www.bjorl.org
Brazilian
Journal
of
OTORHINOLARYNGOLOGY
ORIGINAL
ARTICLE
The
investigation
of
semantic
memory
deficit
in
chronic
tinnitus:
a
behavioral
report
夽
Maryam
Karimi
Boroujeni
a,
Saeid
Mahmoudian
b,
Farnoush
Jarollahi
a,∗aIranUniversityofMedicalSciences(IUMS),SchoolofRehabilitationSciences,DepartmentofAudiology,Tehran,Iran bIranUniversityofMedicalSciences(IUMS),ENTandHead&NeckResearchCenter,Tehran,Iran
Received14April2018;accepted5November2018 Availableonline28December2018
KEYWORDS Tinnitus; Semantics; Memory
Abstract
Introduction:Tinnitusisacentralauditorydisorderinwhichdifferentprocessingsystemsare involvedasanetwork.Oneofthesenetworksismemory.Previousstudieshavedemonstrated somedeficitsinvarioustypesofmemoryinchronictinnitus.
Objectives: Themainpurposeofthepresentstudywastoinvestigatethesemanticmemory, whichisnotyetinvestigatedinthetinnituspopulation.
Methods:Inthiscase---controlstudy,15subjectswithchronictinnitusand16matchedhealthy controlswereincluded.40semanticallyrelatedand40semanticallyunrelatedwordpairswere presentedtotheparticipantsinacounter-balancedfashion.Theywereaskedtomakedecision abouttheirsemanticrelatedness.Thentheparticipants’reactiontimesandtheaccuracyof responseswerecalculated.
Results:Meanofreactiontimeswere significantlylongerinthetinnitus group(M=1034ms, SD=0.31) compared to the controlgroup (Mean=1016ms, SD=0.13),p<0.05. However, no significantdifference wasfoundfor themeanpercentageofcorrectresponsesbetweenthe twogroups.
Conclusion: Thecurrentstudyprovidedbehavioralevidencethatchronictinnituscanaffect thesemanticmemory.Suchbehavioraloutcomesmayprovidenewinsightsintomoreresearch activitiesinthefieldofelectrophysiologyandneuroimaginginthetinnituspopulation. © 2018 Associac¸˜ao Brasileira de Otorrinolaringologia e Cirurgia C´ervico-Facial. Published by Elsevier Editora Ltda. This is an open access article under the CC BY license (http:// creativecommons.org/licenses/by/4.0/).
夽 Pleasecitethisarticle as:KarimiBoroujeniM,MahmoudianS,Jarollahi F.Theinvestigationofsemanticmemory deficitinchronic tinnitus:abehavioralreport.BrazJOtorhinolaryngol.2020;86:185---90.
∗Correspondingauthor.
E-mail:jarollahi.f@iums.ac.ir(F.Jarollahi).
PeerReviewundertheresponsibilityofAssociac¸ãoBrasileiradeOtorrinolaringologiaeCirurgiaCérvico-Facial. https://doi.org/10.1016/j.bjorl.2018.11.003
1808-8694/©2018Associac¸˜aoBrasileiradeOtorrinolaringologiaeCirurgiaC´ervico-Facial.PublishedbyElsevierEditoraLtda.Thisisanopen accessarticleundertheCCBYlicense(http://creativecommons.org/licenses/by/4.0/).
PALAVRAS-CHAVE Zumbido;
Semântica; Memória
Investigac¸ãododéficitdememóriasemânticanozumbidocrônico:umrelato comportamental
Resumo
Introduc¸ão:Ozumbidoéumdistúrbioauditivocentral,noqualdiferentessistemasde processa-mentoestãoenvolvidoscomoemumarede.Umadessasredeséamemória.Estudosanteriores demonstraramalgunsdéficitsemváriostiposdememórianozumbidocrônico.
Objetivos: Investigaramemóriasemântica,queaindanãofoiinvestigadanapopulac¸ãocom zumbido.
Método: Nesteestudo de caso-controle,15 indivíduos comzumbido crônico e16 controles saudáveis pareados foram incluídos; 40 pares de palavras semanticamente relacionados e 40 semanticamente não relacionados foram apresentados aos participantes de forma contrabalanc¸ada.Eles foram instruídos a tomar decisões sobre sua relac¸ão semântica. Em seguida,ostemposdereac¸ãodosparticipanteseaprecisãodasrespostasforamcalculados.
Resultados: Amédiadostemposdereac¸ãofoisignificativamentemaiornogrupocomzumbido (M=1,034ms, DP=0,31) em comparac¸ão ao grupo controle (média=1016ms, DP=0,13),
p<0,05.Entretanto,nenhumadiferenc¸asignificantefoiencontradaparaaporcentagemmédia derespostascorretasentreosdoisgrupos.
Conclusão:Opresenteestudoforneceuevidênciascomportamentaisdequeozumbidocrônico pode afetar a memória semântica. Tais resultados comportamentais podem levar a novas percepc¸ões emmaisatividades depesquisanocampodaeletrofisiologiaeneuroimagemna populac¸ãocomzumbido.
© 2018 Associac¸˜ao Brasileira de Otorrinolaringologia e Cirurgia C´ervico-Facial. Publicado por Elsevier Editora Ltda. Este ´e um artigo Open Access sob uma licenc¸a CC BY (http:// creativecommons.org/licenses/by/4.0/).
Introduction
Tinnitusas an auditory phantom perception refers tothe
consciousexperienceofsoundintheabsenceofany
exter-nal acoustic stimuli.1---5 Being considered as a subjective
perception, tinnitus can affect quality of life differently
inpeopleexperiencingit.6Whereassometinnituspatients
cancopewiththeirtinnitusperfectly,othersabysmally
suf-ferfromtheconsequencesresultingfromchronic tinnitus,
suchas anxiety,depression, sleepdisturbance, emotional
disorders,workimpairment,andconcentrationproblems.In
severeconditions,maladaptedcopingbehaviorsmayleadto
suicide.7---10
Suchsymptoms andproblems refer totheinvolvement
of non-auditory areas of the brain which work as a
net-workalongsidetheauditorycortex,albeit,thisco-existing
mechanismsarestillcontroversial.11,12Recentstudieshave
revealedtheinvolvementofnon-auditorystructures,most
notably thoseinvolved in memory, cognitive, attentional,
andemotionalnetworksinchronictinnitus.1,13,14
Specifically, the memory system as oneof the
compo-nentsofthisnetworkplaysasignificantroleintheawareness
oftinnitusandtinnitus-relateddistress.7,11Previousstudies
have revealed that the hippocampus and
parahippocam-palareaswerefunctionallyalteredinchronictinnitus.4,11,15
These regions are crucial in short-term memory and
auditory-verbalmemory.16,17Suchtheseabnormalitieshave
beendetectedinthedorsolateralprefrontalcortexwhichis
involvedin workingmemory.4,18,19 Moreover,theamygdala
andlimbicsystemhavealsoindicatedanoverlapbetween
tinnitusnetworkandthebrainregionsinvolvedinauditory
memory.11,15,20
Amongdifferenttypes ofmemory,thesensorymemory
defect in the central auditory pathway has been indexed
by the reduction of amplitude and area under the curve
of the Mismatch Negativity (MMN) response, an auditory
ERP reflecting the neural basis of the auditory sensory
memory, in tinnitus population.21 In addition, the results
of Autobiographical Memory Test (AMT) in tinnitus
suf-ferers showed difficulty in retrieving specific memories
and longer retrieval latencies, with fewer specific
mem-ories to positive cue words in comparison with a normal
population.22Furthermore,asreportedbyRossiterand
col-leagues, chronic tinnitus affected the auditory working
memory, whichreduced itscapacitytostoreand retrieve
information.23
Semanticmemoryisanotheraspectofmemorythatisthe
storehouseofawiderangeofknowledgeacquiredthrough
experience, which is not reviewed in tinnitus population
yet.20,24,25 This kind of declarative memory encompasses
alltheinformationusedinthoughtsandlanguage,suchas
beliefs, word meaning,all abstractconcepts and
associa-tionsbetweenthem.26,27Thus,semanticmemoryallowsus
toretrievestoredinformationthatisusedinthoughtsand
language.24,28
Although theeffects of tinnitus onaspects of memory
suchasthelong termmemory hasconfirmed,the
seman-tic memoryasa subsetof the long termmemory hasnot
beenspecificallystudiedintinnituspatients.Moreover,the
and the anatomical regions specialized for the different
aspects of semantic processingimpelledus toinvestigate
theinterplayoftinnitusandsemanticmemory.13,14However,
oneprevious study hasdemonstratedthatthe progressive
erosion of semantic memory makes this population more
liabletodeveloptinnitus.29 Accordingly,thepresentstudy
hasassumed thatsemanticmemoryis affectedin tinnitus
patients. Since there are still no studies concerning the
relation between semantic memory and chronic tinnitus,
focusingonthissubjectcanprovideanewinsightintothe
research activities and medical-rehabilitation approaches
that can be used for tinnitus population. Therefore, the
presentstudyaimedtoinvestigatesemanticmemoryin
tinn-ituspatientswithregardtothebasic assumptionthat the
tasksrequiring memorycan beinfluencedby troublesome
tinnitus.
Methods
Participants
The experimental groups consistedof 15tinnitus subjects
experiencingchronictinnitusformorethan6months(mean
age=37.67, SD=±11.47, range: 23---55 years; 5 females)
and16healthysubjectsasacontrolgroup,thetwogroups
werematchedforsexandage.Noneofthesesubjectshad
a history of neurological, mental, or otological diseases,
headtrauma,andalcohol/drugabuse.Allsubjectshadthe
behavioralpure tone audiometrythresholdlevelsof25dB
HL or less at octave frequencies of 250---2000Hz and not
more than 40dB HL in frequencies of 4000 and 8000Hz.
Allparticipantsweremonolingual,nativePersianspeakers.
Havingnormalcognitionstatuswasanotherinclusion
crite-riameasuredusingPersianversionoftheMini-MentalState
Exam(MMSE).30 Allsubjectswerealsogiventhevalidated
Persian version of Hospital Anxiety and Depression Scale
(HADS) and thosewitha scoreof 21 or less (less than 11
for either depression and anxiety subscales, referring not
tohavedepressionoranxietydisorders)wereincluded.31,32
Furthermore, the Persian version of the Tinnitus
Handi-cappedInventory(THI)andTinnitusQuestionnaire(TQ)were
filledbytinnituspatients.33,34Thetinnitussubjectswhohad
scoresmorethan60%inTQand58inTHIwereenrolledin
thestudy.Inaddition,theeducationallevelforparticipation
wasatleastdiploma,asareliablesignofgeneralcognitive
abilities.
Stimuli
Stimuli included 40 semantically related and 40
semanti-cally unrelatedprime-target wordpairs,which areknown
asthe semanticpriming paradigm.35,36 Acrossrelated and
unrelatedconditions,thetargetwordsandtheprimewords
were separately matched for length and frequency. The
relatednessproportionasanothermethodological
consider-ationusedtoprovidesemanticprimingparadigmwas0.5.37
The words selection and matching in the formof
seman-tically related and unrelated pairs were controlled under
twolinguisticexperts’supervision.Thisparadigmwas
vali-dated(CVRscorewasmorethan62%forallwordpairs;CVI
inthetotalscore=0.93)anditsreliabilitywasdetermined
(˛=0.93forsemanticallyrelatedpairs;˛=0.92for
semanti-callyunrelatedpairs;and˛=0.94forallitems).Thesepairs
ofwordswere presentedtotheparticipantsin a
counter-balancedfashion.
Procedure
In a quiet room, the participants heard the word pairs
throughloudspeakers in free fieldin the following order:
(a)the presentationof the primeword; (b) asilence gap
for 1150ms;(c)the presentation of thetarget word;and
(d) a silence gap for 3000ms for participants’ response.
Then the participants were told that they were going to
heartwowords in each trial. At the prompt,theyshould
make adecision whether thereis a semantic relationship
betweenthese twowords or not.To show their semantic
judgment,theywouldpressleft-clickonthemouseforthe
semanticallyrelatedpairsandright-click forthe
semanti-callyunrelatedonesassoonastheyhearthesecondword.It
isnecessarytomentionthattherecordedwordsweregiven
totheparticipantsusingpresentationsoftware.The
inten-sitylevelofstimuliwastypicallyadjustedtotheindividual’s
MostComfortableLevel(MCL).
Alltheproceduresperformedinthisstudywerein
accor-dancewithEthicsCommitteeofIran Universityofmedical
sciences and its later amendments or comparable
ethi-cal standards. All participants had been given a written
informedconsentfortheir participation.Aftercompleting
theirparticipation,patientswhodeclaredaneedforgetting
morehelpwerereferredtothetinnitusclinictobenefitfrom
thetreatmentprogramsavailableinourcountry.
Behavioraldatacollectionandanalysis
Duringtheexperimentaltask,theReactionTimes(RTs)asan
indicatorofprocessingefficiencywereobtainedfor
seman-ticallyrelatedandunrelated pairsseparately.Tothisend,
theRTswerecalculatedfromtheonsetoftargetworduntil
themouse button waspressed by participants. According
toadefineddefaultinthepresentationsoftware,if
partic-ipantspressedthe mousebutton beforetheoffset of the
targetword,thepresenteditemwouldnotbeaccountedas
aresponse.Lastly,meanpercentagesofcorrectresponses
alsoobtainedfortherelatedandunrelatedcondition.
Statisticalanalyses
Firstly,normalityofdistributionsofthedatawasexamined
bycalculatingthestandardizedskewnessandkurtosisindex.
Valuesvaried from−2 to2, indicating that the data
dis-tributionsdidnotdiffersignificantlyfromnormality.Thus,
anindependentt-test(significancelevelof0.05)wasused
tocomparetheRTsbetweenthetinnitussufferersandthe
controlgroup,bothforsemanticallyrelatedandunrelated
pairs.Moreoverfortheaccuracyofresponses,the
percent-age of correct responses obtained through each stimulus
type(therelatedandunrelatedpairs)wasalsoanalyzedby
independentt-test.The Statistical Packagefor Social
Sci-ence(SPSSV.16;Chicago,UnitedStates)wasusedtoperform
Table 1 Summary of participant demographics and the resultsofusedquestionnaires.
Variables Studiedgroups Normal Tinnitus
Sex
Female 7(43.75%) 5(33.33%) Male 9(56.25%) 10(66.66%) Age(mean±SD) 38.25±7.98 37.67±11.47 MMSEscore(mean±SD) 29.90±0.29 29.86±0.35 HADSscore(mean±SD) 7.14±2.19 9.02±1.81 TQscore(mean±SD) --- 70.93±6.18 THIscore(mean±SD) --- 68.53±8.6
Results
As previously mentioned, the current study consisted of 15 tinnitus patients and 16 healthy subjects having been matched in aspect of age, gender, HADS and MMSEscore (p>0.05).Inaddition,theresultsof TQandTHI question-nairesrepresentedthetinnitussubjectsasahomogeneous group.Asummaryofparticipantcharacteristicsisgivenin Table1.
Inthefollowing,anindependentt-testwasconductedto
comparetheRTsbetweenthetwostudiedgroups.Asshown
inTable2,forthesemanticallyrelatedprime-targetwords,
themeanofRTssignificantlydifferedbetweentinnitusgroup
andcontrolgroup(p<0.05).Furthermoreforthe
semanti-cally unrelated pairs,a significant difference wasseen in
themeanofRTsintinnitussubjectscomparedtothecontrol
group(p<0.05).
Theresponses’accuracywasalsocomparedby
indepen-dentt-test.The highcorrect-responserates revealedthat
thetwogroupspaidattentiontostimuliandtaskanddidnot
differsignificantlyinmakingajudgmentaboutthe
seman-ticrelatednessofthewordpairs.Nosignificantdifferences
wereseenbetweenthetwostudiedgroupsforalltheword
pairs(p>0.05).Table3representsmeanpercentageof
cor-rectresponses.
Discussion
The main aim of this study was to investigate
seman-ticmemory inpatients withchronic tinnitus.To this end,
the semantic priming paradigm was used asa behavioral
tool for studying semantic memory. For that, the
accu-racy of responses and the speed in the identification of
semantic relationship which is indexed by the RT were
calculated.38 As expected,notonly the controlgroup but
alsothetinnitussubjectshadshorterRTsinresponsetothe
semanticallyrelatedpairsratherthantheunrelated ones.
This resultcorrespondedclosely tootherstudies usedthe
primingparadigm. Accordingtodistributed models,ifthe
prime andthetarget aresemanticallyrelated,the target
word willberecognizedmore rapidly.36,39,40 Indeed,since
semantic memory is formed froma set of nodesthat are
interconnected based on their semantic similarities, the
processingofsemanticallyrelatedpairswouldbeeasierand
faster.27,28,41
Regarding the main purpose of the present study, the
results of comparison of RTs between the studied groups
shouldbetakenintoconsideration.Thisexperiment
demon-stratedthatthetinnitussubjectssignificantlyrespondedto
ourstimulilaterthanthecontrolgroup,whethertheyare
semanticallyunrelated pairsor not.This incrementin RTs
canbeanindicationofthedeficit insemanticmemory.In
otherwords,themoredifficultyinsemanticprocessing,the
moreincreaseintheRTs.Itseemsthattheoverlapofregions
involvedintinnitusandsemanticprocessingleadsto
defec-tive semantic processing in tinnitus sufferers. According
toMartin,2001,theprefrontalcortexisoneoftheneural
structuresthathasanimportantroleinretrieving,
maintain-ingandselectingsemanticinformation.24Theevidencehas
shown thatthe prefrontalcortexchangesstructurallyand
functionallyinchronictinnitus.13Furthermore,the
involve-mentofthemiddletemporalgyrusintinnitusnetwork42---45
and also in long-term storage of lexical representation28
supports our results. Moreover, MRI data from semantic
dementia patients has revealed an increase in the gray
matteroftheposteriorsuperiortemporalgyrusandsulcus.
These regions contain the association auditory córtex.29
Furthermore,thelimbicsystemasanothercommoncortical
Table2 Meanofreactiontimes(ms).
Stimulustype Studiedgroups p-Value
Normal(mean±SE) Tinnitus(mean±SE)
Semanticallyrelatedwordpairs 1016±0.13 1034±0.31 0.046 Semanticallyunrelatedwordpairs 1029±0.20 1051±0.36 0.041
Table3 Meanpercentagesofcorrectresponses(%).
Stimulustype Studiedgroups p-Value
Normal Tinnitus
Semanticallyrelatedwordpairs 98.90 98.0 0.215
regionplaysamajorroleinbothsemantic processingand chronic tinnitus.20,46 Indeed, the damage involving such
areas in tinnitussubjects can make this population more
susceptibletohavesemanticmemorydeficit.
On the other hand, the longer RTs in tinnitus subjects
canbearesultoftheirpoorperformanceintheprocessof
integrationofthetargetwordwiththeprimeword.As
men-tionedabove,thesemanticprimeparadigmwasusedinthis
study.Accordingtosemanticprocessing,thepresentationof
theprimewordleadstoactivationofthelong-term
seman-ticmemory.Whentheprimewordisretrieved,itshouldbe
heldinshort-termmemorysothatthetargetwordcanbe
integratedwithit.28,40Theholdinginformationinshort-term
memoryisoneoftheresponsibilitiesofworkingmemory.47
Previousstudieshavedemonstratedthatchronictinnitushas
aneffectontheworkingmemory.Thus,itisexpectedthat
thetinnitussubjectsperformpoorlyinthistask.
Considering the high percentage of correct responses,
itappearedthatallsubjectswereattendingtothestimuli
andtask.Accordingly,itcanbeconcludedthatthelonger
RTsinchronictinnituspatientshavenotbeenduetotheir
inattentionanddistraction.
Ontheotherhand,thetinnituspatientshadbeen
homo-geneouslyselectedfromtheaspectofmentalstate,tinnitus
loudness,andtinnitusannoyance.Moreover,theresultsof
theHADSquestionnairerevealednodepressioninthe
tinn-itusgroup.Asdepressioncanbeassociatedwithdisrupted
memory for positive materials and enhanced memory for
negativematerials,48 thelackofdepressioncanshowthat
ourfindingsareexclusivelyduetotinnitus,notdepression.
Accordingly, in the tinnitus management and
rehabilita-tion,theexpertscan capitalizeonsomespecialprograms
targetedatthedifferentaspectsofmemorynetwork.
More-over,sincethehuman’sbeliefsandthoughts arestoredin
semanticmemory,theCognitive BehavioralTherapy(CBT)
can lay a fertile ground for adding specific programs to
change the negative plasticity in tinnitus patients and
improvetheirperformanceinmemorytasks.
Conclusion
The current study indicated apossible deficit insemantic
memoryintinnitussubjects.Inthisregard,tinnitus
suffer-ersrevealedpoorperformanceinusingmeaningfulcontext
toactivatesemanticmemory.ThelongerRTswerea
confir-mationof this report.Althoughthe study hadreached its
purpose,itissuggestedthattheexperimentbeconducted
withalargergroup.ToconfirmtheresultsofRTs,the
struc-tural andfunctional studies can be used for investigating
semanticprocessinginchronictinnitus.
Conflicts
of
interest
Theauthorsdeclarenoconflictsofinterest.
Acknowledgements
This study was a part of MSc thesis project in
audiol-ogy approved and funded by Iran University of Medical
Sciences, School of Rehabilitation Sciences. The authors
would like to thank Dr. Samer Mohsen (Department of
Audiology, School of Rehabilitation sciences, The
Inter-national Campus of Iran University of Medical Sciences,
Tehran, Iran) for his comments and also to Dr. Nilipour
(Departmentof SpeechTherapy, University of Social
Wel-fare and Rehabilitation Sciences, Tehran, Iran) and E.
Saeedi(MScof Biostatistics, ResearchAssistant at Cancer
ResearchCenter,CancerinstituteofTehran,IranUniversity
of Medical Sciences, Tehran, Iran) for their helpful
com-mentsinprovidingsemanticprimingparadigmandstatistical
analysis.
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