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Dysphagia

, 24:83 | Cite as

Role of Cerebral Cortex Plasticity in the Recovery of Swallowing Function Following Dysphagic Stroke

  • Andrew W. Barritt
  • David G. Smithard
Review

Abstract

Effective swallowing is an essential part of life and is performed thousands of times per day, often without conscious consideration. Difficulty in swallowing (dysphagia) commonly arises in stroke patients following ischemia of the cerebral cortex. However, whereas this tends to resolve spontaneously in the majority of patients, a small percentage will be left with a persistent dysphagia, which predisposes to airway compromise and aspiration pneumonia. This article reviews the recent research into ways of restoring swallowing function in these patients through promoting plasticity and reorganisation of the remaining, viable cerebral cortex.

Keywords

Dysphagia Cerebral cortex Plasticity Rehabilitation Deglutition Deglutition disorders 

References

  1. 1.
    Ramsey DJC, Smithard DG. Assessment and management of dysphagia. Hosp Med. 2004;65:274–9.PubMedGoogle Scholar
  2. 2.
    Dodds WJ, Stewart ET, Logemann JA. Physiology and radiology of the normal oral and pharyngeal phases of swallowing. AJR Am J Roentgenol. 1990;154:953–63.PubMedGoogle Scholar
  3. 3.
    Fraser C, Rothwell JC, Power M, Hobson A, Thompson DG, 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.Google Scholar
  4. 4.
    Chee C, Arshad S, Singh S, Mistry S, Hamdy S. The influence of chemical gustatory stimuli and oral anesthesia on healthy human pharyngeal swallowing. Chem Senses. 2005;30:393–400.PubMedCrossRefGoogle Scholar
  5. 5.
    Power M, Fraser C, Hobson A, Rothwell JC, Mistry S, Nicholson DA, et al. Changes in pharyngeal corticobulbar excitability and swallowing behaviour after oral stimulation. Am J Physiol Gastrointest Liver Physiol. 2004;286:45–50.CrossRefGoogle Scholar
  6. 6.
    Ertekin C, Aydogdu I. Neurophysiology of swallowing. Clin Neurophysiol. 2003;114:2226–44.PubMedCrossRefGoogle Scholar
  7. 7.
    Miller AJ. Neurophysiological basis of swallowing. Dysphagia. 1986;1:91–100.CrossRefGoogle Scholar
  8. 8.
    Smithard DG. Substance P and swallowing after stroke. Therapy. 2006;3:291–8.CrossRefGoogle Scholar
  9. 9.
    Hamdy S, Rothwell JC, Brooks DJ, Bailey D, Aziz Q, Thompson DG. Identification of the cerebral loci processing human swallowing with H215O PET activation. J Neurophysiol. 1999;81:1917–26.PubMedGoogle Scholar
  10. 10.
    Sessle BJ, Yao D, Nishiura H, Yoshino K, Lee JC, Martin RE, et al. Properties and plasticity of the primate somatosensory and motor cortex related to orofacial sensorimotor function. Clin Exp Pharmacol Physiol. 2005;32:109–14.PubMedCrossRefGoogle Scholar
  11. 11.
    Yamamura K, Narita N, Yao D, Martin RE, Masuda Y, Sessle BJ. Effects of reversible bilateral inactivation of face primary motor cortex on mastication and swallowing. Brain Res. 2002;944:40–55.PubMedCrossRefGoogle Scholar
  12. 12.
    Narita N, Yamamura K, Yao D, Martin RE, Sessle BJ. Effects of functional disruption of lateral pericentral cerebral cortex on primate swallowing. Brain Res. 1999;824:140–5.PubMedCrossRefGoogle Scholar
  13. 13.
    Gordon C, Hewer RL, Wade DT. Dysphagia in acute stroke. Br Med J (Clin Res Ed). 1987;295:411–4.Google Scholar
  14. 14.
    Mann G, Dip PG, Hankey GJ, Cameron D. Swallowing function after stroke: prognosis and prognostic factors at 6 months. Stroke. 1999;30:744–8.PubMedGoogle Scholar
  15. 15.
    Singh KD, Hamdy S. Dysphagia in stroke patients. Postgrad Med J. 2006;82:382–91.PubMedCrossRefGoogle Scholar
  16. 16.
    Smithard DG, O’Neill PA, England R, Parks C, Wyatt R, Martin DF, et al. The natural history of dysphagia following a stroke. Dysphagia. 1997;12:188–93.PubMedCrossRefGoogle Scholar
  17. 17.
    Ichenstein GW, Kelly PJ, Furie KL, Ambrosi D, Rallis N, Goldstein R, et al. Predictors of feeding gastrostomy tube (FGT) removal in stroke patients with dysphagia. J Stroke Cerebrovasc Dis. 2003;12:169–74.CrossRefGoogle Scholar
  18. 18.
    Barer DH. The natural history and functional consequences of dysphagia after hemispheric stroke. J Neurol Neurosurg Psychiatry. 1989;52:236–41.PubMedCrossRefGoogle Scholar
  19. 19.
    Fraser C, Power M, Hamdy S, Rothwell JC, Hobday D, et al. Driving plasticity in adult human motor cortex is associated with improved motor function after brain injury. Neuron. 2002;34:831–40.PubMedCrossRefGoogle Scholar
  20. 20.
    Hamdy S, Rothwell JC. Gut feelings about recovery after stroke: the organisation and reorganisation of human swallowing motor cortex. Trends Neurosci. 1998;21:278–82.PubMedCrossRefGoogle Scholar
  21. 21.
    Hamdy S, Rothwell JC, Aziz Q, Thompson DG. Organisation and reorganisation of human swallowing motor cortex: implications for recovery after stroke. Clin Sci. 2000;98:151–7.CrossRefGoogle Scholar
  22. 22.
    Hussain A, Woolfrey S, Massey J, Geddes A, Cox J. Percutaneous endoscopic gastrostomy. Postgrad Med J. 1996;72:581–5.PubMedCrossRefGoogle Scholar
  23. 23.
    Smithard DG, O’Neill PA, Parks C, Morris J. Complications and outcome after acute stroke: does dysphagia matter? Stroke. 1996;27:1200–4.PubMedGoogle Scholar
  24. 24.
    Nudo RJ. Plasticity. NeuroRx. 2006;3:420–7.PubMedCrossRefGoogle Scholar
  25. 25.
    Butler AJ, Wolf SL. Transcranial magnetic stimulation to assess cortical plasticity: a critical perspective for stroke rehabilitation. J Rehabil Med. 2003;Suppl 41:20–6.CrossRefGoogle Scholar
  26. 26.
    Ye H, Cotic M, Carlen PL. Transmembrane potential induced in a spherical cell model under low-frequency magnetic stimulation. J Neural Eng. 2007;4:283–93.PubMedCrossRefGoogle Scholar
  27. 27.
    Gallas S, Moirot P, Debono G, Navarre I, Denis P, Marie JP, Verin E. Mylohyoid motor-evoked potentials relate to swallowing function after chronic stroke dysphagia. Neurogastroenterol Motil. 2007;19:453–8.PubMedCrossRefGoogle Scholar
  28. 28.
    Hamdy S, Aziz Q, Rothwell JC. The cortical topography of human swallowing musculature in health and disease. Nat Med.1996;2:1217–24.PubMedCrossRefGoogle Scholar
  29. 29.
    Benecke R, Meyer BU, Schonle P, Conrad B. Transcranial magnetic stimulation of the human brain: responses in muscles supplied by cranial nerves. Exp Brain Res. 1988;71:623–32.PubMedCrossRefGoogle Scholar
  30. 30.
    Muellbacher W, Artner C, Mamoli B. The role of the intact hemisphere in recovery of midline muscles after recent monohemispheric stroke. J Neurol. 1999;246:250–6.PubMedCrossRefGoogle Scholar
  31. 31.
    Brown CE, Li P, Boyd JD, Delaney KR, Murphy TH. Extensive turnover of dendritic spines and vascular remodelling in cortical tissues recovering from stroke. J Neurosci. 2007;27:4101–9.PubMedCrossRefGoogle Scholar
  32. 32.
    Biernaskie J, Corbett D. Enriched rehabilitative training promotes improved forelimb motor function and enhanced dendritic growth after focal ischemic injury. J Neurosci. 2001;21:5272–80.PubMedGoogle Scholar
  33. 33.
    Biernaskie J, Szymanska A, Windle V. Corbett, Bi-hemispheric contribution to functional motor recovery of the affected forelimb following focal ishaemic brain injury in rats. Eur J Neurosci. 2005;21:989–99.PubMedCrossRefGoogle Scholar
  34. 34.
    Nudo RJ, Wise BM, SiFuentes F, Milliken GW. Neural substrates for the effects of rehabilitative training on motor recovery after ischaemic infarct. Science. 1996;272:1791–4.PubMedCrossRefGoogle Scholar
  35. 35.
    Leipert J, Bauder H, Miltner WHR, Taub E, Weiller C. Treatment-induced cortical reorganisation after stroke in humans. Stroke. 2000;31:1210–6.Google Scholar
  36. 36.
    Mark VW, Taub E. Constraint-induced movement therapy for chronic stroke hemiparesis and other disabilities. Restor Neurol Neurosci. 2004;22:317–36.PubMedGoogle Scholar
  37. 37.
    Filbin MT. Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat Rev Neurosci. 2003;4:703–13.PubMedCrossRefGoogle Scholar
  38. 38.
    Silver J, Miller JH. Regeneration beyond the glial scar. Nat Neurosci Rev. 2004;5:146–56.CrossRefGoogle Scholar
  39. 39.
    Huang ZJ, Kirkwood A, Pizzorusso T, Porciatti V, Morales B, Bear MF, et al. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell. 1999;98:739–55.PubMedCrossRefGoogle Scholar
  40. 40.
    Hagemann G, Redecker C, Neumann-Haefelin T, Freund HJ, Witte OW. Increased long-term potentiation in the surround of experimentally induced focal cortical infarction. Ann Neurol. 1998;44:255–8.PubMedCrossRefGoogle Scholar
  41. 41.
    Manganotti P, Patuzzo S, Cortese F, Palermo A, Smania N, Fiaschi A. Motor disinhibition in affected and unaffected hemisphere in the early period of recovery after stroke. Clin Neurophysiol. 2002;113:936–43.PubMedCrossRefGoogle Scholar
  42. 42.
    Liepert J, Hamzei F, Weiller C. Motor cortex disinhibition of the unaffected hemisphere after acute stroke. Muscle Nerve. 2000;23:1761–3.PubMedCrossRefGoogle Scholar
  43. 43.
    Carmichael ST. Plasticity of cortical projections after stroke. Neuroscientist. 2003;9:64–75.PubMedCrossRefGoogle Scholar
  44. 44.
    Cheetham CEJ, Hammond MSL, Edwards CEJ, Finnerty GT. Sensory experience alters cortical connectivity and synaptic function site specifically. J Neurosci. 2007;27:3456–65.PubMedCrossRefGoogle Scholar
  45. 45.
    Ridding MC, Brouwer B, Miles TS, Pitcher JB, Thompson PD. Changes in muscle responses to stimulation of the motor cortex induced by peripheral nerve stimulation in human subjects. Exp Brain Res. 2000;131:135–43.PubMedCrossRefGoogle Scholar
  46. 46.
    Uy J, Ridding MC. Increased cortical excitability induced by transcranial DC and peripheral nerve stimulation. J Neurosci Methods. 2003;127:193–7.PubMedCrossRefGoogle Scholar
  47. 47.
    Hamdy S, Aziz Q, Rothwell JC, Power M, Singh KD, Nicholson DA, et al. Recovery of swallowing after dysphagic stroke relates to functional reorganisation in the intact motor cortex. Gastroenterology. 1998;115:1104–12.PubMedCrossRefGoogle Scholar
  48. 48.
    Hamdy S, Rothwell JC, Aziz Q, Singh KD, Thompson DG. Long term reorganisation of human motor cortex driven by short term sensory stimulation. Nat Neurosci. 1998;1:64–8.PubMedCrossRefGoogle Scholar
  49. 49.
    Power M, Fraser CH, Hobson A, Singh KD, Tyrrell P, Nicholson DA, et al. Evaluating oral stimulation as a treatment for dysphagia after stroke. Dysphagia. 2006;21:49–55.PubMedCrossRefGoogle Scholar
  50. 50.
    Power M, Hamdy S, Singh KD, Tyrrell PJ, Turnbull I, Thompson DG. Deglutive laryngeal closure in stroke patients. J Neurol Neurosurg Psychiatry. 2007;78:141–6.PubMedCrossRefGoogle Scholar
  51. 51.
    Gow D, Rothwell JC, Hobson A, Thompson DG, Hamdy S. Induction of long term plasticity in human swallowing motor cortex following repetitive cortical stimulation. Clin Neurophysiol. 2004;115:1044–51.PubMedCrossRefGoogle Scholar
  52. 52.
    Toni N, Buchs PA, Nikonenko I, Bron CR, Muller D. LTP promotes formation of multiple spine synapses between a single axon terminal and dendrite. Nature. 1999;402:421–5.PubMedCrossRefGoogle Scholar
  53. 53.
    Di Lazzaro V, Pilato F, Dileone M, Profice P, Capone F, Ranieri F, et al. Modulating cortical excitability in acute stroke: a repetitive TMS study. Clin Neurophysiol. 2008;119:715–23.PubMedCrossRefGoogle Scholar
  54. 54.
    Massey JM, Hubscher CH, Wagoner MR, Decker JA, Amps J, Silver J, et al. Chondroitinase ABC digestion of the perineuronal net promotes functional collateral sprouting in the cuneate nucleus after cervical spinal cord injury. J Neurosci. 2006;26:4406–14.PubMedCrossRefGoogle Scholar
  55. 55.
    Tropea D, Caleo M, Maffei L. Synergistic effects of brain-derived neurotrophic factor and chondroitinase ABC on retinal fiber sprouting after denervation of the superior colliculus in adult rats. J Neurosci. 2003;23:7034–44.PubMedGoogle Scholar
  56. 56.
    Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett JW, et al. Reactivation of ocular dominance plasticity in the adult visual cortex. Science. 2002;298:1248–51.PubMedCrossRefGoogle Scholar
  57. 57.
    Barritt AW, Davies M, Marchand F, Hartley R, Grist J, Yip P, et al. Chondroitinase ABC promotes sprouting of intact and injured spinal systems after spinal cord injury. J Neurosci. 2006;26:10856–67.PubMedCrossRefGoogle Scholar
  58. 58.
    Bradbury EJ, McMahon SB. Spinal cord repair strategies: why do they work? Nat Rev Neurosci. 2006;7:644–53.PubMedCrossRefGoogle Scholar
  59. 59.
    Bruckner G, Bringmann A, Hartig W, Koppe G, Delpech B, et al. Acute and long-lasting changes in extracellular-matrix chondroitin-sulphate proteoglycans induced by injection of chondroitinase ABC in the adult rat brain. Exp Brain Res. 1998;121:300–10.PubMedCrossRefGoogle Scholar
  60. 60.
    McGee AW, Yang Y, Fischer QS, Daw NW, Strittmatter SM. Experience-driven plasticity of visual cortex limited by myelin and Nogo receptor. Science. 2005;309:2222–6.PubMedCrossRefGoogle Scholar
  61. 61.
    Allen SJ, Dawbarn D. Clinical relevance of the neurotrophins and their receptors. Clin Sci (Lond). 2006;110:175–91.Google Scholar
  62. 62.
    Patterson SL, Abel T, Deuel TA, Martin KC, Rose JC, Kandel ER. Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron. 1996;16:1137–45.PubMedCrossRefGoogle Scholar
  63. 63.
    Goldstein LB. Amphetamines and related drugs in motor recovery after stroke. Phys Med Rehabil Clin N Am. 2003;14:S125–S134, x.Google Scholar
  64. 64.
    Gilmour G, Iversen SD, O’Neill MF, O’Neill MJ, Ward MA, Bannerman DM. Amphetamine promotes task-dependent recovery following focal cortical ischaemic lesions in the rat. Behav Brain Res. 2005;165:98–109.PubMedCrossRefGoogle Scholar
  65. 65.
    Stroemer RP, Kent TA, Hulsebosch CE. Enhanced neocortical neural sprouting, synaptogenesis, and behavioral recovery with D-amphetamine therapy after neocortical infarction in rats. Stroke. 1998;29:2381–93.PubMedGoogle Scholar
  66. 66.
    Feeney DM, Gonzalez A, Law WA. Amphetamine, haloperidol, and experience interact to affect rate of recovery after motor cortex injury. Science. 1982;217:855–7.PubMedCrossRefGoogle Scholar
  67. 67.
    Goldstein LB, Coviello A, Miller GD. Norepinephrine depletion impairs motor recovery following sensorimotor cortex injury in the rat. Restor Neurol Neurosci. 1991;3:41–7.Google Scholar
  68. 68.
    Goldstein LB, Davis JN. Clonidine impairs recovery of beam-walking after a sensorimotor cortex lesion in the rat. Brain Res. 1990;508:305–9.PubMedCrossRefGoogle Scholar
  69. 69.
    Goldstein LB. Neuropharmacology of TBI-induced plasticity. Brain Injury. 2003;17:685–94.PubMedCrossRefGoogle Scholar
  70. 70.
    Hyman SE. Addiction: a disease of learning and memory. Am J Psychiatry. 2005;162:1414–22.PubMedCrossRefGoogle Scholar
  71. 71.
    Kuo MF, Paulus W, Nitsche MA. Boosting focally-induced brain plasticity by dopamine. Cereb Cortex. 2008;18:648–51.PubMedCrossRefGoogle Scholar
  72. 72.
    Kuo MF, Grosch J, Fregni F, Paulus W, Nitsche MA. Focusing effect of acetylcholine on neuroplasticity in the human motor cortex. J Neurosci. 2007;27:14442–7.PubMedCrossRefGoogle Scholar
  73. 73.
    Hockman CH, Bieger D, Weerasuriya A. Supranuclear pathways of swallowing. Prog Neurobiol. 1979;12:15–32.PubMedCrossRefGoogle Scholar
  74. 74.
    Jia YX, Sekizawa K, Ohrui T, Nakayama K, Sasaki H. Dopamine D1 receptor antagonist inhibits swallowing reflex in guinea pigs. Am J Physiol. 1998;274:76–80.Google Scholar
  75. 75.
    Potulska A, Friedman A, Krolicki L, Spychala A. Swallowing disorders in Parkinson’s Disease. Parkinsonism Relat Disord. 2003;9:349–53.PubMedCrossRefGoogle Scholar
  76. 76.
    Nakagawa T, Sekizawa K, Arai H, Kikuchi R, Manabe K, Sasaki H. High incidence of pneumonia in elderly patients with basal ganglia infarction. Arch Intern Med. 1997;157:321–4.PubMedCrossRefGoogle Scholar
  77. 77.
    Ohrui T. Preventive strategies for aspiration pneumonia in elderly persons. Tohoku J Exp Med. 2005;207:3–12.CrossRefGoogle Scholar
  78. 78.
    Yamaya M, Yanai M, Ohrui T, Arai H, Sasaki H. Interventions to prevent pneumonia among older adults. J Am Geriatr Soc. 2001;49:85–90.PubMedCrossRefGoogle Scholar
  79. 79.
    Graybiel AM. Neurotransmitters and neuromodulators in the basal ganglia. Trends Neurosci. 1990;13:244–54.PubMedCrossRefGoogle Scholar
  80. 80.
    Jin Y, Sekizawa K, Fukushima T, Morikawa M, Nakazawa H, Sasaki H. Capsaicin desensitization inhibits swallowing reflex in guinea pigs. Am J Respir Crit Care Med. 1994;149:261–3.PubMedGoogle Scholar
  81. 81.
    Martinsson L, Hardemark H, Eksborg S. Amphetamines for improving recovery after stroke. Cochrane Database Syst Rev. 2007;CD002090.Google Scholar
  82. 82.
    Byrd KE, Sukay MJ, Dieterle MW, Yang L, Marting TC, Teomim D, et al. Craniofacial and TMJ effects after glutamate and TRH microsphere implantation in proximity to trigeminal motoneurons of growing rats. J Dent Res. 1997;76:1437–52.PubMedCrossRefGoogle Scholar
  83. 83.
    Ichenstein GW, Stein J, Ambrosi D, Goldstein R, Horn M, Bogdahn U. Predictors of survival after severe dysphagic stroke. J Neurol. 2005;252:1510–6.CrossRefGoogle Scholar
  84. 84.
    Parker C, Power M, Hamdy S, Bowen A, Tyrrell P, Thompson DG. Awareness of dysphagia by patients following stroke predicts swallowing performance. Dysphagia. 2004;19:28–35.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  1. 1.Kent and Sussex HospitalTunbridge WellsUK
  2. 2.William Harvey HospitalAshfordUK

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