the effects of monotic and dichotic interference tones on ... · prueba de amplitud modulada (am) y...

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J Am Acad Audiol 19:101–119 (2008)

*School of Audiology and Speech-Language Pathology, University of Memphis

School of Audiology and Speech-Language Pathology, University of Memphis, 807 Jefferson Avenue, Memphis, TN 38105; Phone:901-678-5816; Fax: 901-525-1282; E-mail: [email protected]

Portions of this report were presented at the Twenty-Ninth Annual MidWinter Research Meeting of the Association for Research inOtolaryngology on February 5, 2006, in Baltimore, Maryland and at AudiologyNOW! on April 19, 2007, in Denver, Colorado.

This study was supported by a New Investigator Research Award provided by the American Academy of Audiology Foundation.

The Effects of Monotic and Dichotic InterferenceTones on 40 Hz Auditory Steady-State Responsesin Normal-Hearing Adults

Shaum P. Bhagat*

Abstract

Auditory steady-state responses (ASSRs) recorded with simultaneouspresentation of multiple tones modulated from 77–105 Hz exhibit frequencyspecificity and can be acquired with monotic or dichotic stimulation. This studyexamined the frequency specificity and dichotic characteristics of 40 Hz ASSRsrecorded with amplitude-modulated (AM) probe tones and unmodulated (UM)or AM interfering tones in 27 normal-hearing adults. The effects on ASSRamplitudes of monotically or dichotically presented interfering tones of variousfrequency, modulation depth, and modulation rate were studied. Significantdecreases in ASSR amplitudes occurred when the UM interfering tone wasmonotic, higher in frequency, and approximately within an octave of the probetone. ASSR amplitudes were also reduced when the AM interfering tone wasmonotic and modulated at a lower depth and was an octave above the probetone. Probe and interfering AM tones modulated at different rates producedsimilar reductions in amplitude for ASSRs acquired with monotic and dichoticstimulation. The findings of this study contribute to clarifying the carrier andtemporal envelope interactions between tonal stimuli. Description of the effectsof these stimulus parameters on 40 Hz ASSRs can benefit clinical applicationsof this technique, including evaluating auditory function in adults not capableof participating in behavioral audiometric tests.

Key Words: Auditory evoked potentials, auditory steady-state response,objective audiometry

Abbreviations: A/D = analog-to-digital; AM = amplitude modulated; ASSR =auditory steady-state response; D/A = digital-to-analog; EEG =electroencephalogram; MM = mixed modulated; SNR = signal-to-noise ratio;UM = unmodulated

Sumario

Las respuestas auditivas de estado estable (ASSR) registradas con unapresentación simultánea de múltiples tonos modulados desde 77 a 105 Hz,exhiben especificidad frecuencial y puede ser adquiridas con estimulaciónmonótica o dicótica. Este estudio examinó la especificidad frecuencial y lascaracterísticas dicóticas de las ASSR de 40 Hz registradas con sondas deprueba de amplitud modulada (AM) y con tonos de interferencia no modulados(UM), en 27 sujetos adultos normoyentes. Se estudiaron los efectos sobre lasamplitudes de las ASSR producto de tonos de interferencia presentados enforma monótica o dicótica, caracterizados por diferentes frecuencias,profundidades de modulación y tasa de modulación. Ocurrieron reduccionessignificativas en la amplitud de las ASSR cuando el tono de interferencia UMera monótico, de frecuencia mayor, y aproximadamente dentro de una octava

DOI: 10.3766/jaaa.19.2.2

Journal of the American Academy of Audiology/Volume 19, Number 2, 2008

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An auditory steady-state response(ASSR) is detected by placing surfaceelectrodes on the scalp and occurs

when neural potentials evoked by one audi-tory stimulus temporally overlap with thoseevoked by subsequent auditory stimuli(Picton et al, 2003). Sequential presentationsof continuous amplitude-modulated (AM) ormixed-modulated (MM) tones are commonlyused to evoke the ASSR. The recorded ASSRwaveform is periodic, and spectral analysis ofthe waveform reveals a prominent peak atthe modulation frequency imposed on thecarrier (Rickards and Clark, 1984). In alertadults, the largest ASSRs are evoked bytones modulated near 40 Hz (Kuwada et al,1986; Picton et al, 1987). State of arousalaffects the amplitude of 40 Hz ASSRs, as theresponse is reduced in sleeping or sedatedsubjects (Cohen et al, 1991; Dobie andWilson, 1998). However, ASSRs elicited bytones modulated above 70 Hz are less affect-ed by sleep state (Cohen et al, 1991; Levi etal, 1993). The effects of subject state on 40 HzASSRs have limited their application as aclinical test of auditory function.Consequently, most ASSR research studiesdirected at estimating behavioral hearingthresholds have utilized carriers modulatedat rates above 70 Hz (Aoyagi et al, 1994;Rance et al, 1998; Rance and Rickards, 2002;Vander Werff et al, 2002; Johnson and Brown,2005). Although the clinical use of 40 HzASSRs may be inappropriate in infants andyoung children because of the sleep-inducedeffects on the response, the development of anobjective test to document auditory status in

adult populations (i.e., individuals with hand-icapping conditions or individuals suspectedof having nonorganic hearing loss) not willingor capable of participating in behavioralaudiometric evaluations is warranted. Stateof arousal effects can be monitored moreclosely in adults, and the 40 Hz ASSR tech-nique has been proposed as a frequency-spe-cific method of estimating behavioral hearingthresholds in adults (Kuwada et al, 1986;Petitot et al, 2005; Tomlin et al, 2006).

Another method of recording ASSRs forclinical purposes involves simultaneousmonotic or dichotic presentation of multiplecarrier tones modulated at slightly differentrates (Lins and Picton, 1995; Lins et al, 1996;John et al, 1998; John and Picton, 2000;Herdman and Stapells, 2001; John et al,2001; Perez-Abalo et al, 2001; Dimitrijevic etal, 2002; Herdman and Stapells, 2003; Pictonet al, 2005; Schmulian et al, 2005; Small andStapells, 2005; Van Maanen and Stapells,2005; Vander Werff and Brown, 2005; Attiaset al, 2006; Luts et al, 2006; Savio et al,2006). Spectral analysis of the resultingASSR waveform reveals multiple peaks cor-responding to the modulation frequenciesimposed on each carrier present in the stim-ulus (Lins and Picton, 1995). An advantage ofrecording the simultaneous multiple ASSR isthat several test frequencies can be evaluat-ed at once in one or both ears, potentiallyincreasing test efficiency by minimizing thetime required to acquire the responses. Inorder for the full benefit of this technique tobe realized, interactions between the multi-ple stimuli should be sufficiently limited so

del tono de prueba. Las amplitudes de las ASSR también se redujeron cuandoel tono de interferencia de AM era monótico y modulado a una profundidadmenor y a una octava por encima del tono de prueba. Los tonos de prueba yde interferencia con AM, modulados a diferentes tasas, produjeron reduccionessimilares en la amplitud de las ASSR, cuando se lograban con estimulaciónmonótica o dicótica. Los hallazgos de este estudio contribuyen a aclarar lasinteracciones con la envolvente temporal y la del portador, entre estímulostonales. La descripción de los efectos de estos parámetros del estímulo sobrelas ASSR de 40 Hz pueden beneficiar la aplicación clínica de esta técnica,incluyendo la evaluación de funciones auditivas en adultos no capaces departicipar en pruebas audiométricas conductuales.

Palabras Clave: Potenciales evocados auditivos, respuestas auditivas deestado estable, audiometría objetiva

Abreviaturas: A/D = analógico a digital; AM = amplitud modulada; ASSR =respuestas auditivas de estado estable; D/A = digital a analógico; EEG =electroencefalograma; MM = modulado mixto; SNR = tasa de señal/ruido; UM= no modulado

Effects of Monotic and Dichotic Interference/Bhagat

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that response detection and frequency speci-ficity are not compromised. The advantagesof this technique are negated if stimulusinteractions diminish the ASSR signal-to-noise ratio (SNR) or confound attempts toestimate frequency-specific behavioral hear-ing thresholds. Therefore, selection of appro-priate stimuli that maintain both highresponse SNRs and frequency specificity isadvantageous for clinical applications of thetechnique.

Several studies have compared ASSRsacquired with single and multiple AM carriertones modulated at high rates (77–105 Hz) innormal-hearing adults. These studies foundno differences in response amplitude orlatency between ASSRs acquired with oneAM carrier and ASSRs acquired with up toeight AM carriers (four per ear) presented atequivalent levels and separated by octaveintervals (Lins and Picton, 1995; John et al,1998; John and Picton, 2000). In addition,modulation frequencies imposed on adjacentcarriers could be separated by as little as 1.3Hz without significantly affecting theresponse (John et al, 1998). These findingsimply that the multiple ASSR technique ismore efficient than recording single ASSRs(John et al, 2002).

Frequency specificity of ASSRs obtainedwith multiple carriers modulated at ratesfrom 77–105 Hz has also been the focus ofconsiderable research effort. Utilizing high-pass noise maskers while recording high-rateASSRs, Herdman et al (2002a) surmised thatthe spread of excitation along the basilarmembrane in response to both moderate-level single carriers and multiple carrierspresented at octave intervals was limited toone-half octave above each carrier frequency.Numerous studies provide further evidenceof frequency specificity by demonstratingthat multiple high-rate ASSR thresholds andbehavioral hearing thresholds are well corre-lated from 500–4000 Hz in normal-hearingadults and adults with sensorineural hearingloss (Lins et al, 1996; Dimitrijevic et al, 2002;Herdman and Stapells, 2003; Vander Werffand Brown, 2005; Attias et al, 2006; Scherf etal, 2006). Multiple high-rate ASSR thresh-olds acquired with dichotic stimulation alsoexhibit agreement with the behavioral audio-gram in these groups (Herdman andStapells, 2001; Perez-Abalo et al, 2001;Schmulian et al, 2005).

Previous research shows that proper selec-

tion of stimulus parameters can minimizethe stimulus interactions that may compro-mise the efficiency or accuracy of the multi-ple ASSR technique. However, ASSRs evokedby carriers modulated at high rates exhibitconsiderable SNR variability across test fre-quency and typically require longer averag-ing times for 500 Hz carriers compared to2000 Hz carriers (van der Reijden et al,2004). Discrepancies in averaging multipleASSRs across carrier frequencies can prolongacquisition times and limit the efficiency ofthe technique (John et al, 2002). A possiblesolution to this problem would involve utiliz-ing modulating frequencies that evoke largerASSRs, particularly at lower test frequen-cies. Despite the fact that 40 Hz ASSRsincrease in amplitude with decreasing testfrequency from 4000 Hz to 500 Hz and can beup to five times larger than high-rate ASSRsin adults (Rodriguez et al, 1986; Herdman etal, 2002b), comparatively fewer studies haveexamined the effects of multiple carriers onthe 40 Hz ASSR. The results of two studiesinvestigating stimulus interactions revealedthat 40 Hz ASSR potentials and magneticfields were significantly reduced when theywere acquired with multiple carriers sepa-rated by octave intervals (John et al, 1998;Ross et al, 2003). These results suggest thatstimulus interactions are more evident forAM tones modulated near 40 Hz compared tohigher rates of modulation. This is an unex-pected finding, since for AM tones modulatedin the range of 77–105 Hz, the sideband fre-quencies are more spectrally remote from thecarrier frequency than for AM tones modu-lated near 40 Hz. It is conceivable that stim-ulus envelope interactions, as well as carrierinteractions, may lead to amplitude reduc-tions for 40 Hz ASSRs acquired with multiplestimuli. Distinguishing between these typesof interactions provides information as to theprocess by which multiple 40 Hz ASSRs aregenerated and may contribute to identifyingthe optimal stimulus parameters for clinicaltesting. Carrier and envelope interactionscan potentially be distinguished by compar-ing the effects of unmodulated (UM) and AMinterference tones on 40 Hz ASSRs elicitedwith AM probe tones. Previous evoked poten-tial research examining multiple 40 HzASSRs in human adults has primarilyfocused on the effects of monotically present-ed AM or MM carriers modulated at depthsnear 100%. Therefore, dichotic presentation

of carriers and the effects of modulationdepth on 40 Hz ASSRs warrant furtherscrutiny.

The purpose of this study was to examinethe effects of interfering tone frequency, mod-ulation depth, and modulation rate on 40 HzASSRs elicited with monotic and dichoticstimulation in normal-hearing adults. Theseexperiments were designed to compare theamplitudes of 40 Hz ASSRs acquired in twoconditions: (1) with AM probe tones (one car-rier) and (2) when the AM probe tones werepaired with either UM or AM interferingtones (two carriers).

METHODS

Subjects

In total, 32 subjects aged 19–28 yearswere enrolled in the study initially. However,due to subject attrition, the final sample sizewas 27 subjects. Prior to being enrolled, sub-jects were interviewed regarding their casehistory. Subjects were excluded from partici-pation if they had a history of hearingimpairment and otological or neurologicaldisease. Next, the hearing of each subjectwas screened with a calibrated audiometer(GSI 16) in a sound-treated enclosure. Allsubjects admitted into the study had hearingthresholds at or better than 20 dB HL(American National Standards Institute[ANSI], 1996) in both ears for the standardaudiometric test frequencies from 250–8000Hz. A middle-ear analyzer (GSI Tympstar)was used to perform tympanometry on bothears of each subject. Persons with flat tym-panograms or peak tympanometric pressuresthat exceeded the range of ±100 daPa ineither ear were not admitted into the study.Four people were excluded from participat-ing on the basis of these preliminary tests.Three potential participants failed the hear-ing screening, and the fourth potential par-ticipant had abnormal tympanometryresults. The procedures were explained atthe time of the experimental sessions, andinformed consent was obtained from eachsubject. At the conclusion of the experimentalsessions, each subject received a $25 stipend.

Stimuli

Continuous AM tones were digitally gen-erated by multiplying two sine wave func-

tions using Tucker-Davis Technologies soft-ware (SigGen) and a two-channel 16-bit digi-tal-to-analog (D/A) converter (Tucker-DavisTechnologies, model DA1) at a 10 kHz sam-pling rate. The two channels of the D/A con-verter were utilized in an attempt to sepa-rate the electrical waveforms of probe andinterfering AM tones in order to minimizedistortion-product artifacts. A waveform gen-erator (Tucker-Davis Technologies, WG1)produced continuous UM interfering tones.Analog signals were sent to programmableattenuators (Tucker-Davis Technologies,model PA4) and headphone buffers (Tucker-Davis Technologies, model HB6) before beingtransduced by insert earphones (Eartone,3A). In order to avoid generating acousticartifacts, the carrier and modulation fre-quencies of AM tones were adjusted to allowan integer number of cycles to occur withinthe time window of 204.8 msec for eachsweep (see “Recording Procedures” sectionbelow). Consequently, carriers with nominalfrequencies of 1000 Hz were adjusted to996.1 Hz so that 204 cycles were completedwithin the 204.8 msec time frame. Nominalmodulation rates at 40 Hz were adjusted to39.055 Hz to allow eight cycles to be complet-ed within the recording period. This stimulusgeneration technique also provides for accu-rate frequency analysis and has been utilizedby previous ASSR studies (Lins and Picton,1995; John et al, 1998; John and Picton,2000). Care was taken to select carrier andmodulation frequencies that were not integermultiples of the nominal mains line frequen-cy. The overall level of each of the probe andinterfering tones was 70 ± 0.5 dB SPL asmeasured in a 2-cc coupler by a sound-levelmeter (Larson-Davis, model DSP82). Toassist in the reading of this paper, carrier andmodulation frequencies are expressed innominal values.

General Experimental Design

The experimental sessions took place in anelectrically shielded, double-walled, sound-treated room. Subjects were seated in a com-fortable reclining chair during the experi-mental procedures and were awake andmaintained mental alertness during theexperimental sessions by reading books ormagazines. The probe tones utilized in thisinvestigation were at frequencies of either500 or 1000 Hz. These frequencies are known


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to elicit large 40 Hz ASSRs (Rodriguez et al,1986), and they were also selected in order tomake direct comparisons with previousresearch. The carrier frequencies and modu-lation characteristics of the interfering toneswere parametrically varied to determinetheir potential effects on the 40 Hz ASSRamplitudes. Subjects were pseudorandomlyassigned to one of three experiments. InExperiments 1 and 2, single presentations ofthe AM probe and simultaneous paired pre-sentations of the AM probe and interferingtones were delivered monotically to the rightear of each subject with a probe assemblycontaining a low-noise microphone (EtymoticResearch, model 10B). Prior to data collec-tion, the stimuli were delivered into a 2-cctest cavity, and the output of the probe micro-phone was routed to a spectrum analyzer(Stanford Research, model SR760) to verifythe accuracy of the modulation characteris-tics by comparing the sideband frequenciesand levels relative to the carrier frequencies.During Experiment 3, simultaneous dichoticpresentations were accomplished in eachsubject by delivering the AM probe tones to

the right ear with the probe assembly, andthe AM interfering tones were delivered tothe left ear with an insert earphone (Eartone,3A). Each experiment required approximate-ly 2.0–2.5 hours to complete. The order ofstimulus presentations was determinedusing a randomization procedure.

The purpose of Experiment 1 was to exam-ine if potential change in 40 Hz ASSR ampli-tudes was related to interactions between thecarriers of the probe and interfering tones.During this experiment, the AM probe had a1000 Hz carrier frequency, 40 Hz modulationfrequency, and modulation depth of 100%.The probe was either presented alone orpaired with one of four UM interfering tonesat 500, 1500, 2000, or 4000 Hz during acqui-sition of ASSRs. The conditions forExperiment 1 are listed in Table 1. Sixteensubjects (one male) aged 20–28 years partici-pated in this experiment, and each subjectcompleted all five conditions examined in theexperiment. The purpose of Experiment 2was to examine the effects of modulationdepth of the AM interfering tones on theamplitude of 40 Hz ASSRs. In this experiment,


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500 and 1000 Hz AM probes were utilized.Each AM probe was modulated at 40 Hz witha modulation depth of 100%. The AM probeswere presented alone in order to acquirebaseline 40 Hz ASSRs. The modulation char-acteristics of the AM interfering tonesmatched those of the AM probe tones, withthe exception that the depth of modulationwas either 12.5%, 25%, 50%, or 100%. The500 Hz probe tone was paired with a 1000 Hzinterfering tone, and the 1000 Hz probe tonewas paired with a 500 Hz interfering tone foreach of the modulation depths studied in theexperimental conditions. Thus, comparisonsbetween conditions when the interfering tonewas either an octave above or an octavebelow the probe tone could be made. Eightfemale subjects aged 19–25 years initiallyparticipated in this experiment, but two sub-jects could not complete all ten conditions ofthe experiment due to time constraints. Thedata from the six remaining subjects wereentered into the data analysis. Table 2 liststhe conditions studied in Experiment 2. Thepurpose of Experiment 3 was to examineinteractions between the temporal envelopesof the AM probe and interfering tones, andtheir potential effects on the 40 Hz ASSRamplitudes. The AM probe had a 1000 Hzcarrier and was modulated at 40 Hz with amodulation depth of 100%. The AM interfer-ing tones had 2000 Hz carriers and weremodulated from 30–80 Hz in approximately

10 Hz steps, each at a depth of 100%. The 40Hz ASSRs were acquired in baseline condi-tions with the AM probe alone, and when theprobe was paired with one of six AM interfer-ing tones, each modulated at a different ratewithin the range of modulation frequenciesstudied. The AM interfering tones werepaired both monotically and dichotically withthe AM probe tone and were presented toeach subject. This resulted in 13 measure-ment conditions comprising Experiment 3.Eight female subjects aged 20–23 years ini-tially participated in this experiment.However, a technical error during data col-lection required the data acquired from onesubject to be excluded, and two other subjectsfailed to complete each of the 13 conditions ofthe experiment due to fatigue. Therefore,data from the five remaining subjects wereentered into the data analysis. The condi-tions studied in Experiment 3 are listed inTable 3.

Recording Procedures

Preparation for recording ASSRs began bylightly abrading the skin of each subject onthe scalp and earlobes. Conducting paste wasapplied to gold-plated electrodes, and theelectrodes were placed at locations accordingto the 10–20 international system (Jasper,1958). The noninverting electrode was placedat the vertex (Cz), the inverting electrode


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was placed at the right earlobe (A2), and theground electrode was placed on the forehead(Fpz). Interelectrode impedances, assessedat 30 Hz, were at or below 2 kOhm.Electrophysiological recordings, data storage,and analysis were performed with Tucker-Davis Technologies software (BioSig). Thesingle-channel recordings were differentiallyamplified 200,000 times and bandpass fil-tered from 10–300 Hz by a bioamplifier con-troller with a rejection rate of -6 dB/octave -(Tucker-Davis Technologies, model DB4). Anadditional low-pass filter (Tucker-DavisTechnologies, model PF1) with a cut-off fre-quency of 100 Hz and a rejection rate of -34dB/octave was used to attenuate carrier fre-quency artifacts, as has been recommendedpreviously (Picton and John, 2004). TheASSRs were digitized using a sampling rateof 10 kHz by a 16-bit analog-to-digital (A/D)converter (Tucker-Davis Technologies, modelAD1). Sweeps containing voltages exceeding90% of the amplitude range of the A/D con-verter were rejected. The ongoing electroen-cephalogram (EEG) waveform was continu-ously monitored, and recording was paused ifexcessive myogenic activity was observed. Inaddition, the ongoing EEG was monitored forthe potential presence of large amplitude,low-frequency components indicative ofdrowsiness in each subject. No evidence ofthese components were found in any subjectduring the recording sessions, findings to beexpected as the subjects were awake duringthe procedure. The time window for eachsweep was 204.8 msec. Each ASSR waveformwas constituted from 512 sweeps averagedcontinuously during the recording period. Atleast two consecutive waveforms wereobtained for each condition examined dur-ing the experimental sessions, resulting in aminimum of 1024 sweeps/condition. If thereplicated ASSR waveform was of poor qual-ity due to excessive myogenic activity, thereplications were repeated. An offline 2048-point fast Fourier transform (FFT) analysiswas performed on each ASSR waveform.Amplitude spectra were examined for peaksthat corresponded to the modulation fre-quency of interest. Using a manual cursor,the amplitude of the Fourier component at39 Hz was determined for each conditionstudied. These measurements wereexpressed in nanovolts and determined themagnitude of the ASSR during each condi-tion studied. Estimates of SNR were

obtained offline by comparing the amplitudeof the spectral peak at 39 Hz to the ampli-tudes of the spectral peaks at 15 adjacentfrequencies. These ratios were convertedinto decibel (dB) values and were evaluatedstatistically with the F test. The ASSR wasconsidered to be present for a given condi-tion if its observed dB value exceeded thecritical dB value for F of 6.42 for 2 and 30degrees of freedom at an alpha level of 0.01(Dobie and Wilson, 1996). In order to fur-ther evaluate the efficacy of this procedure,control waveforms were recorded in 16 sub-jects. The fitting of the transducer in the earcanal, the positioning of the electrodes, andthe recording parameters in these controlconditions were identical to the other exper-imental conditions of the study, with theexception that the transducers wereunplugged from their connections. Spectralanalyses were performed offline on thesecontrol waveforms, and F test statisticalcomparisons were made to determine ifASSRs would be detected.

Data Analysis

The amplitude (in nanovolts) of thedetected 40 Hz ASSRs acquired in initialand replicated recordings were averaged percondition in each subject, and comprised thedatabase for the entire set of experiments.The Statistical Package for the SocialSciences (SPSS) version 14.0 software wasutilized to perform statistical analysis ofthis data. Statistical significance testingwas conducted at an alpha level of 0.05. Thedistribution of the data acquired from the 16subjects in Experiment 1 was examinedwith the one-sample Kolmogorov-Smirnovtest, and was found to be normally distrib-uted. A one way repeated-measures analysisof variance (ANOVA) was conducted on thisdata to determine if there were statisticallysignificant differences in 40 Hz ASSR meanamplitudes between the probe condition andthe conditions when the probe was pairedwith the interfering tones.

If a significant difference was detected,follow-up tests utilizing pairwise compar-isons were performed. Because of the smallnumber of subjects successfully completingall of the conditions of Experiments 2 and 3,no assumptions were made concerning thedistribution of this data. Therefore, non-parametric statistical analyses were per-


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formed. Comparisons between conditions inthese experiments were made with theFriedman test. Significant findings on thistest were further investigated withWilcoxon signed-rank tests. Additionally, inorder to make comparisons with previousstudies, the percentage change across condi-tions was calculated for each subject bydividing response amplitudes in the experi-mental conditions by the response ampli-tudes in the baseline conditions.

RESULTS

Detection of 40 Hz ASSRs

The F test procedure revealed that 40 HzASSRs acquired in baseline conditions with1000 or 500 Hz probe tones exceeded the cri-terion SNR value (in dB) in all subjects.Evaluation of the control waveformsrevealed that none achieved this criterionvalue, suggesting that this methodologywas effective in detecting the presence ofelectrophysiological responses. ASSRs werenot detected in four subjects when the 1000Hz probe was paired with the 1500 Hz inter-

fering tone during Experiment 1. Similarly,the criterion was not met in two subjects fortwo different conditions when the probe tonewas paired dichotically with the interferencetone in Experiment 3. In these cases, theamplitude of the spectral component at themodulation frequency was replaced with theaverage value of the noise obtained from thesurrounding 15 spectral peaks.

Experiment 1

Representative 40 Hz ASSR waveformsand spectra acquired from one subject forselected probe-interfering tone combinationsare displayed in Figure 1. Mean 40 Hz ASSRamplitudes are plotted for the probe condi-tion and as a function of interfering tone fre-quency in Figure 2. Cursory examination ofthe raw data indicated that 40 Hz ASSRamplitudes were reduced the most when theUM interfering tone was higher in frequencyand approximately within an octave of theAM probe tone. These initial observationswere evaluated statistically with the one-wayrepeated-measures ANOVA. The within-subjects factor was Condition (five levels),


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Figure 1. Representative 40 Hz ASSR waveforms and spectra recorded from one subject during Experiment 1. ASSRwaveforms are depicted in the left panels, and spectral analyses of the waveforms are depicted in the right panels.The arrows indicate the spectral peak corresponding to the modulation frequency near 40 Hz. The ASSR waveformswere acquired in the following stimulus conditions: (a) with the 1000 Hz probe tone alone, (b) with the 1000 Hz probeand 500 Hz interfering tones, (c) with the 1000 Hz probe and 1500 Hz interfering tones, (d) with the 1000 Hz probeand 2000 Hz interfering tones, (e) with the 1000 Hz probe and 4000 Hz interfering tones.

and the dependent variable was 40 Hz ASSRamplitude in nanovolts. Mauchly’s test ofsphericity was significant (p < 0.001), neces-sitating a Greenhouse-Geisser adjustment ofthe degrees of freedom during statistical test-ing. A significant overall main effect forCondition was detected (F 2, 31 = 5.20, p =0.011). Further investigation of the signifi-cant main effect with Bonferroni-correctedmultiple pairwise comparisons revealed thatpairing of the 1000 Hz probe tone with UMinterfering tones at either 1500 Hz or 2000Hz produced significantly lower (p < 0.05) 40Hz ASSR amplitudes compared to when the1000 Hz probe tone was presented alone. Nosignificant differences (p > 0.05) in 40 HzASSR amplitudes were observed between thebaseline 1000 Hz probe condition and condi-

tions when the 1000 Hz probe was pairedwith 500 Hz and 4000 Hz UM interferingtones. Mean 40 Hz ASSR amplitudes andamplitude percentages across interferingtone conditions are listed in Table 4.

Experiment 2

Individual and mean 40 Hz ASSR ampli-tudes are plotted for the probe condition andas a function of interfering tone modulationdepth in Figures 3 and 4. Trends in thesedata indicated that 40 Hz ASSR amplitudeswere reduced when the interfering tone wasan octave above the probe tone, and when theinterfering tone was modulated at a lowerdepth than the probe tone. The Friedmanomnibus test conducted on 40 Hz ASSR


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Figure 2. Mean 40 Hz ASSR amplitudes are plotted for the probe condition and interfering conditions as a func-tion of the carrier frequency of the interfering tone. The carrier frequency of the probe was 1000 Hz. The probecondition is depicted with the open triangle. Data points depicted with the filled triangles represent conditionswhen the probe was monotically paired with the UM interfering tones. Error bars represent ± one standarderror of the mean. N = 16.

amplitudes across conditions was significant(p < 0.001). Post-hoc pairwise comparisonsconducted with Wilcoxon signed ranks testsrevealed that compared with the baselineprobe conditions, 40 Hz ASSR amplitudes

were significantly lower (p < 0.05) for condi-tions when the 500 Hz probe tone was pairedwith the 1000 Hz interfering tone modulatedat depths of 12.5% and 25%, but no signifi-cant difference between conditions occurred


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Figure 3. Individual 40 Hz ASSR amplitudes for the six subjects (S1–S6) are plotted for the probe conditionsand interfering conditions as a function of the modulation depth of the AM interfering tone. The probes weremodulated at a modulation depth of 100%. The 500 Hz probe condition is represented by the inverted filled tri-angle, and the 1000 Hz probe condition is represented by the inverted open triangle. Data points depicted withthe filled triangles represent conditions when the 500 Hz probe was paired with the 1000 Hz interfering toneat each of the modulation depths. Data points represented by the open triangles represent conditions when the1000 Hz probe was paired with the 500 Hz interfering tone at each of the modulation depths.

when the 1000 Hz interfering tone was mod-ulated at a depth of 50%. Pairing of the 500Hz probe tone with the 1000 Hz interferingtone when both were at a modulation depthof 100% produced significantly larger (p <0.05) 40 Hz ASSRs compared with the base-line probe condition. No significant differ-ences (p > 0.05) between the baseline 1000Hz probe condition and conditions when the

1000 Hz probe was paired with the 500 Hzinterference tone modulated at any of theexamined modulation depths were observed.In addition, 40 Hz ASSRs elicited with 500Hz probes were not significantly different(p > 0.05) in amplitude from those acquiredwith 1000 Hz probes. Median 40 Hz ASSRamplitudes across the modulation depth con-ditions studied are listed in Table 5.


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Figure 4. Mean 40 Hz ASSR amplitudes are plotted for the probe conditions and interfering conditions as a func-tion of the modulation depth of the AM interfering tone. The probes were modulated at a modulation depth of100%. The 500 Hz probe condition is represented by the inverted filled triangle, and the 1000 Hz probe conditionis represented by the inverted open triangle. Data points depicted with the filled triangles represent conditionswhen the 500 Hz probe was paired with the 1000 Hz interfering tone at each of the modulation depths. Data pointsrepresented by the open triangles represent conditions when the 1000 Hz probe was paired with the 500 Hz inter-fering tone at each of the modulation depths. Error bars represent ± one standard error of the mean.

Experiment 3

Individual and mean 40 Hz ASSR ampli-tudes are plotted for the probe condition andas a function of interfering tone modulationrate in Figures 5 and 6. Examination of theraw data revealed that monotic and dichot-

ic interference tones produced similaramounts of amplitude suppression when theprobe and interfering tones were modulatedat different rates. Friedman omnibus testsindicated that significant differences existedbetween 40 Hz ASSR amplitudes in the probecondition compared to when the probe was


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Figure 5. Individual 40 Hz ASSR amplitudes for the five subjects (S1–S5) are plotted for the probe conditionsand interfering conditions as a function of the modulation frequency of the AM interfering tone. The probe car-rier frequency was 1000 Hz, and the modulation frequency was 40 Hz. The carrier frequency of the interferingtones was 2000 Hz. The probe condition is represented by the filled inverted triangle. Data points depicted withthe filled triangles represent conditions when the probe carrier was monotically paired with the interfering car-rier at each of the modulation frequencies. Data points depicted with the open triangles represent conditions whenthe probe carrier was paired dichotically with the interfering carrier at each of the modulation frequencies.

paired with the monotic (p = 0.004 ) or dichot-ic (p = 0.002) interference tones. Post-hoc test-ing completed with the Wilcoxon signed-ranktests revealed 40 Hz ASSR amplitudes weresignificantly reduced (p < 0.05) in conditionswhen the probe was paired monotically withinterfering tones modulated at 30, 50, 60, 70,and 80 Hz, and when the probe was paireddichotically with interfering tones modulated

at 30, 60, 70, and 80 Hz. No differences in 40Hz ASSR amplitudes were observed betweenthe probe conditions and conditions when theprobe and interfering tones were modulatedat a common rate. Median 40 Hz ASSR ampli-tudes and amplitude percentages across themodulation frequency conditions are listed inTable 6.


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Figure 6. Mean 40 Hz ASSR amplitudes are plotted for the probe condition and interfering conditions as a func-tion of the modulation frequency of the AM interfering tone. The probe carrier frequency was 1000 Hz, and themodulation frequency was 40 Hz. The carrier frequency of the interfering tones was 2000 Hz. The probe con-dition is represented by the filled inverted triangle. Data points depicted with the filled triangles represent con-ditions when the probe carrier was monotically paired with the interfering carrier at each of the modulationfrequencies. Data points depicted with the open triangles represent conditions when the probe carrier was paireddichotically with the interfering carrier at each of the modulation frequencies. Error bars represent ± one stan-dard error of the mean.

DISCUSSION

This investigation examined the effects ofpresenting UM and AM interfering tones

on 40 Hz ASSRs acquired in normal-hearingadults. Comparisons were made between 40Hz ASSRs acquired with a probe tone andASSRs acquired with tone pairs (probe plusinterfering tone conditions). The presence ofan interfering tone influenced the generationof 40 Hz ASSRs for paired stimuli presentedat moderate levels. The findings of this inves-tigation confirmed and extended the resultsof previous ASSR investigations and provid-ed information concerning frequency speci-ficity and the dichotic characteristics of 40 HzASSRs.

Probe and Interfering CarrierInteractions

The results of Experiment 1 revealed that40 Hz ASSRs acquired with 70 dB SPL stim-uli were reduced in amplitude when the fre-quency of the UM interfering tones was high-er than that of the 1000 Hz probe tone.However, the amplitude reduction dependedon the proximity of the AM probe and UMinterfering carriers. Compared to the probecondition, significant amplitude reductionswere seen for paired conditions when the UMinterfering tone was approximately one-halfto one octave above the probe tone. Pairing ofthe 1000 Hz probe tone with UM interferingtones at 1500 Hz and 2000 Hz resulted inamplitude decreases of 32% and 19%, respec-tively. No significant decreases in amplitudewere seen when the UM interfering tone waspresented approximately either two octavesabove or an octave below the probe tone.Dolphin and Mountain (1993) studied enve-lope-following responses recorded with scalpelectrodes in Mongolian gerbils and reportedthat UM interfering tones presented at 10 dBabove a 75 dB SPL probe tone caused maxi-mum reductions in the response within anarrow frequency region above the carrierfrequency of the AM probe. Regions ofreduced response amplitude associated withpresentation of the UM interfering toneextended 1–2 octaves above and one-thirdoctave below the probe tone. These authorsspeculated that when the UM interferingtone is within the immediate vicinity of theAM probe carrier, neural discharges becomesynchronized to the beat frequency between

the probe and interfering tones, disruptingphase-locked responses at the modulation fre-quency of the probe. However, Bernstein(1994) presented evidence in opposition tothis theory, indicating that the addition of theUM interference tone distorted the AM stim-ulus waveform and reduced the amplitude ofthe component at the modulation frequencyto an extent that could sufficiently describemany of the findings of the Dolphin andMountain study without invoking an expla-nation based on disruption of neural syn-chrony. The model proposed by Bernstein didnot account for amplitude reductions provid-ed by more remote, higher-frequency UMinterfering tones that may result from physi-ological interactions between the two carriers.Therefore, the results of the present studymay be explained by interactions between theAM probe and UM interfering tones that dis-tort the stimulus waveform, disrupt neuralsynchrony, or some combination of these fac-tors. In addition, the interference effects seenin the present study were limited to UM car-rier frequencies an octave above the probe fre-quency. Griffiths and Chambers (1991) uti-lized high-pass noise masking techniqueswhile recording 50 Hz amplitude modulation-following responses in normal-hearing adultsand reported that the responses were gener-ated in a narrow frequency region extendingto an octave above the carrier, findings inagreement with the results of the presentstudy. These results suggest that the 40 HzASSRs recorded under the conditions of thepresent study exhibited reasonable frequencyspecificity and were derived from neuralactivity near to the characteristic place on thebasilar membrane corresponding to the probefrequency and not from locations considerablymore apical from this location. The frequencyspecificity of 40 Hz ASSRs demonstrated inthe present study may contribute to the find-ings of previous investigations that indicatedgood agreement between 40 Hz ASSR thresh-olds and behavioral thresholds in normal-hearing adults and adults with sensorineuralhearing loss (Petitot et al, 2005; Van Maanenand Stapells, 2005; van der Reijden et al,2006).

Interference Asymmetry andModulation Depth

The results of Experiment 2 indicated thatcompared with the baseline probe condition,


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reductions in 40 Hz ASSR amplitudesoccurred when the probe tone was pairedwith an interfering tone an octave higher infrequency. This finding confirmed the resultsof Experiment 1 in a separate group of sub-jects. Additionally, reductions in 40 Hz ASSRamplitudes occurred in certain conditionswhen the interfering tone was modulated ata lower modulation depth compared to theprobe tone. No differences in 40 Hz ASSRamplitudes were observed between the base-line condition and conditions when the probewas paired with an interfering tone an octavelower in frequency. These results were con-sistent with the findings of previous physio-logical investigations conducted in humans.John et al (1998) reported that 40 Hz ASSRsrecorded with a 1000 Hz probe tone at 60 dBSPL were smaller in the presence of a 2000Hz carrier tone and larger in the presence ofa 500 Hz carrier tone, compared to a baselineprobe condition. A similar frequency patternemerged in that study for faster rates ofamplitude modulation from 77–105 Hz.However, the interference effects wererestricted to a range less than an octaveabove that of the probe tone for high-rateASSRs. In addition, the probe and additionalcarriers were modulated at slightly differentrates in the John et al (1998) study, whereasthe probe and interfering tones inExperiment 2 of the present study were mod-ulated at a common rate. Ross et al (2003)utilized magnetoencephalography to studythe frequency specificity of the 40 Hz ASSRin humans and found that magnetic fieldselicited by 80 dB SPL 1000 Hz stimuli weresuppressed more when the AM interferingtone was one octave above, rather than oneoctave below, that of the AM probe tone.Greater amounts of magnetic field suppres-sion were also observed for low-frequencyprobe tones compared to high-frequencyprobe tones. The asymmetry of interferenceeffects exhibited in the present study and inprevious studies with higher-frequency inter-ference tones producing more reduction in 40Hz ASSR amplitude than lower-frequencyinterference tones may originate from carrierinteractions within the cochlea. Bacon andMoore (1993) calculated excitation patternsfor a 2000 Hz carrier modulated at a depthnear the modulation detection threshold.They found that when this AM carrier waspresented at 60 dB SPL, their model indicat-ed a spread of excitation to higher frequen-

cies nearly an octave above the carrier. Thesimultaneous addition of a 3200 Hz UMmasking tone at 60 dB SPL to the modelseverely limited the spread of excitationinduced by the AM carrier. These findingsare consistent with the results of Experiment1 of the present study, indicating that the 40Hz ASSR originates from neural activity upto an octave above the probe frequency forcarriers modulated at a depth of 100%. Theaddition of the 1000 Hz interfering tone mod-ulated at depths between 12.5 and 25% to the500 Hz probe tone may have limited thespread of probe excitation at higher frequen-cies, resulting in a reduction of 40 Hz ASSRamplitude. No differences in 40 Hz ASSRamplitudes between the baseline conditionand when the 500 Hz probe was paired withthe 1000 Hz interfering tone modulated at adepth of 50% were observed, but the ampli-tude of the response was enhanced by theaddition of the 1000 Hz interference tonemodulated at a depth of 100%. The ampli-tude of the ASSR in humans is known toincrease linearly with log modulation depthfor modulation depths from 0 to 100% (Reeset al, 1986). This suggests that phase-lockedneural discharges are more synchronized tothe temporal envelope of the stimulus at thehighest modulation depths.

The addition of the interfering tone to theprobe tone when both are modulated at acommon rate and 100% modulation deptheffectively increases the stimulus bandwidth,inducing greater phase-locked neural dis-charges at the modulation frequency.Stürzebecher et al (2001) reported greaterresponse SNRs for a multicarrier stimulusmodulated at a common rate and depth com-pared with responses evoked with a singlecarrier for high-rate ASSRs, suggesting thatthe response amplitude was enhanced in themulticarrier condition. Similar results werefound for 40 Hz ASSRs in the present studywhen the 500 Hz probe and 1000 Hz inter-fering carriers were modulated at a commonrate and each at a modulation depth of 100%.These findings indicate that modulation ofmultiple carriers at a common rate and mod-ulation depth is effective in evoking robust 40Hz ASSRs. The results of Experiment 2 alsosuggest that for 40 Hz ASSRs, a trade-offexists between frequency specificity andresponse SNR. In order to evoke responseswith large amplitudes and high SNRs, tonesneed to be modulated at high depths, reduc-


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ing the frequency specificity of the stimuli.Modulating tones at lower depths increasesstimulus frequency specificity but lowers theSNR due to the small response amplitudesevoked by these stimuli. These findings haveclinical implications, suggesting that differ-ent stimuli are required to maximize theresponse SNR and frequency specificity of 40Hz ASSRs in normal-hearing adults.

Probe and Interfering EnvelopeInteractions

The results of Experiment 3 revealed that40 Hz ASSR amplitudes for the 1000 Hzprobe tone were essentially unchanged withcommon-rate modulation of the AM probeand interfering tone in the monotic anddichotic conditions. However, when theinterfering tone was modulated at ratesabove or below that of the probe tone,greater amplitude reductions were seen inboth monotic and dichotic conditions. Thefindings of the present study were consis-tent with the results of previous investiga-tions and provided new information byextending the range of modulation frequen-cies examined and by making comparisonsbetween conditions when the interferingtones were presented monotically anddichotically. Compared with a baselineprobe condition, two-carrier conditions withmodulation frequency separations of 10–40Hz across the 30–80 Hz range exhibitedreductions in 40 Hz ASSR amplitudes of23–35% in the monotic conditions and17–34% in the dichotic conditions. Thesefindings are comparable to earlier studiesemploying multiple carriers modulated atfrequencies separated by smaller intervals.John et al (1998) found that ASSRs elicitedwith tones modulated from 30–50 Hz inapproximately 4 Hz intervals were reducedby 34% when four carriers were presentedmonotically and 56% when eight carrierswere presented dichotically compared to abaseline condition with a single carriermodulated near 40 Hz. A recent studyessentially replicated these results byreporting a 33% decrease in 40 Hz ASSRamplitude in a four-carrier monotic condi-tion compared to a baseline condition with asingle carrier (Van Maanen and Stapells,2005).

In contrast, Lins and Picton (1995) foundthat the amplitude of the ASSR recorded

with monotic presentation of four AM carri-ers modulated in approximately 8 Hz inter-vals from 81–105 Hz was not significantly dif-ferent than the amplitude of the ASSR evokedby each stimulus presented alone. John et al(1998) obtained baseline ASSR recordingswith a 1000 Hz carrier modulated near 85 Hzand compared these recordings to conditionswhen the 1000 Hz carrier was paired with a2000 Hz carrier modulated at frequenciesseparated from the baseline modulation fre-quency by up to 7.9 Hz. They found that theamplitude of the high-rate ASSR wasunchanged even for differences in modulationfrequency between carriers as little as 1.3 Hz.These findings also agreed with Lins andPicton (1995) high-rate ASSR results, whereup to eight carriers modulated at frequenciesseparated by approximately 8 Hz could bepresented dichotically without inducing a sig-nificant reduction in response amplitude com-pared with the baseline condition.

The results of the present study and pre-vious investigations indicates that the neu-ral encoding of multiple AM stimulusenvelopes modulated at lower rates near 40Hz is more susceptible to interference thanfor AM stimuli modulated at rates above 70Hz. Furthermore, a similar pattern of inter-ference between monotic and dichotic condi-tions seen in the present study suggeststhat the interference effect is mediatedwithin the central auditory nervous systemat a hierarchical level at or beyond the supe-rior olivary nuclei. Evidence from previouselectrophysiological research conductedwith surface electrodes in humans suggeststhat 40 Hz ASSRs are generated by a diffusenetwork of sources from the brainstem tothe cortex (Herdman et al, 2002b; Reyes etal, 2005). Neural phase locking to the enve-lope of AM stimuli declines from the audito-ry nerve to the auditory cortex, with higherrates of modulation more efficiently encodedby caudal structures and lower rates ofmodulation encoded by more rostral struc-tures (Joris et al, 2004). The findings ofExperiment 3 of the present study may beindicative of multiple generators contribut-ing to the scalp-recorded composite 40 HzASSR in normal-hearing adults. From aclinical perspective, this suggests thatunlike for ASSRs evoked by stimuli modu-lated above 70 Hz, multiple carriers modu-lated at different rates may not be the mostefficient stimuli for 40 Hz ASSRs.


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Limitations of the Study

This study compared 40 Hz ASSRs elicitedwith probe tones at 500 or 1000 Hz in base-line conditions to conditions when theseprobes were paired with additional interfer-ing tones. Therefore, the results seen for theprobes in the 500–1000 Hz region may notgeneralize to probes at higher frequencies.The findings of the study are limited toASSRs elicited with two carriers and do notaddress the effects of more than two carrierson the 40 Hz ASSR. In addition, the stimuluslevel was confined to 70 dB SPL. This levelwas selected in an effort to induce potentialstimulus interactions, but these effects maynot be exhibited at lower presentation levels.John et al (1998) presented evidence thatstimulus interactions for multiple carrierspresented at 35 dB SPL were essentially non-existent compared to presentation levels at 75dB SPL where amplitude reductions were evi-dent for ASSRs evoked by tones modulated athigh rates. However, these results probablyreflect increased carrier interactions at high-er intensity levels. Since 40 Hz ASSRs appearto be more susceptible to stimulus envelopeinteractions, the effects of these interactionsat lower presentation levels are unclear atthis time. Another limitation of this studyinvolves the recording apparatus. While thesingle-channel recordings utilized in thisinvestigation probably are comparable withclinical protocols, the use of multichannelelectrode arrays would have elucidated someof the effects seen in the study with greaterprecision. For example, source localizationstudies recorded with multiple channels mayhave provided information concerning the dif-ferential effects of interfering tone modula-tion rate for cortical and/or subcortical gener-ators of the 40 Hz ASSR. In addition, thisstudy utilized a relatively small sample ofyoung normal-hearing adults. While trends inthe individual data exhibited similaritieswithin experimental conditions, it is unclearif the results obtained will apply to a larger,more diverse population. A recent study hasdemonstrated that neural phase locking toAM stimuli differs between younger and olderadults, with younger subjects exhibitinggreater numbers of phase-locked responsesparticularly for low-frequency carriers (Leigh-Paffenroth and Fowler, 2006). Therefore, theeffects of multiple carriers on ASSRs obtainedin elderly individuals may be different than

for younger individuals, although the effectmay be more pronounced for stimuli modulat-ed at rates higher than 40 Hz. Recordings ofmultiple 40 Hz ASSRs acquired in individualswith sensorineural hearing loss were notexplored in the present study, and stimulusinteractions in this population may differ con-siderably compared with results seen in nor-mal-hearing individuals. Future investiga-tions of multiple 40 Hz ASSRs should be con-ducted in these populations.

Conclusions

For conditions examined in the presentstudy:1. Maximal reduction of the 40 Hz ASSR

amplitude occurs when the interferingtone is one-half to one octave above theprobe tone. This indicates reasonable fre-quency specificity of the 40 Hz ASSR tothe probe with minimal apical spread ofexcitation along the cochlea. This impliesthat 40 Hz ASSRs should be accurate inestimating hearing thresholds.

2. Maximal reduction of 40 Hz ASSR ampli-tudes occurs when the interfering tonewas modulated at a lower depth than theprobe tone. This indicates that spread ofprobe excitation to higher frequenciesmay be limited, and therefore theresponse is more frequency specific,although the SNR is poorer.

3. Enhancement of the 40 Hz ASSR ampli-tude occurs when the probe and interfer-ing tones are modulated at a commondepth (100%). This reflects increased neu-ral synchronization of discharges to themodulation frequency, giving rise torobust 40 Hz ASSRs with better SNR butpoorer frequency specificity. Thus, theremay need to be a trade-off/compromisebetween the most robust and most fre-quency-specific 40 Hz ASSRs.

4. The smallest interference effect on the 40Hz ASSR amplitude occurred when theinterference tone and probe tone werepresented either monotically or dichoti-cally and were modulated at a commonrate. This indicates that unlike with the80 Hz ASSR, there are significant stimu-lus envelope interactions when the 40 HzASSR is evoked by tones modulated atdifferent rates. This implies that a multi-carrier stimulus may not be best for evok-ing 40 Hz ASSRs.


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