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RESEARCHARTICLE
Swallowing-relatedneuraloscillation:anintracranialEEG
study
HiroakiHashimoto1,2,3,KazutakaTakahashi4,SeijiKameda1,FumiakiYoshida1,5,
HitoshiMaezawa1,SatoruOshino6,NaokiTani6,HuiMingKhoo6,TakufumiYanagisawa6,
ToshikiYoshimine3,HaruhikoKishima6&MasayukiHirata1,3,6
1DepartmentofNeurologicalDiagnosisandRestoration,GraduateSchoolofMedicine,OsakaUniversity,Yamadaoka2-2,Suita,Osaka,565-0871,
Japan
2DepartmentofNeurosurgery,OtemaeHospital,Chuo-kuOtemae1-5-34,Osaka,Osaka,540-0008,Japan
3EndowedResearchDepartmentofClinicalNeuroengineering,GlobalCenterforMedicalEngineeringandInformatics,OsakaUniversity,
Yamadaoka2-2,Suita,Osaka,565-0871,Japan
4DepartmentofOrganismalBiologyandAnatomy,TheUniversityofChicago,1027E57thSt,Chicago,IL,60637
5DepartmentofAnatomyandPhysiology,SagaMedicalSchoolFacultyofMedicine,SagaUniversity,Nabeshima5-1-1,Saga,Saga,849-8501,Japan
6DepartmentofNeurosurgery,GraduateSchoolofMedicine,OsakaUniversity,Yamadaoka2-2,Suita,Osaka,565-0871,Japan
CorrespondenceAbstract
HiroakiHashimoto,Departmentof
NeurologicalDiagnosisandRestoration,Objective:Swallowingisauniquemovementduetotheindispensableorches-
GraduateSchoolofMedicine,
University,Yamadaoka2-2,Suita,
565-0871,:+81-6-6210-8429;Fax:thattheunderlyingneuralmechanismofswallowingwouldberevealedby
+81-6-6210-8430;E-mail:h-high-:Eightepilepticparticipantsfitted
******@-
MasayukiHirata,DepartmentofNeurological
DiagnosisandRestoration,GraduateSchoolwaterbolusandcorticaloscillatorychanges,includingthehighcband(75–
ofMedicine,OsakaUniversity,Yamadaoka2-150Hz)andbband(13–30Hz),wereinvestigatedatthetimeofmouthopen-
2,Suita,Osaka565-0871,:+81-6-ing,waterinjection,:Increasesinhighcpowerassoci-
6210-8429;Fax:+81-6-6210-8430;E-mail:atedwithmouthopeningwereobservedintheventrolateralprefrontalcortex
******@-(VLPFC)withwaterinjectioninthelateralcentralsulcusandwithswallowing
FundingInformationpower,
ThisworkwassupportedbytheJapanofactivitywasfocalandspecifictoswallowing;however,thebactivitieswere
SocietyforthePromotionofScience(JSPS)
KAKENHI[(Masayukiinvoluntaryswallowing,swallowing-relatedhighcpowerachieveditspeak,and
Hirata),JP18H04166(MasayukiHirata),subsequently,:Wedemonstratedthreedis-
JP18K18366(HiroakiHashimoto)],bythetinctactivitiesrelatedtomouthopening,waterinjection,andswallowing
Communications(MasayukiHirata),byarelatedtoswallowingsuggeststhatduringvoluntaryswallowingphases,thecor-
grantfromtheNationalInstituteof
InformationandCommunicationsTechnologytexisthemaindrivingforceforswallowingasopposedtothebrainstem.
(NICT)(MasayukiHirata),andbyagrant
fromtheNationalInstituteofDentaland
CraniofacialResearch(NIDCR)-RO1
DE023816(KazutakaTakahashi).
Received:14January2021;Revised:26
February2021;Accepted:2March2021
doi:
ª
ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttributionLicense,whichpermitsuse,distributionandreproductioninany
medium,:.
Swallowing-.
IntroductionfMRIhashighspatialresolution,intheorderofmillime-
ters;however,-
Swallowingisaprimitiveandfundamentalfunction,asporalresolutionofMEGishigh,intheorderof
wellasauniquemovementbecausethecooperationmilliseconds19;however,itsspatialresolutionislimited.
betweenvoluntaryandinvoluntarymovementsisneces-Noninvasivemethodshaveeitherweaktemporalorspa-
,theswallowingmove-tialresolution;therefore,weinferredthatsuchmethods
mentisdividedintotwocomponents:voluntaryhadapotentiallimitationfortheinvestigationofneural
-
processingrelatedtoswallowingthattransitionsfromthe
texisassumedtoplayacrucialroleinswallowingmove-voluntarytoinvoluntaryphaseintheorderofmillisec-
,22
triggersswallowingandmodulatesthebrainstem,whereIntracranialEEGs(iEEGs),suchaselectrocorticograms
thecentralpatterngenerator(CPG)forswallowingis(ECoGs),thatrecordneuralactivitiesdirectlyfromthe
,cerebral
3corticalsurfaceofthebrainenableustomeasureneural
cortexdamageduetostrokeorneurodegenerativedis-,
ease4promotesswallowingdisturbance(dysphagia).
usingECoG,wecanmeasurehigh-frequencyneuraloscil-
Theadoptionofdifferentposturesandmodificationoflations,includinghighcbands(>50Hz).Highcactivity
thebolusconsistencyarewidelyacceptedinclinicalprac-isakeyoscillationthatreflectstheneuralprocessingof
–25
sensory,motor,
stimulation,suchaspharyngealelectricalstimulation6or
alsoshowbetterfunctionallocalizationthanthatinlower
transcutaneousneuromuscularstimulation,7andnoninva-23
frequencybandsandhavecometobeknownasuseful
sivebrainstimulationusingrepetitivetranscranialmag-,wehypothe-
neticstimulation(rTMS)8ortranscranialdirectcurrent
sizedthattheanalysisofhighcactivitiesacquiredby
stimulation(tDCS)9arealsobeingstudiedasemerging
ECoGmeasurementswouldbeabletorevealswallowing-
-
fortheseneuromodulationstrategiesfordysphagia;how-
ever,variousintensitiesanddurationshavebeenusedforprovideneuromodulationstrategiesfordysphagiawith
stimulation,10andthebestconditionsforstimulation
beneficialinformation,suchasbrainareasandtimingfor
,thetreatmenteffectsofthesestimulation,thatwillenableustoachievebetterresults.
neuromodulationtherapiesremainlimited,andfurther
studiesarerequiredtoprovideevidenceforovercoming
Wehavecontinuedtoresearchandcontributetothe
fieldofneuromodulationfordysphagiausingourbrain-Participants
machineinterface(BMI),wedevelopedEightpatientswithintractabletemporallobeepilepsypar-
anovelswallow-trackingsystemthatenabledustononin-ticipatedinthisstudy(fourfemales,15–51yearsofage;
,we
)
demonstratedthatdeeptransferlearningappliedto(Table1).TheywereadmittedtoOsakaUniversity
intracranialelectroencephalogram(EEG)signalswasableHospitalfromApril2015toJuly2019andunderwent
-
intracranialelectrodeplacementforaninvasiveEEG
,whichwas
orperipheralorgansregardlessofpatients’
-
executedbythepatients’swallowingintention,ahighersibleconsequencesofthisstudyandwritteninformed
degreeofrecoverywouldbeobtainedbysensoryneuro-
(Nos.
stimulationtriggeredbypatients’,16469).
Theelucidationofswallowing-relatedneuralprocessing
isessentialfortherealizationofsuchaswallow-assisting
,suchasscalpEEG,13positronIntracranialelectrodes
emissiontomography(PET),14near-infraredspectroscopy
1516Foranalysis,wechoseplanar-surfaceplatinumgridelec-
(NIRS),TMS,functionalmagneticresonanceimagingtrodes(495contactsarray)thatwereplacedoverthe
(fMRI),17,18andmagnetoencephalography(MEG),19,20
lateralportionofthecentralsulcuscorrespondingtothe
2ª:.
-RelatedNeuralOscillation
.
NumberoforofacialcontactsNumberofswallowingNumberofmouthopeningNumberofwater
ParticipantSexAgeSide(totalcontacts)instancesinstancesinjections
P1F36L18(68)313131
P2F30L20(84)414141
P3F18R18(55)272727
P4M24L15(69)343434
P5M51L20(72)383838
P6M28R20(96)272727
P7M20L20(94)333333
P8F15L20(68)373737
M,Male;F,Female;R,Right;L,Left.
obtainedfromtheCTimageswereoverlaidontothe3-withthefollowingswallowingstages:stageI(theoral
dimensionalbrainrenderingsfromtheMRIvolumethatstage),stageII(thepharyngealstage),andstageIII(the
wascreatedbyFreeSurfersoftware().ThetimeoftheEGGpeakcorre-
).WeobtainedtheMontrealNeurologi-
calInstitute(MNI)coordinatesoftheimplantedcontactstheoralphaseisvoluntarilycontrolledandthepharyn-
withBrainstormsoftware(,1
instorm/).
thetransitiontimefromvoluntaryswallowingtoinvolun-
taryswallowing().Wecouldalsodetectthetime
Taskandswallowingmonitoring
whentheparticipantopenedhis/hermouthandwhenthe
Theparticipantswereaskedtositonachairandthenexaminerinjectedwaterintotheparticipants’mouth
opentheirmouths,andtheexaminerinjected2mLofusingthevideocapturedbytheRGBcameraofKinect
,whichcorre-
Fornoninvasiveswallowingdetection,weusedanelec-spondedtodifferenttimes,werealsoinsertedintoiEEG
troglottograph(EGG),amicrophone,andamotion-data(thenumberofeachtriggerisshowninTable1).
trackingsystem().Alaryngograph(LaryngographDetailsareprovidedintheDataS1.
Ltd,London,UK)wasusedasanEGGandrecordedthe
neckimpedancechangesassociatedwithswallowing26
Dataacquisitionandpreprocessing
().Soundsofswallowingduetotheboluspassing
throughthepharynxweredetectedbyathroatmicro-TheiEEGsignalsweremeasuredwitha128-channeldigital
phone27().WeconnectedthethroatmicrophoneEEGsystem(EEG2000;NihonKohdenCorporation,
(Inkoumike;SH-12iK,NANZU,Shizuoka,Japan)totheTokyo,Japan).Beforeanyfurtherprocessing,contactscon-
.
Wecapturedthemotionoftheparticipantsat30Throughoutthefollowinganalyses,aband-passfilterusing
framespersecondwiththemotion-trackingsystem,atwo-wayleast-squaresfiniteimpulseresponsefilter
whichwasnewlydevelopedbyususingKinectv2(Micro-(,
soft,Redmond,Washington,USA).11)wasappliedtothe
Anelectricstimulator(NS-101;UniqueMedical,.
Tokyo,Japan)supplieddigitalsynchronizingsignalsto
thelaryngographanda128-channeldigitalEEGsystem.
Spectralanalyses
Themultimodaldataweresynchronizedandenabledus
-frequencyanalysisofthetime-lockediEEGsignals
-
quencyrangefrom1to330Hzandspectralpower(in
dB)