Abstract
The aim of the present study was to reveal the spatiotemporal relations among cortical regions involved in the initiation of voluntary swallowing in humans using magnetoencephalography (MEG). As a control task, finger extension movement, which is purely voluntary, was also investigated using the same techniques. The swallowing-related activity was distributed widely for 2000 ms before the electromyogram onset of the right suprahyoid muscle; however, the finger-related activity occurred in the late stage of the recording. The cingulate cortex, the insula, and the inferior frontal gyrus were the main loci active prior to swallowing. These cortical loci coincide with those suggested by previous human brain mapping studies that investigated the brain mechanism which controls swallowing. Activation in the cingulate cortex was registered in the early stage of swallowing and could be related to the cognitive process regarding the food being safe to swallow. The activation in the insula lasted for a long time before the initiation of swallowing. This suggests that the long-lasting activation in the insula prior to swallowing is essential for the initiation of swallowing.
Similar content being viewed by others
References
AJ Miller (1982) ArticleTitleDeglutition Physiol Rev 62 129–184 Occurrence Handle1:STN:280:Bi2C3cnis1E%3D Occurrence Handle7034008
A Jean (2001) ArticleTitleBrain stem control of swallowing: neuronal network and cellular mechanisms Physiol Rev 81 929–969 Occurrence Handle1:STN:280:DC%2BD3M7oslGgtg%3D%3D Occurrence Handle11274347
J Kitagawa T Shingai Y Takahashi Y Yamada (2002) ArticleTitlePharyngeal branch of the glossopharyngeal nerve plays a major role in reflex swallowing from the pharynx Am J Physiol Regul Integr Comp Physiol 282 R1342–R1347 Occurrence Handle1:CAS:528:DC%2BD38XjslWmurw%3D Occurrence Handle11959674
T Sumi (1977) ArticleTitleInterrelation between rhythmic mastication and reflex deglutition as studied on the unitary activity of trigeminal motoneurons in rabbits Jpn J Physiol 27 687–699 Occurrence Handle1:STN:280:CSeC2srgt1U%3D Occurrence Handle613093
M Takagi T Noda Y Yamada (2002) ArticleTitleComparison of SLN-evoked swallows during rest and chewing in the freely behaving rabbit Brain Res 956 74–80 Occurrence Handle10.1016/S0006-8993(02)03481-9 Occurrence Handle1:CAS:528:DC%2BD38Xotl2hs74%3D Occurrence Handle12426048
RE Martin BJ Sessle (1993) ArticleTitleThe role of the cerebral cortex in swallowing Dysphagia 8 195–202 Occurrence Handle1:STN:280:ByyA28rjtVU%3D Occurrence Handle8359039
RE Martin BG Goodyear JS Gati RS Menon (2001) ArticleTitleCerebral cortical representation of automatic and volitional swallowing in humans J Neurophysiol 85 938–950 Occurrence Handle1:STN:280:DC%2BD3M3htlyntA%3D%3D Occurrence Handle11160524
S Hamdy DJ Mikulis A Crawley S Xue H Lau S Henry NE Diamant (1999) ArticleTitleCortical activation during human volitional swallowing: an event-related fMRI study Am J Physiol 277 G219–G225 Occurrence Handle1:CAS:528:DyaK1MXkslKnsbs%3D Occurrence Handle10409170
KM Mosier WC Liu JA Maldjian R Shah B Modi (1999) ArticleTitleLateralization of cortical function in swallowing: a functional MR imaging study Am J Neuroradiol 20 1520–1526 Occurrence Handle1:STN:280:DyaK1MvktVOqsw%3D%3D Occurrence Handle10512240
S Hamdy JC Rothwell DJ Brooks D Bailey Q Aziz DG Thompson (1999) ArticleTitleIdentification of the cerebral loci processing human swallowing with H 152 O PET activation J Neurophysiol 81 1917–1926 Occurrence Handle1:STN:280:DyaK1M3hvVaitA%3D%3D Occurrence Handle10200226
T Nagamine M Kajola R Salmelin H Shibasaki R Hari (1996) ArticleTitleMovement-related slow cortical magnetic fields and changes of spontaneous MEG- and EEG-brain rhythms Electroencephalogr Clin Neurophysiol 99 274–286 Occurrence Handle1:STN:280:ByiD3MrktlI%3D Occurrence Handle8862117
C Gerloff N Uenishi T Nagamine T Kunieda M Hallett H Shibasaki (1998) ArticleTitleCortical activation during fast repetitive finger movements in humans: steady-state movement-related magnetic fields and their cortical generators Electroencephalogr Clin Neurophysiol 109 444–453 Occurrence Handle10.1016/S0924-980X(98)00045-9 Occurrence Handle1:STN:280:DyaK1M%2Fms1KhtQ%3D%3D Occurrence Handle9851302
R Kristeva–Feige S Rossi B Feige T Mergner CH Lucking PM Rossini (1997) ArticleTitleThe bereitschaftspotential paradigm in investigating voluntary movement organization in humans using magnetoencephalography (MEG) Brain Res Brain Res Protoc 1 13–22 Occurrence Handle10.1016/S1385-299X(97)80327-3 Occurrence Handle1:STN:280:DyaK1c%2FktVWqsg%3D%3D Occurrence Handle9385042
CD Tesche (1996) ArticleTitleMEG imaging of neuronal population dynamics in the human thalamus Electroencephalogr Clin Neurophysiol Suppl 47 81–90 Occurrence Handle1:STN:280:ByiH2snmvVM%3D Occurrence Handle9335971
R Loose S Hamdy P Enck (2001) ArticleTitleMagnetoencephalographic response characteristics associated with tongue movement Dysphagia 16 183–185 Occurrence Handle10.1007/s00455-001-0062-z Occurrence Handle1:STN:280:DC%2BD3MvgtFKgtw%3D%3D Occurrence Handle11453564
S Abe Y Watanabe M Shintani M Tazaki M Takahashi GY Yamane Y Ide Y Yamada M Shimono T Ishikawa (2003) ArticleTitleMagnetoencephalographic study of the starting point of voluntary swallowing Cranio 21 46–49 Occurrence Handle12555931
RC Oldfield (1971) ArticleTitleThe assessment and analysis of handedness: the Edinburgh inventory Neuropsychologia 9 97–113 Occurrence Handle10.1016/0028-3932(71)90067-4 Occurrence Handle1:STN:280:CS2C28vgvFc%3D Occurrence Handle5146491
Brodmann K: Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues. Leipzig: Johann Ambrosius Barth 1909, pp. 119–235
JR Pedersen P Johannsen CK Bak B Kofoed K Saermark A Gjedde (1998) ArticleTitleOrigin of human motor readiness field linked to left middle frontal gyrus by MEG and PET Neuroimage 8 214–220 Occurrence Handle10.1006/nimg.1998.0362 Occurrence Handle1:STN:280:DyaK1cvhsVKlsA%3D%3D Occurrence Handle9740763
M Erdler R Beisteiner D Mayer T Kaindl V Edward C Windischberger G Lindinger L Deecke (2000) ArticleTitleSupplementary motor area activation preceding voluntary movement is detectable with a whole-scalp magnetoencephalography system Neuroimage 11 697–707 Occurrence Handle10.1006/nimg.2000.0579 Occurrence Handle1:STN:280:DC%2BD3cvgt1Chsw%3D%3D Occurrence Handle10860797
S Ohara A Ikeda T Kunieda S Yazawa K Baba T Nagamine W Taki N Hashimoto T Mihara H Shibasaki (2000) ArticleTitleMovement-related change of electrocorticographic activity in human supplementary motor area proper Brain 123 1203–1215 Occurrence Handle10.1093/brain/123.6.1203 Occurrence Handle10825358
J Kaiser W Lutzenberger H Preissl D Mosshammer N Birbaumer (2000) ArticleTitleStatistical probability mapping reveals high-frequency magnetoencephalographic activity in supplementary motor area during self-paced finger movements Neurosci Lett 283 81–84 Occurrence Handle10.1016/S0304-3940(00)00921-6 Occurrence Handle1:CAS:528:DC%2BD3cXhvV2lurg%3D Occurrence Handle10729639
C Babiloni F Carducci V Pizzella I Indovina GL Romani PM Rossini F Babiloni (1999) ArticleTitleBilateral neuromagnetic activation of human primary sensorimotor cortex in preparation and execution of unilateral voluntary finger movements Brain Res 827 234–236 Occurrence Handle10.1016/S0006-8993(99)01360-8 Occurrence Handle1:CAS:528:DyaK1MXis1aktrs%3D Occurrence Handle10320716
J Volkmann A Schnitzler OW Witte H Freund (1998) ArticleTitleHandedness and asymmetry of hand representation in human motor cortex J Neurophysiol 79 2149–2154 Occurrence Handle1:STN:280:DyaK1c3gsV2rsA%3D%3D Occurrence Handle9535974
O Devinsky MJ Morrell BA Vogt (1995) ArticleTitleContributions of anterior cingulate cortex to behaviour Brain 118 279–306 Occurrence Handle7895011
RA West CR Laurson (1995) ArticleTitleNeurons of the anterior mesial cortex related to faciovocal activity in the awake monkey J Neurophysiol 74 1856–1869 Occurrence Handle1:STN:280:BymC2M%2FptVQ%3D Occurrence Handle8592179
K Katayama N Takahashi K Ogawara T Hattori (1999) ArticleTitlePure topographical disorientation due to right posterior cingulate lesion Cortex 35 279–282 Occurrence Handle1:STN:280:DyaK1M3psFOktg%3D%3D Occurrence Handle10369100
PM Grasby CD Frith KJ Friston C Bench RS Frackowiak RJ Dolan (1993) ArticleTitleFunctional mapping of brain areas implicated in auditory—verbal memory function Brain 116 1–20 Occurrence Handle8453452
RE Martin P Kemppainen Y Masuda D Yao GM Murray BJ Sessle (1999) ArticleTitleFeatures of cortically evoked swallowing in the awake primate (Macaca fascicularis) J Neurophysiol 82 1529–1541 Occurrence Handle1:STN:280:DyaK1MvhsVansA%3D%3D Occurrence Handle10482767
SK Daniels AL Foundas (1997) ArticleTitleThe role of the insular cortex in dysphagia Dysphagia 12 146–156 Occurrence Handle1:STN:280:ByiA3szpvFE%3D Occurrence Handle9190100
JR Augustine (1996) ArticleTitleCircuitry and functional aspects of the insular lobe in primates including humans Brain Res Rev 22 229–244 Occurrence Handle10.1016/S0165-0173(96)00011-2 Occurrence Handle1:STN:280:ByiC3Mnkslc%3D Occurrence Handle8957561
T Kobayakawa H Endo S Ayabe–Kanamura T Kumagai Y Yamaguchi Y Kikuchi T Takeda S Saito H Ogawa (1996) ArticleTitleThe primary gustatory area in human cerebral cortex studied by magnetoencephalography Neurosci Lett 212 155–158 Occurrence Handle10.1016/0304-3940(96)12798-1 Occurrence Handle1:CAS:528:DyaK28XksVKhtLg%3D Occurrence Handle8843096
W Penfield ME Faulk (1955) ArticleTitleThe insula. Further observations on its function Brain 78 445–470 Occurrence Handle1:STN:280:CymD2crlsV0%3D Occurrence Handle13293263
RJ Schneider DP Friedman M Mishkin (1993) ArticleTitleA modality-specific somatosensory area within the insula of the rhesus monkey Brain Res 621 116–120 Occurrence Handle10.1016/0006-8993(93)90305-7 Occurrence Handle1:STN:280:ByuD3sngvVM%3D Occurrence Handle8221062
ME Raichle (1991) ArticleTitleMemory mechanisms in the processing of words and word-like symbols. Exploring brain functional anatomy with positron tomography Ciba Found Symp 163 198–204 Occurrence Handle1:STN:280:By2B2svnsVE%3D Occurrence Handle1815892
NF Dronkers (1996) ArticleTitleA new brain region for coordinating speech articulation Nature 384 159–161 Occurrence Handle10.1038/384159a0 Occurrence Handle1:CAS:528:DyaK28XmvFGhtr4%3D Occurrence Handle8906789
F Binkofski A Schnitzler P Enck T Frieling S Posse RJ Seitz HJ Freund (1998) ArticleTitleSomatic and limbic cortex activation in esophageal distention: a functional magnetic resonance imaging study Ann Neurol 44 811–815 Occurrence Handle1:STN:280:DyaK1M%2FjsVantQ%3D%3D Occurrence Handle9818938
RM Beckstead JR Morse R Norgren (1980) ArticleTitleThe nucleus of the solitary tract in the monkey: projections to the thalamus and brain stem nuclei J Comp Neurol 190 259–282 Occurrence Handle1:STN:280:Bi%2BB3cvovFY%3D Occurrence Handle6769981
EJ Mufson MM Mesulam (1984) ArticleTitleThalamic connections of the insula in the rhesus monkey and comments on the paralimbic connectivity of the medial pulvinar nucleus J Comp Neurol 227 109–120 Occurrence Handle1:STN:280:BiuB1M%2Fgslw%3D Occurrence Handle6470205
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Watanabe, Y., Abe, S., Ishikawa, T. et al. Cortical Regulation During the Early Stage of Initiation of Voluntary Swallowing in Humans. Dysphagia 19, 100–108 (2004). https://doi.org/10.1007/s00455-003-0509-5
Issue Date:
DOI: https://doi.org/10.1007/s00455-003-0509-5