Skip to main content
Log in

The Cortical and Subcortical Neural Control of Swallowing: A Narrative Review

  • Review
  • Published:
Dysphagia Aims and scope Submit manuscript

Abstract

Swallowing is a sophisticated process involving the precise and timely coordination of the central and peripheral nervous systems, along with the musculatures of the oral cavity, pharynx, and airway. The role of the infratentorial neural structure, including the swallowing central pattern generator and cranial nerve nuclei, has been described in greater detail compared with both the cortical and subcortical neural structures. Nonetheless, accumulated data from analysis of swallowing performance in patients with different neurological diseases and conditions, along with results from neurophysiological studies of normal swallowing have gradually enhanced understanding of the role of cortical and subcortical neural structures in swallowing, potentially leading to the development of treatment modalities for patients suffering from dysphagia. This review article summarizes findings about the role of both cortical and subcortical neural structures in swallowing based on results from neurophysiological studies and studies of various neurological diseases. In sum, cortical regions are mainly in charge of initiation and coordination of swallowing after receiving afferent information, while subcortical structures including basal ganglia and thalamus are responsible for movement control and regulation during swallowing through the cortico-basal ganglia-thalamo-cortical loop. This article also presents how cortical and subcortical neural structures interact with each other to generate the swallowing response. In addition, we provided the updated evidence about the clinical applications and efficacy of neuromodulation techniques, including both non-invasive brain stimulation and deep brain stimulation on dysphagia.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Matsuo K, Palmer JB. Anatomy and physiology of feeding and swallowing: normal and abnormal. Phys Med Rehabil Clin N Am. 2008;19(4):691–707. https://doi.org/10.1016/j.pmr.2008.06.001.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Jean A. Brain stem control of swallowing: neuronal network and cellular mechanisms. Physiol Rev. 2001;81(2):929–69. https://doi.org/10.1152/physrev.2001.81.2.929.

    Article  CAS  PubMed  Google Scholar 

  3. Martino R, Foley N, Bhogal S, Diamant N, Speechley M, Teasell R. Dysphagia after stroke: incidence, diagnosis, and pulmonary complications. Stroke. 2005;36(12):2756–63. https://doi.org/10.1161/01.STR.0000190056.76543.eb.

    Article  PubMed  Google Scholar 

  4. Lee HT, Lim OK, Park KD, Lee JK. Dysphagia pattern according to stroke location. J Korean Dysphagia Soc. 2014;4(1):28–36.

    Google Scholar 

  5. Wilmskoetter J, Bonilha L, Martin-Harris B, Elm JJ, Horn J, Bonilha HS. Mapping acute lesion locations to physiological swallow impairments after stroke. Neuroimage Clin. 2019;22:101685. https://doi.org/10.1016/j.nicl.2019.101685.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Suttrup I, Warnecke T. Dysphagia in Parkinson’s disease. Dysphagia. 2016;31(1):24–32. https://doi.org/10.1007/s00455-015-9671-9.

    Article  PubMed  Google Scholar 

  7. Flowers HL, AlHarbi MA, Mikulis D, et al. MRI-based neuroanatomical predictors of dysphagia, dysarthria, and aphasia in patients with first acute ischemic stroke. Cerebrovasc Dis Extra. 2017;7(1):21–34. https://doi.org/10.1159/000457810.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Gonzalez-Fernandez M, Kleinman JT, Ky PK, Palmer JB, Hillis AE. Supratentorial regions of acute ischemia associated with clinically important swallowing disorders: a pilot study. Stroke. 2008;39(11):3022–8. https://doi.org/10.1161/STROKEAHA.108.518969.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Alberts MJ, Horner J, Gray L, Brazer SR. Aspiration after stroke: lesion analysis by brain MRI. Dysphagia. 1992;7(3):170–3. https://doi.org/10.1007/BF02493452.

    Article  CAS  PubMed  Google Scholar 

  10. Suntrup S, Kemmling A, Warnecke T, et al. The impact of lesion location on dysphagia incidence, pattern and complications in acute stroke. Part 1: dysphagia incidence, severity and aspiration. Eur J Neurol. 2015;22(5):832–8. https://doi.org/10.1111/ene.12670.

    Article  CAS  PubMed  Google Scholar 

  11. Suntrup-Krueger S, Kemmling A, Warnecke T, et al. The impact of lesion location on dysphagia incidence, pattern and complications in acute stroke. Part 2: oropharyngeal residue, swallow and cough response, and pneumonia. Eur J Neurol. 2017;24(6):867–74. https://doi.org/10.1111/ene.13307.

    Article  CAS  PubMed  Google Scholar 

  12. Steinhagen V, Grossmann A, Benecke R, Walter U. Swallowing disturbance pattern relates to brain lesion location in acute stroke patients. Stroke. 2009;40(5):1903–6. https://doi.org/10.1161/STROKEAHA.108.535468.

    Article  PubMed  Google Scholar 

  13. Wilmskoetter J, Daniels SK, Miller AJ. Cortical and subcortical control of swallowing-can we use information from lesion locations to improve diagnosis and treatment for patients with stroke? Am J Speech Lang Pathol. 2020;29(2S):1030–43. https://doi.org/10.1044/2019_AJSLP-19-00068.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Daniels SK, Foundas AL. Lesion localization in acute stroke patients with risk of aspiration. J Neuroimaging. 1999;9:91–8.

    Article  CAS  PubMed  Google Scholar 

  15. Cola MG, Daniels SK, Corey DM, Lemen LC, Romero M, Foundas AL. Relevance of subcortical stroke in dysphagia. Stroke. 2010;41(3):482–6. https://doi.org/10.1161/STROKEAHA.109.566133.

    Article  PubMed  Google Scholar 

  16. Moon HI, Kim GS, Lee E. Is the location of white matter lesions important in the swallowing function of older patients with mild stroke? Dysphagia. 2019;34(3):407–14. https://doi.org/10.1007/s00455-018-9955-y.

    Article  PubMed  Google Scholar 

  17. Kim JY, Yoon SY, Kim J, Wook KY. Neural correlates of cricopharyngeal dysfunction after supratentorial stroke: a voxel-based lesion-symptom mapping with propensity score matched case-control. Int J Stroke. 2022;17(2):207–17. https://doi.org/10.1177/17474930211006300.

    Article  PubMed  Google Scholar 

  18. Jang S, Yang HE, Yang HS, Kim DH. Lesion characteristics of chronic dysphagia in patients with supratentorial stroke. Ann Rehabil Med. 2017;41(2):225–30. https://doi.org/10.5535/arm.2017.41.2.225.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Lee WH, Lim MH, Seo HG, Seong MY, Oh BM, Kim S. Development of a novel prognostic model to predict 6-month swallowing recovery after ischemic stroke. Stroke. 2020;51(2):440–8. https://doi.org/10.1161/STROKEAHA.119.027439.

    Article  PubMed  Google Scholar 

  20. Galovic M, Leisi N, Muller M, et al. Lesion location predicts transient and extended risk of aspiration after supratentorial ischemic stroke. Stroke. 2013;44(10):2760–7. https://doi.org/10.1161/STROKEAHA.113.001690.

    Article  PubMed  Google Scholar 

  21. Kim JH, Oh SH, Jeong HJ, Sim YJ, Kim DG, Kim GC. Association between duration of dysphagia recovery and lesion location on magnetic resonance imaging in patients with middle cerebral artery infarction. Ann Rehabil Med. 2019;43(2):142–8. https://doi.org/10.5535/arm.2019.43.2.142.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Wilmskoetter J, Martin-Harris B, Pearson WG Jr, et al. Differences in swallow physiology in patients with left and right hemispheric strokes. Physiol Behav. 2018;194:144–52. https://doi.org/10.1016/j.physbeh.2018.05.010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Malandraki GA, Johnson S, Robbins J. Functional MRI of swallowing: from neurophysiology to neuroplasticity. Head Neck. 2011;33(Suppl 1):S14-20. https://doi.org/10.1002/hed.21903.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Lima MS, Mangilli LD, Sassi FC, Andrade CR. Functional magnetic resonance and swallowing: critical literature review. Braz J Otorhinolaryngol. 2015;81(6):671–80. https://doi.org/10.1016/j.bjorl.2015.08.006.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Humbert IA, Robbins J. Normal swallowing and functional magnetic resonance imaging: a systematic review. Dysphagia. 2007;22(3):266–75. https://doi.org/10.1007/s00455-007-9080-9.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Hamdy S, Rothwell JC, Brooks DJ, Bailey D, Aziz Q, Thompson DG. Identification of the cerebral loci processing human swallowing with H2(15)O PET activation. J Neurophysiol. 1999;81(4):1917–26. https://doi.org/10.1152/jn.1999.81.4.1917.

    Article  CAS  PubMed  Google Scholar 

  27. Harris ML, Julyan P, Kulkarni B, et al. Mapping metabolic brain activation during human volitional swallowing: a positron emission tomography study using [18F]fluorodeoxyglucose. J Cereb Blood Flow Metab. 2005;25(4):520–6. https://doi.org/10.1038/sj.jcbfm.9600042.

    Article  PubMed  Google Scholar 

  28. David H, Zald JVP. The functional neuroanatomy of voluntary swallowing. Ann Neurol. 2001;46:281–6. https://doi.org/10.1002/1531-8249(199909)46:3%3c281::AID-ANA2%3e3.0.CO;2-L.

    Article  Google Scholar 

  29. Abe S, Wantanabe Y, Shintani M, Tazaki M, Takahashi M, Yamane GY, Ide Y, Yamada Y, Shimono M, Ishikawa T. Magnetoencephalographic study of the starting point of voluntary swallowing. Cranio. 2003;21:46–9.

    Article  PubMed  Google Scholar 

  30. Dziewas R, Sörös P, Ishii R, et al. Neuroimaging evidence for cortical involvement in the preparation and in the act of swallowing. Neuroimage. 2003;20(1):135–44. https://doi.org/10.1016/s1053-8119(03)00285-4.

    Article  CAS  PubMed  Google Scholar 

  31. Furlong PL, Hobson AR, Aziz Q, et al. Dissociating the spatio-temporal characteristics of cortical neuronal activity associated with human volitional swallowing in the healthy adult brain. Neuroimage. 2004;22(4):1447–55. https://doi.org/10.1016/j.neuroimage.2004.02.041.

    Article  CAS  PubMed  Google Scholar 

  32. Loose R, Hamdy S, Enck P. Magnetoencephalographic response characteristics associated with tongue movement. Dysphagia. 2001;16(3):183–5. https://doi.org/10.1007/s00455-001-0062-z.

    Article  CAS  PubMed  Google Scholar 

  33. Watanabe Y, Abe S, Ishikawa T, Yamada Y, Yamane GY. Cortical regulation during the early stage of initiation of voluntary swallowing in humans. Dysphagia. 2004;19(2):100–8. https://doi.org/10.1007/s00455-003-0509-5.

    Article  PubMed  Google Scholar 

  34. Ertekin C, Turman B, Tarlaci S, Celik M, Aydogdu I, Secil Y, Kiylioglu N. Cricopharyngeal sphincter muscle responses to transcranial magnetic stimulation in normal subjects and in patients with dysphagia. Clin Neurophysiol. 2001;112:86–94.

    Article  CAS  PubMed  Google Scholar 

  35. Rödel RMW, Laskawi R, Markus H. Tongue representation in the lateral cortical motor region of the human brain as assessed by transcranial magnetic stimulation. Ann Otol Rhinol Laryngol. 2003;112:71–6.

    Article  PubMed  Google Scholar 

  36. Hiraoka K. Movement-related cortical potentials associated with saliva and water bolus swallowing. Dysphagia. 2004;19(3):155–9. https://doi.org/10.1007/s00455-004-0002-9.

    Article  PubMed  Google Scholar 

  37. Huckabee M, Deecke L, Cannito MP, Gould HJ, Mayr W. Cortical control mechanisms in volitional swallowing: the bereitschaftspotential. Brain Topogr. 2003;16:3–17.

    Article  PubMed  Google Scholar 

  38. Satow AI T, Yamamoto J-I, Begum T, Thuy DHD, Matsuhashi M, Mima T, Nagamine T, Baba K, Mihara T, Inoue Y, Miyamoto S, Hashimoto N, Shibasaki H. Role of primary sensorimotor cortex and supplementary motor area involitional swallowing: a movement-related cortical potential study. Am J Physiol Gastrointest Liver Physiol. 2003. https://doi.org/10.1152/ajpgi.00323.2003.

    Article  Google Scholar 

  39. Hamdy S, Mikulis DJ, Crawley A, Xue S, Lau H, Henry S, Diamant NE. Cortical activation during human volitionalswallowing: an event-related fMRI study. Am J Physiol-Gastrointest Liver Physiol. 1999;277:219–25.

    Article  Google Scholar 

  40. Tae WS, Lee S, Choi S, Pyun SB. Effects of aging on brain networks during swallowing: general linear model and independent component analyses. Sci Rep. 2021;11(1):1069. https://doi.org/10.1038/s41598-020-79782-1.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Hashimoto H, Takahashi K, Kameda S, et al. Swallowing-related neural oscillation: an intracranial EEG study. Ann Clin Transl Neurol. 2021;8(6):1224–38. https://doi.org/10.1002/acn3.51344.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Hashimoto H, Takahashi K, Kameda S, et al. Motor and sensory cortical processing of neural oscillatory activities revealed by human swallowing using intracranial electrodes. iScience. 2021;24(7):102786. https://doi.org/10.1016/j.isci.2021.102786.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Groppa S, Oliviero A, Eisen A, et al. A practical guide to diagnostic transcranial magnetic stimulation: report of an IFCN committee. Clin Neurophysiol. 2012;123(5):858–82. https://doi.org/10.1016/j.clinph.2012.01.010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Ertekin C, Aydogdu I. Neurophysiology of swallowing. Clin Neurophysiol. 2003;114(12):2226–44. https://doi.org/10.1016/s1388-2457(03)00237-2.

    Article  PubMed  Google Scholar 

  45. Levine R, Robbins JA, Maser A. Periventricular white matter changes and oropharyngeal swallowing in normal individuals. Dysphagia. 1992;7:142–7.

    Article  CAS  PubMed  Google Scholar 

  46. Mosier K, Patel R, Liu WC, Kalnin A, Maldjian J, Baredes S. Cortical representation of swallowing in normal adults: functional implications. Laryngoscope. 1999;109(9):1417–23. https://doi.org/10.1097/00005537-199909000-00011.

    Article  CAS  PubMed  Google Scholar 

  47. Mosier KM, Liu W-C, Maldjian JA, Shah R, Modia B. Lateralization of cortical function in swallowing: a functional MR imaging study. Am J Neuroradiol. 1999;20:1520–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Martin RE, Goodyear BG, Gati JS, Menon RS. Cerebral cortical representation of automatic and volitional swallowing in humans. J Neurophysiol. 2001;85:938–50.

    Article  CAS  PubMed  Google Scholar 

  49. Mosier K, Bereznaya I. Parallel cortical networks for volitional control of swallowing in humans. Exp Brain Res. 2001;140(3):280–9. https://doi.org/10.1007/s002210100813.

    Article  CAS  PubMed  Google Scholar 

  50. Kern M, Birn R, Jaradeh S, Jesmanowicz A, Cox R, Hyde J, Shaker R. Swallow-related cerebral cortical activity maps are not specific to deglutition. Am J Physiol Gastrointest Liver Physiol. 2001;280:531–8.

    Article  Google Scholar 

  51. Hartnick C, Rudolph C, Willging J, Holland S. Functional magnetic resonance imaging of the pediatric swallow: imaging the cortex and the brainstem. Laryngoscope. 2001. https://doi.org/10.1097/00005537-200107000-00010.

    Article  PubMed  Google Scholar 

  52. Kern MK, Jaradeh S, Arndorfer RC, Shaker R. Cerebral cortical representation of reflexive and volitional swallowing in humans. Am J Physiol Gastrointest Liver Physiol. 2001;280(3):G354–60. https://doi.org/10.1152/ajpgi.2001.280.3.G354.

    Article  CAS  PubMed  Google Scholar 

  53. Suzuki M, Asada Y, Ito J, Hayashi K, Inoue H, Kitano H. Activation of cerebellum and basal ganglia on volitional swallowing detected by functional magnetic resonance imaging. Dysphagia. 2003;18(2):71–7. https://doi.org/10.1007/s00455-002-0088-x.

    Article  PubMed  Google Scholar 

  54. Martin RE, MacIntosh BJ, Smith RC, Barr AM, Stevens TK, Gati JS, Menon RS. Cerebral areas processing swallowing and tongue movement are overlapping but distinct: a functional magnetic resonance imaging study. J Neurophysiol. 2004;92:2428–43. https://doi.org/10.1152/jn.01144.2003.

    Article  PubMed  Google Scholar 

  55. Toogood JA, Barr AM, Stevens TK, Gati JS, Menon RS, Martin RE. Discrete functional contributions of cerebral cortical foci in voluntary swallowing: a functional magnetic resonance imaging (fMRI) “Go, No-Go” study. Exp Brain Res. 2005;161(1):81–90. https://doi.org/10.1007/s00221-004-2048-1.

    Article  PubMed  Google Scholar 

  56. Daniels SK, Corey DM, Fraychinaud A, DePolo A, Foundas AL. Swallowing lateralization: the effects of modified dual-task interference. Dysphagia. 2006;21(1):21–7. https://doi.org/10.1007/s00455-005-9007-2.

    Article  PubMed  Google Scholar 

  57. Mistry S, Verin E, Singh S, et al. Unilateral suppression of pharyngeal motor cortex to repetitive transcranial magnetic stimulation reveals functional asymmetry in the hemispheric projections to human swallowing. J Physiol. 2007;585(Pt 2):525–38. https://doi.org/10.1113/jphysiol.2007.144592.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Teismann IK, Steinstraeter O, Stoeckigt K, et al. Functional oropharyngeal sensory disruption interferes with the cortical control of swallowing. BMC Neurosci. 2007;8:62. https://doi.org/10.1186/1471-2202-8-62.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Malandraki GA, Sutton BP, Perlman AL, Karampinos DC, Conway C. Neural activation of swallowing and swallowing-related tasks in healthy young adults: an attempt to separate the components of deglutition. Hum Brain Mapp. 2009;30(10):3209–26. https://doi.org/10.1002/hbm.20743.

    Article  PubMed  PubMed Central  Google Scholar 

  60. Peck KK, Branski RC, Lazarus C, et al. Cortical activation during swallowing rehabilitation maneuvers: a functional MRI study of healthy controls. Laryngoscope. 2010;120(11):2153–9. https://doi.org/10.1002/lary.21125.

    Article  PubMed  Google Scholar 

  61. Mistry S, Michou E, Singh S, et al. Using diffusion weighted MR imaging to dissect the neuroanatomy of human swallowing related behaviours. Gut. 2011;60(Suppl 1):A39–40. https://doi.org/10.1136/gut.2011.239301.78.

    Article  Google Scholar 

  62. Logemann JA, Shanahan T, Rademaker AW, Kahrilas PJ, Lazar R, Halper A. Oropharyngeal swallowing after stroke in the left basal ganglion/internal capsule. Dysphagia. 1993;8:230–4.

    Article  CAS  PubMed  Google Scholar 

  63. Robbins J, Levine RL, Maser A, Rosenbek JC, Kempster GB. Swallowing after unilateral stroke of the cerebral cortex. Arch Phys Med Rehabil. 1993;74(12):1295–300. https://doi.org/10.1016/0003-9993(93)90082-l.

    Article  CAS  PubMed  Google Scholar 

  64. Daniels SK, Foundas AL, Iglesia GC, Sullivan MA. Lesion site in unilateral stroke patients with dysphagia. J Stroke Cerebrovasc Dis. 1996;6(1):30–4. https://doi.org/10.1016/s1052-3057(96)80023-1.

    Article  CAS  PubMed  Google Scholar 

  65. Daniels SK, Foundas AL. The role of the insular cortex in dysphagia. Dysphagia. 1997;12:146–56. https://doi.org/10.1007/PL000095298.

    Article  CAS  PubMed  Google Scholar 

  66. Suntrup S, Warnecke T, Kemmling A, et al. Dysphagia in patients with acute striatocapsular hemorrhage. J Neurol. 2012;259(1):93–9. https://doi.org/10.1007/s00415-011-6129-3.

    Article  PubMed  Google Scholar 

  67. Lin CW, Chang YC, Chen WS, Chang K, Chang HY, Wang TG. Prolonged swallowing time in dysphagic Parkinsonism patients with aspiration pneumonia. Arch Phys Med Rehabil. 2012;93(11):2080–4. https://doi.org/10.1016/j.apmr.2012.07.010.

    Article  PubMed  Google Scholar 

  68. Maeshima S, Osawa A, Yamane F, Ishihara S, Tanahashi N. Dysphagia following acute thalamic haemorrhage: clinical correlates and outcomes. Eur Neurol. 2014;71(3–4):165–72. https://doi.org/10.1159/000355477.

    Article  PubMed  Google Scholar 

  69. Ellerston JK, Heller AC, Houtz DR, Kendall KA. Quantitative measures of swallowing deficits in patients with Parkinson’s disease. Ann Otol Rhinol Laryngol. 2016;125(5):385–92. https://doi.org/10.1177/0003489415617774.

    Article  PubMed  Google Scholar 

  70. Kim YH, Oh BM, Jung IY, Lee JC, Lee GJ, Han TR. Spatiotemporal characteristics of swallowing in Parkinson’s disease. Laryngoscope. 2015;125(2):389–95. https://doi.org/10.1002/lary.24869.

    Article  PubMed  Google Scholar 

  71. Galovic M, Leisi N, Muller M, et al. Neuroanatomical correlates of tube dependency and impaired oral intake after hemispheric stroke. Eur J Neurol. 2016;23(5):926–34. https://doi.org/10.1111/ene.12964.

    Article  CAS  PubMed  Google Scholar 

  72. Galovic M, Leisi N, Pastore-Wapp M, et al. Diverging lesion and connectivity patterns influence early and late swallowing recovery after hemispheric stroke. Hum Brain Mapp. 2017;38(4):2165–76. https://doi.org/10.1002/hbm.23511.

    Article  PubMed  PubMed Central  Google Scholar 

  73. Moon HI, Nam JS, Leem MJ, Kim KH. Periventricular white matter lesions as a prognostic factor of swallowing function in older patients with mild stroke. Dysphagia. 2017;32(4):480–6. https://doi.org/10.1007/s00455-017-9788-0.

    Article  PubMed  Google Scholar 

  74. Fandler S, Gattringer T, Eppinger S, et al. Frequency and predictors of dysphagia in patients with recent small subcortical infarcts. Stroke. 2017;48(1):213–5. https://doi.org/10.1161/STROKEAHA.116.015625.

    Article  PubMed  Google Scholar 

  75. May NH, Pisegna JM, Marchina S, Langmore SE, Kumar S, Pearson WG Jr. Pharyngeal swallowing mechanics secondary to hemispheric stroke. J Stroke Cerebrovasc Dis. 2017;26(5):952–61. https://doi.org/10.1016/j.jstrokecerebrovasdis.2016.11.001.

    Article  PubMed  Google Scholar 

  76. Lee WH, Lim MH, Nam HS, et al. Differential kinematic features of the hyoid bone during swallowing in patients with Parkinson’s disease. J Electromyogr Kinesiol. 2019;47:57–64. https://doi.org/10.1016/j.jelekin.2019.05.011.

    Article  PubMed  Google Scholar 

  77. Schiffer BL, Kendall K. Changes in timing of swallow events in Parkinson’s disease. Ann Otol Rhinol Laryngol. 2019;128(1):22–7. https://doi.org/10.1177/0003489418806918.

    Article  PubMed  Google Scholar 

  78. Lapa S, Claus I, Reitz SC, et al. Effect of thalamic deep brain stimulation on swallowing in patients with essential tremor. Ann Clin Transl Neurol. 2020;7(7):1174–80. https://doi.org/10.1002/acn3.51099.

    Article  PubMed  PubMed Central  Google Scholar 

  79. Miller AJ. The neurobiology of swallowing and dysphagia. Dev Disabil Res Rev. 2008;14(2):77–86. https://doi.org/10.1002/ddrr.12.

    Article  PubMed  Google Scholar 

  80. Oliveira-Maia AJ, de Araujo IE, Monteiro C, Workman V, Galhardo V, Nicolelis MA. The insular cortex controls food preferences independently of taste receptor signaling. Front Syst Neurosci. 2012;6:5. https://doi.org/10.3389/fnsys.2012.00005.

    Article  PubMed  PubMed Central  Google Scholar 

  81. Gogolla N. The insular cortex. Curr Biol. 2017;27(12):R580–6. https://doi.org/10.1016/j.cub.2017.05.010.

    Article  CAS  PubMed  Google Scholar 

  82. Uddin LQ, Nomi JS, Hebert-Seropian B, Ghaziri J, Boucher O. Structure and function of the human insula. J Clin Neurophysiol. 2017;34(4):300–6. https://doi.org/10.1097/WNP.0000000000000377.

    Article  PubMed  PubMed Central  Google Scholar 

  83. Wei KC, Hsiao MY, Wang TG. The kinematic features of hyoid bone movement during swallowing in different disease populations: a narrative review. J Formos Med Assoc. 2022. https://doi.org/10.1016/j.jfma.2022.04.007.

    Article  PubMed  PubMed Central  Google Scholar 

  84. Ghaemi H, Sobhani-Rad D, Arabi A, Saifpanahi S, Ghayoumi AZ. Role of basal ganglia in swallowing process: a systematic review. Iran Rehabil J. 2017;14(4):239–45. https://doi.org/10.18869/nrip.irj.14.4.239.

    Article  Google Scholar 

  85. Lenz FA, Gracely RH, Zirh TA, Leopold DA, Rowland LH, Dougherty PM. Human thalamic nucleus mediating taste and multiple other sensations related to ingestive behavior. J Neurophysiol. 1997;77(6):3406–9. https://doi.org/10.1152/jn.1997.77.6.3406.

    Article  CAS  PubMed  Google Scholar 

  86. Schmahmann JD, Smith EE, Eichler FS, Filley CM. Cerebral white matter: neuroanatomy, clinical neurology, and neurobehavioral correlates. Ann N Y Acad Sci. 2008;1142:266–309. https://doi.org/10.1196/annals.1444.017.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Brown S, Ngan E, Liotti M. A larynx area in the human motor cortex. Cereb Cortex. 2008;18(4):837–45. https://doi.org/10.1093/cercor/bhm131.

    Article  PubMed  Google Scholar 

  88. Huang CS, Hiraba H, Murray GM, Sessle BJ. Topographical distribution and functional properties of cortically induced rhythmical jaw movements in the monkey (Macaca fascicularis). J Neurophysiol. 1989;61(3):635–50. https://doi.org/10.1152/jn.1989.61.3.635.

    Article  CAS  PubMed  Google Scholar 

  89. Li WQ, Lin T, Li X, et al. TMS brain mapping of the pharyngeal cortical representation in healthy subjects. Brain Stimul. 2020;13(3):891–9. https://doi.org/10.1016/j.brs.2020.02.031.

    Article  PubMed  Google Scholar 

  90. Hamdy S, Aziz Q, Rothwell JC, et al. The cortical topography of human swallowing musculature in health and disease. Nat Med. 1996;2(11):1217–24. https://doi.org/10.1038/nm1196-1217.

    Article  CAS  PubMed  Google Scholar 

  91. Morecraft RJ, Stilwell-Morecraft KS, Rossing WR. The motor cortex and facial expression: new insights from neuroscience. Neurologist. 2004;10(5):235–49. https://doi.org/10.1097/01.nrl.0000138734.45742.8d.

    Article  PubMed  Google Scholar 

  92. Gonzalez-Fernandez M, Ottenstein L, Atanelov L, Christian AB. Dysphagia after stroke: an overview. Curr Phys Med Rehabil Rep. 2013;1(3):187–96. https://doi.org/10.1007/s40141-013-0017-y.

    Article  PubMed  PubMed Central  Google Scholar 

  93. Ertekin C. Voluntary versus spontaneous swallowing in man. Dysphagia. 2011;26(2):183–92. https://doi.org/10.1007/s00455-010-9319-8.

    Article  PubMed  Google Scholar 

  94. Leopold NA, Daniels SK. Supranuclear control of swallowing. Dysphagia. 2010;25(3):250–7. https://doi.org/10.1007/s00455-009-9249-5.

    Article  PubMed  Google Scholar 

  95. Michou E, Hamdy S. Cortical input in control of swallowing. Curr Opin Otolaryngol Head Neck Surg. 2009;17(3):166–71. https://doi.org/10.1097/MOO.0b013e32832b255e.

    Article  PubMed  Google Scholar 

  96. Cheng I, Takahashi K, Miller A, Hamdy S. Cerebral control of swallowing: An update on neurobehavioral evidence. J Neurol Sci. 2022;442:120434. https://doi.org/10.1016/j.jns.2022.120434.

    Article  PubMed  Google Scholar 

  97. Ariani GWM, Lingnau A. Decoding internally and externally driven movement plans. J Neurosci. 2015;35(42):14160–71. https://doi.org/10.1523/JNEUROSCI.0596-15.2015.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Kiernan JA. Anatomy of the temporal lobe. Epilepsy Res Treat. 2012;2012:176157. https://doi.org/10.1155/2012/176157.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Devinsky O, Morrell MJ, Vogt BA. Contributions of anterior cingulate cortex to behaviour. Brain. 1995. https://doi.org/10.1093/brain/118.1.279.

    Article  PubMed  Google Scholar 

  100. Yukie M. Neural connections of auditory association cortex with the posterior cingulate cortex in the monkey. Neurosci Res. 1995;22:179–87.

    Article  CAS  PubMed  Google Scholar 

  101. Florio TM, Scarnati E, Rosa I, et al. The Basal Ganglia: More than just a switching device. CNS Neurosci Ther. 2018;24(8):677–84. https://doi.org/10.1111/cns.12987.

    Article  PubMed  PubMed Central  Google Scholar 

  102. Mücke D, Hermes A, Roettger TB, et al. The effects of thalamic deep brain stimulation on speech dynamics in patients with essential tremor: an articulographic study. PLOS ONE. 2018;13(1):e0191359. https://doi.org/10.1371/journal.pone.0191359.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Chiu SY, Nozile-Firth K, Klassen BT, et al. Ataxia and tolerance after thalamic deep brain stimulation for essential tremor. Parkinsonism Relat Disord. 2020;80:47–53. https://doi.org/10.1016/j.parkreldis.2020.09.009.

    Article  PubMed  Google Scholar 

  104. Aumann TD. Cerebello-thalamic synapses and motor adaptation. Cerebellum. 2002;1(1):69–77. https://doi.org/10.1080/147342202753203104.

    Article  CAS  PubMed  Google Scholar 

  105. Marmarou CR. Periventricular white matter. In: Kreutzer JS, DeLuca J, Caplan B, editors. Encyclopedia of clinical neuropsychology. New York: Springer; 2011. p. 1914–5.

    Chapter  Google Scholar 

  106. Hazzaa NM, Mancini L, Thornton J, Yousry TA. Somatotopic organization of corticospinal/corticobulbar motor tracts in controls and patients with tumours: a combined fMRI-DTI study. Neuroimage Clin. 2019;23:101910. https://doi.org/10.1016/j.nicl.2019.101910.

    Article  PubMed  PubMed Central  Google Scholar 

  107. Janelle F, Iorio-Morin C, D’Amour S, Fortin D. Superior longitudinal fasciculus: a review of the anatomical descriptions with functional correlates. Front Neurol. 2022;13:794618. https://doi.org/10.3389/fneur.2022.794618.

    Article  PubMed  PubMed Central  Google Scholar 

  108. Ringo JL, Doty RW, Demeter S, Simard PY. Time is of the essence: a conjecture that hemispheric specialization arises from interhemispheric conduction delay. Cereb Cortex. 1994;4(4):331–43. https://doi.org/10.1093/cercor/4.4.331.

    Article  CAS  PubMed  Google Scholar 

  109. Aziz Q, Furlong PL, Barlow J, et al. Topographic mapping of cortical potentials evoked by distension of the human proximal and distal oesophagus. Electroencephalogr Clin Neurophysiol. 1995;96(3):219–28. https://doi.org/10.1016/0168-5597(94)00297-r.

    Article  CAS  PubMed  Google Scholar 

  110. Kober SE, Wood G. Changes in hemodynamic signals accompanying motor imagery and motor execution of swallowing: a near-infrared spectroscopy study. Neuroimage. 2014;93(Pt 1):1–10. https://doi.org/10.1016/j.neuroimage.2014.02.019.

    Article  PubMed  Google Scholar 

  111. Soros P, Inamoto Y, Martin RE. Functional brain imaging of swallowing: an activation likelihood estimation meta-analysis. Hum Brain Mapp. 2009;30(8):2426–39. https://doi.org/10.1002/hbm.20680.

    Article  PubMed  Google Scholar 

  112. Mateos-Aparicio P, Rodriguez-Moreno A. The impact of studying brain plasticity. Front Cell Neurosci. 2019;13:66. https://doi.org/10.3389/fncel.2019.00066.

    Article  PubMed  PubMed Central  Google Scholar 

  113. Hamdy S, Aziz Q, Rothwell JC, Power M, Singh KD, Nicholson DA, Tallis RC, Thompson DG. Recovery of swallowing after dysphagic stroke relates to functional reorganization in the intact motor cortex. Gastroenterology. 1998;115(5):1104–12. https://doi.org/10.1016/s0016-5085(98)70081-2.

    Article  CAS  PubMed  Google Scholar 

  114. Gow D, Rothwell J, Hobson A, Thompson D, Hamdy S. Induction of long-term plasticity in human swallowing motor cortex following repetitive cortical stimulation. Clin Neurophysiol. 2004;115(5):1044–51. https://doi.org/10.1016/j.clinph.2003.12.001.

    Article  PubMed  Google Scholar 

  115. Jefferson S, Mistry S, Singh S, Rothwell J, Hamdy S. Characterizing the application of transcranial direct current stimulation in human pharyngeal motor cortex. Am J Physiol Gastrointest Liver Physiol. 2009;297(6):G1035–40. https://doi.org/10.1152/ajpgi.00294.2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Yang W, Cao X, Zhang X, Wang X, Li X, Huai Y. The effect of repetitive transcranial magnetic stimulation on dysphagia after stroke: a systematic review and meta-analysis. Front Neurosci. 2021;15:769848. https://doi.org/10.3389/fnins.2021.769848.

    Article  PubMed  PubMed Central  Google Scholar 

  117. Li L, Huang H, Jia Y, et al. Systematic review and network meta-analysis of noninvasive brain stimulation on dysphagia after stroke. Neural Plast. 2021;2021:3831472. https://doi.org/10.1155/2021/3831472.

    Article  PubMed  PubMed Central  Google Scholar 

  118. Du J, Yang F, Liu L, et al. Repetitive transcranial magnetic stimulation for rehabilitation of poststroke dysphagia: a randomized, double-blind clinical trial. Clin Neurophysiol. 2016;127(3):1907–13. https://doi.org/10.1016/j.clinph.2015.11.045.

    Article  PubMed  Google Scholar 

  119. Khedr EM, Abo-Elfetoh N, Rothwell JC. Treatment of post-stroke dysphagia with repetitive transcranial magnetic stimulation. Acta Neurol Scand. 2009;119(3):155–61. https://doi.org/10.1111/j.1600-0404.2008.01093.x.

    Article  CAS  PubMed  Google Scholar 

  120. Michou E, Mistry S, Jefferson S, Tyrrell P, Hamdy S. Characterizing the mechanisms of central and peripheral forms of neurostimulation in chronic dysphagic stroke patients. Brain Stimul. 2014;7(1):66–73. https://doi.org/10.1016/j.brs.2013.09.005.

    Article  PubMed  PubMed Central  Google Scholar 

  121. Park JW, Oh JC, Lee JW, Yeo JS, Ryu KH. The effect of 5Hz high-frequency rTMS over contralesional pharyngeal motor cortex in post-stroke oropharyngeal dysphagia: a randomized controlled study. Neurogastroenterol Motil. 2013;25(4):324-e250. https://doi.org/10.1111/nmo.12063.

    Article  PubMed  Google Scholar 

  122. Zhang C, Zheng X, Lu R, Yun W, Yun H, Zhou X. Repetitive transcranial magnetic stimulation in combination with neuromuscular electrical stimulation for treatment of post-stroke dysphagia. J Int Med Res. 2019;47(2):662–72. https://doi.org/10.1177/0300060518807340.

    Article  PubMed  Google Scholar 

  123. Park E, Kim MS, Chang WH, et al. Effects of bilateral repetitive transcranial magnetic stimulation on post-stroke dysphagia. Brain Stimul. 2017;10(1):75–82. https://doi.org/10.1016/j.brs.2016.08.005.

    Article  PubMed  Google Scholar 

  124. Cheng I, Sasegbon A, Hamdy S. Effects of neurostimulation on poststroke dysphagia: a synthesis of current evidence from randomized controlled trials. Neuromodulation. 2021;24(8):1388–401. https://doi.org/10.1111/ner.13327.

    Article  PubMed  Google Scholar 

  125. Di Pino G, Pellegrino G, Assenza G, et al. Modulation of brain plasticity in stroke: a novel model for neurorehabilitation. Nat Rev Neurol. 2014;10(10):597–608. https://doi.org/10.1038/nrneurol.2014.162.

    Article  PubMed  Google Scholar 

  126. Lyons MK. Deep brain stimulation: current and future clinical applications. Mayo Clin Proc. 2011;86(7):662–72. https://doi.org/10.4065/mcp.2011.0045.

    Article  PubMed  PubMed Central  Google Scholar 

  127. Vedam-Mai V, van Battum EY, Kamphuis W, Feenstra MGP, Denys D, Reynolds BA, Okun MS, Hol EM. Deep brain stimulation and the role of astrocytes. Mol Psychiatr. 2012;17(2):124–31. https://doi.org/10.1038/mp.2011.61.

    Article  CAS  Google Scholar 

  128. McIntyre CC, Anderson RW. Deep brain stimulation mechanisms: the control of network activity via neurochemistry modulation. J Neurochem. 2016;139(Suppl 1):338–45. https://doi.org/10.1111/jnc.13649.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Chang MC, Park JS, Lee BJ, Park D. The effect of deep brain stimulation on swallowing function in Parkinson’s disease: a narrative review. Dysphagia. 2021;36(5):786–99. https://doi.org/10.1007/s00455-020-10214-y.

    Article  PubMed  Google Scholar 

  130. Lester DB, Rogers TD, Blaha CD. Neuronal pathways involved in deep brain stimulation of the subthalamic nucleus for treatment of Parkinson’s disease. Annu Int Conf IEEE Eng Med Biol Soc. 2009;2009:3302–5. https://doi.org/10.1109/IEMBS.2009.5333771.

    Article  PubMed  Google Scholar 

  131. Adam EM, Brown EN, Kopell N, McCarthy MM. Deep brain stimulation in the subthalamic nucleus for Parkinson’s disease can restore dynamics of striatal networks. Proc Natl Acad Sci U S A. 2022;119(19):e2120808119. https://doi.org/10.1073/pnas.2120808119.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Agarwal R, Sarma SV. The effects of DBS patterns on basal ganglia activity and thalamic relay : a computational study. J Comput Neurosci. 2012;33(1):151–67. https://doi.org/10.1007/s10827-011-0379-z.

    Article  MathSciNet  PubMed  Google Scholar 

  133. Yu H, Takahashi K, Bloom L, Quaynor SD, Xie T. Effect of deep brain stimulation on swallowing function: a systematic review. Front Neurol. 2020;11:547. https://doi.org/10.3389/fneur.2020.00547.

    Article  PubMed  PubMed Central  Google Scholar 

  134. Xie T, Vigil J, MacCracken E, et al. Low-frequency stimulation of STN-DBS reduces aspiration and freezing of gait in patients with PD. Neurology. 2015;84(4):415–20. https://doi.org/10.1212/WNL.0000000000001184.

    Article  PubMed  PubMed Central  Google Scholar 

  135. Xie T, Bloom L, Padmanaban M, et al. Long-term effect of low frequency stimulation of STN on dysphagia, freezing of gait and other motor symptoms in PD. J Neurol Neurosurg Psychiatry. 2018;89(9):989–94. https://doi.org/10.1136/jnnp-2018-318060.

    Article  PubMed  Google Scholar 

  136. Troche MS, Brandimore AE, Foote KD, et al. Swallowing outcomes following unilateral STN vs GPi surgery: a retrospective analysis. Dysphagia. 2014;29(4):425–31. https://doi.org/10.1007/s00455-014-9522-0.

    Article  PubMed  PubMed Central  Google Scholar 

  137. Robertson LT, St George RJ, Carlson-Kuhta P, Hogarth P, Burchiel KJ, Horak FB. Site of deep brain stimulation and jaw velocity in Parkinson disease. J Neurosurg. 2011;115(5):985–94. https://doi.org/10.3171/2011.7.JNS102173.

    Article  PubMed  PubMed Central  Google Scholar 

  138. Cheng I, Sasegbon A, Hamdy S. Dysphagia treatments in Parkinson’s disease: a systematic review and meta-analysis. Neurogastroenterol Motil. 2022. https://doi.org/10.1111/nmo.14517.

    Article  PubMed  PubMed Central  Google Scholar 

  139. Simons A, Hamdy S. The use of brain stimulation in dysphagia management. Dysphagia. 2017;32(2):209–15. https://doi.org/10.1007/s00455-017-9789-z.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

Nil.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ming-Yen Hsiao.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wei, KC., Wang, TG. & Hsiao, MY. The Cortical and Subcortical Neural Control of Swallowing: A Narrative Review. Dysphagia 39, 177–197 (2024). https://doi.org/10.1007/s00455-023-10613-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00455-023-10613-x

Keywords

Navigation