Skip to main content
SpringerLink
Log in

Swallowing Preparation and Execution: Insights from a Delayed-Response Functional Magnetic Resonance Imaging (fMRI) Study

  • Original Article
  • Published:
Dysphagia Aims and scope Submit manuscript

Abstract

The present study sought to elucidate the functional contributions of sub-regions of the swallowing neural network in swallowing preparation and swallowing motor execution. Seven healthy volunteers participated in a delayed-response, go, no-go functional magnetic resonance imaging study involving four semi-randomly ordered activation tasks: (i) “prepare to swallow,” (ii) “voluntary saliva swallow,” (iii) “do not prepare to swallow,” and (iv) “do not swallow.” Results indicated that brain activation was significantly greater during swallowing preparation, than during swallowing execution, within the rostral and intermediate anterior cingulate cortex bilaterally, premotor cortex (left > right hemisphere), pericentral cortex (left > right hemisphere), and within several subcortical nuclei including the bilateral thalamus, caudate, and putamen. In contrast, activation within the bilateral insula and the left dorsolateral pericentral cortex was significantly greater in relation to swallowing execution, compared with swallowing preparation. Still other regions, including a more inferior ventrolateral pericentral area, and adjoining Brodmann area 43 bilaterally, and the supplementary motor area, were activated in relation to both swallowing preparation and execution. These findings support the view that the preparation, and subsequent execution, of swallowing are mediated by a cascading pattern of activity within the sub-regions of the bilateral swallowing neural network.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Dziewas R, Soros P, Ishii R, Chau W, Henningsen H, Ringelstein EB, Knecht S, Pantev C. Neuroimaging evidence for cortical involvement in the preparation and in the act of swallowing. Neuroimage. 2003;20(1):135–44.

    Article  CAS  PubMed  Google Scholar 

  2. Furlong PL, Hobson AR, Aziz Q, Barnes GR, Singh KD, Hillebrand A, Thompson DG, Hamdy S. 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. doi:10.1016/j.neuroimage.2004.02.041.

    Article  CAS  PubMed  Google Scholar 

  3. 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.

    CAS  PubMed  Google Scholar 

  4. 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(4):G531–8.

    CAS  PubMed  Google Scholar 

  5. 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.

    CAS  PubMed  Google Scholar 

  6. Hamdy S, Mikulis DJ, Crawley A, Xue S, Lau H, Henry S, Diamant NE. Cortical activation during human volitional swallowing: an event-related fMRI study. Am J Physiol. 1999;277(1 Pt 1):G219–25.

    CAS  PubMed  Google Scholar 

  7. Lund JP, Lamarre Y. Activity of neurons in the lower precentral cortex during voluntary and rhythmical jaw movements in the monkey. Exp Brain Res. 1974;19(3):282–99.

    Article  CAS  PubMed  Google Scholar 

  8. Malandraki GA, Sutton BP, Perlman AL, Karampinos DC. Age-related differences in laterality of cortical activations in swallowing. Dysphagia. 2010;25(3):238–49. doi:10.1007/s00455-009-9250-z.

    Article  PubMed  Google Scholar 

  9. 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. doi:10.1002/hbm.20743.

    Article  PubMed  Google Scholar 

  10. Martin RE, Goodyear BG, Gati JS, Menon RS. Cerebral cortical representation of automatic and volitional swallowing in humans. J Neurophysiol. 2001;85(2):938–50.

    CAS  PubMed  Google Scholar 

  11. Martin RE, Kemppainen P, Masuda Y, Yao D, Murray GM, Sessle BJ. Features of cortically evoked swallowing in the awake primate (Macaca fascicularis). J Neurophysiol. 1999;82(3):1529–41.

    CAS  PubMed  Google Scholar 

  12. 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(4):2428–43. doi:10.1152/jn.01144.2003.

    Article  PubMed  Google Scholar 

  13. Martin RE, Murray GM, Kemppainen P, Masuda Y, Sessle BJ. Functional properties of neurons in the primate tongue primary motor cortex during swallowing. J Neurophysiol. 1997;78(3):1516–30.

    CAS  PubMed  Google Scholar 

  14. Mosier K, Bereznaya I. Parallel cortical networks for volitional control of swallowing in humans. Exp Brain Res. 2001;140(3):280–9.

    Article  CAS  PubMed  Google Scholar 

  15. 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. doi:10.1097/00005537-199909000-00011.

    Article  CAS  PubMed  Google Scholar 

  16. 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. doi:10.1007/s00221-004-2048-1.

    Article  PubMed  Google Scholar 

  17. 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(1–2):40–55.

    Article  CAS  PubMed  Google Scholar 

  18. Yao D, Yamamura K, Narita N, Martin RE, Murray GM, Sessle BJ. Neuronal activity patterns in primate primary motor cortex related to trained or semiautomatic jaw and tongue movements. J Neurophysiol. 2002;87(5):2531–41.

    PubMed  Google Scholar 

  19. Teismann IK, Steinstraeter O, Warnecke T, Zimmermann J, Ringelstein EB, Pantev C, Dziewas R. Cortical recovery of swallowing function in wound botulism. BMC Neurol. 2008;8:13. doi:10.1186/1471-2377-8-13.

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  21. Zald DH, Pardo JV. The functional neuroanatomy of voluntary swallowing. Ann Neurol. 1999;46(3):281–6.

    Article  CAS  PubMed  Google Scholar 

  22. 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. doi:10.1007/s00455-002-0088-x.

    Article  PubMed  Google Scholar 

  23. 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(1):140–5.

    Article  CAS  PubMed  Google Scholar 

  24. Teismann IK, Steinstraeter O, Stoeckigt K, Suntrup S, Wollbrink A, Pantev C, Dziewas R. Functional oropharyngeal sensory disruption interferes with the cortical control of swallowing. BMC Neurosci. 2007;8:62. doi:10.1186/1471-2202-8-62.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Mihai PG, Otto M, Platz T, Eickhoff SB, Lotze M. Sequential evolution of cortical activity and effective connectivity of swallowing using fMRI. Hum Brain Mapp. 2014;35(12):5962–73. doi:10.1002/hbm.22597.

    Article  PubMed  Google Scholar 

  26. Cohen D, Halgren E. Magnetoencephalography. In: Squire LR, editor. Encyclopedia of neuroscience, vol 5. Amsterdam/Boston: Elsevier/Academic Press; 2009. p. 615–22.

  27. Alexander GE, Crutcher MD. Preparation for movement: neural representations of intended direction in three motor areas of the monkey. J Neurophysiol. 1990;64(1):133–50.

    CAS  PubMed  Google Scholar 

  28. Backus DA, Ye S, Russo GS, Crutcher MD. Neural activity correlated with the preparation and execution of visually guided arm movements in the cingulate motor area of the monkey. Exp Brain Res. 2001;140(2):182–9.

    Article  CAS  PubMed  Google Scholar 

  29. Dum RP, Strick PL. Motor areas in the frontal lobe of the primate. Physiol Behav. 2002;77(4–5):677–82.

    Article  CAS  PubMed  Google Scholar 

  30. Lee KM, Chang KH, Roh JK. Subregions within the supplementary motor area activated at different stages of movement preparation and execution. Neuroimage. 1999;9(1):117–23. doi:10.1006/nimg.1998.0393.

    Article  CAS  PubMed  Google Scholar 

  31. Riehle A, Requin J. Monkey primary motor and premotor cortex: single-cell activity related to prior information about direction and extent of an intended movement. J Neurophysiol. 1989;61(3):534–49.

    CAS  PubMed  Google Scholar 

  32. Russo GS, Backus DA, Ye S, Crutcher MD. Neural activity in monkey dorsal and ventral cingulate motor areas: comparison with the supplementary motor area. J Neurophysiol. 2002;88(5):2612–29. doi:10.1152/jn.00306.2002.

    Article  PubMed  Google Scholar 

  33. Yazawa S, Ikeda A, Kunieda T, Ohara S, Mima T, Nagamine T, Taki W, Kimura J, Hori T, Shibasaki H. Human presupplementary motor area is active before voluntary movement: subdural recording of Bereitschafts potential from medial frontal cortex. Exp Brain Res. 2000;131(2):165–77.

    Article  CAS  PubMed  Google Scholar 

  34. Zang Y, Jia F, Weng X, Li E, Cui S, Wang Y, Hazeltine E, Ivry R. Functional organization of the primary motor cortex characterized by event-related fMRI during movement preparation and execution. Neurosci Lett. 2003;337(2):69–72.

    Article  CAS  PubMed  Google Scholar 

  35. Cunnington R, Windischberger C, Deecke L, Moser E. The preparation and readiness for voluntary movement: a high-field event-related fMRI study of the Bereitschafts-BOLD response. Neuroimage. 2003;20(1):404–12.

    Article  PubMed  Google Scholar 

  36. Simon SR, Meunier M, Piettre L, Berardi AM, Segebarth CM, Boussaoud D. Spatial attention and memory versus motor preparation: premotor cortex involvement as revealed by fMRI. J Neurophysiol. 2002;88(4):2047–57.

    PubMed  Google Scholar 

  37. Weilke F, Spiegel S, Boecker H, von Einsiedel HG, Conrad B, Schwaiger M, Erhard P. Time-resolved fMRI of activation patterns in M1 and SMA during complex voluntary movement. J Neurophysiol. 2001;85(5):1858–63.

    CAS  PubMed  Google Scholar 

  38. Toogood JA, Smith RC, Stevens TK, Gati JS, Menon RS, Martin RE. Distinguishing swallowing preparation and swallowing execution with event-related functional magnetic resonance imaging (fMRI). In: Human brain mapping meeting, Florence, Italy, June 2006, 2006.

  39. Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9(1):97–113.

    Article  CAS  PubMed  Google Scholar 

  40. Logemann JA, Kahrilas PJ, Cheng J, Pauloski BR, Gibbons PJ, Rademaker AW, Lin S. Closure mechanisms of laryngeal vestibule during swallow. Am J Physiol. 1992;262(2 Pt 1):G338–44.

    CAS  PubMed  Google Scholar 

  41. Barberi EA, Gati JS, Rutt BK, Menon RS. A transmit-only/receive-only (TORO) RF system for high-field MRI/MRS applications. Magn Reson Med. 2000;43(2):284–9.

    Article  CAS  PubMed  Google Scholar 

  42. Hu X, Kim SG. Reduction of signal fluctuation in functional MRI using navigator echoes. Magn Reson Med. 1994;31(5):495–503.

    Article  CAS  PubMed  Google Scholar 

  43. Birn RM, Bandettini PA, Cox RW, Shaker R. Event-related fMRI of tasks involving brief motion. Hum Brain Mapp. 1999;7(2):106–14.

    Article  CAS  PubMed  Google Scholar 

  44. Menon RS. Postacquisition suppression of large-vessel BOLD signals in high-resolution fMRI. Magn Reson Med. 2002;47(1):1–9.

    Article  PubMed  Google Scholar 

  45. Goebel R. BrainVoyager. 4.9.2.0 edn. Maastricht: Brain Innovation B.V.; 2000.

    Google Scholar 

  46. Talairach J, Tournoux P. Co-planar stereotaxic atlas of the human brain: 3-dimensional proportional system: an approach to cerebral imaging. New York: Georg Thieme; 1988.

    Google Scholar 

  47. Boynton GM, Engel SA, Glover GH, Heeger DJ. Linear systems analysis of functional magnetic resonance imaging in human V1. J Neurosci. 1996;16(13):4207–21.

    CAS  PubMed  Google Scholar 

  48. Cohen MS. Parametric analysis of fMRI data using linear systems methods. Neuroimage. 1997;6(2):93–103. doi:10.1006/nimg.1997.0278.

    Article  CAS  PubMed  Google Scholar 

  49. Paus T. Primate anterior cingulate cortex: where motor control, drive and cognition interface. Nat Rev Neurosci. 2001;2(6):417–24. doi:10.1038/35077500.

    Article  CAS  PubMed  Google Scholar 

  50. Sahyoun C, Floyer-Lea A, Johansen-Berg H, Matthews PM. Towards an understanding of gait control: brain activation during the anticipation, preparation and execution of foot movements. Neuroimage. 2004;21(2):568–75. doi:10.1016/j.neuroimage.2003.09.065.

    Article  CAS  PubMed  Google Scholar 

  51. Hanakawa T, Dimyan MA, Hallett M. Motor planning, imagery, and execution in the distributed motor network: a time-course study with functional MRI. Cereb Cortex. 2008;18(12):2775–88. doi:10.1093/cercor/bhn036.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Lagerlof F, Dawes C. The volume of saliva in the mouth before and after swallowing. J Dent Res. 1984;63(5):618–21.

    Article  CAS  PubMed  Google Scholar 

  53. Okada A, Honma M, Nomura S, Yamada Y. Oral behavior from food intake until terminal swallow. Physiol Behav. 2007;90(1):172–9. doi:10.1016/j.physbeh.2006.09.032.

    Article  CAS  PubMed  Google Scholar 

  54. Steele CM, Miller AJ. Sensory input pathways and mechanisms in swallowing: a review. Dysphagia. 2010;25(4):323–33. doi:10.1007/s00455-010-9301-5.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Akkal D, Bioulac B, Audin J, Burbaud P. Comparison of neuronal activity in the rostral supplementary and cingulate motor areas during a task with cognitive and motor demands. Eur J Neurosci. 2002;15(5):887–904.

    Article  CAS  PubMed  Google Scholar 

  56. Hoshi E, Tanji J. Differential roles of neuronal activity in the supplementary and presupplementary motor areas: from information retrieval to motor planning and execution. J Neurophysiol. 2004;92(6):3482–99. doi:10.1152/jn.00547.2004.

    Article  PubMed  Google Scholar 

  57. Thickbroom GW, Byrnes ML, Sacco P, Ghosh S, Morris IT, Mastaglia FL. The role of the supplementary motor area in externally timed movement: the influence of predictability of movement timing. Brain Res. 2000;874(2):233–41.

    Article  CAS  PubMed  Google Scholar 

  58. Wildgruber D, Erb M, Klose U, Grodd W. Sequential activation of supplementary motor area and primary motor cortex during self-paced finger movement in human evaluated by functional MRI. Neurosci Lett. 1997;227(3):161–4.

    Article  CAS  PubMed  Google Scholar 

  59. Elsinger CL, Harrington DL, Rao SM. From preparation to online control: reappraisal of neural circuitry mediating internally generated and externally guided actions. Neuroimage. 2006;31(3):1177–87. doi:10.1016/j.neuroimage.2006.01.041.

    Article  CAS  PubMed  Google Scholar 

  60. Paradiso G, Cunic D, Saint-Cyr JA, Hoque T, Lozano AM, Lang AE, Chen R. Involvement of human thalamus in the preparation of self-paced movement. Brain. 2004;127(Pt 12):2717–31. doi:10.1093/brain/awh288.

    Article  PubMed  Google Scholar 

  61. Lotze M, Montoya P, Erb M, Hulsmann E, Flor H, Klose U, Birbaumer N, Grodd W. Activation of cortical and cerebellar motor areas during executed and imagined hand movements: an fMRI study. J Cogn Neurosci. 1999;11(5):491–501.

    Article  CAS  PubMed  Google Scholar 

  62. Roth M, Decety J, Raybaudi M, Massarelli R, Delon-Martin C, Segebarth C, Morand S, Gemignani A, Decorps M, Jeannerod M. Possible involvement of primary motor cortex in mentally simulated movement: a functional magnetic resonance imaging study. NeuroReport. 1996;7(7):1280–4.

    Article  CAS  PubMed  Google Scholar 

  63. Fassbender C, Murphy K, Foxe JJ, Wylie GR, Javitt DC, Robertson IH, Garavan H. A topography of executive functions and their interactions revealed by functional magnetic resonance imaging. Brain Res Cogn Brain Res. 2004;20(2):132–43. doi:10.1016/j.cogbrainres.2004.02.007.

    Article  CAS  PubMed  Google Scholar 

  64. Glascher J, Adolphs R, Damasio H, Bechara A, Rudrauf D, Calamia M, Paul LK, Tranel D. Lesion mapping of cognitive control and value-based decision making in the prefrontal cortex. Proc Natl Acad Sci USA. 2012;109(36):14681–6. doi:10.1073/pnas.1206608109.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Gonzalez-Rosa JJ, Inuggi A, Blasi V, Cursi M, Annovazzi P, Comi G, Falini A, Leocani L. Response competition and response inhibition during different choice-discrimination tasks: evidence from ERP measured inside MRI scanner. Int J Psychophysiol. 2013;89(1):37–47. doi:10.1016/j.ijpsycho.2013.04.021.

    Article  PubMed  Google Scholar 

  66. Rushworth MF, Behrens TE. Choice, uncertainty and value in prefrontal and cingulate cortex. Nat Neurosci. 2008;11(4):389–97. doi:10.1038/nn2066.

    Article  CAS  PubMed  Google Scholar 

  67. Simmonds DJ, Pekar JJ, Mostofsky SH. Meta-analysis of Go/No-go tasks demonstrating that fMRI activation associated with response inhibition is task-dependent. Neuropsychologia. 2008;46(1):224–32. doi:10.1016/j.neuropsychologia.2007.07.015.

    Article  PubMed  Google Scholar 

  68. Ohara S, Lenz FA. Medial lateral extent of thermal and pain sensations evoked by microstimulation in somatic sensory nuclei of human thalamus. J Neurophysiol. 2003;90(4):2367–77. doi:10.1152/jn.00450.2003.

    Article  PubMed  Google Scholar 

  69. Li S, Stevens JA, Rymer WZ. Interactions between imagined movement and the initiation of voluntary movement: a TMS study. Clin Neurophysiol. 2009;120(6):1154–60. doi:10.1016/j.clinph.2008.12.045.

    Article  PubMed  PubMed Central  Google Scholar 

  70. Hamdy S, Aziz Q, Rothwell JC, Singh KD, Barlow J, Hughes DG, Tallis RC, Thompson DG. The cortical topography of human swallowing musculature in health and disease. Nat Med. 1996;2(11):1217–24.

    Article  CAS  PubMed  Google Scholar 

  71. Hamdy S, Aziz Q, Rothwell JC, Crone R, Hughes D, Tallis RC, Thompson DG. Explaining oropharyngeal dysphagia after unilateral hemispheric stroke. Lancet. 1997;350(9079):686–92. doi:10.1016/S0140-6736(97)02068-0.

    Article  CAS  PubMed  Google Scholar 

  72. Daniels SK, Foundas AL. The role of the insular cortex in dysphagia. Dysphagia. 1997;12(3):146–56. doi:10.1007/PL00009529.

    Article  CAS  PubMed  Google Scholar 

  73. Riecker A, Gastl R, Kuhnlein P, Kassubek J, Prosiegel M. Dysphagia due to unilateral infarction in the vascular territory of the anterior insula. Dysphagia. 2009;24(1):114–8. doi:10.1007/s00455-008-9164-1.

    Article  PubMed  Google Scholar 

  74. Mulak A, Kahane P, Hoffmann D, Minotti L, Bonaz B. Brain mapping of digestive sensations elicited by cortical electrical stimulations. Neurogastroenterol Motil. 2008;20(6):588–96. doi:10.1111/j.1365-2982.2007.01066.x.

    Article  CAS  PubMed  Google Scholar 

  75. Soros P, Marmurek J, Tam F, Baker N, Staines WR, Graham SJ. Functional MRI of working memory and selective attention in vibrotactile frequency discrimination. BMC Neurosci. 2007;8:48. doi:10.1186/1471-2202-8-48.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Small DM, Gregory MD, Mak YE, Gitelman D, Mesulam MM, Parrish T. Dissociation of neural representation of intensity and affective valuation in human gustation. Neuron. 2003;39(4):701–11.

    Article  CAS  PubMed  Google Scholar 

  77. Jabbi M, Bastiaansen J, Keysers C. A common anterior insula representation of disgust observation, experience and imagination shows divergent functional connectivity pathways. PLoS ONE. 2008;3(8):e2939. doi:10.1371/journal.pone.0002939.

    Article  PubMed  PubMed Central  Google Scholar 

  78. Augustine JR. Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res Brain Res Rev. 1996;22(3):229–44.

    Article  CAS  PubMed  Google Scholar 

  79. Krakauer J, Ghez C. Voluntary movement. In: Kandel E, Schwartz J, Jessell T, editors. Principles of neural science. 4th ed. New York: McGraw-Hill; 2000. p. 756–81.

    Google Scholar 

  80. Martin RE, Sessle BJ. The role of the cerebral cortex in swallowing. Dysphagia. 1993;8(3):195–202.

    Article  CAS  PubMed  Google Scholar 

  81. Al-Otaibi F, Wong SW, Shoemaker JK, Parrent AG, Mirsattari SM. The cardioinhibitory responses of the right posterior insular cortex in an epileptic patient. Stereotact Funct Neurosurg. 2010;88(6):390–7. doi:10.1159/000321182.

    Article  PubMed  Google Scholar 

  82. Oppenheimer SM, Gelb A, Girvin JP, Hachinski VC. Cardiovascular effects of human insular cortex stimulation. Neurology. 1992;42(9):1727–32.

    Article  CAS  PubMed  Google Scholar 

  83. 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. doi:10.1002/hbm.20680.

    Article  PubMed  Google Scholar 

  84. Soros P, Al-Otaibi F, Wong SW, Shoemaker JK, Mirsattari SM, Hachinski V, Martin RE. Stuttered swallowing: electric stimulation of the right insula interferes with water swallowing. A case report. BMC Neurol. 2011;11:20. doi:10.1186/1471-2377-11-20.

    Article  PubMed  PubMed Central  Google Scholar 

  85. Isnard J, Guenot M, Sindou M, Mauguiere F. Clinical manifestations of insular lobe seizures: a stereo-electroencephalographic study. Epilepsia. 2004;45(9):1079–90. doi:10.1111/j.0013-9580.2004.68903.x.

    Article  PubMed  Google Scholar 

  86. Afif A, Minotti L, Kahane P, Hoffmann D. Anatomofunctional organization of the insular cortex: a study using intracerebral electrical stimulation in epileptic patients. Epilepsia. 2010;51(11):2305–15. doi:10.1111/j.1528-1167.2010.02755.x.

    Article  PubMed  Google Scholar 

  87. Ehrsson HH, Geyer S, Naito E. Imagery of voluntary movement of fingers, toes, and tongue activates corresponding body-part-specific motor representations. J Neurophysiol. 2003;90(5):3304–16. doi:10.1152/jn.01113.2002.

    Article  PubMed  Google Scholar 

  88. Nair DG, Purcott KL, Fuchs A, Steinberg F, Kelso JA. Cortical and cerebellar activity of the human brain during imagined and executed unimanual and bimanual action sequences: a functional MRI study. Brain Res Cogn Brain Res. 2003;15(3):250–60.

    Article  PubMed  Google Scholar 

  89. Stippich C, Ochmann H, Sartor K. Somatotopic mapping of the human primary sensorimotor cortex during motor imagery and motor execution by functional magnetic resonance imaging. Neurosci Lett. 2002;331(1):50–4.

    Article  CAS  PubMed  Google Scholar 

  90. Dodds WJ, Man KM, Cook IJ, Kahrilas PJ, Stewart ET, Kern MK. Influence of bolus volume on swallow-induced hyoid movement in normal subjects. Am J Roentgenol. 1988;150(6):1307–9. doi:10.2214/ajr.150.6.1307.

    Article  CAS  Google Scholar 

  91. Hamlet SL. Dynamic aspects of lingual propulsive activity in swallowing. Dysphagia. 1989;4(3):136–45.

    Article  CAS  PubMed  Google Scholar 

  92. Saper CB. Hypothalamic connections with the cerebral cortex. Prog Brain Res. 2000;126:39–48. doi:10.1016/S0079-6123(00)26005-6.

    Article  CAS  PubMed  Google Scholar 

  93. Hodge CJ Jr, Huckins SC, Szeverenyi NM, Fonte MM, Dubroff JG, Davuluri K. Patterns of lateral sensory cortical activation determined using functional magnetic resonance imaging. J Neurosurg. 1998;89(5):769–79. doi:10.3171/jns.1998.89.5.0769.

    Article  PubMed  Google Scholar 

  94. Burton H, Benjamin R. Central projections of the gustatory system. In: Handbook of sensory physiology. Berlin: Springer; 1971. p. 148–63.

  95. Cerf B, Lebihan D, Van de Moortele PF, MacLeod P, Faurion A. Functional lateralization of human gustatory cortex related to handedness disclosed by fMRI study. Ann NY Acad Sci. 1998;855:575–8.

    Article  CAS  PubMed  Google Scholar 

  96. Faurion A, Cerf B, Le Bihan D, Pillias AM. fMRI study of taste cortical areas in humans. Ann NY Acad Sci. 1998;855:535–45.

    Article  CAS  PubMed  Google Scholar 

  97. Weinrich M, Wise SP, Mauritz KH. A neurophysiological study of the premotor cortex in the rhesus monkey. Brain. 1984;107(Pt 2):385–414.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by: Premier’s Research Excellence Award (to Ruth E. Martin), Ontario Ministry of Health Career Scientist Award (to Ruth E. Martin), Natural Sciences and Engineering Research Council (NSERC) Grant (to Ruth E. Martin), Canadian Research Chair Support (to Ravi S. Menon), and Canadian Institutes of Health Research (CIHR) Maintenance Grant (to Ravi S. Menon), Ontario Graduates Scholarship (OGS) (to Jillian A. Toogood).

Author information

Authors and Affiliations

  1. Western University, London, ON, N6A 5B9, Canada

    Jillian A. Toogood, Rebecca C. Smith, Julie Theurer, Sarah Weisz & Ruth E. Martin

  2. Dalhousie University, Halifax, Canada

    Todd K. Stevens

  3. Robarts Research Institute, London, Canada

    Joe S. Gati & Ravi S. Menon

  4. Central Michigan University, Mount Pleasant, USA

    Rebecca H. Affoo

Authors
  1. Jillian A. Toogood
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rebecca C. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Todd K. Stevens
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Joe S. Gati
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ravi S. Menon
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Julie Theurer
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sarah Weisz
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Rebecca H. Affoo
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Ruth E. Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ruth E. Martin.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 29 kb)

Supplementary material 2 (DOCX 33 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Toogood, J.A., Smith, R.C., Stevens, T.K. et al. Swallowing Preparation and Execution: Insights from a Delayed-Response Functional Magnetic Resonance Imaging (fMRI) Study. Dysphagia 32, 526–541 (2017). https://doi.org/10.1007/s00455-017-9794-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00455-017-9794-2

Keywords

Search

Navigation