Mismatch negativity in children and adults,and effects of an attended task

HILARY GOMES,a,b SOPHIE MOLHOLM,a,c WALTER RITTER,c DIANE KURTZBERG,b,c

NELSON COWAN,d and HERBERT G. VAUGHAN, JR.b,c,e

aDepartment of Psychology, City College of the City University of New York, New York, USADepartments ofbNeurology,cNeuroscience, andePediatrics, Albert Einstein College of Medicine, Bronx, New York, USAdDepartment of Psychology, University of Missouri, Columbia, USA

Abstract

Attention has been shown to modulate the amplitude of the mismatch negativity~MMN ! elicited by a small deviationin auditory stimuli in adults. The present study examined the effects of attention and deviant size on MMN amplitudein children. Children and adults were presented with sequences of tones containing standards~1000 Hz! and threedeviants varying in degree of deviance from the standard~1050, 1200, and 1500 Hz!. Tones were presented in three con-ditions:~1! while participants ignored them;~2! while participants listened to them and responded to all three deviants;and~3! while participants again ignored them. We found that the MMNs elicited by the hard deviant~1050 Hz! werelarger when the children were actively discriminating the stimuli than when they were ignoring them. However, theMMNs elicited by the easy and medium deviants~1500 and 1200 Hz, respectively! in the children and by all threedeviants in the adults were not affected by attention.

Descriptors: Mismatch negativity, Attention, Children, Development, Auditory event-related potentials

Mismatch negativity~MMN ! is thought to reflect an automaticneuronal response to a change in auditory stimuli and has beenstudied extensively as an index of processes related to auditorydiscrimination and auditory sensory memory in adults~Näätänen,1992; Näätänen & Alho, 1997; Ritter, Deacon, Gomes, Javitt, &Vaughan, 1995; Winkler, Schröger, & Cowan, in press!. Recently,investigators have also begun to use the MMN to explore similarprocesses in children. These studies have found that the MMN canbe elicited reliably in children and that the characteristics of MMNselicited from children are similar, although often somewhat longerin latency, to those elicited from adults~e.g., Gomes et al., 1999;Korpilahti & Lang, 1994; Kraus et al., 1996; Kurtzberg, Vaughan,Kreuzer, & Fliegler, 1995!. However, because developmentalchanges in auditory discrimination and memory have been dem-onstrated using both behavioral~Keller & Cowan, 1994! and event-related potential~ERP! techniques~Gomes et al., 1999!, it is riskyto assume that factors modulating the MMN affect children andadults in the same manner.

MMN is most commonly elicited by a deviant auditory stim-ulus in a train of repetitive, homogeneous stimuli~termedstan-dards!. A comparison of the ERPs elicited by the standards and

deviants reveals a potential that is larger for the deviant tones, andis negative at the midline and often positive at the mastoids whenthe nose is used as the reference. The peak latency of the MMN inadults is generally between 100 and 250 ms. MMN has beenelicited by changes in a variety of acoustic features, such as in-tensity, frequency, duration, and perceived location, and by changesin auditory patterns~see Näätänen, 1992, for a review!, but gen-erally is elicited only by acoustic differences that the subject canalso discriminate behaviorally~e.g., Kraus et al, 1995; Näätänen,Schröger, Karakas, Tervaniemi, & Paavilainen, 1993; Sams,Paavilainen, Alho, & Näätänen, 1985!. Furthermore, the amplitudeand the latency of the MMN are usually related to the size of thedeviance. When the separation between the standard and the de-viant is great, the associated MMN is large and early, and when theseparation is minimal, the MMN is small and late~Tiitinen, May,Reinikainen, & Näätänen, 1994!.

MMN is generally assumed to be preattentive because multiplestudies have demonstrated that robust MMNs can be elicited whenadult and child participants are engaged in some other activity~e.g., reading a book, watching a video, monitoring another stim-ulus set! and not actively attending to the stimuli~Näätänen, 1992,for a review!. Furthermore, in a number of studies in adults, activemanipulation of attention has failed to affect the amplitude of theMMN ~Alho, Sams, Paavilainen, Reinikainen, & Näätänen, 1989;Alho, Woods, & Algazi, 1994; Novak, Ritter, Vaughan, & Wiz-nitzer, 1990; Paavilainen, Tiitinen, Alho, & Näätänen, 1993; Ritteret al., 1992!. Nonetheless, focus of attention in selective attentionparadigms has been shown to modulate the amplitude of the MMNelicited by a small deviance in adults. When attention is strongly

This work was supported by National Institutes of Health GrantsHD01799, NS30029, DC00223, and HD21338.

We thank Jacqueline Lobosco for her help preparing the data for themanuscript.

Address reprint requests to: Hilary Gomes, Kennedy Center Room 828,Albert Einstein College of Medicine, 1410 Pelham Parkway South, Bronx,NY 10461, USA. E-mail: hilary@balrog.aecom.yu.edu.

Psychophysiology, 37~2000!, 807–816. Cambridge University Press. Printed in the USA.Copyright © 2000 Society for Psychophysiological Research

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focused on a difficult task, the MMNs elicited by a small deviantdelivered to the unattended ear are smaller than the MMNs elicitedby the same deviant when it is in the attended channel, whether ornot it is the target to be identified~Alho, Woods, Algazi, & Näätänen,1992; Näätänen, Paavilainen, Tiitinen, Jiang, & Alho, 1993; Trejo,Ryan-Jones, & Kramer, 1995; Woldorff, Hackley, & Hillyard, 1991;Woldorff, Hillyard, Gallen, Hampson, & Bloom, 1998; Woods,Alho, & Algazi, 1992!. MMNs elicited by deviants that are easilydiscriminated usually have not been found to be sensitive to at-tentional modulations~Alho et al, 1992; Woods et al., 1992!.

Although there may be some effect of attention on the ampli-tude of the MMN in selective attention studies, an active attentiontask is not ordinarily required to elicit the MMN in adults~Näätänen& Alho, 1997!. Consequently, MMN has been proposed as a toolfor exploring developmental changes in auditory discriminationand memory in normal children, as well as those children withauditory processing deficits, without the potential confound ofindividual differences in attention and task strategies inherent inbehavioral studies~Cheour et al, 1997; Gomes et al., 1999; Krauset al., 1996!. Studies of MMN in children have generally foundeffects that parallel those described in adults~e.g., Ceponiene,Cheour, & Näätänen, 1998; Gomes et al., 1999; Korpilahti & Lang,1994; Kraus et al., 1996; Kurtzberg et al., 1995!; however, signif-icant developmental differences have been found in MMNs elic-ited by deviants at the beginning of trains of tones separated bydiffering time periods~Gomes et al., 1999!, and pilot data from ourlaboratory suggest that larger deviants are required to elicit MMNsin children than in adults. Therefore, although MMN may holdpotential as a tool for investigating auditory processes associatedwith discrimination and memory in children, it cannot be assumedto be identical to adult MMNs in all cases.

It is particularly important to consider attention effects beforeembarking on developmental or clinical MMN studies becauseproblems may arise in assuming that all groups ignore stimuliequivalently when they are engaged in some other task, such aswatching a movie or reading a book. If attention affects the MMNin children, group differences in the amplitude of the MMN mightbe attributable to differences in the amount of attention directedtoward the ignored stimuli during the experiment. Researchersconducting studies with adult subjects have not had to worry aboutvariable attention to the ignored stimuli because the effects ofattention have been shown to be minimal in most instances.

The present study was designed to examine the effects of at-tention and active discrimination on the amplitude of MMN inchildren and to extend the findings on the effects of attention onMMNs elicited from adults. Specifically, in children, does attend-ing to the tones result in larger MMNs than when the tones areignored, and does the size of the deviance modulate the effect?Based on the findings in adults from selective attention tasks, wehypothesized that as the discrimination became more difficult, theeffects of attention would become more pronounced. Further, doadults and children show attention effects for the same deviants, orare there developmental changes in the size of the deviance asso-ciated with attention effects? To address these questions, standardtones ~1000 Hz! and three deviant tones varying in degree offrequency deviance from the standard~1050, 1200, and 1500 Hz!were presented randomly in the same run. Presenting all of thedeviants in the same run ensured that changes in “state” or moti-vation would not affect the deviants differentially. Further, thisarrangement allowed for the collection of data more quickly, re-ducing the length of the paradigm. ERPs were recorded in threeconditions:~1! participants ignored the tones and watched a video

or read a book~“first ignore condition”!; ~2! participants listenedto the stimuli and pushed a button whenever they heard any of thethree deviants~“attend condition”!; and ~3! participants again ig-nored the stimuli~“second ignore condition”!. An ignore conditionwas always presented first to elicit a MMN free from the potentiallearning effects of the attention condition~Kraus et al., 1995;Näätänen, Schröger, et al., 1993; Tremblay, Kraus, Carrell, & Mc-Gee, 1997!. The second ignore condition was presented to ensurethat any increase in MMN amplitude during the attend conditionwas not attributable to exposure to the stimuli during the first ig-nore condition. The attention task was expected to be moderatelydifficult for the children, given the inclusion of three deviants in thesame stimulus stream and the proximity of the hard deviant to thestandard. The questions of attention effects on MMN were addressedby comparing the ignore and the attend conditions.

Method

ParticipantsParticipants were 10 adults~5 men, 5 women! and 14 children~10boys, 4 girls!. The adults ranged in age from 21 to 47 years of age~M 5 30.9 years,SD5 8.6!. The children ranged in age from 8 to12 years of age~M 5 9.7 years,SD5 1.2!. All of the children werein the age-appropriate grade in school. Three of the children andone of the adults were left handed. All participants had normalhearing according to self- or parent report and all passed a hearingscreen. Two additional children were excluded: one because hecomplained of a headache and wanted to discontinue testing andthe other because of significant movement artifact. Some of thechildren and many of the adults had participated in other ERPexperiments in our laboratories. The children were paid $50 for theentire session and the adults $10 per hour for participating in thestudy.

Prior to testing, all children signed assent forms that were readand explained to them in the presence of their guardian. All guard-ians and adult subjects signed consent forms.

StimuliThe stimuli were 1000-Hz~standards!, 1050-Hz ~hard deviant!,1200-Hz~medium deviant!, and 1500-Hz~easy deviant! tones. Thestimuli were 100 ms in duration~10 ms rise and fall! and werepresented binaurally through insert earphones at 80 dB SPL. Allstimuli were presented in the same run with an 850-ms stimulusonset asynchrony~SOA!. Stimulus order was pseudorandomizedwith the standard occurring 70% of the time and each of thedeviants occurring 10% of the time with the restriction that devi-ants had to be separated by at least one standard.

ProcedureThree conditions with different assigned tasks were presented. Inthe first, participants sat quietly and ignored the stimuli, eitherwatching videos without sound or reading a book of their choosing~“first ignore condition”!. Most of the children elected to watchvideos whereas most of the adults chose to read books. In thesecond condition, they attended to the stimuli and were instructedto press a response key whenever they heard a tone that differedfrom the standard~“attend condition”!. To motivate the childrenand keep them focused on this task, they were given one M&Mchocolate candy for every five correct responses. The M&Ms weregiven at the end of the run so as not to distract the child duringthe task. In the third condition, participants again ignored the

808 H. Gomes et al.

stimuli, either watching a movie or reading a book~“second ignorecondition”!.

Stimuli were presented in runs of approximately 7 min: 500stimuli per run. Five runs were presented for each condition for atotal of 250 possible deviants of each type in each condition.

An adult sat with each child during the experiment to monitorattention and minimize movement artifact. Short and long breakswere given as required. During short breaks~3–5 min!, partici-pants remained in their chair but were allowed to stretch and shiftpositions. During longer breaks~10–20 min!, participants weredisconnected from the recording apparatus and allowed to walkaround. Children required more frequent and longer breaks of bothtypes than the adults. Total experiment time was 3–4 hr, includingapproximately 1 hr of electrode application, 2–2.5 hr of testingwith breaks, and 0.5 hr of electrode removal and debriefing.

The protocol for the study was reviewed and approved by theethics committees at the Albert Einstein College of Medicine andthe City College of New York before any subjects were tested.

Electrode Placement and Recording TechniquesThe recordings were obtained using a 31-channel electrode capwhich incorporated a subset of the International 10-10 system~new modified combinatorial nomenclature; American Electro-encephalographic Society, 1990!: Fpz, Fz, Cz, Pz, Oz, FP1, FP2,F7, F8, F3, F4, FC5, FC6, FC1, FC2, T7, T8, C3, C4, CP5, CP6,CP1, CP2, P7, P8, P3, P4, O1, O2, LM~left mastoid!, and RM~right mastoid!. Vertical eye movements were recorded with abipolar configuration of FP2 and an electrode below the right eye.Horizontal eye movements were monitored at F7 and F8. A noseelectrode served as the reference and an electrode at PO9 served asthe ground. All impedances were maintained below 5 kV. Ampli-fiers with a gain of 30,000 and filter settings of 0.05–100 Hz wereused. The continuous electroencephalogram for all channels wasmonitored during the recordings so that problems with electrodescould be identified and corrected and feedback about excessivemotor movement could be given. The total recording epoch was550 ms including a prestimulus interval of 100 ms. The digitizationrate was 256 Hz. Each epoch was baseline corrected across theentire sweep before artifact rejecting and averaging. The averagesfrom each block were baseline corrected again using the averageamplitude of the prestimulus portion of the epoch. Artifact rejectlevels were set at6100mV for all electrodes to exclude blinks andmovement artifacts. Individual block averages were visually ex-amined for residual artifact.

Data AnalysisBehavioral data.During the attend phase of the experiment, re-action time~RT! and accuracy measures were recorded for eachsubject for each type of deviant. The response windows were 100–1,000 ms for adults and 200–1,050 ms for children. Average RTsand percent correct responses for each subject for each devianttype were calculated and compared using two-way repeated-measures analyses of variance~ANOVAs!. Frequency of false alarmswas also measured for each subject and compared across age groupsusing at test.

Electrophysiological data.Averages for each subject for thethree conditions were constructed for the standards and for each ofthe three deviants. These averages were low-pass filtered at 20 Hzto reduce noise. Grand mean averages for each age group anddeviant type elicited during the three conditions were obtained

for purposes of display and examination of MMN topographicdistribution.

To select latency windows for amplitude measurements of theMMN, MMN peak latencies for the grand means were identified indifference waveforms obtained by subtracting the ERPs elicited bythe standard from the ERPs elicited by each of the three deviants.Peak latencies were defined by examining both the latency of thenegative difference response at Fz and the inversion at the mas-toids ~see Figures 5 and 6!. Peak latencies for adults were asfollows: ~1! first ignore condition: 120 ms easy, 115 ms medium,125 ms hard deviant;~2! attend condition: 105 ms easy, 105 msmedium, 120 ms hard deviant; and~3! second ignore condition:110 ms easy, 105 ms medium, 125 ms hard deviant. In the grandaverages for the children’s data, there were no clear MMNs to thehard deviants~1050 Hz! in either the first or second ignore con-ditions; thus for these two conditions, the peaks were chosen byexamining the peak latencies of the individual children who ex-hibited MMNs in these conditions. Peak latencies used for ampli-tude measures in the children were as follows:~1! first ignorecondition: 140 ms for all three deviants;~2! attend condition: 130 mseasy, 125 ms medium, 115 ms hard; and~3! second ignore condi-tion: 125 ms easy, 125 ms medium, 135 ms hard. The windowschosen for average amplitude measurements were the 50 ms sur-rounding the peak latency~25 ms on each side of the peak! of thegrand-average MMN.

Analysis of the amplitude data occurred in two stages. First, asis customary in the MMN literature, analyses of the average am-plitude of the ERPs elicited by the standard and deviant tones inthe region of the MMN were undertaken to ensure that the ob-served amplitude differences between the waveforms were signif-icantly different from chance. Average amplitudes of the standardand deviant tones were compared using planned comparisons~Hays,1963!, which are a type of a priori analysis. Once the presence ofsignificant MMNs for most comparisons was demonstrated, thesecond stage of analysis was undertaken in which the amplitude ofthe MMN across conditions and age groups was compared usingANOVAs and Tukey post hoc tests.

An alpha level of .05 was used for all statistical tests. Geisser–Greenhouse corrections were used in reportingp values whenappropriate.

Results

Behavioral DataThe behavioral data collected during the attend task are presentedin Table 1. An ANOVA~3 3 2! comparing RTs across deviant typeand age found a main effect of deviant,F~2,44! 5 44.36,p , .001,E 5 0.6132, and a trend toward a main effect of age,F~1,22! 53.22,p5 .09. RTs were fastest for the easy deviant and slowest forthe hard deviant for both age groups, and the adults respondedsomewhat faster than the children.

An ANOVA ~3 3 2! comparing percent correct across devianttype and age found main effects of both age,F~1,22! 5 7.56,p 5.012, and deviant,F~2,44! 5 20.90,p , .001,E 5 0.7010. Bothsubject groups were more accurate with the easy deviant than withthe hard deviant. Further, the adults were more accurate than thechildren for all deviant types. Six of the children responded to thehard deviant less than 10% of the time. In three of these childrenwe presented an additional behavioral task in which only the harddeviant and the standard were presented. Two of the children con-tinued to perform poorly~9.7% and 14.0%! and one performedadequately~51.6%!.

MMN in children 809

A trend toward more false alarms in children than in adults wasalso found,t~22! 5 21.68,p 5 .11. It should be recalled that ourSOA was relatively fast and that our response windows were set todisregard ambiguous responses~responses that followed a standardpreceded by a deviant!. Consequently, what may be a late “correct”response to a deviant~one that occurs after the next stimulus! wasconsidered a false alarm. A secondary analysis of the children’sdata opening up the response windows to include ambiguous re-sponses, found that 50% of the false alarms occurred to standardsfollowing deviants suggesting that “real” false-alarm rates may besomewhat smaller than reported.

Electrophysiological DataFigures 1 and 2 display the grand mean waveforms elicited by thestandard~thin line! and the easy deviant tones~thick line! in theattend condition at all recording sites for the adults and children,respectively. This condition was chosen for display so that the

topographic distribution of both MMN and P3 could be seen. AdultERPs ~Figure 1! were characterized by a small P1 peaking atapproximately 50 ms, N1 at 100 ms, and P2 at 170 ms. N2 wasseen in the ERPs peaking at approximately 220 ms and P3 wasevident in the ERPs peaking at between 320 and 380 ms.

The children’s ERPs~Figure 2! were characterized by a largeP1 peaking at approximately 80 ms, a negative-going dip at about120 ms, and a large negativity peaking at about 240 ms. N1 wasseen at the T7 and T8 electrode tracings peaking at approximately155 ms. This wave configuration is consistent with other devel-opmental studies that have used relatively short interstimulus in-tervals~Courchesne, 1990; Gomes et al., 1999; Kurtzberg et al.,1995!. P3 was observed in the children’s ERPs peaking at approx-imately 360 ms.

For both the adults and children, MMN was identified as theseparation between the waveforms in the vicinity of the N10P2components. Consistent with the literature, MMN was largest inthe frontocentral region, very small across the sides of the head~e.g., T7, T8!, and inverted in polarity at the mastoids.

Figures 3~adults! and 4~children! display grand mean differ-ence waveforms calculated by subtracting the standard ERPs fromeach of the three deviant ERPs~1050 Hz5 dashed0dotted line;1200 Hz5 dotted line; 1500 Hz5 solid line!. Difference wave-forms for all three conditions are presented for the frontocentralsites and for the mastoids. For the adults, clear MMNs~defined asnegative going waves at Fz with an inversion of the potential at themastoids! were seen for all three deviants in both of the ignoreconditions peaking between 105 and 125 ms~also see Figure 5!. Inthe attend condition, two negative peaks were seen at Fz for allthree deviants. The first, MMN, peaking at approximately 110 ms,inverted at the mastoids and the second, N2, peaking at approxi-mately 220 ms did not invert. The amplitude of the MMN waslargest for the easiest deviant and became smaller as the separationbetween the deviant and the standard was reduced. These obser-

Table 1. Behavioral Data for the Attend Condition

Adult Child

Easy deviantReaction time~ms! 384 ~85! 430 ~74!Percent correct~%! 97.3 ~1.9! 81.0 ~18.2!

Medium deviantReaction time~ms! 413 ~87! 473 ~79!Percent correct~%! 91.4 ~10.6! 56.7 ~33.8!

Hard deviantReaction time~ms! 475 ~115! 558 ~110!Percent correct~%! 63.5 ~40.1! 36.2 ~38.5!

False alarms~responses to standards! 6.7 ~4.9! 47.7 ~76.7!

Note: Standard deviations in parentheses.

Figure 1. Grand mean event-related potentials~ERPs!elicited from adults in the attend condition at all electrodesites. The thin lines are the ERPs elicited by the standardfrequency tone~1000 Hz! and the thick lines are the ERPselicited by the easy frequency deviant tones~1500 Hz!. Inthis and all subsequent figures, stimuli were presented attime zero.

810 H. Gomes et al.

vations were confirmed by planned comparisons~Table 2!; theamplitude of the MMN was significant at almost all electrode sitesexamined for all three deviants in all three conditions.

For the children~Figure 4! in the two ignore conditions, MMNswere observed for the easy and medium deviants that peaked be-tween 125 and 140 ms~also see Figure 6!. No clear MMN was

observed for the hard deviant in either ignore condition. In theattend condition, the negativity at Fz was characterized by a singlepeak, MMN, at approximately 125 ms, which inverted at the mas-toids. In contrast to the ignore conditions, MMN was observed forall three deviants in this condition. These observations were alsoconfirmed by the planned comparisons~Table 3!. Significant MMNamplitudes were measured for all three deviants at almost all elec-trode sites examined for the attend condition and for the easydeviant in the first ignore condition. The MMNs for the harddeviants were not significant in either of the ignore conditions for

Figure 2. Grand mean event-related potentials~ERPs!elicited from children in the attend condition at all elec-trode sites. The thin and thick lines as in Figure 1.

Figure 3. Grand mean difference waveforms elicited from adults in thefirst ignore, attend, and second ignore conditions obtained by subtractingthe event-related potentials~ERPs! elicited by the standard frequency tonesfrom the ERPs elicited by each of the three deviant frequency tones. Thesolid, dotted, and dashed0dotted lines are the difference waveforms asso-ciated with the easy~1500 Hz!, medium~1200 Hz!, and hard~1050 Hz!frequency deviants, respectively.

Figure 4. Grand mean difference waveforms elicited from children in thefirst ignore, attend, and second ignore conditions obtained as in Figure 3.The solid, dotted, and dashed0dotted lines are the same as in Figure 3.

MMN in children 811

the children. For the medium deviants in both ignore conditionsand for the easy deviant in the second ignore condition, MMNamplitude was significant only at the mastoids.

To determine if any of the children exhibited MMNs to the harddeviants in the ignore conditions, MMNs for each subject wererated as clearly present, clearly absent, or questionable~Table 4!.The ratings were made independently by two individuals who wereexperienced in examining MMN. If the raters agreed on one of thethree ratings~81.0% of the waveforms!, the waveform was giventhat rating. If they did not, the waveform was rated as questionable.An examination of the ratings for the children’s waveforms in-

dicted a pattern similar to that observed in the planned compari-sons~see Table 3!. Most children had MMNs for all three deviantsin the attend condition and for the easy and medium deviants in thefirst ignore condition. However, only 4 of the 14 children in thefirst ignore condition exhibited MMNs to the hard deviant andonly 7 of the 14 in the second ignore condition did so.

Attention effects.Because any potential differences were ex-pected to be small, a measure of the MMN amplitude between Fzand the mastoids~Fz–mastoid MMN measure! was used for theseamplitude analyses. It was calculated as the average amplitude ofthe MMN between Fz and the mastoids~Fz 2 @LM 1 RM#02!.This calculation is comparable to using linked mastoids as thereference, instead of the nose~Tervaniemi, Ilvonen, Karma, Alho,& Näätänen, 1997!. Figures 5~adult! and 6 ~child! depict theFz–mastoid MMN measure as average amplitude between Fz~solidline! and the two mastoids~dashed lines! for each of the threedeviants in all task conditions. To determine if attending to thestimuli affected the amplitude of the MMN, an ANOVA~2 33 3 3! was performed comparing the amplitude of the Fz–mastoidMMN measure across age, deviant type, and condition~ignore 1,attend, and ignore 2!. There was a main effect of condition,F~2,44! 5 11.51, p , .001, E 5 0.9181, and an interaction ofcondition and age group,F~2,44! 5 4.92,p 5 .014,E 5 0.9181.There was also a main effect of deviant type indicating largerMMN for the easier deviant,F~2,44! 5 28.17, p , .001, E 50.8263. No other effects were significant.

To further explore the effects of attention and deviant type ineach of the age groups, condition~ignore 1, attend, and ignore 2!by deviant type ANOVAs~3 3 3! were calculated for each agegroup separately. For the adults, the ANOVA yielded main effectsof deviant type,F~2,18! 5 37.69, p, .001, E 5 0.8633, andcondition,F~2,18! 5 6.62, p, .05, E 5 0.9198. Tukey post hoctests were calculated to compare the Fz–mastoid MMN measureacross condition for each deviant~e.g., MMN elicited by the easydeviant in the first ignore condition was compared with MMNselicited by the easy deviant in the attend and second ignore con-ditions; MMN elicited by the easy deviant in the attend conditionwas also compared with that elicited in the second ignore condi-tion!. The only significant finding was that the MMN elicited bythe easy deviant in the first ignore condition was larger than the

Figure 5. Grand mean difference waveforms elicited from adults in thefirst ignore, attend, and second ignore conditions obtained as in Fig-ure 3. The solid, dotted, and dashed0dotted lines are the waveforms atFz, right mastoid, and left mastoid, respectively.

Table 2. MMN Average Amplitudes (mV) and F values fromthe Planned Comparisons for Adult Participants

Ignore 1 Attend Ignore 2

Amp F Amp F Amp F

EasyFz 22.7 393.7** 22.5 265.3** 21.6 199.0**Cz 21.6 127.3** 21.1 49.3** 20.7 37.5**FC1 22.3 272.6** 22.0 177.2** 21.3 122.8**FC2 22.3 282.1** 21.9 161.1** 21.3 117.2**LM 1.6 132.1** 1.0 46.3** 1.6 188.2**RM 1.3 87.2** 0.9 37.4** 1.3 135.8**

MediumFz 21.7 149.1** 21.4 81.3** 21.3 133.6**Cz 21.1 65.7** 20.5 9.4** 20.8 51.2**FC1 21.4 108.8** 21.0 40.5** 21.1 92.1**FC2 21.4 110.2** 21.1 48.7** 21.3 122.1**LM 0.6 18.1** 1.1 48.2** 0.8 53.8**RM 0.5 14.2** 0.7 20.8** 0.5 17.6**

HardFz 20.4 10.1** 21.2 60.9** 20.6 23.2**Cz 20.1 0.1 20.6 16.1** 20.4 11.3**FC1 20.1 0.9 20.9 35.5** 20.5 18.5**FC2 20.3 4.5* 20.9 38.9** 20.5 20.1**LM 0.8 32.7** 0.4 8.7** 0.3 8.0**RM 0.6 17.6** 0.4 6.8* 0.4 11.8**

Note: MMN 5 mismatch negativity.*p , .05. **p , .01

812 H. Gomes et al.

one elicited in the second ignore. Attending to the stimuli did noteffect the amplitude of the MMN in the adults.

For the children, the two-way ANOVA also yielded main ef-fects of deviant type,F~2,26! 5 6.03, p, .05, E 5 0.8105, andcondition,F~2,26! 5 11.54, p, .001,E5 0.9129. Tukey post hoctests were again performed to compare the Fz–mastoid MMNmeasure across conditions for each deviant. The MMN elicited bythe hard deviant in the first ignore condition was smaller~ p , .05!than the one elicited by the hard deviant in the attend condition. Inaddition, the MMNs elicited in the second ignore condition by theeasy and hard deviants were significantly smaller~ p , .01! than

those elicited in the attend condition and the MMN elicited by themedium deviant approached significance. Comparing the first andsecond ignore conditions, the MMN elicited by the easy deviantwas significantly smaller~ p , .05! in the second ignore conditionthan in the first. No other deviant by condition comparisons weresignificant in the children.

Relationship between behavioral and ERP data.Pearson cor-relations between the amplitude of the Fz–mastoid MMN mea-sure and detection accuracy in the attend condition were calculatedto explore the relationship between behavioral discrimination andsize of MMNs in children. For the hard deviant there was asignificant correlation,r 5 .61, p , .05. In general, child par-ticipants who were more accurate at detecting the hard deviantsexhibited larger amplitude MMNs than children who were lessaccurate. The correlations were not significant for the mediumand easy deviants, possibly due to a more restricted range of theaccuracy measure.

The detection accuracy of the children who exhibited MMNsto the hard deviant in the first and second ignore conditions wasalso examined~see Table 4!. These children were no more likely

Figure 6. Grand mean difference waveforms elicited from children inthe first ignore, attend, and second ignore conditions obtained as inFigure 3. The solid, dotted, and dashed0dotted lines as in Figure 5.

Table 3. MMN Average Amplitudes (mV) and F values fromthe Planned Comparisons for Child Participants

Ignore 1 Attend Ignore 2

Amp F Amp F Amp F

EasyFz 21.8 52.9** 21.7 52.6** 20.2 0.6Cz 21.5 36.6** 0.7 8.6** 0.1 0.2FC1 21.8 51.1** 20.6 7.5** 20.1 0.3FC2 21.9 58.8** 20.9 15.2** 20.2 1.0LM 0.9 13.2** 1.8 63.0** 0.7 12.0**RM 0.9 12.8** 1.3 33.4** 0.5 6.4*

MediumFz 20.4 3.3 21.1 23.0** 20.1 0.3Cz 0.1 0.3 0.5 10.2** 0.2 0.9FC1 20.0 0.0 20.6 6.8* 0.0 0.0FC2 20.2 0.7 20.6 7.0** 20.1 0.1LM 1.0 15.8** 1.0 17.8** 0.7 11.6**RM 1.0 16.2** 1.0 19.2** 0.5 6.3*

HardFz 0.0 0.0 21.4 35.4** 20.3 2.1Cz 0.4 3.0 0.1 0.4 20.9 18.2**FC1 0.2 0.9 20.7 8.3** 20.7 12.3**FC2 0.4 2.6 20.9 14.5** 20.5 6.8*LM 0.4 2.6 0.9 16.8** 20.2 0.9RM 0.8 10.7** 0.9 14.7** 20.1 0.1

Note: MMN 5 mismatch negativity.*p , .05. **p , .01

Table 4. Number of Child Participants with Clearly Present,Clearly Absent, and Questionable MMNs

Group Present Absent Questionable

Ignore 1Easy 13 0 1Medium 8 3 3Hard 4 7 3

AttendEasy 11 1 2Medium 8 3 3Hard 8 2 4

Ignore 2Easy 6 3 5Medium 7 4 3Hard 7 4 3

Note: MMN 5 mismatch negativity.

MMN in children 813

to accurately detect the hard deviants during the attend conditionthan were the children without identifiable MMNs during theignore conditions. The 4 children with MMNs to the hard devi-ants in the first ignore condition identified 49.8% of the harddeviants during the attend condition and the 7 children withMMNs to the hard deviants in the second ignore identified 38.1%of the hard deviants.

Discussion

This study was designed to examine the effects of attention andactive discrimination on the amplitude of the MMN in children andadults and to determine if the effects were mediated by the size ofthe deviance. We found that the MMNs elicited by the hard deviantwere larger when the children were actively discriminating thestimuli than when they were ignoring the stimuli and watching avideo ~see Figure 6!. The MMNs elicited by the easy and mediumdeviants were not affected by attention in the children~when thefirst ignore and the attend conditions are compared!. Further, noneof the MMNs elicited by the three deviants from the adults wereaffected by attention~see Figure 5!.

The larger amplitude of the MMN elicited by the hard deviantfrom the children during the attend condition may be explained byassuming that~1! some form of learning has occurred due to ex-posure to the deviants during the first ignore condition,~2! in theattend condition MMN is overlapped by an attention dependentcomponent, such as N2b, or~3! the amplitude of the elicited MMNis modified by attention. It is possible that the increase in theamplitude of the MMN recorded from the first ignore condition tothe attend condition could be due to exposure to the stimuli. A fewstudies have demonstrated that MMN amplitude can be modifiedwith practice or training in some adult participants~Kraus et al.,1995; Näätänen, Schröger, et al., 1993; Tremblay et al., 1997!.This explanation is considered unlikely to apply to the currentresults for several reasons. First, if learning had occurred, it wouldbe expected to be maintained through the second ignore condition,but these MMNs were significantly smaller than those elicited inthe attend condition. Second, the learning effects described in theliterature were not observed in all adult participants and requiredactive discrimination, not just passive exposure~Näätänen, Schröger,et al., 1993!. The participants in our study were not informed aboutthe nature of the deviants or asked to discriminate the deviantsuntil the first ignore condition was completed and so presumablywere not engaging in the kind of active learning that would carryover to the attend condition.

With respect to the second explanation that there is an over-lapping attention-dependent component, this explanation is alsoconsidered unlikely. The timing and the topography of the effect donot appear to be consistent with an N2b. In the grand means for theadult participants, the N2b was separable from the MMN with apeak latency of approximately 220 ms as compared with 110 msfor the MMN ~Figure 1!. Further, the N2b had the characteristiclack of polarity inversion at the mastoids~Figure 5!. In the chil-dren, N2b was not easily identifiable; however, the peak of theMMN, at approximately 120 ms, was much earlier than would beexpected for the N2b given its latency in the adults. Also, thenegativity inverted in polarity at the mastoids, which would beexpected of MMN but not N2b. Finally, if the N2b was responsiblefor the increased amplitude of the MMN, the effect should begreater for the easy deviant than for the hard, given the betterdetection of easy than hard deviants. However, in our data thesignificant amplitude increase was observed only for the MMN

associated with the hard deviant. Consequently, it does not seemreasonable to postulate that the increase in the amplitude of theMMN in children is due to an overlapping N2b.

Our data strongly suggest that attention does in some casesmodify the amplitude of MMN elicited from children, just as at-tention can modify the amplitude of the MMNs elicited from adults.Further, for the children in our study and the adults reported in theliterature, these effects were greater for hard-to-discriminate stim-uli than for easy to discriminate stimuli, suggesting that automaticprocessing may be less efficient for difficult discriminations thanfor easy discriminations. In addition, not surprisingly, there aredevelopmental changes in what is considered a difficult discrimi-nation. In our study, children had more difficulty discriminatingthe hard deviants than did the adults and the amplitude of MMNselicited by this deviant was affected by attention for the childrenbut not for the adults.

Effects of Deviance SizeAn examination of the MMN elicited by the three deviants in eachof the three conditions showed that as the separation between thestandard and the deviant increased, the amplitude of the MMN gotlarger for both the children and adults. This result extends thefindings of Tiitinen et al.~1994! and Sams et al.~1985! to childrenand to a more complicated ignore paradigm in adults~in Tiitinenet al. and Sams et al., the various deviants were presented in sep-arate runs!. Further, in the attend condition, the mean RTs and ac-curacy also followed this pattern. Participants responded faster andmore accurately to the easy deviants than the hard deviants~also seeNovak et al., 1990!.

The Second Ignore ConditionWe were surprised to find that the MMN elicited by the easydeviants in the second ignore condition were significantly smallerthan those elicited in the first ignore condition for all subjects.However, reduced MMNs have been reported by other investiga-tors over the course of a long recording session~Lang et al., 1995!.Further, Sallinen and Lyytinen~1997! argued that the amplitude ofthe MMN is attenuated during periods in which the subject feelssleepy.

Developmental Changes in Attentional ProcessingWe know from this present study and others that infants and chil-dren show robust MMNs for a variety of deviants when they areignoring the stimuli. This finding indicates that infants and chil-dren are able to automatically discriminate some sounds, espe-cially moderately large deviants that are the only deviants in a run.However, it appears that when the stimulus environment becomemore complex and discrimination of the critical deviant featurebecomes more difficult, children need to actively attend to thestimuli to differentiate the deviants. It is possible that easy-to-discriminate stimuli are handled automatically from infancy butthat difficult auditory discrimination is initially a controlled pro-cess requiring focused attention. Further, it is possible that manyinitially difficult discriminations become automatic over time, prob-ably as a consequence of active discrimination and general audi-tory experience. This movement from controlled, or attentional,processing to automatic processing has been shown repeatedly inthe behavioral literature~for an example see Spelke, Hirst, & Neisser,1976!.

Attention probably affects processing at multiple stages of in-formation processing. Early in processing, attention may lead tostronger encoding of the physical features of the attended stimuli

814 H. Gomes et al.

and longer-lasting activation of the standard~Cowan, 1995!. Bothprocesses would facilitate comparison of the standard and devianttones, and hence increase the probability that MMNs would beelicited. Evidence exists for attention related effects on ERPs asearly as 20–30 ms following the stimulus~Hackley, Woldorff, &Hillyard, 1990; Woldorff, Hansen, & Hillyard, 1987!. Enhancedencoding and increased activation might positively affect the pro-cesses underlying the MMN without necessarily resulting in goodperformance on active discrimination tasks. In our study, MMNswere elicited from the children by the hard deviants even thoughdetection was on average 36%. Active discrimination requires ad-ditional processes and is influenced by task strategies~Kail, 1990!.

The above developmental hypothesis that difficult auditory dis-crimination is initially a controlled, attention demanding processthat becomes automatic with experience, could account for therange of individual differences seen in this and other studies~Krauset al., 1996; Lang et al., 1990; Näätänen, Schröger, et al., 1993!. Inaddition, this hypothesis is consistent with the findings from stud-ies exploring the effects of learning on the MMN~Kraus et al.,1995; Näätänen, Schröger, et al., 1993; Tremblay et al., 1997!.Some participants exhibit MMNs to deviants that are extremelydifficult to discriminate without training, other participants do notexhibit MMNs initially but do after extensive training, and stillothers fail to exhibit MMNs even by the end of training~Näätänen,Schröger, et al., 1993!. For the group that exhibits learning effectson the MMN, active discrimination and practice alter the system insome way such that ignored deviants that did not elicit MMNsinitially begin to elicit them.

This proposal argues that attention affects the processing of thestimuli at a stage before the MMN, so in this sense the MMN canstill be considered free from direct attentional influences~also seeRitter, Sussman, Deacon, Cowan, & Vaughan, 1999!. However,this hypothesis has significant implications for using the MMN toexamine developmental processes and clinical groups. First, be-cause easy-to-discriminate deviants do not appear to be affected byattention at least in normal children, ignore paradigms can be usedto ask some developmental and clinical questions. However, whatis considered a “difficult” discrimination seems to change withdevelopment so discriminability of the deviant by the differentgroups must be established with behavioral testing. Second, stud-ies with complex or potentially difficult-to-discriminate stimulithat compare children of different ages or from different clinicalgroups must monitor the attention directed toward the stimuli ofinterest during ignore tasks. In these situations the amplitude of theMMN may be affected by attention and different groups may onaverage attend to the “ignored” stimuli to differing degrees. Ideallyparticipants should be engaged in some unrelated task in whichperformance can be measured and a judgment of attention alloca-tion can be made. Third, in children and probably in clinical pop-ulations, measures of automatic discrimination~such as MMN tounattended stimuli!, attentionally enhanced automatic discrimina-tion ~such as MMN to attended stimuli! and active discrimination~such as behavioral performance! are not always related~also seeMolholm, Gomes, & Ritter, submitted!. Consequently, all threemeasures should be included in studies designed to comprehen-sively assess a group’s ability to discriminate stimuli of interest.

REFERENCES

Alho, K., Sams, M., Paavilainen, P., Reinikainen, K., & Näätänen, R.~1989!. Event-related brain potentials reflecting processing of relevantand irrelevant stimuli during selective listening.Psychophysiology, 26,514–528.

Alho, K., Woods, D. L., & Algazi, A.~1994!. Processing of auditory stimuliduring auditory and visual attention as revealed by event-related po-tentials.Psychophysiology, 31, 469–479.

Alho, K., Woods, D. L., Algazi, A., & Näätänen, R.~1992!. Intermodalselective attention. II. Effects of attentional load on processing of au-ditory and visual stimuli in central space.Electroencephalography andClinical Neurophysiology, 82, 356–368.

American Electroencephalographic Society.~1990!. Standard electrode po-sition nomenclature. Bloomfield, CT: American Electroencephalo-graphic Society.

Ceponiene, R., Cheour, M., & Näätänen, R.~1998!. Interstimulus intervaland auditory event-related potentials in children: Evidence for multiplegenerators.Electroencephalography and Clinical Neurophysiology, 108,345–354.

Cheour, M., Haapanen, M. L., Hukki, J., Ceponiene, R., Kurjenluoma, S.,Alho, K., Tervaniemi, M., Ranta, R., & Näätänen, R.~1997!. The firstneurophysiological evidence for cognitive brain dysfunctions in chil-dren with CATCH.NeuroReport, 8, 1785–1787.

Courchesne, E.~1990!. Chronology of postnatal human brain development:Event-related potentials, positron emission tomography, myelinogene-sis, and synaptogenesis studies. In J. W. Rohrbaugh, R. Parasuraman, &R. Johnson, Jr.~Eds.!, Event-related brain potentials: Basic issues andapplications~pp. 210–241!. New York: Oxford University Press.

Cowan, N.~1995!. Attention and memory: An integrated framework. NewYork: Oxford University Press.

Gomes, H., Sussman, E., Ritter, W., Kurtzberg, D., Cowan, N., & Vaughan,H. G., Jr.~1999!. Electrophysiological evidence of developmental changesin the duration of auditory sensory memory.Developmental Psychol-ogy, 35, 294–302.

Hackley, S. A., Woldorff, M., & Hillyard, S. A.~1990!. Cross-modal se-lective attention effects on retinal. myogenic, brainstem, and cerebralevoked potentials.Psychophysiology, 27, 195–208.

Hays, W. L.~1963!. Statistics for psychologists. New York: Holt, Rinehartand Winston.

Kail, R. ~1990!. The development of memory in children. New York: W.Freeman.

Keller, T. A., & Cowan, N.~1994!. Developmental increase in the durationof memory for tone pitch.Developmental Psychology, 30, 855–863.

Korpilahti, P., & Lang, H. A.~1994!. Auditory ERP components and mis-match negativity in dysphasic children.Electroencephalography andClinical Neurophysiology, 91, 256–264.

Kraus, N., McGee, T., Carrell, T. D., King, C., Tremblay, K., & Nicol, T.~1995!. Central auditory system plasticity associated with speech dis-crimination training.Journal of Cognitive Neuroscience, 7, 25–32.

Kraus, N., McGee, T., Carrell, T. D., Zecker, S. G., Nicol, T. G., & Koch,D. B. ~1996!. Auditory neurophysiologic responses and discriminationdeficits in children with learning problems.Science, 273, 971–973.

Kurtzberg, D., Vaughan, H. G., Jr., Kreuzer, J. A., & Fliegler, K. Z.~1995!.Developmental studies and clinical applications of mismatch negativ-ity: Problems and prospects.Ear and Hearing, 16, 105–117.

Lang, A. H., Eerola, O., Korpilanti, P., Holopainen, I., Salo, S., & Aaltonen,O. ~1995!. Practical issues in the clinical application of mismatch neg-ativity. Ear and Hearing, 16, 118–130.

Lang, A. H., Nyrke, T., Ek, M., Aaltonen, O., Raimo, I., & Näätänen, R.~1990!. Pitch discrimination performance and auditory event-relatedpotentials. In C. H. M. Brunia, A. W. K. Gaillard, A. Kok~Eds.!,Psychophysiological brain research~Vol. 1, pp. 294–298!. Tilburg:Tilburg University Press.

Molholm, S., Gomes, H., & Ritter, W.~submitted!. The detection of con-stancy amidst change: A dissociation of preattentive and intentionalprocesses in children.

Näätänen, R.~1992!. Attention and brain function. Hillsdale, NJ: Erlbaum.Näätänen, R., & Alho, K.~1997!. Mismatch negativity—The measure for

central sound representation accuracy.Audiology and Neuro-Otology,2, 341–353.

Näätänen, R., Paavilainen, P., Tiitinen, H., Jiang, D., & Alho, K.~1993!.Attention and memory.Psychophysiology, 30, 436–450.

Näätänen, R., Schröger, E., Karakas, S., Tervaniemi, M., & Paavilainen, P.

MMN in children 815

~1993!. Development of a memory trace for a complex sound in thehuman brain.NeuroReport, 4, 503–506.

Novak, G. P., Ritter, W., Vaughan, H. G., Jr., & Wiznitzer, M. L.~1990!.Differentiation of negative event-related potentials in an auditory dis-crimination task.Electroencephalography and Clinical Neurophysiol-ogy, 75, 255–275.

Paavilainen, P., Tiitinen, H., Alho, K., & Näätänen, R.~1993!. Mismatchnegativity to slight pitch changes outside strong attentional focus.Bio-logical Psychology, 37, 23–41.

Ritter, W., Deacon, D., Gomes, H., Javitt, D., & Vaughan, H. G., Jr.~1995!.The mismatch negativity of event-related potentials as a probe of tran-sient auditory memory: A review.Ear and Hearing, 16, 52–67.

Ritter, W., Paavilainen, P., Lavikainen, J., Reinikainen, K., Alho, K., Sams,M., & Näätänen, R.~1992!. Event-related potentials to repetition andchange of auditory stimuli.Electroencephalography and Clinical Neuro-physiology, 83, 306–321.

Ritter, W., Sussman, E., Deacon, D., Cowan, N., & Vaughan, H. G., Jr.~1999!. Two cognitive systems simultaneously prepared for oppositeevents.Psychophysiology, 36, 835–838.

Sallinen, M., & Lyytinen, H.~1997!. Mismatch negativity during objectiveand subjective sleepiness.Psychophysiology, 34, 694–702.

Sams, M., Paavilainen, P., Alho, K., & Näätänen, R.~1985!. Auditoryfrequency discrimination and event-related potentials.Electroenceph-alography and Clinical Neurophysiology, 62, 437–448.

Spelke, E., Hirst, W., & Neisser, U.~1976!. Skills of divided attention.Cognition, 4, 215–230.

Tervaniemi, M., Ilvonen, T., Karma, K., Alho, K., & Näätänen, R.~1997!.The musical brain: Brain waves reveal the neurophysiological basis ofmusicality in human subjects.Neuroscience Letters, 226, 1–4.

Tiitinen, H., May, P., Reinikainen, K., & Näätänen R.~1994!. Attentivenovelty detection in humans is governed by pre-attentive sensory mem-ory. Nature, 372, 90–92.

Trejo, L. J., Ryan-Jones, D. L., & Kramer, A. F.~1995!. Attentional mod-ulation of the mismatch negativity elicited by frequency differencesbetween binaurally presented tone burst.Psychophysiology, 32, 319–328.

Tremblay, K., Kraus, N., Carrell, T. D., & McGee, T.~1997!. Centralauditory system plasticity: Generalization to novel stimuli followinglistening training.Journal of the Acoustical Society of America, 102,3762–3773.

Winkler, I., Schröger, E., & Cowan, N.~in press!. The role of large-scaleperceptual organization in the mismatch negativity event-related brainpotential.Journal of Cognitive Neuroscience.

Woldorff, M. G., Hackley, S. A., & Hillyard, S. A.~1991!. The effects ofchannel-selective attention on the mismatch negativity wave elicited bydeviant tones.Psychophysiology, 28, 30–42.

Woldorff, M. G., Hansen, J. C., & Hillyard, S. A.~1987!. Evidence foreffects of selective attention in the mid-latency range of the humanauditory event-related potential. In R. Johnson, Jr., J. W. Rohrbaugh, &R. Parasuraman~Eds.!, Current trends in event-related potential re-search. Electroencephalography and Clinical Neurophysiology~Sup-plement 40, pp. 146–154!. Amsterdam: Elsevier.

Woldorff, M. G., Hillyard, S. A., Gallen, C. C., Hampson, S. R., & Bloom,F. E. ~1998!. Magnetoencephalographic recordings demonstrate atten-tional modulation of mismatch-related neural activity in human audi-tory cortex.Psychophysiology, 35, 283–292.

Woods, D. L., Alho, K., & Algazi, A.~1992!. Intermodal selective atten-tion. I. Effects on event-related potentials to lateralized auditory andvisual stimuli.Electroencephalography and Clinical Neurophysiology,82, 341–355.

~Received April 23, 1999;Accepted January 7, 2000!

816 H. Gomes et al.