stimulus context determines p3a and p3b

Stimulus context determines P3a and P3b

JUN’ICHI KATAYAMA a and JOHN POLICHb

aFaculty of Education, Hokkaido University, Sapporo, JapanbDepartment of Neuropharmacology, The Scripps Research Institute, La Jolla, CA, USA

Abstract

P300 differences for target~.10!, nontarget~.10!, and standard tones~.80! were assessed using a three-stimulus oddballparadigm in which participants responded only to the target~n 5 12!. Target0standard~easy or difficult! and nontarget0standard~large or small! pitch differences were manipulated orthogonally. In all conditions, target tones elicited aparietal P300, which was affected only by the target0standard discrimination ease. Nontarget in the easy0large anddifficult0small conditions elicited a parietal but smaller P300 than the target but in the easy0small condition elicitedsimilar ERPs to the standard. However, nontarget stimuli in the difficult0large condition elicited an anterior maximumand earlier P300~P3a! component. The findings suggest that target P300s are not influenced by the nontarget stimulusconfiguration, whereas the nontarget P300 outcomes are determined directly by the stimulus context. The theoreticalimplications are discussed.

Descriptors: P300, P3a, P3b, Event-related potential~ERP!, Task difficulty, Three-tone oddball paradigm

The P300 component of the event-related brain potential~ERP!reflects fundamental cognitive processes~Donchin & Coles, 1988;Johnson, 1988; Picton, 1992; Polich, 1993a! and has been used ina wide variety of theoretical, empirical, and clinical applications~Donchin, Karis, Bashore, Coles, & Gratton, 1986; Polich, 1993b!.In particular, the P300 has been considered as an index of workingmemory~Donchin et al., 1986!, such that its amplitude reflects theallocation of attentional resources~Humphreys & Kramer, 1994;Wickens, Kramer, Vanasse, & Donchin, 1983!, and its peak latencyis considered proportional to stimulus evaluation time~e.g., Kutas,McCarthy, & Donchin, 1977; Magliero, Bashore, Coles, & Donchin,1984; Polich, 1986, 1987!. The P300 often is obtained using theso-called oddball paradigm, wherein two stimuli are presented in arandom order, one of which occurs less frequently than the other.The participant is required to discriminate the rare stimulus~target!from the frequent one~standard! by noting the occurrence of thetarget—typically by pressing a button or mentally counting~e.g.,Duncan-Johnson & Donchin, 1977; Polich, 1989b, 1990; Verleger& Berg, 1991!. The P300 elicited by the target in this task is alarge, positive-going potential that is largest over the parietal elec-trode sites and occurs at about 300 ms in normal young adults.

Three-Stimulus Paradigm and P3a

A modification of the oddball paradigm also has been used inwhich a third, infrequent-nontarget stimulus is presented in addi-tion to the sequence of standard and target stimuli. Using thismethod, Courchesne, Hillyard, and Galambos~1975! initially re-ported that colorful, unrecognizable slides~novel stimulus!, whichwere interspersed in a random sequence of frequent standard andinfrequent target slides, elicited a frontocentrally distributed P300,sometimes called “P3a,” whereas the infrequent-target stimuluselicited a parietal maximum P300 or “P3b”—a distinction firstmade by Squires, Squires, and Hillyard~1975!, but observed clearlywith a traditional two-stimulus oddball task in only about 10% ofnormal participants~Polich, 1988!. This “novelty” P300 has beenreported for auditory~Courchesne, Kilman, Galambos, & Lincoln,1984; Knight, 1984! and somatosensory~Yamaguchi & Knight,1991a, 1991b! stimulus modalities. Because the novelty P300 pro-duces an anterior scalp distribution, has shorter latency than thetarget P300, and habituates rapidly~Courchesne et al., 1975; Fried-man & Simpson, 1994!, it has been interpreted as reflecting frontallobe function ~cf., Ebmeier et al., 1995; Friedman & Simpson,1994; Friedman, Simpson, & Hamberger, 1993!.

In addition, Courchesne et al.~1975! also reported that easily rec-ognized~i.e., not novel! infrequent nontarget visual stimuli eliciteda centroparietal rather than a frontocentral P300~cf. Courchesne,1978; Courchesne, Courchesne, & Hillyard, 1978!, which is some-times referred to as a “no-go” P300. In the auditory modality, Pfef-ferbaum, Ford, Roth, and Kopell~1980; Pfefferbaum, Ford,Wenegrat, Roth, & Kopell, 1984! found that an infrequently pre-sented nontarget tone inserted into the traditional oddball tone se-quence elicited a parietal P300 that was smaller and later than thetarget P300. Furthermore, Grillon, Courchesne,Ameli, Elmasian, andBraff ~1990! compared the ERPs from novel sounds with those from

This study was conducted during J. Katayama’s stay at the Departmentof Neuropharmacology, The Scripps Research Institute as a Guest Scientist.This research was supported by NIDA DA08363-02 to J. Polich. This paperis publication NP10380 from The Scripps Research Institute.

We thank Dr. Aaron Ilan for his very helpful comments on a previousversion of this manuscript.

Address reprint requests to: Jun’ichi Katayama, Faculty of Education,Hokkaido University, Sapporo 060 Japan. E-mail: [email protected];or John Polich, Department of Neuropharmacology, TPC-10, The ScrippsResearch Institute, 10550 North Torrey Pines Road, La Jolla, CA 92037,USA. E-mail: [email protected].

Psychophysiology, 35~1998!, 23–33. Cambridge University Press. Printed in the USA.Copyright © 1998 Society for Psychophysiological Research

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infrequent-nontarget tones and reported that the novel stimuli elic-ited a central maximum P300, although the infrequent nontarget toneelicited a centroparietal P300 whose amplitude was smaller than thatfrom the novel stimulus. Several recent reports also have suggestedthat the P300 component from a go0no-go task can be decomposedinto two subcomponents that appear related to the stimulus andresponse characteristics of the task~Falkenstein, Hohnsbein, & Hoor-mann, 1994; Falkenstein, Koshlykova, Kiroj, Hoormann, & Hohns-bein, 1995; Hohnsbein, Falkenstein, & Hoormann, 1991!. Whentaken together with the P3a subcomponent findings outlined above,this evidence suggests that the “P300” may be composed of at leasttwo constituent potentials that reflect distinct information process-ing events~cf. Eimer, 1993; Falkenstein, Hohnsbein, & Hoormann,1993; Falkenstein, Hohnsbein, Hoormann, & Blanke, 1991!. Thus,the P300 component appears to vary in its locus of scalp distribu-tion magnitude and peak latency as a function of the stimulus context.

However, despite the theoretical and empirical importance ofdistinguishing among these various P300 components, systematicassessments of major ERP variables on P300 from target and non-target in a three-stimulus paradigm are not readily available. To-ward this end, Katayama and Polich~1996b! manipulated theprobability of target and nontarget stimuli in a three-tone paradigmto assess how this variable affects the P300 from each stimuluscategory. They reported that nontarget tone stimuli produced P300components that were similar to, although generally smaller than,those from the target stimuli and that the target and nontarget P300components were affected by the probability of eliciting stimuli inthe same fashion as that observed for two-tone oddball tasks~e.g.,Duncan-Johnson & Donchin, 1977; Polich, 1987!. In addition,target P300 amplitude and latency in the three-tone paradigm werenot affected by the probabilities of either the standard or nontargettone. A second study~Katayama & Polich, 1996a! found that thetarget P300 from the three-tone paradigm was essentially the sameas that found in a two-tone or single-tone paradigms~Polich, Eis-chen, & Collins, 1994; Polich & Heine, 1996!. These findingssuggest that P300 amplitude and latency from target and nontargetstimuli in the three-tone paradigm are determined in similar waysby stimulus probability variation.

Although Courchesne et al.~1975! claimed that their novelty P300was different from the P3a reported by Squires et al.~1975!, someresearchers have labeled the P300 elicited by the novel stimulus asP3a~e.g., Holdstock & Rugg, 1993; Knight, 1987; Rugg et al., 1993;Yamaguchi & Knight, 1991a, 1991b!. There is still no consensus fornaming the P300s elicited by the several types of nontarget stimuli:infrequent stimuli in a passive condition, physically novel stimuli,or infrequent-nontarget stimuli in a three-item or more oddball task,whereas a target stimulus P300 from an active oddball task is con-sistently referred to asP3b. From at least one theoretical viewpoint,Näätänen~1990! distinguished P3a and P3b such that P3a is con-sidered to be a reflection of the attentional switch produced fromthe mismatch between a stimulus presented and passively formedneuronal trace, whereas P3b reflects the match between the stim-ulus and voluntarily maintained attentional trace~cf. Falkensteinet al., 1991, 1993!. In the present study, the P300 with a parietalscalp distribution is referred to asP3b, and the other types ofP300s with more anterior distribution are referred to asP3a fordescriptive simplicity.

Present Study

The purpose of the present study was to examine the basic char-acteristics of the P300 elicited in the three-tone oddball paradigm

by manipulating another important ERP variable—task difficulty,as defined by the degree of stimulus similarity. In the traditionaltwo-stimulus oddball task, when the discrimination of the targetfrom the standard stimulus is difficult, target stimulus P300 am-plitude is smaller and its latency is longer than when the discrim-ination is relatively easy~Ford, Roth, & Kopell, 1976; Polich,1986, 1987!. To isolate the effects of task difficulty on infrequent-nontarget stimulus processing, the magnitude of the differences inpitch between the nontarget and frequent-standard stimuli relativeto the target were varied orthogonally. Based on previous findingsfor the three-stimulus paradigm~Katayama & Polich, 1996b!, tar-get P300 should not be affected by the deviation magnitude be-tween the nontarget and standard. For the nontarget P300, there aretwo possibilities. First, Katayama and Polich~1996b! demon-strated that the nontarget P300 was affected by the probabilityof the eliciting stimulus in the same fashion as the target P300, sothat when the pitch difference magnitude between nontarget andstandard tone were manipulated, similar components could be ob-served for the nontarget and target P300. Second, target discrim-ination difficulty and nontarget deviation magnitude may haveeffects on nontarget P300 because the context in which the non-target 300 is elicited would vary dramatically among conditions asthe target0standard discrimination task varies in difficulty. Thus, ifstimulus context does affect the nontarget differently from thetarget P300, such differences could shed light on the underlyingrelationship between P3a and P3b subcomponents if these poten-tials reflect distinct processing differences.

The theoretical rationale for this approach stems from consid-eration of P3a versus P3b differences:~a! “surprising” stimuliversus typical or task-relevant stimuli,~b! frontocentral versuscentral-parietal amplitude scalp distributions, and~c! short versuslonger peak latencies. The extant data suggest that independent anddistinct neural generators produce the two subcomponents~Eb-meier et al., 1995; Johnson, 1989; Knight, Scabini, Woods, &Clayworth, 1989; Verleger, Heide, Butt, & Kömpf, 1994; Yamagu-chi & Knight, 1991b!, that the P3a is not readily apparent in allindividuals ~Polich, 1988; Squires et al., 1975!, and that stimu-lus configurations and attributes dramatically affect P3a elicita-tion, whereas similar variables do not as strongly affect the P3b~cf. Courchesne et al., 1975, 1978; Covington & Polich, 1996;Friedman et al., 1993!. These considerations imply that the elec-trophysiological events observed at the scalp in response to puta-tively “novel” stimuli that produce the P3a may arise, at least inpart, because of the neural context in which the eliciting eventsoccur. Indeed, virtually all reliable reports of the P3a phenomenonhave used novel stimuli that produce a frontocentral “alerting”response that most likely originates from neural sources related toinitial attention allocation~cf. Ebmeier et al., 1995; Pardo, Fox, &Raichle, 1991; Posner, 1992; Posner & Petersen, 1990!. Presenta-tion of a target stimulus in an oddball task may also elicit a P3acomponent initially and, when subsequent attentional resource andmemory operations are engaged, the parietal maximum canonicalP3b from temporal-parietal activity~Johnson, 1993; Knight, 1996;Polich et al., 1997!. Hence, it is likely that at least two different butrelated sets of neural activities comprise the “P300” component: anearly frontal source and a later parietal locus, but the frontal sourceis difficult to observe at the scalp without extraordinary stimulusdiscrimination conditions that overcome the larger, later, and pa-rietal P3b. If this perspective is accurate, the context in whichtarget and nontarget stimuli occur may be a powerful determinantof P300 generation because it is exactly this context that producesthe neural representation that is changed by “novel” stimuli. To

24 J. Katayama and J. Polich

assess these hypotheses directly, P300 components were elicitedwith a three-tone paradigm under the conditions in which stimuluspitch differences between the target and standard and between thestandard and infrequent-nontarget tone were varied orthogonally tomanipulate target discrimination difficulty and nontarget deviationmagnitude, respectively.

Method

ParticipantsTwelve young adults served as participants~M 5 23.1 years,SD53.8 years! and received course credit or payment. Equal numbersof each sex were assessed, and all participants reported being freeof neurological or psychiatric disorders.

Recording ConditionsElectroencephalographic~EEG! activity was recorded at the F30F4, F70F8, C30C4, T70T8, P30P4, P70P8, Fz, Cz, and Pz electrodesites of the 10-20 system, using an Electro-Cap system, referred tolinked earlobes, with a forehead ground and impedance at 10 kVor less. Additional electrodes were placed at the outer canthus andbelow the left eye to monitor electrooculogram~EOG! activitywith a bipolar recording. The filter bandpass was 0.01–30 Hz~6 dBoctave0slope!. The EEG was digitized at 3.0 ms per point for768 ms, with a 75-ms prestimulus baseline. Waveforms were av-eraged off-line, such that trials with a response error or those onwhich the EEG or EOG exceeded690 mV were rejected auto-matically. All experimental conditions were recorded with eyesopen, and rest periods were provided between trial blocks.

ProceduresStimulus tones were presented binaurally through headphones ina random series, once every 2 s at 75 dB SPL~50-ms plateau,10-ms rise0fall!. In each experimental condition, 350 tones werepresented, consisting of target, standard, and nontarget tones withprobabilities of .10, .80, and .10, respectively. Four task condi-tions were defined by a combination of two levels of target0standard discrimination difficulty~easy vs. difficult! and thenontarget0standard deviation magnitude~large vs. small!. Thetone frequencies for each stimulus type and experimental condi-tion are summarized in Table 1. The values were developed withpilot testing and designed to minimize P300 tone frequency effects~Polich, 1989a; Sugg & Polich, 1995!. The participant’s taskwas to respond to the target tone by pushing a mouse buttonwith the right index finger as quickly as possible. Each experi-mental condition lasted about 12 min. All participants receivedthe easy0large condition first to facilitate task performance forsubsequent conditions. The order of the remaining three condi-tions was counterbalanced across participants.

Data AnalysesThe P300 component was defined as the largest positive-goingpeak occurring within a specific latency window defined by thetask conditions. For the target stimulus P300; this latency windowwas 250–400 ms for the easy conditions~easy0large and easy0small! and 250–500 ms for the difficult conditions~difficult0largeand difficult0small!. For the nontarget stimulus P300; this latencywindow was 250–400 ms for the large deviation conditions~easy0large and difficult0large! and 250–500 ms for the small deviationconditions~easy0small and difficult0small!. Because the focus ofthe present study was the effects of stimulus context on the targetand nontarget stimuli, only the P300 components from these stim-uli were assessed. Peak amplitude was measured relative to theprestimulus baseline, and peak latency was measured from thetime of stimulus onset. All analyses of variance~ANOVAs! em-ployed Greenhouse–Geisser corrections to the degrees of freedomwhen appropriate, and only the corrected probability values arereported. The Tukey method was used for post hoc comparisons,with a significance level of .05.

Results

Behavioral PerformanceThe behavioral data are summarized in Table 2. A two-factor~2 Tar-get0Standard Discrimination Difficulties3 2 Nontarget0StandardDeviations! analysis of the reaction time to the target tone foundthat the reaction time in the easy tasks was shorter than in thedifficult tasks,F~1,11! 5 47.3,p , .001. The interaction also wassignificant,F~1,11! 5 8.4,p , .02, indicating that although therewas no effect of nontarget0standard deviation when the task waseasy, the reaction time was longer in the small deviation than in thelarge deviation condition when the task was difficult. A similaranalysis found that the hit rate was higher in the easy than in thedifficult tasks,F~1,11! 5 16.5,p , .002. The interaction also wassignificant,F~1,11! 5 5.9,p , .04, indicating that although therewas no effect of nontarget0standard deviation when the task waseasy, the hit rate was higher in the large than in the small deviationcondition when the task was difficult. The false positive rate forthe standard and nontarget tone was assessed by a three-factor~2 Target0Standard Discrimination Difficulties3 2 Nontarget0Standard Deviations3 2 Stimulus Types! analysis but no signif-icant main effects or interactions were observed.

ERP AnalysesThe grand average ERPs from the target, standard, and nontargettones for the easy and difficult task conditions are presented inFigures 1 and 2, respectively. For the easy tasks, the target tone

Table 1. Tone Stimulus (Probabilities) Frequencies (Hz) forEach Stimulus Type and Experimental Condition

Target0standard discrimination Easy Difficult

Nontarget0standard deviation Large Small Large Small

Target~.10! 2000 2000 2000 2000Standard~.80! 1000 1000 1940 1940Nontarget~.10! 500 970 970 1880

Table 2. Mean Reaction Time and Performance Rates for EachTask Condition

Easy Difficult

Large Small Large Small

Reaction time~ms! 492 491 614 648Hit targets~%! 98.8 99.8 87.4 81.0False positive~%!

Standard 0.03 0.00 0.47 0.81Nontarget 0.73 0.24 0.24 0.24

Stimulus context, P3a, and P3b 25

elicited P300 components that were largest over the midline andparietal electrodes. Although large deviant nontarget tones elicitedP300 components~upper!, small deviant nontarget stimuli elicitedP300s that were similar to those from the standard tone~lower!.For the difficult tasks, target tones elicited large P300 components,with smaller amplitudes and longer latencies than those from thetarget stimuli in the easy tasks. The small deviant nontarget stimulielicited P300s as large as those from the nontarget in the easy0largetask condition~lower!. In contrast, the large deviant nontargetelicited a P300 that was larger and earlier than the P300 elicited bythe target at the frontal and central electrodes, whereas the targetstimulus P300 at the parietal sites was larger than that from thenontarget stimuli~upper!. Statistical analyses of these outcomesare presented next.

P300 amplitude.The mean P300 amplitudes from the targetand nontarget stimuli for each experimental condition and elec-trode site are illustrated in Figure 3. The data from just the midlineelectrodes were assessed initially with a four-factor~2 Stimulus@S#Types 3 2 Target0Standard Discrimination@T# Difficulties 3 2Nontarget0Standard Deviations@N# 3 3 Electrodes@E#! ANOVA.Additional analyses employing all electrode sites are presentedbelow.

The results of this analysis are summarized in Table 3, in whichonly the significant effects are presented. Because the four-wayinteraction was significant, separate three-factor~2 S3 2 N 3 3 E!analyses on easy and difficult tasks were performed. The maineffects of stimulus type, nontarget0standard deviation, and elec-trode were still significant in both analyses. Only the S3 E in-

Figure 1. Grand averaged event-related potentials from easy tasks with large~upper! and small~lower! nontarget deviation conditionsfor each tone type and recording site~n 5 12!. Target, standard, and nontarget stimuli were presented with probabilities of .10, .80,and .10, respectively. Tone pitches of the target, standard, and nontarget stimuli in the easy0large condition were 2000, 1000, and500 Hz; in the easy0small condition, 2000, 1000, and 970 Hz, respectively.


teraction was significant for the analysis on easy task, indicatingthat the target tone elicited larger P300 than the nontarget and thatthe parietal maximum effect was stronger for the target than for thenontarget P300. In contrast, the S3 N, S 3 E, and S3 N 3 Einteractions were significant for the difficult task analysis~ p , .05in all cases!. Post hoc comparisons indicated that the interactionsstemmed from the nontarget P300 amplitude distribution, whichwas different between nontarget0standard deviation conditions~ p , .05!. Even though there was no effect of nontarget deviationmagnitude on the target P300 amplitude, the target P300 amplitudeat Pz was larger than at Cz, which was larger than at the Fzelectrode. Although the nontarget P300 from the difficult0smallcondition demonstrated the same tendency as the target P300, forthe difficult0large condition component amplitude at Fz electrodewas smaller than those from Cz and Pz electrode, which were not

different from each other. Thus, stimulus context influenced taskdifficulty and, therefore, the relative amplitudes of the target andnontarget P300.

Vector analysis.To assess these scalp distribution differencesamong conditions, P300 amplitude data from target and nontargetstimulus were reanalyzed after the data were normalized by vectorlength ~McCarthy & Wood, 1985!, where each amplitude valuewas divided by the square root of the sum of squared amplitudesover the three midline electrode locations for each condition~i.e.,vector length for each condition!. This analysis normalized theeffects of stimulus type, target0standard discrimination difficulty,and nontarget0standard deviation so that only the scalp distributioninformation was compared across task conditions~cf. Johnson,1993!.

Figure 2. Grand averaged event-related potentials from difficult tasks with large~upper! and small~lower! nontarget deviationconditions for each tone type and recording site~n 5 12!. Target, standard, and nontarget stimuli were presented with probabilities of.10, .80, and .10, respectively. Tone pitches of the target, standard, and nontarget stimuli in the difficult0large condition were 2000,1940, and 970 Hz; in the difficult0small condition, 2000, 1940, 1880 Hz, respectively.


Figure 3. Mean P300 peak amplitudes from the target and nontarget stimuli in each task condition as a function of coronal electrodesite for the frontal, central, and parietal electrode positions~LL 5 left lateral, LM 5 left medial, M5 midline, RM 5 right medial,RL 5 right lateral!.

Table 3. Summary of the Four-Factor Analysis of Variance Performed on the P300 Peak Amplitude, Vector Length,and Latency Data

Amplitude Vector Latency

Source~df ! F p e F p e F p e

Stimulus type~1,11! 27.0 .001 — — — —Target0standard discrimination difficulty~1,11! — — — 80.7 .001 —Nontarget0standard deviation~1,11! 40.4 .001 — 27.5 .001 —Electrode~2,22! 47.3 .001 .83 7.3 .01 .75S 3 T ~1,11! 25.6 .001 — 50.8 .001 —S 3 N ~1,11! 5.4 .04 — 39.5 .001 —S 3 E ~2,22! 17.7 .001 .97 — — — 5.4 .02 1.00T 3 N ~1,11! — — — — — —T 3 E ~2,22! 6.0 .02 .69 — — — — — —N 3 E ~2,22! — — — 7.6 .01 .66 — — —S 3 T 3 N ~1,11! — — — — — —S 3 T 3 E ~2,22! 4.3 .04 .76 19.9 .001 .73 — — —S 3 N 3 E ~2,22! — — — 9.3 .01 .60 — — —T 3 N 3 E ~2,22! — — — — — — — — —S 3 T 3 N 3 E ~2,22! 5.2 .03 .75 — — — — — —

Note: The four-factor ANOVA5 2 Stimulus Types3 2 Target0Standard Discrimination Difficulty3 2 Nontarget0Standard Devia-tions 3 3 Electrode Sites. S5 stimulus type, T5 target0standard discrimination, N5 nontarget0standard deviations, E5 elec-trode site.


The data were analyzed with the same four-factor analysis em-ployed previously. As presented in Table 3, the N3 E, S3 T 3E, and S3 N 3 E interactions were significant. Tests of partialinteraction confirmed the findings of the original amplitude anal-yses: The scalp distribution of target P300 was determined only bythe target0standard discrimination difficulty in the absence ofnontarget0standard deviation effects, whereas nontarget P300 dem-onstrated a different distribution according to each task condition.

P300 latency.Mean P300 latencies for each experimental con-dition and electrode site are illustrated in Figure 4. The samefour-factor ANOVA was conducted on the midline latency data,with the outcomes also summarized in Table 3. The S3 T and S3N interactions were significant and demonstrated that target stim-ulus P300 latency was shorter in the easy than in the difficult tasks,with no effects of nontarget deviation magnitude observed. In con-trast, P300 latency for the nontarget stimulus tone was shorter inthe large than in the small nontarget deviation conditions, with noeffects of target0standard discrimination difficulty. The S3 Einteraction occurred because target tone latency was shorter at thefrontal than at the central and parietal sites, although there was noeffect of electrode on nontarget P300 latency.

Electrode location.The data obtained from all 15 electrodeswere analyzed with separate analyses performed on easy and dif-ficult tasks conducted with four factors~2 Stimulus Types3 2Nontarget0Standard Deviations3 3 Anterior-to-Posterior@A# 3 5Lateral@L# Electrodes!. The electrode factors were arranged suchthat the lateral~coronal! electrode arrays were nested under theanterior-to-posterior factor locations~F7–F3–Fz–F4–F8 vs. T7–C3–Cz–C4–T8 vs. P7–P3–Pz–P4–P8!, which yielded two orthog-onal electrode factors. This approach permitted the direct assessmentof interactions between the frontal-to-parietal topography distribu-tions across lateral electrode with respect to the experimental in-dependent variables. To promote descriptive simplicity and to avoidunnecessary repetition on the previous midline electrode findings,only the significant effects involving lateral electrode factor arereported here.

The analysis on P300 amplitude from the easy task indicatedthat the midline maximum effect~L!, F~4,44! 5 37.4,p , .001,e 5 0.46, increased from the frontal to parietal electrode site, toproduce a significant A3 L interaction,F~8,88! 5 9.3,p , .001,e 5 0.33. This pattern showed stronger P300 amplitude for thetarget than for the nontarget to produce significant three-way~S 3A 3 L!, F~8,88! 5 5.8,p , .002,e 5 0.43, and two-way~S 3 L!,

Figure 4. Mean P300 peak latencies from the target and nontarget stimuli in each task condition as a function of coronal electrode sitefor the frontal, central, and parietal electrode positions~LL 5 left lateral, LM5 left medial, M5 midline, RM5 right medial, RL5right lateral!.


F~4,44! 5 20.7,p , .001,e 5 0.35, interactions. In addition, thistendency was stronger for large than for small nontarget0standarddeviation, which also produced a significant interaction of thenontarget factor~N 3 L!, F~4,44! 5 6.9,p , .02,e 5 0.37. Theseoutcomes stemmed from the fact that nontarget stimulus in easy0small condition elicited the P300 without the midline tendency.

Analysis of component amplitude from the difficult task foundthat the midline tendency was stronger for large than for smallnontarget0standard deviation~N 3 L!, F~4,44! 5 6.6,p , .01,e 50.46, and the effect increased from the frontal to parietal electrode~A 3 L!, F~8,88! 5 11.6,p , .001,e 5 0.47. The main effect oflateral electrode also was significant,F~4,44! 5 49.1,p , .001,e 5 0.38. However, there were no significant interactions includ-ing stimulus type factor.

Latency data were analyzed separately for easy and difficulttasks with the same four-factor analysis as calculated for amplitudedata. There were no main effects of lateral electrode or interactionsincluding lateral factor in both analyses.

Discussion

Reaction time and hit rate results confirmed the successful manip-ulation of task difficulty by varying the tone pitch differencesbetween the target and standard stimuli. When the target was sim-ilar in pitch to the standard tone, reaction time increased and hitrate decreased compared with when the target was very differentfrom the standard. Furthermore, the behavioral data also indicatedthat there was no effect of nontarget0standard deviation magnitudewhen the task was easy. When the task was difficult, however,small nontarget0standard differences produced increased reactiontime and decreased hit rate. Thus, when both the target and non-target were very similar to the standard tone, the participant had toprocess all stimuli to perform the task; when the nontarget wasvery different from the other tones, the participant could easilyreject the very deviant nontarget and make a decision based solelyon the other two tone types.

Target P300The target tone in each task condition elicited a P300 componentthat was largest over the parietal and midline electrode sites. Thetarget P300 was affected by target0standard discrimination diffi-culty. When the target was very similar to the standard, amplitudedecreased and latency lengthened—a result in agreement with re-ports using a two-tone oddball paradigm~Ford et al., 1976; Polich,1986, 1987!. This outcome supports the previous finding that thetarget P300 elicited in the three-tone paradigm is essentially iden-tical to the target P300 from a two-tone oddball or a single-stimulus auditory paradigm~cf. Katayama & Polich, 1996a; Polich& Heine, 1996; Polich et al., 1994!. Thus, the results indicate thatthe target P300~P3b! obtained in this study is the same as a P300elicited in the traditional two-tone oddball task.

The analyses of component amplitude, vector length, and la-tency measures clearly indicated that target P300 was affectedprimarily by variables contributing to the target0standard discrim-ination difficulty, whereas nontarget deviation magnitude did notaffect target component amplitude or latency. These findings ex-tend previous results in which the target P300 from a three-toneparadigm was determined only by the eliciting stimulus probabilityand was not affected by the probability configuration of the twonontarget tones~Katayama & Polich, 1996b!. However, the presentP300 findings disagree with the behavioral data, which suggest aninfluence of nontarget0standard deviation magnitude in the diffi-

cult task conditions. Longer reaction time and lower hit rate werefound in the difficult0small compared with the difficult0large con-dition. Based on the view that P300 latency is proportional tostimulus evaluation time~Kutas et al., 1977; Magliero et al., 1984;Polich, 1987; Ritter, Simpson, Vaughan, & Macht, 1983!, the timerequired for evaluating the target was independent of the nontargetvariables, although reaction time increased with increases innontarget0standard tone similarity because P300 latency to thetarget was not affected. Given this interpretation, the increasedreaction time might reflect posttarget classification processes, suchas reconsideration of whether the stimulus is a target. Furthermore,target P300 amplitude also was unaffected by the nontarget con-figuration, suggesting that component amplitude may reflect onlyattentional resources specific to target classification but not allaspects of the processing for performing the task.

Finally, the target P300 from difficult conditions showed twosubcomponents, which are most clearly observed in the difficult0large condition~upper part of the Figure 2!. The results are inagreement with the recent reports by Falkenstein et al.~1993,1994, 1995; Hohnsbein et al., 1991!, who demonstrated two P300subcomponents: an early central and later parietal peak, the pari-etal peak being observable only in a difficult task condition forchoice or go0no-go paradigm. Although the two P300 peaks of thepresent study were not assessed separately because of the peakidentification method used, latency data showed the early peakswere primarily picked up at frontal electrodes for difficult condi-tions ~Figure 4!. The amplitude of the later peak was smaller thanthat of the early peak at the frontal electrodes, so that the strongerparietal tendency for the difficult compared with the easy condi-tions would be obtained even if the later component amplitude wasassessed. In addition, Falkenstein et al.~1994! discussed the earlysubcomponent does not contribute to P3a but does affect P3b.Inspection of ERPs from the difficult0large condition indicate thatthe scalp distribution of the early component for the target P300 isdifferent relative to that for the nontarget P300 in this condition.Thus, it can be assumed that the early subcomponent of the targetP300 from the difficult conditions was different from the nontargetP300 in the difficult0large condition.

Nontarget P300The nontarget tone P300 amplitude was different in each taskcondition, although nontarget P300 latency was determined onlyby the nontarget0standard pitch difference without the effects oftask difficulty. When the nontarget deviation magnitude was small,component latency increased compared with when the deviationwas large. Given that P300 latency is an index of stimulus classi-fication time, only the amount of pitch difference affected thenontarget classification time.

In the easy0small condition, the nontarget elicited a very smallP300 because the target discrimination was easy, and the partici-pant would only be required not to respond to the standard andsimilar nontarget. Hence, the participant could adjust the allocationof attentional resources so that the different target stimulus wasreadily processed but not enough to discriminate nontarget tonesfrom the standard.

In the easy0large condition, the nontarget elicited a smaller P300than the target stimulus but produced a parietal maximal amplitudedistribution. There was no difference between target and nontargetP300 latency in this condition. The difficult0small condition dem-onstrated a similar pattern of amplitude and latency results. In thesetwo conditions, the target and nontarget pitch differences from thestandard were the same—both large or both small. These P300 re-


sults are in close agreement with previous three-tone paradigm find-ings~Grillon et al., 1990; Katayama & Polich, 1996a!, although somestudies observed longer P300 latencies for the nontarget than for thetarget components~Pfefferbaum et al., 1980, 1984!, whereas no la-tency differences between the target and nontarget components werefound in the present study. Katayama and Polich~1996b! also re-ported no latency effects on both P300s and attributed the results totheir relatively long interstimulus interval and easy discriminationtask for both the target0standard and nontarget0standard. These find-ings suggest that a major determinant of the nontarget P300 latencymay be duration of the interstimulus interval and not task diffi-culty per se, because even when the task was difficult P300 latencyfrom the nontarget was the same as that from the target stimulus~cf. Katayama & Polich, 1996a, 1996b; Pfefferbaum et al., 1980,1984!. Given the present and previous findings, the nontarget P300component observed in these two conditions can probably be con-sidered as a P3b.

P3a RevisitedPerhaps the most interesting results occurred in the difficult0largecondition. The nontarget tone in this task elicited an anterior P300.In this condition, the target was very similar to the standard so thatthe target0standard discrimination was difficult, whereas the non-target0standard deviation was very large. Hence, this manipulationof nontarget0standard tone stimulus context produced a task envi-ronment in which the nontarget stimulus quickly engaged focal at-tention in a manner similar to that observed previously for highly“novel” stimuli ~Courchesne et al., 1975, 1978; Friedman & Simp-son, 1994; Friedman et al., 1993; Knight, 1984, 1987!. The anteriormaximum nontarget P300 of the present study can, therefore, be con-sidered as a manifestation of the P3a, which may be the same as thenovelty P300~cf. Snyder & Hillyard, 1976; Squires et al., 1975!.The present findings suggest that the context in which stimuli arepresented—their similarity, probability of occurrence, and so forth—contribute to the final P300 distribution and latency~Donchin, 1981;Donchin et al., 1986; Picton, 1992!. Thus, it may be possible to pro-duce an anterior P300 potential without using novel stimuli per se,although additional research is required to examine the other char-acteristics that contribute to this component~e.g., habituation rate,interstimulus interval, etc.! to support a firm conclusion about theanterior nontarget P300 observed in the present study.

Another possible interpretation of the anterior P300 in thiscondition comes from the no-go P300 task, in which the participantis presented with visual stimuli and instructed to produce~go! orto inhibit ~no-go! a motor response. In this context, the no-gostimulus produces a central maximum P300, whereas the go stim-ulus produces a parietal P300~Falkenstein et al., 1995; Pfeffer-

baum & Ford, 1988; Pfefferbaum, Ford, Weller, & Kopell, 1985!.Although the present study’s nontarget deviation of the difficult0large condition was very distinctive, the participants were forced toinhibit their tendency to press a button to the nontarget tone~i.e.,a no-go response!, so that the present anterior P300 may be relatedto the no-go P300. However, the present study observed an ab-sence of no-go P300 potentials in the other conditions in which thenontarget elicited the parietal P300~Eimer, 1993; Falkensteinet al., 1994!. In previous studies, the discrimination between the goand no-go stimuli was very easy and was similar to the easyconditions of the present study. In addition, no-go P300 latenciesare typically longer than go P300 latencies, but in the present casetarget P300 latency was longer than nontarget latency. In sum,these results imply the present anterior P300 is not a variant of theno-go P300.

P300s in the Three-Stimulus Oddball TaskTarget P300 amplitude and latency demonstrated similar tenden-cies across experimental conditions, the magnitude of which de-pended on the task difficulty independent of the nontarget stimulusconfiguration. Nontarget P300 latency was determined primarilyby the nontarget deviation magnitude from the standard in all fourtask conditions. In contrast, nontarget P300 amplitude was muchmore sensitive to stimulus context as defined by the combinationof target discriminability and nontarget deviation magnitude. Theo-retically, the neural representation of the stimulus environmentprovides the “context” upon which attentional processes operate. Ifthis context is defined primarily by a difficult target0standard dis-crimination, attentional redirection to the nontarget would occur bymeans of frontal lobe activation that may underlie short-latencyP3a components~Pardo et al., 1991; Posner & Petersen, 1990!. Arelatively easy target0standard discrimination, however, would mit-igate this effect because the stimulus context would not demand asmuch attentional effort so that the nontarget stimulus could morereadily be ignored~Katayama & Polich, 1996a, 1996b!. Althoughthe neural loci of these operations is still unknown, hippocampalinvolvement for both P3a and P3b generation has been reported~Knight, 1996; Johnson, 1993; Polich & Squire, 1993!. If the neuro-electric events that underlie P300 generation are related to frontallobe and hippocampal function, as has been suggested~Knight,1990; Polich et al., 1997!, it is reasonable to suppose that taskcondition manipulations such as those used in the present studycan be used to assess this possibility directly. Thus, the three-stimulus oddball paradigm appears to produce a rich set of exper-imental possibilities for delineating the cognitive processes engagedwhen a well-defined stimulus context is confronted by an un-expected event.

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~Received December 2, 1996;Accepted May 12, 1997!


stimulus context determines p3a and p3b

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