Skip to main content
Top
Published in: Dysphagia 4/2017

01-08-2017 | Original Article

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

Authors: Jillian A. Toogood, Rebecca C. Smith, Todd K. Stevens, Joe S. Gati, Ravi S. Menon, Julie Theurer, Sarah Weisz, Rebecca H. Affoo, Ruth E. Martin

Published in: Dysphagia | Issue 4/2017

Login to get access

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.
Appendix
Available only for authorised users
Literature
1.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
2.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
3.
go back to reference 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.PubMed 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.PubMed
4.
go back to reference 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.PubMed 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.PubMed
5.
go back to reference 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.PubMed 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.PubMed
6.
go back to reference 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.PubMed 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.PubMed
7.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
9.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
10.
go back to reference 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.PubMed 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.PubMed
11.
go back to reference 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.PubMed 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.PubMed
12.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
13.
go back to reference 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.PubMed 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.PubMed
14.
go back to reference Mosier K, Bereznaya I. Parallel cortical networks for volitional control of swallowing in humans. Exp Brain Res. 2001;140(3):280–9.CrossRefPubMed Mosier K, Bereznaya I. Parallel cortical networks for volitional control of swallowing in humans. Exp Brain Res. 2001;140(3):280–9.CrossRefPubMed
16.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
17.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
18.
go back to reference 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 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
21.
go back to reference Zald DH, Pardo JV. The functional neuroanatomy of voluntary swallowing. Ann Neurol. 1999;46(3):281–6.CrossRefPubMed Zald DH, Pardo JV. The functional neuroanatomy of voluntary swallowing. Ann Neurol. 1999;46(3):281–6.CrossRefPubMed
22.
23.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
25.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
26.
go back to reference Cohen D, Halgren E. Magnetoencephalography. In: Squire LR, editor. Encyclopedia of neuroscience, vol 5. Amsterdam/Boston: Elsevier/Academic Press; 2009. p. 615–22. Cohen D, Halgren E. Magnetoencephalography. In: Squire LR, editor. Encyclopedia of neuroscience, vol 5. Amsterdam/Boston: Elsevier/Academic Press; 2009. p. 615–22.
27.
go back to reference 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.PubMed 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.PubMed
28.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
29.
go back to reference Dum RP, Strick PL. Motor areas in the frontal lobe of the primate. Physiol Behav. 2002;77(4–5):677–82.CrossRefPubMed Dum RP, Strick PL. Motor areas in the frontal lobe of the primate. Physiol Behav. 2002;77(4–5):677–82.CrossRefPubMed
31.
go back to reference 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.PubMed 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.PubMed
32.
33.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
34.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
35.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
36.
go back to reference 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 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
37.
go back to reference 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.PubMed 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.PubMed
38.
go back to reference 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. 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.
go back to reference Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9(1):97–113.CrossRefPubMed Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9(1):97–113.CrossRefPubMed
40.
go back to reference 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.PubMed 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.PubMed
41.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
42.
go back to reference Hu X, Kim SG. Reduction of signal fluctuation in functional MRI using navigator echoes. Magn Reson Med. 1994;31(5):495–503.CrossRefPubMed Hu X, Kim SG. Reduction of signal fluctuation in functional MRI using navigator echoes. Magn Reson Med. 1994;31(5):495–503.CrossRefPubMed
43.
go back to reference Birn RM, Bandettini PA, Cox RW, Shaker R. Event-related fMRI of tasks involving brief motion. Hum Brain Mapp. 1999;7(2):106–14.CrossRefPubMed Birn RM, Bandettini PA, Cox RW, Shaker R. Event-related fMRI of tasks involving brief motion. Hum Brain Mapp. 1999;7(2):106–14.CrossRefPubMed
44.
go back to reference Menon RS. Postacquisition suppression of large-vessel BOLD signals in high-resolution fMRI. Magn Reson Med. 2002;47(1):1–9.CrossRefPubMed Menon RS. Postacquisition suppression of large-vessel BOLD signals in high-resolution fMRI. Magn Reson Med. 2002;47(1):1–9.CrossRefPubMed
45.
go back to reference Goebel R. BrainVoyager. 4.9.2.0 edn. Maastricht: Brain Innovation B.V.; 2000. Goebel R. BrainVoyager. 4.9.2.0 edn. Maastricht: Brain Innovation B.V.; 2000.
46.
go back to reference 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. 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.
47.
go back to reference 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.PubMed 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.PubMed
52.
go back to reference Lagerlof F, Dawes C. The volume of saliva in the mouth before and after swallowing. J Dent Res. 1984;63(5):618–21.CrossRefPubMed Lagerlof F, Dawes C. The volume of saliva in the mouth before and after swallowing. J Dent Res. 1984;63(5):618–21.CrossRefPubMed
55.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
56.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
57.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
58.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
61.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
62.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
65.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
70.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
76.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
78.
go back to reference Augustine JR. Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res Brain Res Rev. 1996;22(3):229–44.CrossRefPubMed Augustine JR. Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res Brain Res Rev. 1996;22(3):229–44.CrossRefPubMed
79.
go back to reference 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. 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.
80.
go back to reference Martin RE, Sessle BJ. The role of the cerebral cortex in swallowing. Dysphagia. 1993;8(3):195–202.CrossRefPubMed Martin RE, Sessle BJ. The role of the cerebral cortex in swallowing. Dysphagia. 1993;8(3):195–202.CrossRefPubMed
81.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
82.
go back to reference Oppenheimer SM, Gelb A, Girvin JP, Hachinski VC. Cardiovascular effects of human insular cortex stimulation. Neurology. 1992;42(9):1727–32.CrossRefPubMed Oppenheimer SM, Gelb A, Girvin JP, Hachinski VC. Cardiovascular effects of human insular cortex stimulation. Neurology. 1992;42(9):1727–32.CrossRefPubMed
87.
88.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
89.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
90.
91.
go back to reference Hamlet SL. Dynamic aspects of lingual propulsive activity in swallowing. Dysphagia. 1989;4(3):136–45.CrossRefPubMed Hamlet SL. Dynamic aspects of lingual propulsive activity in swallowing. Dysphagia. 1989;4(3):136–45.CrossRefPubMed
94.
go back to reference Burton H, Benjamin R. Central projections of the gustatory system. In: Handbook of sensory physiology. Berlin: Springer; 1971. p. 148–63. Burton H, Benjamin R. Central projections of the gustatory system. In: Handbook of sensory physiology. Berlin: Springer; 1971. p. 148–63.
95.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
96.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
97.
go back to reference Weinrich M, Wise SP, Mauritz KH. A neurophysiological study of the premotor cortex in the rhesus monkey. Brain. 1984;107(Pt 2):385–414.CrossRefPubMed Weinrich M, Wise SP, Mauritz KH. A neurophysiological study of the premotor cortex in the rhesus monkey. Brain. 1984;107(Pt 2):385–414.CrossRefPubMed
Metadata
Title
Swallowing Preparation and Execution: Insights from a Delayed-Response Functional Magnetic Resonance Imaging (fMRI) Study
Authors
Jillian A. Toogood
Rebecca C. Smith
Todd K. Stevens
Joe S. Gati
Ravi S. Menon
Julie Theurer
Sarah Weisz
Rebecca H. Affoo
Ruth E. Martin
Publication date
01-08-2017
Publisher
Springer US
Published in
Dysphagia / Issue 4/2017
Print ISSN: 0179-051X
Electronic ISSN: 1432-0460
DOI
https://doi.org/10.1007/s00455-017-9794-2

Other articles of this Issue 4/2017

Dysphagia 4/2017 Go to the issue