Braz. j. . vol.81 número6

www.bjorl.org

Brazilian

Journal

of

OTORHINOLARYNGOLOGY

ORIGINAL

ARTICLE

Long-latency

auditory

evoked

potentials

with

verbal

and

nonverbal

stimuli

夽

,

夽夽

Sheila

Jacques

Oppitz

,

Dayane

Domeneghini

Didoné

,

Débora

Durigon

da

Silva

,

Marjana

Gois

,

Jordana

Folgearini

,

Geise

Corrêa

Ferreira

,

Michele

Vargas

Garcia

a_{HumanCommunicationDisorders,UniversidadeFederaldeSantaMaria(UFSM),SantaMaria,RS,Brazil} b_{UniversidadeFederaldeSantaMaria(UFSM),SantaMaria,RS,Brazil}

c_{FundodeIncentivoàPesquisa(FIPE),SantaMaria,RS,Brazil} d_{UniversidadeFederaldeSãoPaulo(UNIFESP),SãoPaulo,SP,Brazil}

Received24June2014;accepted8October2014 Availableonline7September2015

KEYWORDS

Audiology; Electrophysiology; Evokedpotentials, auditory;

Event-related potentials,P300

Abstract

Introduction:Long-latencyauditoryevokedpotentialsrepresentthecortical activityrelated toattention,memory,andauditorydiscriminationskills.Acousticsignalprocessingoccurs dif-ferentlybetweenverbalandnonverbalstimuli,influencingthelatencyandamplitudepatterns.

Objective: TodescribethelatenciesofthecorticalpotentialsP1,N1,P2,N2,andP3,aswell asP3amplitude, withdifferentspeech stimuliandtonebursts,andtoclassifythem inthe presenceandabsenceofthesedata.

Methods:A total of30 subjects withnormalhearing were assessed,aged 18---32 yearsold, matchedbygender.Nonverbalstimuliwereused(toneburst;1000Hz---frequentand4000Hz --- rare);andverbal(/ba/---frequent;/ga/,/da/,and/di/---rare).

Results:ConsideringthecomponentN2fortoneburst,thelowestlatencyfoundwas217.45ms for theBA/DIstimulus;thehighestlatencyfound was256.5ms.For theP3component,the shortestlatencywithtoneburststimuliwas298.7withBA/GAstimuli,thehighest,was340ms. For theP3 amplitude, therewas no statisticallysignificant difference among the different stimuli.ForlatenciesofcomponentsP1,N1,P2,N2,P3,therewerenostatisticaldifferences amongthem,regardlessofthestimuliused.

Conclusion: TherewasadifferenceinthelatencyofpotentialsN2andP3amongthestimuli employedbutnodifferencewasobservedfortheP3amplitude.

© 2015Associac¸ãoBrasileira de Otorrinolaringologiae CirurgiaCérvico-Facial. Publishedby ElsevierEditoraLtda.Allrightsreserved.

夽

Pleasecitethisarticleas:OppitzSJ,DidonéDD,daSilvaDD,GoisM,FolgeariniJ,FerreiraGC,etal.Long-latencyauditoryevoked

potentialswithverbalandnonverbalstimuli.BrazJOtorhinolaryngol.2015;81:647---52.

夽夽_{Institution:UniversidadeFederaldeSantaMaria(UFSM),SantaMaria,RS,Brazil.}

∗_{Correspondingauthor.}

E-mail:[email protected](S.J.Oppitz). http://dx.doi.org/10.1016/j.bjorl.2014.10.005

PALAVRAS-CHAVE

Audiologia; Eletrofisiologia; Potenciaisevocados auditivos;

Potencialevocado P300

Potenciaisevocadosauditivosdelongalatênciacomverbaisenãoverbais

Resumo

Introduc¸ão:Ospotenciaisevocadosauditivosdelongalatênciarepresentamaatividadecortical relacionadaàshabilidadesdeatenc¸ão,memóriaediscriminac¸ãoauditiva.Oprocessamentodo sinal acústicoocorre demaneira diferente entre estímulosverbais enão verbais, podendo interferirnospadrõesdelatênciaeamplitude.

Objetivo:DescreveraslatênciasdospotenciasP1,N1,P2,N2eP3eaamplitudedoP3comos diferentesestímuloseclassificarempresenc¸aeausênciaestasinformac¸ões.

Método: Foramavaliados30indivíduos,comfaixaetáriade18a32anos.Equiparadosquanto ao gêneroenormo-ouvintes. Foramutilizadosestímulosnão verbais(1.000HZ -frequentee 4.000Hz-raro)everbais(/ba/-frequentee/ga/,/da/,/di/-raros).

Resultados: ConsiderandoocomponenteN2,para otoneburstencontrou-seamenor latên-ciaemtornode217,45msepara oestímuloBA/DIamaiorlatênciaemtornode256,5ms. NoquedizrespeitoacomponenteP3,alatênciaencontradacomtoneburstfoiamenorem tornode298,7msecomoestimuloBA/GAamaioremtornode340ms.Paraaamplitudeem P3,nãohouvediferenc¸aestatisticamentesignificanteentreosdiferentesestímulos.Quantoàs informac¸õesreferentesaosvaloresdaslatênciasdoscomponentesP1,N1,P2,N2eP3, inde-pendentedoestímuloutilizadohouvepresenc¸adoscomponentes semdiferenc¸asestatísticas entreeles.

Conclusão:Houvediferenc¸analatênciadopotencialN2eP3entreosestímulos,masnãofoi observadadiferenc¸aparaaamplitudedoP3.

©2015Associac¸ãoBrasileira deOtorrinolaringologiaeCirurgiaCérvico-Facial.Publicadopor ElsevierEditoraLtda.Todososdireitosreservados.

Introduction

Long-latencyauditoryevokedpotentials(LLAEP)havebeen usedinclinical practicetocomplementbehavioral assess-mentsofauditoryprocessing.Theyaredescribedaspositive (P)andnegative(N)peaks,whichrepresentcorticalactivity relatedtoattention, memory,andauditory discrimination skills.

TheLLAEP includethepositive1(P1),negative1(N1), positive2(P2),negative2(N2),andpositive3(P3)waves, andaresubdivided intoexogenouspotentials(P1, N1,P2, N2),whichareinfluencedbythephysicalcharacteristicsof thestimulus,suchasintensity,duration,andfrequency,and theendogenouspotential(P3),predominantlyinfluencedby theeventsrelatedtocognitiveskill.1

Frequent and rarestimuli (oddballparadigm) are used toobtainthecorticalpotentials. Themostusedstimuliin clinicalpracticearethetoneburst,representedbyalower frequency(frequentstimulus)andahigherfrequency(rare stimulus). However,a series of different stimuli, such as vowel,syllable,andwordcontrastsandevensentencescan beusedtoevokethesepotentials.2,3

Some studies4,5 _{have reported that acoustic signal} processing occurs differently between verbal and non-verbalstimuli,whichmayinfluencethepatternsoflatency and amplitude of cortical potentials. Despite the lack of standardization ofcortical potentialswithspeechstimuli, some studies indicate that these stimuli would be ideal for studying the neural basis of speech detection and discrimination,3,6 _{and for contributing toadditional} infor-mationregardingcomplexsignalprocessing.

Speech stimuli have been used to provide speech signal processing information in situations where behav-ioral assessment is not a precise method, helping in the identification of alterations in speech detection or discrimination.7

Basedontheabovementionedfactsandtheneedto char-acterizecorticalpotentials withdifferentstimuli,theaim ofthisstudywastocomparethelatencyofcortical poten-tialsP1,N1,P2,N2,andP3,aswellasP3amplitude,with differentspeechandtoneburststimuli.

Methods

ThisstudywasapprovedbytheResearchEthicsCommittee (REC)underprotocolNo.25933514.1.0000.5346.

Individualssigned the informedconsent,agreeingwith thestudyobjectivesandparticipation.

Atotalof 30individuals,aged18---32years,15 females and 15 males, with normal hearing and no risk history for hearing, neurological, and language alterations were assessed.

Thevisualinspectionoftheexternalauditorycanalwas initiallyperformedusingaclinicalWelch-Allynotoscopeto rule out any alterations that could influence audiometric thresholds.

individualswerethosewiththree-toneaverage(500,1000, and2000Hz)≤25dBHL(decibelhearinglevel).8

Acoustic impedance measurements were performed usinganInteracousticsAT235middleearanalyzertoassess the tympanometric curve and acoustic reflexes. Reflexes were assessed at the frequencies 500---4000Hz bilaterally inthe contralateralmode. The sampleincluded only indi-viduals with type A tympanogram with present acoustic reflexes.9

Two-channelIntelligentHearingSystemsequipmentwas used for the detection of long-latency auditory evoked potentials.Theskinwascleanedwithabrasivepasteandthe electrodeswereplacedusingelectrolyticpasteandadhesive tape, inthe A1(leftmastoid), A2(right mastoid), andCz (vertex)positions, withtheground electrode(Fpz)placed ontheforehead.Theimpedancevalueoftheelectrodeswas requiredtobe≤3k_.

The patient wasinstructed to pay attention to differ-entstimuli(rarestimulus)thatappearedrandomlywithina seriesofequalstimuli(frequentstimulus).Thepercentage ofoccurrenceofrarestimuliwas20%,and80%forfrequent stimuli.

Non-verbal stimuli were used (tone burst) at the fre-quenciesof 1000Hz (frequentstimulus) and4000Hz(rare stimulus),aswellasverbalstimuli(syllables/ba/---frequent stimulus and /ga/, /da/,and /di/ --- rare stimulus), pre-sentedbinaurallyatanintensityof75dBHL.Foreachtype ofstimulus(verbal/nonverbal) atotalof 300stimuliwere used(approximately240frequentand60rare)toobtainthe potentials.Thetracingswerenotreplicated,asreplication canturnararestimulusintoafrequentoneforthepatient. TheparametersaredescribedinTable1.

Thestudystartedwiththepairs/ba/and/ga/,followed by/ba/and/di/,/ba/and/da/,andtoneburst,withall speechstimuliandtoneburstpresentedpriortotracing,so thatpatientscouldbecomefamiliarizedwiththedifferent stimuli.Aftertheassessmentofthefirsttwospeechstimuli, patientswereinstructedtorest,sothatfatiguewouldnot influencetheanswersofthelasttwosequencesofstimuli. Latencyvalueswere obtainedbyidentifyingthe waves atthehighestpeakamplitude,withtheP3component con-sideredonlyinthetracingoftherarestimuli,whereasP1, N1,P2,N2wereconsideredinthefrequentstimulus,with norecordedreproductionofthesewaves,asthecollection

Table1 MeanandstandarddeviationfortheP1,N1,P2,N2,andP3componentswithallspeechstimuli(BA-GA/BA-DA/BA-DI) andtoneburst(1000Hz×4000Hz).

Variables Stimuli p§

BA×GA BA×DA BA×DI 1000×4000Hz

n Mean SD n Mean SD n Mean SD n Mean SD

P1

RE 26 62.2 8.1 27 59.8 8.1 25 65.5 18.3 22 62.2 11.9 0.393 LE 25 62.6 10.9 25 60.4 7.0 25 67.2 17.5 21 64.1 13.3 0.382

p-Value§ _{0.909 0.944 0.057 0.557}

N1

RE 30 103.8ab _{10.4 30 103.3}ab _{11.9 30 107.8}a

18.2 30 99.3b _{14.7 0.038}

LE 30 108.3 10.5 30 103.7 10.9 30 109.3 17.9 30 101.9 16.2 0.067

p-Value <0.001 0.726 0.178 0.135

P2

RE 30 173.2ab _{19.9 30 175.7}ab _{20.4 30 182.7}a _{26.2 30 171.5}b _{26.7 0.026}

LE 30 176.9b _{17.0 30 175.5}b _{24.5 30 187.1}a

24.1 30 175.5b _{28.6 0.017}

p-Value 0.140 0.945 0.016 0.153

N2

RE 23 245.7ab _{37.0 16 237.1}b _{43.4 14 251.6}a _{37.7 10 216.4}c _{34.8 0.006}

LE 22 255.3ab _{29.6 14 232.6}b _{38.7 13 261.4}a

33.2 13 218.5c 39.2 0.003

p-Value 0.188 0.526 0.720 0.517

P3

RE 26 341.7a _{44.2 26 301.5}c _{47.5 25 324.2b 59.2 25 297.0}b _{27.3 0.005}

LE 26 344.4a _{46.5 28 303.4}c _{46.3 21 329.9}ab _{63.4 24 300.4}b _{36.4 0.002}

p-Value 0.171 0.325 0.619 0.163

AmplitudeofP3

RE 27 6.2 2.2 30 6.9 5.3 24 6.3 2.8 26 5.8 2.1 0.208

LE 26 6.6b _{2.1 28 7.8}a _{5.4 21 6.7}b _{2.5 24 6.1}c _{2.3 0.027}

p-Value 0.700 0.095 0.999 0.737

§ _{Analysisofvarianceforrepeatedmeasures---posthocBonferroni,wheremeansfollowedbythesameletters(inline)donotdiffer}

Table2 AbsolutedistributionandrelativetothepresenceandabsenceofinformationonthedataforcomponentsP1,N1,P2, andN2withallspeechstimuli(BA---GA/BA---DA/BA---DI)andtoneburst(1000Hz×4000Hz).

Variables Stimuli

BA×GA BA×DA BA×DI 1000×4000Hz Yes No Yes No Yes No Yes No

n % n % n % n % n % n % n % n %

P1

RE 26 86.7 4 13.3 27 90.0 3 10.0 25 83.3 5 16.7 22 73.3 8 26.7 LE 25 83.3 5 16.7 25 83.3 5 16.7 25 83.3 5 16.7 21 70.0 9 30.0

N1

RE 30 100.0 0 0.0 30 100.0 0 0.0 30 100.0 0 0.0 30 100.0 0 0.0 LE 30 100.0 0 0.0 30 100.0 0 0.0 30 100.0 0 0.0 30 100.0 0 0.0

P2

RE 30 100.0 0 0.0 30 100.0 0 0.0 30 100.0 0 0.0 30 100.0 0 0.0 LE 30 100.0 0 0.0 30 100.0 0 0.0 30 100.0 0 0.0 30 100.0 0 0.0

N2

RE 23 76.7 7 23.3 16 53.3 14 46.7 14 46.7 16 53.3 10 33.3 20 66.7 LE 22 73.3 8 26.7 14 46.7 16 53.3 13 43.3 17 56.7 13 43.3 17 56.7

P3

RE 26 86.7 4 13.3 26 86.7 4 13.3 25 83.3 5 16.7 25 83.3 5 16.7 LE 26 86.7 4 13.3 28 93.3 2 6.7 21 70.0 9 30.0 24 80.0 6 20.0

AmpP3

RE 27 90.0 3 10.0 30 100.0 0 0.0 24 80.0 6 20.0 26 86.7 4 13.3 LE 26 86.7 4 13.3 28 93.3 2 6.7 21 70.0 9 30.0 24 80.0 6 20.0

replicationcouldresultinfatigueandimpairtheassessment outcome,sinceitdependsontheindividual’sattention.

Dataweretabulatedandstatisticallyanalyzed, compar-ing the latencies of components P1, N1, P2, N2, and P3 betweenspeechstimuliandtoneburst.

Results

Theresultsrefertothesampleof30assessedindividuals, withameanageof23.3(±3.5)years,withaminimumof 18and maximumof 32 years.Therewasan equal gender distribution,with50.0%(n=15)formenandwomen.

Mean, and standard deviation measurements were obtainedforthelatencyvaluesofcomponentsP1, N1,P2, N2,andP3asshowninTable1.

ForP1,N1andP2components,therewerenosignificant differencesdetectedbetweenstimuliinboththeREandthe LE.

For the N2 component, a significant difference was observed (p-value 0.006 and 0.003 for RE and LE respec-tively)for the latency measured in response todifferent stimuli,withthelowerlatencyfoundfortoneburstandthe higherlatencyfortheBA/DIstimulus.

RegardingtheP3component,therewasasignificant dif-ference(p-value0.005and0.002forREandLE,respectively) betweentheusedstimuliandobservedlatency.Thelowest latencywasfoundwithtoneburstandthehighestlatency withtheBA/GAstimulus.

Therewas nostatistically significant differenceamong thedifferentstimulifortheamplitudeinP3.

Asfortheinformationregardinglatencyvaluesof com-ponentsP1,N1,P2,N2andP3,forthefourdifferentstimuli, they were classified in the presence and absence of this information.

Regardlessofthestimulusused,therewerecomponents withnostatisticaldifferencesbetweenthem;Table2shows datafortheabsoluteandrelativedistributions.

Discussion

Despite the hemispheric differentiation and undeniable inequality in functional importance of the cerebral hemispheres, therewerenodifferencesbetween the per-formance of the right and leftears in the present study. Other studies have reported the absence of differences betweenears,10---12_{sothediscussionwillfocusonthe} com-parisonbetween speechstimuliand tone burst,regarding thelatencyofexogenouscomponents,andthelatencyand amplitudeoftheendogenouscomponentP3.

This findingcorroboratesthestudy10 _{thatreportedthat} the stimulus used did not evoke any difference for the latency of components N1 and P2, but did influence the latencyofcomponentsN2andP3.Thisfactwasexpected, astheP3componentis acognitivepotentialthat is influ-enced by the stimulus and, therefore, these data are consistent withwhat has been previously reported in the literature.11,13,14

Regarding the comparison of speech and tone burst stimuli,thedifferencebetweenthemwasexpected, consid-ering that the central activations are different for each stimulus, which corroborates the authors10 _{who reported} that the type of stimulus used is an important variable in obtaining the N2 and P3 components. Verbal stimuli constitute a more difficult listening task when compared to non-verbal stimulus discrimination. Some authors15,16 observedthattheP3latencyincreaseswhenthe‘‘targets’’ fordiscriminationaremore‘‘difficult’’thanthestandard, i.e.,latencyissensitivetothetaskprocessingdemand.

This study showed thatthe speechstimulus influenced the N2 component, which has been observed by other authors,17 _{who mentioned that the N2 component} regis-tration appears to be related to the identification and attention processing of the rare stimulus, with a posi-tive correlation between the value of itslatency and the levelofdifficultyofthediscriminationtask.Inonestudy10 the same fact was observed, where N2 was influenced by the speech stimuli and, in that study, the difference betweenstimuliwasobservedbetweenvowelandconsonant contrasts.

Asfor theamplitude,nodifferencewasobservedwhen comparingthestimuli.7,11,13,14,18 _{Somestudiesdescribethe} reductioninamplitudeofcomponentP3withtheincreased level of difficulty of the discrimination task. However, this correlation was not significant in the present study, which corroborates the findings of another study.10 _The amplitude of potential P3 has been described as hav-ing greatvariabilityin the literature,19---21 _{and the normal} range for the P300 amplitude is between 1.7␮V and 19.0␮V.

Inthisstudy,itwaspossibletoobtaintherecordsofthe cortical and cognitive auditory evokedpotentials P3with speech stimulus with good producibility and morphology, demonstratingthisisaviableproceduretobeappliedin clin-icalpractice.Thisinformationwasalsoreportedbyanother author.1 _{All assessedcomponents wereobserved with the} fourdifferentstimuliin thisstudy(Table2),showing that for young adults,themorphological characteristics of the waves,aswellasthepresenceofcomponentsdonotdepend onthetypeofstimulustobeelicited.

Nevertheless, it is known that the cognitive auditory evokedpotential P3generatedby speechstimulican also beusedtoprovideinformationonspeechsignalprocessing, whichaccordingtotheauthor11_{helpstoidentifychangesin} detectionordiscrimination---informationthatcanguidean individual’stherapeuticrehabilitation.

The BA/GA stimulus brings more difficulty in syllable discrimination due to its proximity, when compared, for instance, to BA/DI syllables. Thus, this study makes an importantcontribution totheclinical andresearch areas, helpingtheprofessionalchoosethemostappropriate stim-ulusforthesubjecttobeassessed.

Conclusion

There was a difference in latency of N2 and P3 poten-tialsbetweenthestimuliused;however,nodifferencewas observedfortheP3amplitude.

Conflicts

of

interest

Theauthorsdeclarenoconflictsofinterest.

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