) Oropharyngeal stimulation with air-pulse trains increases swallowing frequency in healthy adults. Dysphagia 20(4):254–260
Theurer JA et al (2009) Effects of oropharyngeal air-pulse stimulation on swallowing in healthy older adults. Dysphagia 24(3):302–313
Theurer JA et al (2013) Proof-of-principle pilot study of oropharyngeal air-pulse application in individuals with dysphagia after hemispheric stroke. Arch Phys Med Rehabil 94(6):1088–1094
Thoenen H et al (1991) The synthesis of nerve growth factor and brain-derived neurotrophic factor in hippocampal and cortical neurons is regulated by specific transmitter systems. Ann N Y Acad Sci 640:86–90
Turkington LG, Ward EC, Farrell AM (2017) Carbonation as a sensory enhancement strategy: a narrative synthesis of existing evidence. Disabil Rehabil 39(19):1958–1967
Valdez DT et al (1993) Swallowing and upper esophageal sphincter contraction with transcranial magnetic-induced electrical stimulation. Am J Physiol 264(2 Pt 1):G213–G219
Vasant DH et al (2014) Transcranial direct current stimulation reverses neurophysiological and behavioural effects of focal inhibition of human pharyngeal motor cortex on swallowing. J Physiol 592(Pt 4):695–709
Vasant DH et al (2015) High-frequency focal repetitive cerebellar stimulation induces prolonged increases in human pharyngeal motor cortex excitability. J Physiol 593(22):4963–4977
Vasant DH et al (2016) Pharyngeal electrical stimulation in dysphagia poststroke: a prospective, randomized single-blinded interventional study. Neurorehabil Neural Repair 30(9):866–875
Verin E, Leroi AM (2009) Poststroke dysphagia rehabilitation by repetitive transcranial magnetic stimulation: a noncontrolled pilot study. Dysphagia 24(2):204–210
Verin E et al (2011) Submental sensitive transcutaneous electrical stimulation (SSTES) at home in neurogenic oropharyngeal dysphagia: a pilot study. Ann Phys Rehabil Med 54(6):366–375
Verin E et al (2012) “Virtual” lesioning of the human oropharyngeal motor cortex: a videofluoroscopic study. Arch Phys Med Rehabil 93(11):1987–1990
Ward NS et al (2003) Neural correlates of outcome after stroke: a cross-sectional fMRI study. Brain 126(Pt 6):1430–1448
Wassermann EM (1998) Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5-7, 1996. Electroencephalogr Clin Neurophysiol 108(1):1–16
Weerasuriya A, Bieger D, Hockman CH (1979) Basal forebrain facilitation of reflex swallowing in the cat. Brain Res 174(1):119–133
Wolters A et al (2003) A temporally asymmetric Hebbian rule governing plasticity in the human motor cortex. J Neurophysiol 89(5):2339–2345
Yang EJ et al (2012) Effects of transcranial direct current stimulation (tDCS) on post-stroke dysphagia. Restor Neurol Neurosci 30(4):303–311
Yang SN et al (2015) Effectiveness of non-invasive brain stimulation in dysphagia subsequent to stroke: a systemic review and meta-analysis. Dysphagia 30(4):383–391
Yao D et al (2002) Neuronal activity patterns in primate primary motor cortex related to trained or semiautomatic jaw and tongue movements. J Neurophysiol 87(5):2531–2541
Zald DH, Pardo JV (1999) The functional neuroanatomy of voluntary swallowing. Ann Neurol 46(3):281–286
Zhu J-N et al (2006) The cerebellar-hypothalamic circuits: potential pathways underlying cerebellar involvement in somatic-visceral integration. Brain Res Rev 52(1):93–106
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer International Publishing AG
About this chapter
Cite this chapter
Michou, E., Sasegbon, A., Hamdy, S. (2018). Direct and Indirect Therapy: Neurostimulation for the Treatment of Dysphagia After Stroke. In: Ekberg, O. (eds) Dysphagia. Medical Radiology(). Springer, Cham. https://doi.org/10.1007/174_2017_147
Download citation
DOI: https://doi.org/10.1007/174_2017_147
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-68571-7
Online ISBN: 978-3-319-68572-4
eBook Packages: MedicineMedicine (R0)