www.bjorl.org
Brazilian
Journal
of
OTORHINOLARYNGOLOGY
ORIGINAL
ARTICLE
Temporal
processing
and
long-latency
auditory
evoked
potential
in
stutterers
夽
Raquel
Prestes
∗,
Adriana
Neves
de
Andrade,
Renata
Beatriz
Fernandes
Santos,
Andrea
Tortosa
Marangoni,
Ana
Maria
Schiefer,
Daniela
Gil
UniversidadeFederaldeSãoPaulo(UNIFESP),DepartamentodeFonoaudiologia,SãoPaulo,SP,Brazil
Received12December2015;accepted16February2016 Availableonline28April2016
KEYWORDS Stutteringadult; Auditoryprocessing disorder;
Auditoryevoked potential
Abstract
Introduction:Stutteringisaspeechfluencydisorder,andmaybeassociatedwith neuroaudio-logicalfactorslinkedtocentralauditoryprocessing,includingchangesinauditoryprocessing skillsandtemporalresolution.
Objective:Tocharacterizethetemporalprocessingandlong-latencyauditoryevokedpotential instutterersandtocomparethemwithnon-stutterers.
Methods:The study included41right-handed subjects,aged 18---46 years,dividedinto two groups:stutterers(n=20)andnon-stutters(n=21),comparedaccordingtoage,education,and sex.Allsubjectsweresubmittedtothedurationpatterntests,randomgapdetectiontest,and long-latencyauditoryevokedpotential.
Results:IndividualswhostuttershowedpoorerperformanceonDurationPatternandRandom GapDetectiontestswhencomparedwithfluentindividuals.Inthelong-latencyauditoryevoked potential,therewasadifferenceinthelatencyofN2andP3components;stutterershadhigher latencyvalues.
Conclusion:Stutterershavepoorperformanceintemporalprocessingandhigherlatencyvalues forN2andP3components.
© 2017 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 Pleasecitethisarticleas:PrestesR,deAndradeAN,SantosRB,MarangoniAT,SchieferAM,GilD.Temporalprocessingandlong-latency
auditoryevokedpotentialinstutterers.BrazJOtorhinolaryngol.2017;83:142---6.
∗Correspondingauthor.
E-mails:raquelprestesfono@yahoo.com.br,raquelprestesfono@gmail.com.br(R.Prestes).
PeerReviewundertheresponsibilityofAssociac¸ãoBrasileiradeOtorrinolaringologiaeCirurgiaCérvico-Facial. http://dx.doi.org/10.1016/j.bjorl.2016.02.015
PALAVRAS-CHAVE Gagueiraadulta; Distúrbiodo processamento auditivo;
Potencialevocado auditivo
Processamentotemporalepotencialevocadoauditivodelongalatência emindivíduosgagos
Resumo
Introduc¸ão: Agagueiraéum distúrbiodafluênciadafala, epodeestarassociadaafatores neuroaudiológicos ligados ao processamento auditivo central, entre eles as alterac¸ões das habilidadesauditivasdeprocessamentoeresoluc¸ãotemporal.
Objetivo: Caracterizar o processamento temporal e o potencial evocado auditivo de longa latênciaemindivíduosgagos,ecompará-loscomindivíduossemgagueira.
Método: Participaramdo estudo 41 indivíduosdestros, nafaixa de 18 a46 anos deidade, distribuídosemdoisgrupos:20comgagueirae21semgagueira,compararadossegundoidade, escolaridadeegênero.Todososindivíduosforamsubmetidosaostestesdepadrãodedurac¸ão, testedeidentificac¸ãodeintervalosaleatórioseopotencialevocadoauditivodelongalatência.
Resultados: Indivíduoscomgagueiraapresentarampiordesempenhonostestesdepadrãode durac¸ãoeRandomGapDetection,quandocomparadosaosindivíduosfluentes.Nopotencial evocadoauditivo delongalatência,houve diferenc¸a nalatênciadoscomponentes N2eP3, sendoqueosindivíduosgagosapresentarammaioresvaloresdelatência.
Conclusão:Os indivíduos com gagueiraapresentaram processamento temporalcom desem-penhoabaixodoesperadoeummaiorvalordelatênciaparaoscomponentesN2eP3. © 2017 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
Individualswithspeechandlanguagedisordersmayexhibit changesintheprocessingof informationreceivedthrough the sense of hearing. Studies have shown that thereis a correlation between the processing of auditory informa-tion, visual pathways, and expressive language difficulty, which can affect speech fluency and be characterized as stuttering.1---3
Stuttering isknownasabreakintheflow ofspeech,a multifactorial disorder in which biological, psychological, and social aspects are correlated in a complex manner.1 Changes in perception or auditory information processing areamongthebiologicalaspects.2,4---6
Theprocessingofauditoryinformationisrelatedtothe temporalityofthesounds,rhythm,andprosody,aspectsin whichstutterersmayshowchanges.1Particularlywhenthe degree of dysfluency is severe, the processing abnormali-ties inthese areas have been proposedasthe immediate cause of stuttering, sincetemporal auditory processingis critical for speech perception and closely related to the spokenlanguageprocessing.1,7,8 Therefore,itis necessary toevaluatetheneuroaudiologicalprocessesofthis popula-tion,whichcanbeperformed throughauditorybehavioral testsandauditoryevokedpotentials.
Auditory temporal processing refers to an individual’s ability todetect changes in temporalfeatures of sounds, suchasduration,intensity,frequency,andpausesbetween stimuli.9 There are several procedures available to eval-uate the temporal processing aurally, such as the tests of frequency pattern and duration with pure tone10---12 andmusical tone.13 The discriminationofpausesbetween stimuli can be evaluated with the with the Random Gap DetectionTest(RGDT).14
Inastudyofchildrenwithdevelopmentalstutteringthat evaluatedthe temporal patterns (frequency and duration
aspects),it was found that stuttering children had worse performanceandgreater numberofchanges comparedto theirnon-stutteringpeers.1Someauthorshavestudiedthe temporal resolution and observed worse performance in stutterers.15,16
Oneoftheelectrophysiologicalproceduresavailable to evaluate the aspects related to attention, memory, and auditorydiscrimination17isthelong-latencyauditoryevoked potential(LLAEP).Studies thatinvestigatedstutteringand theLLAEPhavereporteddifferencesinP3amplitudes,with stutterersshowingaloweramplitude.4,18 Inanotherstudy, therewasnodifferenceinlatencies andamplitudesof P3 betweenstutterersandnon-stutterers.19
Recent national studies showedno differences in P300 latencieswhencomparingstutterersandnon-stutterers.5,6
Giventhesefindingsintheliterature,itisevidentthat there are links between the auditory ability of tempo-ralprocessing andthe occurrenceof stuttering. However, thereis still no consensuson the waythrough which the skillsoftemporalprocessing,long-latencyauditoryevoked potentials,and manifestationof stuttering correlate.One hypothesisforthelackofconsensusintheliteraturewould be the heterogeneity of stutterers groups in each study. Moreover,asstutteringisamultifactorialdisorderwith bio-logical, psychosocial, and environmental influences, such factorscanalsoleadtoinconclusiveresults,requiringmore studiestoincreasetheknowledgeabouttheserelationships. Thus,theaimofthisstudywastocharacterize tempo-ralprocessingandlong-latencyauditoryevokedpotentialin stutterersandcomparewithnon-stutterers.
Methods
stuttererswasselectedatanevaluationanddiagnostic audi-ology service from a school hospital, and the sample of non-stutterers, consisting of volunteers, was selected by convenience,matching the stutterers regardingage, edu-cation,andsex.
For participation in this study, the following inclu-sioncriteriawereestablished:right-handpreference,ages between18and55years,auditorythresholdswithinnormal limits(withthresholdsofupto25dBHLinsoundfrequencies of250---258kHz),type-Atympanometriccurveandpresence ofcontralateralstapedialacousticreflex(insound frequen-cies of 500---504kHz), and negative history of conductive hearinglossand/orneurologicaldisorders.
Also,forthegroupofstutterers(GS),subjectshadmild tomoderatestuttering,according totheStuttering Sever-ity Instrument(SSI-3),20 and for the comparison group of non-stutterers(GNS),subjectsshouldhavenospeech dys-fluencies.
Behavioral assessmentof temporalprocessingwas per-formedwiththeaidofthefollowingequipment:soundproof booth, Philips Expanium discman, Grason-Stadler GSI-61 audiometerandsupra-auralTDH-50Pearphones, Compact-DiscwithDurationPatternTest(DPT)11andRGDT.14
The DPT withpure tone11 was presented binaurally at 50dBHL,basedontheaverage oftheauditorythresholds of500Hz,1000Hz,and2000Hz.Thirtysequenceswere pre-sentedbinaurally,withsixpossiblecombinations(LLC,CCL, LCL, CLC, LCC, and CLL). Subjects were asked to name thecombinationpresentedtothem.Thenormalitycriterion usedwasatleast83%ofcorrectanswers.10,11
RGDTwaspresentedbinaurallyat50dBHL,basedonthe averageoftheauditorythresholdsof500Hz,1000Hz,and 2000Hz.Thetestbeganwiththepresentationofatraining range,with0.5kHzstimuliinwhichtheinter-stimulus inter-valsvariedfromzero to40ms,appearingin anincreasing manner,thatis:0;2;5;10;15;20;25;30;and40ms.After successfultraining,subtests were initiated in frequencies of0.5k; 1k;2k;and 4kHz.In each frequency,sequences ofninestimuliwerepresented,withrandomlydistributed gaps.14 For each stimulus, the subject was instructed to reportif he/she had detected one or twotones; that is, identifiedthepresence of a gap(interval). The normality criterionwastheaveragegapbelow10ms.21
For electrophysiological evaluation, the two-channel equipment (Smart EP USB Jr Intelligent Hearing Systems [his]),insertearphones(ER-3A),abrasivepaste,electrolytic paste,microporoustape,andsilver electrodeswereused. Theauditoryevokedpotentialswereobtainedinan acous-tically and electrically treated room, with the subject accommodatedcomfortablyinarecliningchair.After clean-ingtheskinwithabrasivepaste,theelectrodeswerefixed withadhesivetapeandarrangedinthe10---20system22 on thevertex(Cz),earlobes(A1leftandA2right),andonthe forehead (the ground, Fpz). The impedance of the elec-trodeswasthenchecked,sothatthevalueswereequalto orlessthan5k.23
To capture theLLAEP,thetone-burst stimuliwasused, presented binaurally at 70dB HL, in the frequencies of 1000Hz (frequent stimulus that represented 80% of the stimuli) and 2000Hz (rare stimulus that represented 20% of thestimuli), witha total of 300 stimuli, with1.1 sec-ondpresentation rate, withalternatingpolarity, filters at
1---30Hz,anda600mswindow.N1,N2,andP2components wereanalyzed inthetraceoffrequent stimulus,whileP3 wasanalyzedinthetraceresultingfromthesubtractionof frequent stimulus bythe rarestimulus. The normalrange for each component is24:N1, 80---150ms;P2, 145---180ms; N2,180---250ms;17---20yearsofage,225---365ms;and30---50 yearsofage,290---380ms.
Forstatistical analysis, Mann---Whitney tests (for DPT), Friedman test (for RGDT), and nonparametric analysis of variance with repeated measures (for LLAEP) were used todeterminewhetherthereweredifferencesbetweenthe groups(GSandGNS).Asignificancelevelof5%wasadopted, and tests with statistically significant results were high-lightedwithanasterisk(*).
Results
Forty-onesubjects,aged18---46years,ofbothsexes,were dividedintotwogroups: groupofstutterers (GS), consist-ing of 20subjects withmild tomoderate stuttering, nine females and11males,and groupofnon-stutterers (GNS), consistingof21non-stutteringindividuals,tenfemalesand 11males.Themeanageforbothgroupswas30years.
TheMann---WhitneytestwasusedforDPTandthe Fried-mantest,forRGDT.
Thestatisticalanalysistechniqueusedwas nonparamet-ricanalysisofvariancewithrepeatedmeasures.
Intheassessmentoftemporalprocessing(Table1), sta-tisticallysignificantdifferenceswerefoundintheresultsof theDPTandRGDTbetweentheGSandtheGNS,withtheGS presentingthelowerpercentageofcorrectanswersinDPT and highervaluesin gap detectioncomparedtothe GNS, thevaluesofbothDPTandRGDTwereabnormalintheGS andnormalintheGNS.
IntheevaluationofLLAEP(Table2),therewereno differ-encesbetweenthelatencyvaluesinbothgroupsforN1and P2 components. A difference wasobserved only between therightandleftearsforbothgroupsintheN1component, with the right ear presenting lower latency than the left earforthiscomponent.AsfortheN2andP3components,it wasfoundthatGSlatenciesweregreaterthaninGNS.There werenosignificantdifferencesbetweenthelatenciesofthe rightandleftearsinbothgroups.
Discussion
The present study assessed the behavioral aspects of auditorytemporalprocessingtestsandthecaptureof elec-trophysiological potential that are related to attention, discrimination, and auditory memory, and found a dis-crepancy in individuals who stutter when compared with non-stutterers.
Table1 DescriptivemeasuresoftheDPT(%)andRGDT(ms)responsesintheGNSandGSgroups.
Variable Group N Mean Standarddeviation p-Value
DPT (%)
GNS 21 89.2 7.9 0.009a
GS 20 74.8 21.5
RGDT (ms)
GNS 21 7.3 2.7 0.012a
GS 20 10.4 7.1
DPT,DurationPatternTest;RGDT,RandomGapDetectionTest;N,samplesize;GNS,groupofnon-stutterers;GS,groupofstutterers.
a Statisticallysignificant.
Table2 DescriptivemeasuresoftheN1,P2,N2,andP3latencies(ms)intheGNSandGSgroupsperear.
Wave Ear Group N Mean Standarddeviation p-Valuebetweengroups p-Valuebetweenears
N1 Right GNS 21 99.7 8.8 0.376 0.006a
GS 20 96.2 10.8
Left GNS 21 99.9 8.7 0.376
GS 20 99.7 10.8
P2 Right GNS 21 174.1 26.0 0.902 0.650
GS 20 167.7 25.1
Left GNS 21 169.0 24.6 0.902
GS 20 172.0 25.1
N2 Right GNS 21 221.2 39.9 0.003a 0.526
GS 20 245.5 48.9
Left GNS 21 214.7 40.1 0.003a
GS 20 247.0 45.6
P3 Right GNS 21 293.7 23.0 0.006a 0.438
GS 20 328.7 56.4
Left GNS 21 289.0 30.4 0.006a
GS 20 332.7 61.8
N,samplesize;GNS,groupofnon-stutterers;GS,groupofstutterers.
a Statisticallysignificant.
TheGShadstatisticallysignificantlyhigherRGDT thresh-olds when compared with the GNS. The auditory skill evaluated in this test is associated with the recogni-tion of speech sounds, changes in duration, gaps, and rate of syllables.25 These aspects are important for the auditory feedback; a study with computer model that reproduced stuttering found a delayed auditory feedback in this model.31 There is no agreement in the literature regardingthe temporalresolutionof individualswho stut-ter.Gonc¸alvesandArcuri6,30 foundnodifferencesbetween stutterers and non-stutterers when applying such testsin their samples, but Andrade28 found responses similar to the present study, showing the relationship between the temporalprocessingandthemanifestationofstutteringin thispopulation.Thefactthatthereisnoagreementonits association can bejustifiedby previous studies that were conductedwithanon-homogeneoussample onthedegree ofstutteringseverity,education,andage.Itisknownthat suchfactorsaffecttheresultsofauditoryprocessingtests. Thetemporalimprecisioninspeechperception,aswellas the change in auditory feedback32 may contribute to the moments of dysfluency,33 explaining the low performance ofGSinDPTandRGDTtestsinthisstudy.
As for LLAEP, there were significant differences in N2 and P3 latencies for both the right and left ears; the GS presented the longer latency (Table 2). Some authors
foundnoP300differencescomparedtostutterersand non-stutterers.19 In more recent studies, morealtered results wereobservedinstutterers.5,6NostudiesanalyzingtheN2 componentinindividualswhostutterwereretrieved.Thus, it can behypothesized that stutterers require more time toelicit thiscomponent, affectingthe speedof the audi-toryprocessing ofsound response,which alsoexplainthe high rate of change in the tests evaluating the temporal processingskillappliedinthisstudy.
Inthepresent study,although significantdifferencesin LLAEPlatencywereobserved,theyrepresentednochange in this potential. Unlike behavioral tests, these data can beexplainedby thefactthat thenormalrangefor LLAEP latencyisquitewideandthecomponents’generatingsites are diffused in the central auditory system; thus, it was observedthattheauditoryprocessingbehavioraltestswere moresensitiveforthispopulation.
Despite these limitations, greater knowledge of hear-ingdisabilities in the population of stutterers contributes toabetter treatment planning andpossible intervention, whichmayincludeacousticallycontrolledauditorytraining, aimingfor animprovementinhearingthatmayleadtoan improvementinspeechfluency.
Conclusion
Individuals who stutter presented poorer than expected results in the behavioral tests that assess temporal processing,aswellaslongerlatenciesinlong-latency audi-toryevokedpotential.
Conflicts
of
interest
Theauthorsdeclarenoconflictsofinterest.
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