Multiple Auditory Steady-State Responses to Bone ...€¦ · dB HL bone-conduction stimuli and to 30–60 dB HL air-conduction stimuli were compared.The effect of alternating stimulus

J Am Acad Audiol 16:172–183 (2005)

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*School of Audiology and Speech Sciences, University of British Columbia Vancouver, BC, Canada

David R. Stapells, School of Audiology and Speech Sciences, University of British Columbia, 5804 Fairview Avenue Vancouver,British Columbia V6T 1Z3; Phone: 604-822-5795; Fax: 604-822-6569; E-mail: [email protected]

Multiple Auditory Steady-State Responsesto Bone-Conduction Stimuli in Adults withNormal Hearing

Susan A. Small*David R. Stapells*

Abstract

ASSR thresholds to bone-conduction stimuli were determined in 10 adults withnormal hearing using mastoid placement of the bone oscillator. ASSRs to 0–50dB HL bone-conduction stimuli and to 30–60 dB HL air-conduction stimuli werecompared.The effect of alternating stimulus polarity on air- and bone-conductionASSRs was also investigated. Stimuli were bone- and air-conduction amplitude-modulated tones (500–4000 Hz carrier frequencies, modulated at 77–101Hz). ASSRs were recorded using the Rotman MASTER research system.Mean (1SD) bone-conduction ASSR thresholds were 22(11), 26(13), 18(8), and18(11) dB HL for 500, 1000, 2000, and 4000 Hz, respectively.Except for a steeperslope at 500 Hz, ASSR intensity-amplitude functions for binaural bone- andair-conduction stimuli showed the same slopes; intensity-phase-delay functionswere steeper at 1000 Hz for ASSRs to bone-conduction stimuli. ASSRamplitudes and phases did not differ for single- versus alternated-stimuluspolarities for both bone- and air-conduction stimuli.The steeper amplitude slopefor ASSRs to 500 Hz stimuli may reflect a nonauditory contribution to the ASSR.

Key Words: Audiometry, auditory steady-state response, bone conduction,evoked potential normal hearing

Abbreviations: AC = air conduction; A/D = analog-to-digital conversion rate;ANSI = American National Standards Institute; ASSR = auditory steady-stateresponse; BC = bone conduction; D/A = digital-to-analog conversion rate; FFT= Fast Fourier Transform; RETFL = reference equivalent threshold force level;RETSPL = reference equivalent threshold sound pressure level

Sumario

Se determinaron umbrales de conducción ósea para las ASSR en 10 adultoscon audición normal, colocando un oscilador óseo en el hueso mastoides. Secompararon las ASSR obtenidos con estímulos por conducción ósea entre 0a 50 dB, y de 30 a 60 db obtenidos con estímulos por conducción aérea.Tambiénse investigó el efecto en las ASSR de alternar la polaridad en los estímulospresentados por vía aérea y ósea. Los estímulos fueron tonos de amplitudmodulada conducidos por vía ósea y aérea (frecuencias portadoras de 500– 4000Hz, moduladas a 77 – 101 Hz). Las ASSR fueron registradas utilizandoel sistema de investigación Rotman MASTER. Los umbrales medios (1DS) paralas ASSR por conducción ósea fueron 22(11), 26(13), 18(8), y 18(11) dB HLpara 500, 1000, 2000 y 4000 Hz, respectivamente. Las funciones de intensidad-amplitud para las ASSR con los estímulos binaurales conducidos por víaaérea y ósea mostraron las mismas pendientes, excepto por una pendientemás pronunciada en 500 Hz; las funciones de retardo de intensidad-fasetuvieron pendientes más pronunciadas para las ASSR con estímulos de

Auditory evoked potentials (AEPs) arerequired to estimate hearingthresholds at audiometric frequencies

for individuals who cannot be tested usingconventional behavioral measures. Infants,young children, and multiply handicappedindividuals who are difficult to test aretypically the individuals that benefit mostfrom evoked potential audiometry. There arealso adults who are assessed using AEPs incases where hearing loss is a condition underconsideration for monetary compensation.Auditory brainstem responses (ABRs) arethe AEPs that are currently used clinically forthreshold assessment in infants and youngchildren. ABRs may be evoked by air- andbone-conduction brief-tone stimuli to obtainfrequency-specific audiometric information insleeping and relaxed subjects (Stapells andRuben, 1989; Foxe and Stapells, 1993; Cone-Wesson and Ramirez, 1997; Stapells, 2000a,b). One shortcoming of the ABR technique isthat only one ear and one frequency can betested at the same time. Another limitationof the ABR to brief tones is that detection ofa response in the waveform depends onskilled, subjective assessment of replicatedresponses, allowing for error in judgement ofthe presence of responses depending on theexperience of the clinician (Stapells, 2000a).

Auditory steady-state responses (ASSRs)use amplitude and/or frequency modulatedstimuli to evoke AEPs, and are currently ofgreat interest because they can quickly andobjectively obtain frequency-specificthresholds (for review, see Picton et al, 2003).ASSRs can be recorded for single- or multiple-carrier frequencies to one, or both, earssimultaneously. ASSRs are detectedobjectively using statistical tests (John and

Picton, 2000); their detection does not rely onthe experience of the clinician. MultipleASSRs are thus of considerable interest as anassessment tool because of their objectivityand potential for reducing clinical testingtime.

ASSRs to air-conduction stimuli havebeen found to provide reasonably accurateprediction of hearing sensitivity at theaudiometric frequencies for adults and youngchildren (for review, see Picton et al, 2003).In order to distinguish between sensorineural,conductive and mixed hearing losses, AEPtechniques must provide thresholds for bothair- and bone-conduction stimuli, as isroutinely done in behavioral audiometry.Frequency-specific thresholds andidentification of type of hearing loss arenecessary to make decisions regardingmedical intervention and planning aural(re)habilitation. Accurate bone-conductionthresholds are particularly important whenassessing children who have unilateral orbilateral otitis media or atresia (Jahrsdoerferet al, 1985; Stapells and Ruben, 1989). ASSRsto bone-conduction stimuli have not beenthoroughly investigated. At the outset of thepresent study, only three previous studieshad reported findings for ASSRs elicited bybone-conduction stimuli. Two of these studiesused bone-conduction stimuli presented at theforehead to elicit ASSRs in adults with normalhearing (Lins et al, 1996; Dimitrijevic et al,2002); a third study, conducted in our lab,recorded ASSRs to bone-conduction stimulipresented at the mastoid of adults withsevere-to-profound hearing loss (Small andStapells, 2004).

All three studies that recorded ASSRs tobone-conduction stimuli reported results that

Bone-Conduction ASSRs/Small and Stapells

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conducción ósea en 1000 Hz. Las amplitudes y fases de las ASSR no fuerondiferentes para estímulos de polaridad sencilla versus polaridad alternante, tantopara la conducción ósea como aérea. La pendiente de amplitud máspronunciada para las ASSR con estímulos de 500 Hz puede reflejar unelemento no auditivo en los ASSR.

Palabras Clave: Audiometría, respuestas auditivas de estado estable,conducción ósea, potencial evocado, audición normal

Abreviaturas: AC = conducción aérea; A/D = tasa de conversión analógicaa digital; ANSI = Instituto Nacional Americano de Normas; ASSR = respuestaauditiva de estado estable; BC = conducción ósea; D/A = tasa de conversióndigital a analógica; FFT = transformación rápida de Fourier; RETFL = nivel defuerza umbral de referencia equivalente; RETSPL = nivel umbral de presiónsonora de referencia equivalente

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are different for 500 Hz compared to highercarrier frequencies. Lins et al (1996) andDimitrijevic et al (2002) assessed responsesto bone-conduction stimuli no more than20–30 dB above threshold and founddifferences in amplitude/phase measures forbone- versus air-conduction ASSRs,particularly, for 500 and 1000 Hz carrierfrequencies. In a previous study, we recordedASSRs in individuals who could not hear thestimuli and clearly showed that bone- andhigh-intensity air-conduction stimuli canproduce spurious “responses,” especially for500 and 1000 Hz carrier frequencies (Smalland Stapells, 2004). Based on these findings,it is possible that some of the results reportedby Lins et al and Dimitrijevic et al may havebeen contaminated by stimulus artifact.

The presence of spurious responses insubjects that cannot hear the stimulus isexplained, in part, by the presence of high-amplitude stimulus artifact in the EEG(electroencephalogram) produced by the boneoscillator. A significant problem with bone-conduction stimulus artifact in the EEG isthat this energy can alias to exactly the samefrequency as the ASSR modulation rate of thestimulus, and be interpreted as a response.“Alternating” the stimulus polarity is acommon technique used to remove or reducestimulus artifact when recording ABRs (e.g.,Hall, 1992, p. 319) and can also be used toreduce the effect of stimulus artifact that ispresent in the EEG when recording ASSRs.For ASSR recordings, this can beaccomplished by inverting the stimulus, thenaveraging offline the responses to the invertedand noninverted stimuli to obtain a responserepresenting the “alternated stimuluspolarity.” In our previous study (Small andStapells, 2004), we investigated ways toreduce or eliminate stimulus artifact. Wefound that the use of 500 Hz or 1000 Hzanalog-to-digital conversion (A/D) rates andsingle-polarity stimuli, which have beencommonly used to record ASSRs (Dimitrijevicet al, 2002; Herdman and Stapells, 2001,2003), resulted in significant artifactualresponses for 500, 1000, and 2000 Hz carrierfrequencies. Use of an alternated stimuluspolarity significantly reduced the number ofspurious responses at these rates by cancelingout artifact in the ASSRs. Use of a 1250 HzA/D rate and insertion of a 300 Hz steeplowpass anti-aliasing EEG filter helped avoidspurious responses by preventing aliasing. In

some of the subjects with severe-to-profoundhearing loss, spurious responses to 500 Hzremained even after changing the A/D rateand adding in an additional anti-aliasingfilter, and may be nonauditory physiologicresponses (perhaps vestibular in nature).

Based on the results of our previousresearch in individuals with severe-to-profound hearing sensorineural loss (Smalland Stapells, 2004), we concluded thatartifactual responses to bone-conductionstimuli are present for the followingconditions. For single-polarity 500 and 1000Hz stimuli, artifactual responses are presentat: (1) 20–40 dB HL and higher for a 500and 1000 Hz A/D rate, and (2) 50–60 dB HLand higher for a 1250 Hz A/D rate. For single-polarity 2000 Hz stimuli, artifactualresponses are present at: (1) 50 dB HL andhigher for 500 Hz and 1000 Hz A/D rates, and(2) not present for a 1250 Hz A/D rate.Artifactual responses are not present tosingle-polarity 4000 Hz stimuli at any A/Drate. Based on these findings, it is likely thatLins et al (1996) and Dimitrijevic et al (2002)used stimuli that were in the intensity andfrequency range that result in artifactualresponses.

The present study had three purposes.First, to determine ASSR thresholds tomultiple bone-conduction stimuli presentedat the mastoid, in participants with normalhearing, using stimulus and recordingparameters selected to minimize stimulusartifact in the EEG and its resultant spuriousresponses. Second, to investigate the effectsof changing stimulus polarity on the ASSRsin normal-hearing subjects. Third, to compareamplitude and phase characteristics of ASSRsto bone-conduction, presumed to reflect theresponse of both cochleae, to ASSRs elicitedby air-conduction stimuli presentedbinaurally (diotically), known to reflect theresponse of both cochleae.

METHODS

Participants

Two groups of individuals with normalhearing participated. ASSRs to air-conductionstimuli were recorded for a group (AC-ASSR)of ten adults aged 19 to 37 years. ASSRs tobone-conduction stimuli were recorded in


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another group (BC-ASSR) of ten adults aged20 to 48 years. Initially, we obtained AC- andBC-ASSR recordings for the same group ofadults but realized that we had stimulusartifact in our bone-conduction results. Wethus obtained BC-ASSRs using a higher A/Drate in a different group of adults; stimulusartifact was not an issue for the AC-ASSRsusing the lower rate; thus, the air-conductionrecordings were not repeated. All participantshad normal hearing, with behavioral air-and bone-conduction thresholds of 20 dB HL(ANSI, 1996) or better in both ears from 250to 8000 Hz. The mean behavioral pure-toneair- and bone-conduction thresholds, shownin Table 1, are similar for these two groups.

Stimuli

All stimuli were sinusoidal tones with thecarrier frequencies 500, 1000, 2000, and 4000Hz that were 100% amplitude modulated at77.148, 84.961, 92.773, and 100.586 Hz,respectively. The stimuli were presentedsimultaneously for all conditions tested. Air-and bone-conduction stimuli were generatedby the Rotman MASTER research system(John and Picton, 2000), routed throughTucker-Davis Technologies SM3 and HB6modules to allow presentation of noninvertedand inverted stimuli, and attenuated througha clinical audiometer (Interacoustics AC40).

Bone-conduction stimuli were presentedto a Radioear B-71 bone oscillator that washeld in position on the temporal bone within2 cm of the pinna with a wide elasticheadband fastened with VelcroTM (UniversalFacial Band #210, Design Veronique,Oakland, CA) with 450–550 g of force. Bone-conduction stimuli were presented using 10dB steps at: (1) 0 to 50 dB HL for noninvertedstimuli, (2) 30 to 50 dB HL for invertedstimuli, and (3) 30 to 50 dB HL for“alternated” stimuli. ASSRs to “alternated”stimuli were obtained by averaging offline theASSR waveforms to noninverted and inverted

stimuli (Small and Stapells, 2004). ASSRs toalternated stimuli were not tested at levelslower than 30 dB HL because stimulusartifact and aliasing is considered negligiblefor bone-conduction stimuli less than 30 dBHL, provided a 1250 Hz A/D rate is used(Small and Stapells, 2004); that is, alternatedstimuli were not needed to help reduce theeffects of stimulus artifact at these levels.

Air-conduction stimuli were presentedusing EAR-3A insert earphones. Air-conduction stimuli were presented binaurally(diotically) at 30, 40, and 60 dB HL to becomparable to the bone-conduction stimulithat were presented across a range ofintensities. Stimulus artifact is not expectedto be a problem for air-conduction stimulipresented at moderate levels, therefore, onlysingle-polarity stimuli (“noninverted”) wereused. Additionally, as a check of whether“alternating” stimuli degraded the ASSR,monaural air-conduction stimuli werepresented at 40 dB HL using noninvertedand inverted stimuli. A 40 dB HL air-conduction stimulus was used to ensure thatstimulus artifact was not an issue; monauralpresentation avoided possible additionalcomplexities of stimulating both cochleae.

Calibration

The bone-conduction stimuli werecalibrated in reference equivalent thresholdforce levels (RETFLs) in dB re:1µNcorresponding to 0 dB HL for the mastoid(ANSI S3.6-1996) using a Brüel and KjaerModel 2218 sound level meter and Model4930 artificial mastoid. The oscillator wascoupled to the artificial mastoid with 550 gof force. Air-conduction stimuli werecalibrated in reference equivalent thresholdsound pressure levels (RETSPLs)corresponding to 0 dB HL (ANSI S3.6-1996)using a Quest Model 1800 sound level meterand a Brüel and Kjaer DB0138 2-cc coupler.

Table 1. Mean (1 SD) Pure-Tone Behavioral Air- and Bone-Conduction Thresholds (dB HL) forTwo Groups of Adult Participants with Normal Hearing (N = 10 per group)

Group MODE 500 Hz 1000 Hz 2000 Hz 4000 Hz

AC-ASSR AIR 4.5 (8.3) 3.5 (5.8) 4.0 (7.0) 1.0 (5.7) BONE 1.0 (5.2) -3.5 (6.4) 1.0 (6.3) -7.5 (4.3)

BC-ASSR AIR 4.4 (5.8) 2.8 (4.4) 0.0 (7.9) 3.3 (7.5)BONE 4.9 (7.7) -3.1 (4.9) 4.4 (6.3) -3.6 (6.3)


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ASSR Recording

ASSRs were recorded using the RotmanMASTER system. Three gold-plated electrodeswere used to record the electrophysiologicresponses; the noninverting electrode wasplaced at Cz, the inverting electrode waspositioned at the nape of the neck, just belowthe hairline, and an electrode placed at thehigh forehead acted as ground. Allinterelectrode impedances were below 3kOhms at 10 Hz.

For ASSRs elicited by bone-conductionstimuli, the EEG was filtered using a 30–250Hz filter (12 dB/oct) and amplified 80,000times (Nicolet HGA-200A and Nic501A). TheEEG was further filtered using a 300 Hzlowpass anti-aliasing filter (Stanford ResearchSystems; 115 dB/oct), and the EEG was thenprocessed using a 1250 Hz A/D conversionrate. The digital-to-analog (D/A) rate was31,250 Hz. Each EEG recording sweep wasmade up of 16 epochs of 1024 data points andlasted a total of 13.107 seconds.

For ASSRs elicited by air-conductionstimuli, the EEG was filtered using a 30–250Hz (12 dB/oct) filter, amplified 80,000 times(Nicolet HGA-200A and Nic501A) andprocessed using a 500 Hz A/D rate (Herdmanand Stapells, 2001, 2003). The D/A rate was32,000 Hz. Each EEG recording sweep wasmade up of 16 epochs of 1024 data points andlasted a total of 16.384 seconds. Artifactrejection for bone- and air-conduction stimuliwas set to eliminate epochs ofelectrophysiologic activity that exceeded ± 40µV in amplitude in order to reducecontributions to the EEG due to muscleartifact.

ASSRs were averaged in the time domainthen analyzed online into the frequencydomain using a Fast Fourier Transform (FFT).The FFT resolution was 0.060 and 0.093 Hzfor the 500 and 1250 Hz A/D rates,respectively, over a range of 0 to 250 Hz.Amplitudes were measured baseline-to-peakand expressed in nV. An F-ratio was calculatedby MASTER to estimate the probability thatthe amplitude of the ASSR at the modulationfrequency for each carrier frequency wassignificantly different from the averageamplitude of the background noise in adjacentfrequencies within ±60 bins of the modulationfrequency (“noise”) (John and Picton, 2000).A response was considered to be present if theF-ratio, compared to the critical values for F(2,

240), was significant at a level of p < .05. Aresponse was considered to be absent if p > .05and the amplitude of the noise was less than11 nV. Alternatively, a response was alsoconsidered to be absent when responseamplitude was <10 nV and if the p value ≥ .30.

Amplitude values were averaged acrosssubjects, including ASSR amplitudes forresponses that were not significant. The phasevalues from MASTER were adjusted byadding 90º to yield the onset phase (John andPicton, 2000). Onset phase values were thenconverted to phase delay (P) by subtractingthe onset phase value from 360º. Any phase-delay values that differed ≥180º from anadjacent measure were “unwrapped” byadding 360º to their value (John and Picton,2000). Phase values for ASSRs that were notsignificant were excluded from mean phase-delay calculations. Phase-delay values wereaveraged across subjects. Results are onlyreported if at least five subjects contributedto the mean.

Procedure

Testing was performed in a double-walledsound-attenuating booth. Participantsreclined in a comfortable chair and wereinstructed to relax or sleep during the ASSRtest session. Behavioral thresholds for pure-tone air- and bone-conduction stimuli wereobtained at the beginning of the session toestablish normal hearing thresholds. ASSRswere elicited to bone-conduction stimuli indescending order of intensity. ASSRs wereelicited to air-conduction stimuli in arandomized order of intensity. The totaltesting time was approximately 1.5 hours,including the time to obtain behavioralthresholds. Participants signed a consentform before commencing any of theexperiments and were paid an honorarium atthe end of each session.

Data Analyses

Changes in ASSR amplitude and phasedelay were compared across stimulus polaritycondition (“noninverted versus inverted”,“noninverted versus alternated” and “invertedversus alternated”) and carrier frequency(500, 1000, 2000, and 4000 Hz) and betweenmode of stimulus presentation (bone- versusbinaural air-conduction). Mean amplitudeand phase-delay values were calculated for


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ASSRs elicited by monaural air-conductionstimuli. The slopes of the amplitude andphase-delay functions with intensity werecalculated from 30–50 dB HL for bone-conduction stimuli, and 30–60 dB HL forbinaural air-conduction stimuli. In order tocompare bone conduction to air conduction(binaural), phase delay was also converted tolatency (in milliseconds), after correcting forthe insert earphone delay (-0.92 msec).

Comparisons across stimulus polarityand carrier frequency for amplitude andphase-delay measures were made for ASSRsto monaural air-conduction stimuli presentedat 40 dB HL using a two-way repeated-measures analysis of variance (ANOVA).Comparisons across stimulus polarity andcarrier frequency for the slopes of theintensity-amplitude and intensity-phase-delay functions for ASSRs elicited by bone-conduction stimuli were also made using atwo-way repeated-measures ANOVA.Comparisons between mode of presentationand across carrier frequency for the slopes ofamplitude- and phase-delay-intensityfunctions for ASSRs elicited by binaural air-and bone-conduction stimuli were made usinga mixed ANOVA. Only alternated bone-conduction ASSR phase-delay results wereincluded in the mixed ANOVA. Huynh-Feldtepsilon-adjustments for repeated measureswere made when appropriate. Newman-Keulspost hoc comparisons were performed forsignificant main effects and interactions. Thecriterion for statistical significance was p <.05 for all analyses.

RESULTS

Normal Bone-Conduction ASSRThresholds

The mean (1 SD) bone-conduction ASSR

thresholds in these subjects with normalhearing were 22.0 (11.4), 26.0 (13.5), 18.0(7.9), and 18.0 (11.4) dB HL for 500, 1000,2000, and 4000 Hz, respectively. Thepercentage of participants who had thresholds≤20 dB HL were 60, 40, 90, and 60% at 500,1000, 2000, and 4000 Hz, respectively. Thepercentage of participants who had thresholds≤30 dB HL were 90, 70, 100, and 100% at 500,1000, 2000, and 4000 Hz, respectively.

Monaural Air-Conduction Stimuli(Single- and Alternated-StimulusPolarities)

As shown in Table 2, the mean amplitudeand phase-delay values for ASSRs elicitedby monaural air-conduction stimuli presentedat 40 dB HL were similar for the noninverted,inverted, and alternated stimulus polarityconditions. The mean amplitude values acrossfrequency were 46.5, 40.0, and 42.7 nV fornoninverted, inverted, and alternatedstimulus polarities, respectively. Results of anANOVA comparing ASSR amplitudes acrosspolarity and carrier frequency revealed thatthere was no effect of frequency or interactionbetween frequency and polarity, but therewas a small but significant effect of polarity(p = .030) (Table 3). Post hoc comparisonsindicated that the significant polarity maineffect was due to a small but significantdifference between amplitudes for“noninverted versus inverted” stimuluspolarities. There were no significantdifferences between ASSR amplitudes to“noninverted versus alternated” or “invertedversus alternated” stimulus polarities.

Results of an ANOVA comparing ASSRphase delay across polarity and carrierfrequency revealed no interaction betweenfrequency and polarity but significant maineffects of polarity (p = .035) and frequency (p = .007). The mean phase-delay values

Table 2. Air Conduction: Mean (1 SD) Amplitude and Phase-Delay Values for Multiple ASSRsObtained in Participants with Normal Hearing (N = 10) to Single- and Alternated-Stimulus

Polarity Elicited by 40 dB HL Stimuli Presented Monaurally

POLARITY 500 Hz 1000 Hz 2000 Hz 4000 Hz

AMPLITUDE NON 46 (32) 45 (25) 46 (12) 49 (20) (nV) INV 33 (26) 43 (29) 46 (12) 37 (13)

ALT 38 (28) 43 (28) 45 (12) 44 (15) PHASE DELAY NON 134 (32) 162 (63) 108 (31) 103 (17)(degrees) INV 120 (49) 164 (57) 121 (29) 126 (58)

ALT 125 (42) 167 (62) 114 (28) 107 (19)

Note: NON = non-inverted stimulus polarity; INV = inverted stimulus polarity; ALT = alternated stimulus polarity.


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across frequency were 125.6, 138.8, and 129.2degrees for noninverted, inverted, andalternated stimulus polarities, respectively.Post hoc comparisons indicated the smalldifference in ASSR phase delay for“noninverted versus inverted” stimuluspolarities was significant, but no significantdifference was present for “noninvertedversus alternated” or “inverted versusalternated” stimulus polarities. Post hoccomparisons also indicated that phase delaywas significantly longer for 1000 Hz comparedto 2000 and 4000 Hz; no differences werefound for 500 Hz compared to higher carrierfrequencies.

Bone-Conduction Stimuli (Single- andAlternated-Stimulus Polarities)

As shown in Table 4, there were nodifferences in the slopes of the intensity-

amplitude functions between alternated- andsingle-polarity stimuli for bone-conductionASSRs. Amplitude slope tended to increasewith decreases in frequency, which is alsoindicated in Figures 1 and 2 and Table 4. Atwo-way repeated measures ANOVA indicatedthat there was no effect of polarity orinteraction between stimulus polarity andcarrier frequency for amplitude; however,there were significant differences acrosscarrier frequency, as shown in Table 5. Posthoc comparisons indicated that the meanslope for amplitude was significantly steeperfor the 500 Hz carrier frequency compared tohigher carrier frequencies.

As shown in Table 4, there were also nodifferences in the slopes of the intensity-phase-delay functions between alternated-and single-polarity stimuli for bone-conduction ASSRs. Figures 3 and 4 and Table4 indicate that the phase-delay slopes for

Table 3. Air-Conduction Stimuli:Two-Way Repeated-Measures ANOVA Showing Comparisonsof Mean Amplitude and Phase-Delay Values for Three Stimulus Polarities and Four Carrier

Frequencies for ASSRs to Monaural Stimuli Presented at 40 dB HL in Normal-HearingParticipants

Source df F εa pb

Amplitude Polarity 218 6.37 0.526 .030* Frequency 327 0.26 0.698 0.834 Polarity x Frequency 654 1.79 0.112

Phase delay Polarity 218 5.49 0.637 .032* Frequency 327 5.25 0.693 .007* Polarity x Frequency 654 0.57 0.754

a Huyhn-Feldt epsilon (ε) correction factor for degrees of freedom; b Probability reflects corrected degrees of freedom; *significant (p < .05).

Table 4. Mean (1 SD) Slope for Amplitude- and Phase-Delay for Bone- and Binaural Air-Conduction Stimuli for Single- and Alternated-Stimulus Polarities

Frequency (Hz)

Group Mode Polarity 500 1000 2000 4000

Amplitude (nV/dB) BC-ASSR BC NON 5.41 3.02 2.38 2.03 (4.66) (1.92) (2.49) (1.18)

BC-ASSR BC INV 4.27 3.58 2.16 2.12 (2.61) (1.95) (1.39) (1.55)

BC-ASSR BC ALT 4.63 3.36 2.29 2.12(2.46) (1.88) (1.83) (1.18)

AC-ASSR AC NON 1.57 1.9 1.66 2.11 (1.77) (1.26) (1.06) (1.06)

Phase delay (degrees/dB) BC-ASSR BC NON -3.93 -5.06 -2.58 -2.63 (2.08) (3.55) (1.20) (1.63)

BC-ASSR BC INV -1.77 -3.97 -2.25 -2.53 (2.59) (2.52) (1.04) (1.43)

BC-ASSR BC ALT -2.56 -3.65 -2.5 -2.67 (2.42) (2.79) (0.84) (1.27)

AC-ASSR AC NON -0.18 -2.84 -2.29 -1.47 (1.94) (1.21) (0.68) (0.56)

Note: BC = bone conduction; AC = binaural air-conduction; NON = noninverted stimulus polarity; INV = inverted stimuluspolarity; ALT = alternated stimulus polarity.


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ASSRs to 500, 2000, and 4000 Hz stimulitended to be similar; the phase-delay slopesfor ASSRs to 1000 Hz stimuli tended to besteeper than the other carrier frequencies. Atwo-way repeated measures ANOVA, shownin Table 5, indicated that, for phase delay,there was no effect of polarity or interactionbetween stimulus polarity and carrierfrequency; however, there were significantdifferences across carrier frequency. Post hocpair-wise comparisons indicated that themean slope for phase-delay for the 1000 Hzcarrier frequency was significantly steepercompared to the 500, 2000, and 4000 Hzcarrier frequencies.

Bone-Conduction versus Binaural Air-Conduction ASSRs

Figures 1 and 2 and Table 4 show thatamplitudes for ASSRs to binaural air-

conduction stimuli (30, 40, and 60 dB HL) andbone-conduction stimuli (30, 40, and 50 dBHL) had the same slope with increasedintensity for 1000, 2000, and 4000 Hz carrierfrequencies. For 500 Hz, the increase inamplitude with intensity was steeper forbone-conduction ASSR amplitudes (single-and alternated-stimulus polarities) comparedto air-conduction ASSR amplitudes (Table4). Results of a two-way mixed ANOVA foramplitude showed that ASSRs to bone-conduction stimuli had steeper intensity-amplitude slopes than ASSRs to air-conduction stimuli. There was also asignificant main effect for frequency and asignificant interaction between mode ofstimulus and carrier frequency (Table 6).Post hoc pair-wise comparisons for theinteraction between frequency and mode ofstimulus indicated that the slope foramplitude for ASSRs to the 500 Hz bone-

Table 5. Bone-Conduction Stimuli:Two-Way Repeated Measures ANOVA for Bone-ConductionASSRs Comparing Slopes of Amplitude- and Phase-Delay-Intensity Functions for Three

Stimulus Polarities and Four Carrier Frequencies

Source df F εa pb

Amplitude Polarity 218 0.24 0.516 0.642 Frequency 327 6.21 0.588 .012* Polarity x Frequency 354 0.61 0.72

Phase delay Polarity 216 1.49 0.609 0.259 Frequency 324 4.04 0.622 .042* Polarity x Frequency 648 1 0.438

a Huynh-Feldt epsilon (ε) correction factor for degrees of freedom; b Probability reflects corrected degrees of freedom; * significant (p < .05).

Figure 1. Mean (±1 SD) amplitudes for bone- and air-conduction (binaural) multiple ASSRs for partici-pants with normal hearing. Responses shown wereelicited by single-polarity (noninverted) stimuli. Theresponse noise floor is denoted by a dotted line.

Figure 2. Mean (±1 SD) amplitudes for bone- and air-conduction (binaural) multiple ASSRs for partici-pants with normal hearing. Responses shown wereelicited by alternated-polarity stimuli. The responsenoise floor is denoted by a dotted line.


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conduction stimulus was significantly steeperthan any of the ASSRs to bone-conductionstimuli at higher frequencies or air-conduction stimuli at any frequency.

Figures 3 and 4 and Table 4 show thatthe intensity-phase-delay functions acrosscarrier frequencies for air- and bone-conduction ASSRs tended to be steeper at1000 Hz. The increase in phase delay withintensity was steeper for bone-conductionASSR phase delay compared to air-conductionASSR phase delay. Results of a two-waymixed ANOVA showed that ASSRs to bone-conduction stimuli had steeper slopes forphase delay than those to air-conductionstimuli and that there were differences inslope across carrier frequencies. There wasno significant interaction between mode ofstimulus and carrier frequency (Table 6).

Post hoc comparisons of carrier frequency(pooled across air- and bone-conduction mode)indicated that the slope for phase delay wassignificantly steeper for 1000 Hz stimulicompared to 2000 or 4000 Hz but no differencewas found between 500 and 1000 Hz stimuli.

Figures 3 and 4 also show that bone-conduction ASSRs had longer phase delaysthan binaural air-conduction ASSRs. Phasedelay was converted to milliseconds byaveraging the phase delay of the ASSRselicited by 30 and 40 dBHL stimuli anddividing by (360 x modulation frequency).The mean differences in phase delay inmilliseconds between bone- (noninverted)and air-conduction ASSRs were 2.49, 3.52,3.48, and 3.81 msec at 500, 1000, 2000, and4000 Hz, respectively. Similarly, the meandifferences in phase delay between bone-

Figure 3. Mean (±1 SD) phase delay for bone- andair-conduction (binaural) multiple ASSRs for partic-ipants with normal hearing. Responses shown wereelicited by single-polarity (noninverted) stimuli. Aminimum of five subjects contributed to each meanvalue plotted.

Figure 4. Mean (±1 SD) phase delay for bone- andair-conduction (binaural) multiple ASSRs for partic-ipants with normal hearing. Responses shown wereelicited by alternated stimuli. A minimum of fivesubjects contributed to each mean value plotted.

Table 6.Two-Way Mixed ANOVA Showing Comparisons of the Slope of Intensity-AmplitudeFunction and Intensity-Phase-Delay Functions for Two Stimulus Modes (bone- versus binauralair-conduction stimulus presentation) and Four Carrier Frequencies (within-subjects factor).

Source df F εa pb

Amplitude Mode 118 6.04 .024* Frequency 354 3.06 0.884 .043* Mode x Frequency 354 5.06 .004*

Phase delay Mode 117 11.14 .004* Frequency 351 3.97 0.697 .026* Mode x Frequency 351 1.38 0.261

Note: The bone-conduction ASSRs were elicited using an alternated stimulus polarity. a Huynh-Feldt epsilon (ε) correction factor for degrees of freedom; b Probability reflects corrected degrees of freedom;

* significant (p < .05).


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(alternated) and air-conduction ASSRs were2.42, 3.32, 3.48, and 3.91 msec at 500, 1000,2000, and 4000 Hz, respectively.

DISCUSSION

The bone-conduction ASSR thresholds inthe present study range from 18–26 dB

HL for 500, 1000, 2000, and 4000 Hz stimuli,respectively. As shown in Table 7, comparisonof the bone-conduction ASSR thresholds topreviously reported results (Lins et al, 1996;Herdman and Stapells, 2001; Dimitrijevic etal, 2002; Jeng et al, 2004) indicates valueswith substantial variability across studies.All bone-conduction thresholds in Table 7,except for the thresholds obtained in thepresent study, are reported in dB HL afteradjusting for forehead-mastoid differences (-14.0, -8.5, -11.5, and -8.0 dB at 500, 1000,2000, and 4000, respectively) and the occlusioneffect (16.0, 8.0, 0.0, and 2.0 dB at 500, 1000,2000, and 4000, respectively). Averaged acrossfrequencies, thresholds in the present studyare approximately 5 dB higher than thosereported by Dimitrijevic et al (2002), 4 dBlower than those of Lins et al (1996), and 18dB lower than those reported by Jeng et al(2004). Much of the variability in the thresholdvalues may be due to: (1) differences in theplacement of the bone oscillator (foreheadversus mastoid), (2) occluded versus unoccludedears, (3) method of stimulus calibration, (4)inherent variability in bone-conductioncalibration, and (5) small sample sizes. Theapplication of correction factors to allowcomparisons across studies also introducesvariability. Differences in ASSR thresholds tobone-conduction stimuli across studies shouldtherefore be interpreted cautiously because ofthese sources of variability in its measurement.

Bone-conduction ASSR thresholds in thepresent study are similar to air-conduction

ASSR thresholds reported by other studies.For example, as shown in Table 7, Herdmanand Stapells (2001) reported air-conductionthresholds (converted to dB HL) that arewithin 3–7 dB of our bone-conduction ASSRthresholds (in dB HL).

Bone-conduction ASSRs have longerlatencies compared to air-conduction ASSRs.The direction of these results is consistent withthose reported by Boezeman et al (1983) andGorga et al (1993) for ABR wave V. However,the ASSR latency differences in the presentstudy (2.42–3.91 msec) are substantially greaterthan the differences reported by Boezeman etal (0.88 msec for a 2000 Hz brief tone) andGorga and colleagues (0.16–0.41 msec for 250to 4000 Hz brief tones). Possible explanationsfor these results are: (1) latency differencesderived from ASSR phase delays may not beexactly the same as ABR latencies, and/or (2)bone conduction at the mastoid may not beequivalent in effective level to binaural airconduction. Stenfelt and Hakansson (2002)found a 6–10 dB difference in loudness betweenair- and bone-conduction stimuli for 250 to4000 Hz stimuli presented at 30–80 dB HL.They attributed this result to distortion fromthe bone transducer, multimodal stimulation,and differences in transmission path affectingthe perceived loudness.

The differences in amplitude between air-and bone-conduction ASSRs elicited in thepresent study are similar to the results reportedby Dimitrijevic et al (2002). In both studies,ASSR intensity-amplitude functions weresteeper for 500 Hz bone-conduction stimulicompared to air-conduction stimuli. Dimitrijevicet al (2002) used bone-conduction white-noisemasking in an attempt to eliminate themultiple ASSRs to bone-conduction stimuli inorder to confirm that the responses werephysiologic, not artifactual. They found that notall ASSRs to bone-conduction stimuli presented

Table 7. Across-Study Comparison of ASSR Thresholds in dB HL

STUDY MODE 500 Hz 1000 Hz 2000 Hz 4000 Hz

PRESENT STUDY BONE • 22 26 18 18 Lins et al,1996 BONE * 31 29 20 19 Dimitrijevic et al, 2002 BONE † 32 18 10 13 Jeng et al, 2004 BONE § 48 33 41 38 Herdman and Stapells, 2001 AIR ∞ 17 19 15 15

Note: Thresholds have been corrected, where necessary, to account for forehead-mastoid differences and for occlusioneffects.

• Multiple AM tones, mastoid placement, unoccluded; * Multiple AM tones, forehead placement, occluded; † MultipleAM/FM tones, forehead placement, occluded; thresholds were calculated from ASSR (AM tones) minus behavioral (AM tones)threshold differences (A. Dimitrijevic, pers. comm.); § Multiple AM tones, forehead placement, occluded; ∞ Multiple AM tones,single ear (insert earphone).


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at 30 dB SL were eliminated by masking;responses were present in 17.5% of the subjects,which was significantly greater than the 5%expected by chance. The majority of theseresponses were to 1000 Hz stimuli (A.Dimitrijevic, pers. comm.). Dimitrijevic et al(2002) suggested that this result was either dueto undermasking or that a small amount ofstimulus artifact was present in the response.Dimitrijevic et al used a 1000 Hz A/D rate, arate that we have shown can result in aliasingof stimulus artifact in the EEG at higher bone-conduction intensities (Small and Stapells,2004).

Lins et al (1996) also found differencesbetween air- and bone-conduction ASSRamplitudes to 500 and 1000 Hz carrierfrequencies compared to higher carrierfrequencies, but they were unable to explaintheir results. They used a 679 Hz A/D rate todigitize the EEG. Although aliasing wouldlikely have occurred, artifact in the EEG wouldnot have aliased at exactly the modulationrate of the carrier frequency because of the679 Hz A/D rate. Although aliasing may nothave been an issue, “nonauditory” physiologicresponses to 500 and 1000 Hz stimuli mayaccount for their unexpected results (Smalland Stapells, 2004).

In the present study, we found that ASSRphase delay systematically decreased withincreasing intensity for air- and bone-conduction stimuli (Figures 3 and 4) except for500 Hz air-conduction stimuli. Dimitrijevic etal (2002) reported similar results for air-conduction stimuli but found no clearrelationship between onset phase and intensityfor bone-conduction stimuli. The presence ofaliasing may have confounded their bone-conduction results. The lack of change in phasedelay with intensity for the air-conduction 500Hz results in the present study is not wellunderstood.

The possibility of artifactual responses(whether nonauditory physiologic or stimulusartifact) in the ASSR is demonstrated by thepresence of spurious responses to 50 and 60 dBHL 500 Hz bone-conducted stimuli inparticipants with severe-to-profound hearinglosses who cannot hear the bone-conductionstimuli (Small and Stapells, 2004). Our resultsfor subjects with normal hearing (presentstudy) show that alternating the stimuluspolarity has no effect on the slope of theintensity-amplitude or intensity-phase-delayfunctions for ASSRs to 500 Hz or any othercarrier frequencies. Because alternating

polarity does not alter the responses of normalsubjects, the findings of the present study lendsupport to the possibility that these responsesare physiologic rather than the result ofstimulus artifact. Previous studies have shownthat vestibular-evoked myogenic potentialscan be elicited by high-intensity clicks andtone bursts (Colebatch, 2001). Recently, Nonget al (2000) reported an acoustically evokedshort-latency negative response at 3–4 msecwhen recording ABRs in patients with profoundhearing loss. The results of the present studyalso confirm that an “alternating” stimuluspolarity does not, in itself, distort the amplitudeor phase characteristics, as indicated by theresults for the ASSRs to a 40 dB HL monauralair-conduction stimulus.

SUMMARY

Normal ASSR thresholds to amplitude-modulated bone-conduction stimuli are

22, 26, 18, and 18 dB HL for 500, 1000, 2000,and 4000 Hz, respectively. Alternating thepolarity of the stimulus does not significantlychange the amplitude or phase of the ASSRsand, thus, can be used to reduce thecontribution of spurious responses in bone-conduction ASSRs resulting from stimulusartifact in the EEG. Spurious responses arealso avoided by using a 1250 Hz A/D rateand a steep anti-aliasing filter. In adults withnormal hearing, ASSR amplitudes are largerfor 500 Hz compared to higher carrierfrequencies for bone-conduction stimuli,despite alternating the stimulus polarity.Bone-conduction amplitude measures forASSRs to 500 Hz stimuli are also largercompared to binaural air-conduction ASSRs(all carrier frequencies). The change in ASSRphase delay with intensity is steeper for 1000Hz compared to 500, 2000, and 4000 Hz. Thechange in phase-delay with intensity issteeper for bone-conduction ASSRs comparedto binaural air-conduction ASSRs. The steeperintensity-amplitude slope for bone-conductionASSRs to 500 Hz may be related to ourprevious findings that artifactual responsesare present to high-intensity bone-conductionstimuli for single- and alternated-stimuluspolarities (Small and Stapells, 2004).

CONCLUSIONS AND CLINICALIMPLICATIONS

Multiple ASSRs to bone-conductionstimuli can be used to assess threshold


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at 500, 1000, 2000, and 4000 Hz in adultswith normal hearing. Multiple ASSRs canpotentially be used to assess bone-conductionthresholds in individuals with mild-to-moderate hearing loss. For 500 Hz stimuli,however, the possibility of nonauditoryphysiologic responses for levels 50 dB HL orgreater limits recording ASSRs at thisfrequency to intensities 40 dB HL and lower(Small and Stapells, 2004). Based on thisstudy’s results, this gives a maximum rangeof approximately 18 dB (i.e., 40 dB HL minusnormal hearing threshold of 22 dB HL) at 500Hz, possibly limiting clinical conclusions at500 Hz to determine whether thresholds are“normal” or “elevated.” For higher carrierfrequencies, stimulus artifact andnonauditory physiologic responses are notlikely to be an issue, and the testing rangeis limited only by the output characteristicsof the transducer. It must be noted, however,that there are no normative threshold datafor infants and no threshold data from anysubjects with impaired hearing (infants oradults). Bone-conduction ASSRs are,therefore, not yet ready for clinical use.

Acknowledgment. Lindsay Bendickson helped withdata collection and analyses. Dan Black (dB SpecialInstruments) generously supplied calibrationequipment. This research was supported by a MichaelSmith Foundation for Health Research Trainee Awardand by grants from the Canadian Institutes of HealthResearch and the Natural Sciences and EngineeringResearch Council of Canada. Portions of this paperwere presented at the American Auditory SocietyMeeting (Scottsdale, Arizona, March 2003) and theXVIII Biennial Symposium of the InternationalEvoked Response Audiometry Study Group (Tenerife,Canary Islands, Spain, June 2003).

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Multiple Auditory Steady-State Responses to Bone ...€¦ · dB HL bone-conduction stimuli and to 30–60 dB HL air-conduction stimuli were compared.The effect of alternating stimulus