On the Relationship of P3a and the Novelty-P3

 Robert F. Simons, Frances K. Graham, Mark A. Miles & Xun Chen

University of Delaware

The research was supported by a grant from the National Institute of Mental Health (MH42465) to Frances K. Graham and Robert F. Simons and contains aspects of both the Ph.D. dissertation of Mark A. Miles and the MA  thesis of Xun Chen.  Portions of this paper were presented at the 39th annual meeting of the Society for Psychophysiological Research, Granada, Spain, October, 1999.

Address correspondence to Robert F. Simons, Department of Psychology, University of Delaware, Newark, DE 19716.

 

Contents

Abstract

Deviant stimuli give rise to a late positive ERP component with latencies from 250-400 ms.  Target deviants elicit a P300 with maximum amplitude over parieto-central recording sites while the ‘P300’ elicited by deviant nontarget stimuli occurs somewhat earlier and shows a more frontally-oriented scalp distribution.  Two varieties of frontal P300s have been described, elicited either by rare stimuli (target or nontarget) presented in a two-stimulus oddball task (P3a) or by infrequent, unrecognizable stimuli presented in the context of a three-stimulus oddball task (Novelty-P3).  The Novelty-P3 has been observed in a number of subsequent studies; the P3a has not been extensively studied and both its significance and existence have been called into question.  The present report describes a replication of two prototypical studies with ‘frontal’ P3s observed in each context.  Application of factor analysis to the two sets of ERP waveforms does not support a distinction between these two components.

Introduction

In 1975, two papers were published that reported the existence of positive ERP components that were either antecedent or temporally coincident with the oddball-elicited P300 (Courchesne, Hillyard & Galambos, 1975; Squires, Squires & Hillyard, 1975).  In both papers, the positivity had a more anterior scalp distribution than the parieto-central distribution that characterized the traditional P300.  The component described by Squires et al. was referred to as the P3a and was observed in response to infrequent stimuli during an oddball task or to the same stimuli when unattended; Courchesne et al. described a component they labeled the Novels-P3 that they observed in response to rare, unexpected stimuli inserted unexpectedly as a third stimulus type during an otherwise traditional oddball task.  They initially argued that it was the relative uncodability of their novel stimuli that prompted the more anterior P3 response, but it has been subsequently demonstrated by Polich and colleagues (Comerchero, Katayama & Polich, 2000) that codability is not a necessary stimulus characteristic. 

Research on the Novels-P3 (which we will refer to as the Novelty-P3) has been vigorous and the basic phenomenon has been demostrated in many laboratories (e.g., Cycowicz & Friedman, 1999; Katayama & Polich, 1998; Knight, 1984; Mecklinger & Ullsperger, 1995; Spencer, Dien & Donchin, 1999) using visual (Comerchero & Polich, 2000), acoustic (Courchesne et al., 1984), and tactile stimuli (Knight, 1996) with little apparent difference across modalities.  Knight & Scabini (1998) describe the Novelty-P3 as an ERP measure of “neural activity in a distributed multimodal corticolimbic-orienting system that processes novel events”.   

The P3a is a more evanescent component (Squires et al., 1977; but see also Snyder & Hillyard, 1976) and research targeting the P3a, qua P3a, has waned.   There are no studies in the literature that directly compare the P3a and the Novelty-P3 and it is increasingly common for the two labels to be used interchangeably.  In some recent papers, for example (Clark et al., 2000; Comerchero & Polich, 2000; Knight, 1996), P3a explicitly refers to announced deviants in three-stimulus attention tasks while in other papers (Harmony et al., 2000; Kaipio et al., 2000; Mathalon, Ford & Pfefferbaum, 2000) P3a is used in its more traditional sense (i.e., as in Squires et al., 1975).

The existence of these more frontally oriented positive components in addition to the more commonly observed parietal (P3b) component has important theoretical implications relevant to attention and orienting and distinctions between the two frontal components may be important as well.  To date, however, evidence that these two frontal positivities are distinct and independent has been largely anecdotal or based on preliminary speculations of Courchesne et al. (1975).   Because much of this evidence favoring a distinction has not withstood empirical scrutiny (see Discussion) and because of the confusion in terminology, we undertook the present analysis to revisit the two components and to address the nature of their relationship.   As part of two independent projects, we elicited the P3a and the Novelty-P3 with prototypical procedures, conducted factor analyses of the data sets containing the two components, then employed a variety of methods recommended by Roemer, Josiassen & Shagass (1990) for determining whether the principal components and their associated factor scores based on the two sets of ERP waveforms span the same or different factor space.  To remain consistent with the initial description and labels of the two components, we refer to P3a as the anterior positivity that is elicited by rare stimuli in traditional two-stimulus oddball tasks and the Novelty-P3 as the anterior positivity elicited by the unexpected novel stimuli delivered to  subjects during three-stimulus novelty tasks.

Methods

Subjects

Nine University of Delaware undergraduate students (6 female) served as subjects in the replication of Squires et al. (1975) and were paid $5.00/ hour for their participation.   Four additional volunteers were excluded – one had a recent loss of consciousness, one for a hearing disability that made pitch discrimination too difficult, and two for apparatus problems.  Twenty-four undergraduate subjects participated in the replication of Courchesne et al. (1975) and these subjects received either course credit or were paid at $5.00 per hour.  The data from one subject was lost due to apparatus failure.  Nine subjects (6 female) were randomly selected from the remaining group of twenty-three and the data from these subjects were retained for the present analysis.  None of the nine subjects had participated in the Squires task.

Procedure

Because Courchesne et al. (1984) and numerous others have observed the Novelty-P3 in response to acoustic stimuli and because we wished to avoid any possible modality confound in our analysis of the two components, the procedures we employed to elicit the relevant ERPs were exclusively acoustic.  Exact replication of the Squires et al. (1975; Experiment 2) procedures were used to elicit the P3a.  Two 70 dB (A) acoustic stimuli, differing in pitch (1000 Hz & 1500 Hz) were presented in a random sequence.  Stimulus duration was 50 ms and the inter-stimulus interval was 1.1 s.  In different blocks of stimuli, the probability of the 1500 Hz tone was 0.1, 0.5, and 0.9.  The probability of the 1000 Hz tone was complimentary.  Subjects were instructed to count the high tone, the low tone or to ignore all tones in different blocks.  The resulting nine blocks (three probability levels X three instructions) were presented twice, in reverse order .

Three acoustic stimuli were employed in the Courchesne replication and were presented to subjects during three trial blocks of 170 trials each.  Two of the stimuli were synthesized speech sounds (‘me’, ‘you’) and the third was novel – described by Courchesne et al. as “a patchwork of natural sounds consisting of human vocalizations, mechanical noises and digitally synthesized nonsense sounds”.  All stimuli used in this procedure were digitized from an audiotape obtained directly from E. Courchesne.  The duration of each stimulus was 200 ms; they were presented at 75 dB (A) with inter-trial intervals of 1700 ms.  During the first block of trials, only ‘me’-standards (p=0.9) and  ‘you’-targets (p=0.1) were presented.  In a second block of trials, a single exemplar of the novels category was introduced, unannounced, and presented on 10% of the trials interspersed with targets (p=.10)  and standards (p=0.8).  During a third block of trials, novels again constituted 10% of the trials, but in this case, each novel was unique.  The order of the second and third trial-blocks was counterbalanced across subjects and the novels and targets were matched for ordinal position within each block.  As in the Squires task, subjects were instructed to simply count targets1. 

Data reduction and analysis

As in the Squires at al. (1975) and Courchesne et al. (1975, 1984) studies, EEG was recorded from three midline recording sites (Fz, Cz, and Pz) referenced to the right mastoid.   The EEG (.5-35 Hz) was digitized at 500 cps and corrected for vertical eye movement and blink artifact (Gratton, Coles & Donchin, 1983; Miller, Gratton & Yee, 1988).  From the Squires task, ERPs were retained from the four 200 stimulus blocks in which subjects were instructed to count the infrequent stimuli (p=0.1; either high or low tone) and the four 200 stimulus blocks in which subjects counted the frequent stimuli.  Averages were then computed at each electrode site for rare target, rare nontarget, frequent target and frequent nontarget stimuli.  From the Courchesne task, ERPs were retained for all eight instances of standard, target and novel stimuli. 

To evaluate the similarity of the P3a and the Novelty-P3 in the manner suggested by Roemer et al. (1990), the twenty-four ERP averages from the two data sets were combined and submitted to factor analysis (PCA) using the covariance matrix.  The PCA was conducted twice. The first PCA computed basis waves solely from the ‘Squires’ ERPs and used these basis waves to compute factor scores for all ERPs in the combined data set.  The second PCA used only ‘Courchesne’-derived basis waves for the computation of the factor scores.  To better visualize the late positive components in the factor space, the PCA was restricted to the epoch from 220-420 ms following stimulus onset.  

Results

The ERP waveforms from the two data sets are presented in Figure 1 (left).  The ERPs recorded in the Squires et al. paradigm are consistent with the description provided in the original article of ERPs elicited by rare stimuli.  The P3a can be seen as a small deflection on the leading edge of the much larger, parieto-central P3b.  ERPs recorded in response to the Courchesne et al. stimuli are more centrally focused and the late positive components are less distinct, one from the other.  Thus, although both sets of ERPs are associated with prominent late positive components, their morphologies differ, at least superficially, and the substantial  component overlap obviates a direct comparison of the early positive component based on direct measurement of the ERP waveforms themselves.  

Roemer et al. (1990) suggest two criteria for concluding that two sets of ERPs have identical factor structures; one criterion is based on the basis waves, the second is based on the factor scores.  The first criterion is to determine the relationship between the basis waves of the two data sets by computing either canonical or multiple correlations.   Statistically, this approach evaluates the extent to which the PCA of one data set spans the solution based on the second data set.  To this end, we computed an R2 between each basis wave (factor) of the first data set with all basis waves of the second set and then repeated the procedure moving in the opposite direction.  The results of this analysis are presented in Table 1.  As the data indicate, the four basis waves obtained from ‘Squires’ are accounted for almost perfectly by the basis waves of “Courchesne” and vice versa.  All R2 values exceed 0.95, strongly suggesting that the two data sets have equivalent factors in the 220-420 ms data epoch. 

The second method of exploring the similarity of the two factor structures, based on factor scores, involves the computation of simple correlations between the factor scores derived from a basis wave from the first data set and factor scores of one or more basis waves from the second data set.    The results of this analysis are presented in Table 2.  Particularly important to the present question is the relationship between the P3a factor in ‘Squires’ and the Novelty-P3 factor in ‘Courchesne’.  The high correlation between the two (r=0.80) suggests that the two basis waves, though obtained with different subjects in a different experimental context, produce nearly equivalent factor scores.

To augment the criteria suggested by Roemer et al., we also conducted ANOVAs on the data from each set using both sets of derived factor scores.  That is, we analyzed the data from each experiment twice.  The first analysis of each data set employed factor scores derived from basis waves indigenous to the data set.  Factor scores for the second analysis were derived from the complimentary set of basis waves.  The logic of this procedure is that an identity of P3a and the Novelty-P3 factors should yield identical ANOVAs regardless of which basis waveforms underlie the factor scores.  The results are presented in Figure 2 (Means) and Table 3 (ANOVA).  On the top of the figure are the Stimulus (rare targets vs. rare nontargets) X Site P3a means obtained in the “Squires” procedure.  The left-hand panel reflects the use of the ‘Squires’ basis waves; the data on the right were generated using the ‘Courchesne’ basis waves.  In both cases, the early positivity had a central focus (though it was more linear when computed as S:C than from S:S) and did not differ when elicited by either target or nontarget rare stimuli (Table 3).  Similarly, the bottom panel of Figure 2 depicts the central focus of the early positive component observed during Courchesne’s novelty task and the significant impact of novel stimuli on this component.  Again, the Stimulus (targets vs. novels) X Site effects were virtually identical when analyzed using either the “Squires” or “Courchesne” basis waves to generate the factor scores (Table 3).

Finally, we compared the (midline) scalp distribution of the P3a and the Novelty-P3 by scaling the data from each set for each condition according to the min/max method described by McCarthy and Wood (1985).  The data are presented in Figure 3.  The distribution across the midline had significant linear and quadratic components (Flin=(1,16) = 7.20, p<.05; Fquad(1,16) = 89.74, p<.001) in the two tasks, with the quadratic trend accounting for nearly 80% of the location variance.  The midline distribution did not interact with stimulus type (F(2,32) < 1) and most importantly, the midline distribution of the respective factor scores did not vary with task (F(2,32) < 1) – i.e., the distribution of the P3a factor scores and the Novelty-P3 factor scores were statistically indistinguishable.

Discussion

The present data analysis was undertaken to address the question of independence of two positive ERP components that precede and overlap the ubiquitous P3b component during two and three stimulus oddball tasks.  Our results suggest that these components are very similar, potentially the same.  To recapitulate the evidence, despite the apparent morphological difference in the ERP waveforms (Figure 1, left), the factors identified as the P3a and the Novelty-P3 appear identical to the eye (Figure 1, right).  More important, multiple regression shows that basis waves from the two data sets are highly correlated and the factor scores derived from the two sets of basis waves are highly correlated as well.  The multiple regression analysis suggests that the principal components from the P3a data set span the same factor space as those derived from the Novelty-P3 data set (Roemer et al., 1990).  Then, the results of ANOVAs using factor scores as dependent measures were equivalent in all essential aspects regardless of which data set produced the basis wave that generated the factor scores corresponding to the P3a or the Novelty-P3.  Lastly, when the factor scores were scaled to eliminate main effects and evaluate the midline distribution more directly (McCarthy & Woods, 1985), distributional differences did not approach statistical significance.

As part of the initial description of the Novelty-P3, Courchesne et al. (1975) argued that there was little connection between it and the P3a described by Squires et al. (1975).  This assertion, unchallenged for the most part, was based on four observations.  First, the Novelty-P3 occurred under conditions of active attention while P3a occurred during passive attention.  Second, the Novelty-P3 habituated while habituation of P3a was not noted by Squires et al.  Third, the Novelty-P3 was elicited only by complex, unrecognizable stimuli while P3a was elicited by simple stimuli.  Fourth, P3a occurred earlier and was smaller than the Novelty-P3.  Although space does not permit a detailed discussion of these issues, it should be noted that latency and amplitude differences are insufficient criteria for independence, that Katayama and Polich (1998) have convincingly demonstrated that the Novelty-P3 can be elicited by simple acoustic stimuli, that P3a is observed under both passive and active attention conditions (Snyder & Hillyard, 1976; Squires et al., 1975) and that while habituation of the Novelty-P3 has been amply demonstrated (e.g., Knight, 1996),  habituation of the P3a has never been systematically studied. 

We appreciate the difficulty of establishing an identity – it is, of course, akin to ‘proving’ the null hypothesis.  In general, null hypothesis significance testing and typical publication criteria favor distinctions rather than identities.  Furthermore, our comparison of the two components has inherent limitations.  We limited our measurement to the three midline sites employed in the original studies and we employed a relatively small sample of subjects.  A more elaborate recording montage might be more sensitive to subtle between component differences that are not apparent on the midline.  Likewise, the enhanced power that accompanies an increase in sample size may have highlighted midline differences that we were unable to detect with nine subjects per condition.   To compensate for these limitations, we examined the two components from multiple vantage points.  Based on the present analysis, we would argue that the P3a and the Novelty-P3 may be indistinguishable.   While we acknowledge the limitations of our study and all the difficulties inherent in supporting the null hypothesis, our conclusion is nonetheless consistent with recent data from other laboratories.  Knight (1996), for example, presented novel tactile or acoustic stimuli to subjects unannounced during a standard target-detection task.  The novel stimuli prompted a substantial anterior P300 (Novelty-P3) while rare target stimuli were associated with a typical P3b.  Knight noted, as did Squires et al. (1975) under target-detection conditions, that the P3b was preceded by a small, fronto-central positivity (P3a; see also Figure 1 above).  Subjects with posterior hippocampal lesions had a normal P3b, but a markedly reduced Novelty-P3.  Especially relevant to the identity question, Knight observed that hippocampal damage also eliminated the P3a that was associated with the rare targets.   Likewise, studies of patients with Parkinson’s disease have found amplitude reductions over frontal recording sites in the Novelty-P3 (Tsuchiya, Yamaguchi & Kobayashi, 2000) and a virtual absence of the early positive peak (P3a) associated with rare targets in the traditional oddball task (Lagopoulos et al., 1998).  And, using a high-density electrode array, Spencer, Dien & Donchin (in press) identified a Novelty-P3 factor based on a combination of temporal and spatial information that was evident in response to both ‘novel’ stimuli and to rare targets. 

In sum, we believe that the arguments originally marshaled in support of the distinction between the Novelty-P3 and the P3a have not been empirically supported, and we believe that new data such as those obtained from our own factor analysis, those obtained from high-density electrode arrays, and those obtained from patients with neurological lesions are more consistent with an identity hypothesis and now shift the burden of proof back to those who wish to continue a case for distinction.   


References 


Footnote

1.  Discriminating among the stimuli was an easy task.  Thirteen of the 18 subjects were completely accurate, three subjects were within plus or minus 1 of the correct count for the experiment.  Two subjects were confused by the introduction of the unexpected novels during the Courchesne task, but quickly righted themselves and made no additional errors.  The overall error-rate did not differ in the two procedures.  

 

 

 

 

 

 

 

 

 

 

 


 Figure Captions

Figure 1.  ERP waveforms (left) and PCA basis waves (right) obtained from infrequent targets during the Squires (top) task and infrequent nontargets/novels during the Courchesne (bottom) task.  PCA was conducted during the 220-420 ms epoch following stimulus onset and four factors were extracted from each data set.

Figure 2.  Factor scores for Squires- (top) and Courchesne-task (bottom) data.  Two sets of factor scores were computed:  The first associated with the basis wave corresponding to P3a in the Squires (:S) replication and the second associated with the Novelty-P3 from the Courchesne (:C) replication.

Figure 3.  Scaled factor scores for Squires- (left) and Courchesne-task (right) data.  Scores were scaled using the McCarthy & Woods (1985) min/max procedure separately for each stimulus condition removing all main effects other than electrode location.

 

 

 

 

 

 

 

 

 
Table 1.
  Relationships (Multiple Correlations) between PCA basis waves (factors) obtained from ERPs elicited in the Squires and Courchesne tasks.

 

Factor

C:Sa

S:Cb

1

0.992

0.962

2

0.984

0.992

3

0.996

0.986

4

0.951

0.983

 

aC:S – entire set of basis waves derived from the Courchesne-task data is correlated with each basis wave from the Squires-task data

bS:C – entire set of basis waves derived from the Squires-task data is correlated with each basis wave from the Courchesne-task data

 

 

 


Table 2.  Product-moment correlation coefficients between factor scores based on PCA of the Squires-task and Courchesne-task data sets.  Factor 2 refers to the Novelty-P3 in the Courchesne-task and the P3a in the Squires task.

 

 

C: Factor 1

C: Factor 2

C: Factor 3

C: Factor 4

S: Factor 1

.56

-.15

.83

.07

S: Factor 2

.21

.80

-.12

-.27

S: Factor 3

-.09

.28

.13

.90

S: Factor 4

.60

.01

-.41

.05

 

 

 

 

 


Table 3.  Results of analysis of variance of the P3a and Novelty-P3 factors derived from the Squires- and Courchesne-task data sets.

 

Procedure

Analysis

ANOVA Factor

 

 

Squires

 

 

S:Sa

Stimulus

df=1, 8

Site

df=1, 8

Stim X Site

df=1, 8

 

F < 1

Flin=2.4, p > .10

Flin < 1

Fquad=9.5, p < .05

Fquad=2.2, p > .10

 

S:Cb

 

F < 1

Flin=15.3, p < .01

Flin < 1

Fquad=7.3, p < .05

Fquad=1.4, p > .10

 

 

Courchesne

 

 

C:Cc

 

F = 6.6, p < .05

Flin=4.4, p > .05

Flin < 1

Fquad=39.9, p <.01

Fquad < 1

 

C:Sd

 

F = 6.7, p< .05

Flin < 1

Flin=2.0, p > .10

Fquad=32. 9, p < .01

Fquad=4.9, p > .05

aS:S – P3a factor derived from Squires-task basis waves

bS:C – P3a factor derived from Courchesne-task basis waves

cC:C – Novelty-P3 factor derived from Courchesne-task basis waves

dC:S – Novelty-P3 factor derived from Squires-task basis waves

 

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