447
Electroencephah)graphy and clinical Neurophysiology, 1991, 7 8 : 4 4 7 - 4 5 5 '~ t991 Elsevier Scientific Publishers Ireland, Ltd. 0013-4649/91/$03.50 A D O N I S 0013464991001012
EEG 89609
Effects of crossmodal divided attention on late E R P components. II. Error processing in choice reaction tasks M. Falkenstein, J. Hohnsbein, J. Hoormann and L. Blanke lnstitut fi;tr A rbeitsphysiologie, A bt. Sinnes- und Neurophysiologie, D-4600 Dortmund ( F. R. G.) (Accepted for publication: 6 August 1990)
Summary Reaction times and event-related potentials in correct and incorrect trials were studied in a bimanual choice reaction task. In a focused attention (FA) condition, the stimulus modality was constant (visual or auditory); in a divided attention (DA) condition, the modality was varied at random from trial to trial. Stimulus- and response-triggered averages were computed from the midline EEG leads. In error trials, the ERP amplitude was reduced in the P300 range (300-500 msec) and enhanced in the slow wave range (500-700 msec) compared to correct reaction trials. Difference plots between the ERPs (incorrect minus correct reaction trials) revealed a large fronto-central negativity ( " N ~ " ) and a parieto-occipital "'slow wave." These components appeared larger in the response-triggered averages. We believe that they reflect two different stages of error processing. After auditory stimuli the N E peaked m u c h later for D A than for FA, which supports the idea of an asymmetrical allocation of processing resources to the disadvantage of the auditory modality in our D A condition. Key words: Error processing; Divided attention; Choice reaction; Event-related potentials
Relatively little is known about error processing, i.e., the cognitive processes leading to, or following, incorrect responses. Moreover, the influence of attentional mechanisms on information processing stages may be different in trials that yield correct and incorrect responses. We propose that the event-related potential (ERP) may be a valuable tool for analyzing such differences. Surprisingly, very few studies explicitly focus upon ERP differences between correct and incorrect reactions in choice reaction tasks. Renault et al. (1980) found larger N200-P300 amplitudes in erroneous trials as compared to correct ones in a bimodal choice reaction task. Two studies applied feedback stimuli following "correct" or "incorrect" trials in a time-estimation task (Campbell et al. 1979; Horst et al. 1980). The main findings were larger P300 amplitudes following feedback stimuli with low (as opposed to high) subjective probability. However, the meaning of the feedback stimulus ("correct" or "incorrect" trial) did not influence the feedback-elicited P300. Kutas et al. (1977) found in an oddball task that incorrect responses occurred earlier than correct ones, whereas the latency of P300 remained constant. However, no quantitative ERP data for the incorrect trials were reported. Donchin et al. (1988) repeated and ex-
Correspondence to: Dr. M. Falkenstein, Institut ftir Arbeitsphysiologie, Abt. Sinnes- und Neurophysiologie, Ardeystr. 67. D-4600 Dortmund (F.R.G.).
tended the Kutas et al. study. In error trials they found a P300-1ike positivity which peaked later than the P300 in correct trials. This finding was interpreted by postulating a delay of the P300 in error trials, caused by the processing of the error. However, other interpretations, such as a second P300 in error trials, were also considered by the authors (see also Donchin 1984, p. 254-285). Coles et al. (1985, 1988) presented resuhs of a bimanual choice reaction task paradigm in which they differentiated not only between correct and incorrect responses but also between levels of incorrect response tendencies, revealed by E M G and hand squeeze measurements. The incorrect reaction tendencies were induced mainly by incompatible distractors, i.e., incorrect responses were induced by presenting the competing stimulus at the same time as the target. Among other results, the authors found prolonged P300 latencies with rising incorrect response tendency. This is in accordance with the Donchin et al. study. However, Coles et al. interpret their P300 delay as a prolongation of stimulus evaluation time caused by the distractors. Since some of the cited studies are not aimed at the error issue or their results and, more important, their interpretations seem to be controversial, the main aim of the present study was to elucidate the effects of errors on the ERP in a choice reaction task, and to discuss them in terms of error processing. It is very likely that an error, which is an important event, is reflected also in the ERP of error trials. This possibility of an additional process in error trials was also consid-
448 ered by Donchin et al. (1988). These authors postulated a "process that occurs when the subject processes the commitment of an error (a recognition that need not reach the subject's awareness)." However, such a process is not clearly seen in the results of Donchin et al. In order to decide whether possible error effects are related to the stimulus or to the (incorrect) response, we thought that the computation of both stimulus-triggered and response-triggered averages would be helpful, To overcome the problem that the number of trials in which an error occurs is too low to yield usable averages, the error rate was enhanced by a time-pressure regimen. A second question addressed in the present study was whether error processing can be influenced by attention. In the companion paper (Hohnsbein et al., this issue) we reported results from correct trials in a paradigm in which the subjects were forced to divide their attention because stimuli were presented randomly to the visual and auditory systems. Results in that study revealed (i) that response-related processes were impaired by the division of attention, and (ii) that this effect was larger following auditory stimuli. This was interpreted as supporting the idea of an asymmetrical allocation of attention in favor of the visual modality in the divided-attention condition. In the present study we asked whether these conclusions drawn from "correct" trials are confirmed by the RT and ERP results from incorrect trials.
Methods
Procedure The procedure has been described in full detail in the companion paper (Hohnsbein et al., this issue). Eleven right-handed healthy paid subjects participated in the study. The data of 2 females had to be discarded because of alpha activity. The remaining 9 subjects (4 males and 5 females) had a mean age of 24.3 years (range: 15-43). In 4 sessions, single letter stimuli ( " F " or " J " ) were presented to the subjects in r a n d o m order with equal probability. The ISI was randomized in the range of 750-2250 msec. In the focused-attention condition 100 letters were either presented visually (on a TV monitor), or auditorily (via headphones) within one block. In the divided-attention condition 100 visual and 100 auditory stimuli were presented within one block, with the modality varying at r a n d o m with equal probability. The task was to respond to each letter by pressing the appropriate key of a keyboard ( " F " left, " J " right index finger). Time pressure (TP) was induced by a feedback stimulus (a 60 dB SPL tone), which was given when the subject's response did not occur within 550 msec after stimulus onset. The subjects were instructed to react fast enough to avoid the feedback tone, even at the risk of committing errors.
M. FALKENSTEIN ET AL.
Data collection and analysis" The first 2 sessions were practice sessions in which the subjects reached a rather stable performance level. Only the ERP and R T data of the last 2 sessions were pooled across sessions and letters and evaluated. The E E G was recorded from Fz, Cz, Pz, and Oz against linked mastoids, the E O G from the left eye. All data were filtered (0.03-60 Hz) and digitized with 200 samples/sec. The artifact rejection (cf., Hohnsbein et al., this issue) was performed during the off-line averaging. Correct and incorrect trial ERPs were averaged separately. Averaging was performed by using either the stimulus (stimulus-triggered averaging, STA) or the key-press (reaction-triggered averaging, RTA) as trigger. The averaging epochs had a length of 750 msec, of which 400 msec were pre-trigger in the RTA mode. The averaged data were digitally low-pass filtered (cut-off: 17 Hz; Ruchkin and Glaser 1978). Since the number of available trials was about 6 times as large in the "correct" as in the "error" condition, the signal-to-noise ratio was estimated to be a factor f 6 - = 2.45 smaller, and the variance correspondingly larger in the error trials as compared to the correct trials. This variance inhomogeneity may cause problems in amplitude estimation and statistical analysis. The A N O V A is known to be robust against violations of variance homogeneity up to variance ratios of 1 : 1 0 (Lindman 1974, p. 33). Nevertheless, we considered only effects that yielded P < 0.03 to be significant, which we feel is conservative. However, the higher noise levels in error trial ERPs are likely to introduce systematic errors in peak amplitude (but not in latency) estimation, in such a way that the absolute amplitude is overestimated in error-related ERPs. Therefore, the ERP amplitudes were evaluated by a window analysis. The idea was to define ERP windows of fixed length which included certain components and to enter equidistant sample points covering the entire window into A N O V A with sample time (T) in the window as additional factor. Compared to integral measures the window analysis has the advantage of being sensitive not only to mean amplitude differences in the window (main effect of a factor, F), but also to differences between curve shapes (F × T interactions). In our case, the 10-to-10 msec samples of certain E R P windows of 200 msec length (2 windows for each averaging mode) were subjected to 5-way A N O V A s (BMDP4V, Dixon 1983), with the factors electrode (L; levels: Fz, Cz, Pz, Oz). stimulus modality (M; visual, auditory), attention (A; focused, divided), response correctness (C; correct, incorrect) and sample time (T; 20 levels). In addition to the window analysis, the latency of the largest relative m a x i m u m at Pz in the window 300-500 msec of the stimulus-triggered averages was measured as the P300 latency. The latency values were subjected to a 3-way A N O V A (design: M, A, C). Difference
ERROR PROCESSING A N D ERPs
449 VIS
waves between correct and incorrect ERPs were also computed. The peak latency values at Cz of the negative component of the difference wave (see below) were subjected to A N O V A (design: M, A). Reaction time (RT) was recorded in each trial. The mean RTs were subjected to a 3-way A N O V A (design: M, A, C). The error rates were likewise subjected to an A N O V A (design: M, A). For all ANOVAs the degrees of freedom were corrected by using the GreenhouseGeisser procedure, which is included in BMDP4V.
0
Results
Behavioral data Table I presents the reaction time (RT) results and the error rates. The mean RT was about 20 msec shorter in error than in correct trials ( P = 0.0003). Moreover, it was longer for divided than for focused attention ( P = 0.0003). This difference was larger for auditory (68 msec) than for visual stimuli (17 msec) which was reflected in the modality x attention interaction ( P = 0.0004). This asymmetry was not different for correct and error trials (the modality x attention x correctness interaction was not significant). The error rate was about 15%. It did not differ significantly across conditions.
200
g.O0
AUD
600
ms
0
200
&O0
600
ms
Fig. l. Stimulus-triggered single trial (upper panel) and averaged ERPs (lower panel) for correct (thin lines) and error trials (heavy lines) for one representative subject (focused-attention condition; the averaged ERPs are from the two recording sessions). Left panel: visual ERPs; right panel: auditory FRPs.
E R P data Fig. 1 gives typical examples for single sweep and stimulus-triggered averages (STA) for one representative subject, showing large differences between correct and incorrect trials for both modalities. In general, an amplitude reduction in the range of about 300--500 msec and a late positive wave in the range of about 500-700 msec was seen in error compared to correct trials.
"FABLE 1 (A) Mean reaction times (in msec) and (interindividual) S.D.s (in parentheses) to visual and auditory stimuli for incorrect and correct responses. e = percentage of errors; FA = focused attention; DA = divided attention. (B) ANOVA results for the RTs. Incorrect
e
Correct
Mean
Visual FA DA
347 (30) 367 (21)
16.0 15.4
378 (28) 392 (17)
363 380
Mean DA FA
357 20
385 14
371 17
Auditory FA DA
323 (40) 387 (35)
332 (29) 403 (27)
328 395
Mean D A - FA
355 64
368 71
362 68
(A)
16.5 14.9
(B) Source
af
F
P
Modality (M) Attention (A) Correctness (C) MxA MxC AxC MxAxC
1,8 1, 8 1, 8 1, 8 1, 8 1,8 1,8
1.98 36.78 36.68 32.72 5.27 0.06 1.64
ns 0.0003 0.0003 0.0004 0.0508 ns ns
450
M. F A L K E N S T E I N
Figs. 2 and 3 show the grand means of the visual and the auditory ERPs. The stimulus-triggered averages (STA) are given in the left panels of both figures, the A N O V A results in Table II. In correct trials a clear P300 was seen, In error trials the ERP structure was quite different. In the window including the P300 (300500 msec), the amplitude of the ERP was severely reduced compared to "correct" trials ( P = 0.0009). The significant lead × correctness interaction ( P = 0.0003) and the subsequent simple tests for the 4 leads revealed this effect to be maximal at Fz ( P = 0.0002). Despite the amplitude reduction, a positive peak was seen with Pz maximum in the latency range of the correct trial P300. In the window 500-700 msec a positive complex without a distinct peak was seen; the amplitude in the window appeared larger for error than for correct trials, which was significant for Oz only ( P = 0.0122). The positive complex appeared to be later and smaller in the auditory than in the visual ERPs, which was reflected in
VISUAL STA
ET AL.
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Fig, 3. G r a n d m e a n s of the ERPs to auditory stimuli. Refer to legend of Fig. 2 for details.
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Fig. 2. Grand means of the ERPs to visual stimuli (n = 9). Upper panels: focused attention (FA; constant stimulus modality). Lower panels: divided attention (DA; stimulus modality is varied at random from trial to trial). STA: stimulus-triggered averages; RTA: responsetriggered averages. Heavy lines: incorrect trials; thin lines: correct trials. The associated reaction times are given as vertical thin and heavy bars in the STAs (Oz lead).
the modality main effect and the interactions with modality. The P300 latency was clearly different across modalities ( P = 0.0003). (This was also re,flected in the significant modality effect and the lead x modality interaction in the window analysis (300-500 msec), cf., Table II.) No P300 latency difference was found between correct and error trials, but a strong tendency for a modality × correctness interaction ( P = 0.0513). However, the test of simple effects (modality fixed) revealed no significant P300 latency difference between correct and error trials in both modalities. The reaction-triggered averages (RTA) are given in the right panels of Figs. 2 and 3, the A N O V A results in Table III. These data reveal similar differences between correct and error trials, which proved to be highly significant in the windows - 5 0 to +150 msec and +150 to +350 msec (relative to the key-press). Both effects appeared to be stronger in the reaction- than in the stimulus-triggered averages, which was also reflected in the larger F values of Table Ill compared to Table II.
ERROR PROCESSING A N D ERPs
451
To isolate the correctness effects, the differences between incorrect and correct trial ERPs were computed for both triggering modes. The grand means of these difference waves are shown in Fig. 4. For both averaging modes, a marked negativity with fronto-central maximum, and a subsequent positivity with parieto-occipital maximum, can be seen. The negativity is referred to as "error negativity" (NE), the positivity as "slow wave" in the following. In the response-trigger mode the N E appeared larger and less smeared than in the stimulus-trigger mode. In the stimulus-trigger mode the peak of the N L at Cz was delayed for divided compared to focused attention by
about 60 msec ( P = 0.0004). Because oF the significant modality × attention interaction ( P = 0.0040), tests for simple effects (modality fixed) were run for each modality. They revealed the delay to be only significant for auditory (P = 0.0001), but not for visual ( P = 0.2972) stimuli. A similar asymmetrical delay was seen in the response-trigger mode. In this data set the peak of the N E at Cz was delayed by 39 msec for auditory stimuli (P = 0.0230), whereas again no effect was found for visual stimuli ( P = 0.2159). Fig. 5 gives an overview of RTs and P300, as well as N E latencies (stimulus-triggered averages). After visual stimuli, the division of attention caused a latency shift
TABLE I1 ANOVA results of the window analysis for the stimulus-triggered averages (STA). To save space, only significant effects ( P < 0.03) are given. (A) Time window 300--500 msec (including the P300). (B) The simple effect (leads fixed) in the window 300-500 msec for corectness (C). (C) Time window 500-700 msec (including the slow wave). (D) The simple effect (leads fixed) in the window 500-700 msec for correcmess (C).
Source
df
F
P
7.42 12.70 26.07 8.78 10.82 23.92 7.83 12.67 9.11 8.20
0.0190 0.0074 0.0009 0.0029 0.0019 0.0003 0.0232 0.0008 0.0002 0.0058
(A) Electrode (L) Modality (M) Correctness (C) L× M L×A L× C A×C M ×T L× M ×T AxC×T
1.19, 1, 1, 1.35, 1.74, 1.30, 1, 1.84, 3.35, 1.79,
9.56 8 8 10.79 13.92 10.43 8 14.68 26.80 13.80
(B) Fz
C
Cz
Pz
Oz
df
F
P
F
P
F
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F
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1,8
44.12
0.0002
37.71
0.0003
15.51
0.0043
1.15
0.3149
(c)
df
F
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Electrode (L) Modality (M) Time (T) L×M L×C M×C M×T LxMxC AxC×T
1.60,12.80 1, 8 1.40,11.23 1.64, 13,14 1.31, 10.49 1, 8 2.19, 17.54 1.51, 12.04 2.69, 21.50
9.56 18.93 20.13 11.28 6.20 8.09 8.58 5.39 5.70
0.0042 0.0024 0.0004 0.0021 0.0249 0.0217 0.0021 0.0279 0.0061
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0.7378
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3.65
0.0925
10.39
0.0122
452
M. FALKENSTEIN ET AL.
TABLE Ill ANOVA results of the window analysis for the response-triggered averages (RTA). To save space, only significant effects ( P < 0.03) are given. (A) Time window - 5 0 to + 150 msec. (B) The simple effect (leads fixed) in the window - 5 0 to + 150 msec for correctness (C). (C) Time window + 150 to + 350 msec. (D) The simple effect (leads fixed) in the window + 150 to + 350 msec for correctness (C).
Source
df
F
P
9.75 25.77 30.70 5.95 33.94 10.38 4.12 21.70 5.24 6.83
0.0085 0.0010 0.0005 0.0140 0.0000 0.0004 0.0263 0.0000 0.0040 0.0022
(A) Electrode (L) Modality (M) Correctness (C) L× A L× C L× T A×T C×T L× A× T L× C ×T
1.24, 1, 1, 1.50, 1.85, 2.59, 2.42, 2.84, 3.24, 2.82,
9.89 8 8 11.98 14.83 20.68 19.39 22.71 27.65 22.56
(B) Fz
C
Cz
Pz
Oz
df
F
P
F
P
F
P
F
P
1,8
41.22
0.0002
42.25
0.0002
28.70
0.0007
1.15
0.3 149
(c) df
Electrode (L) Modality (M) Correctness (C) Time (T) L× M L× C L×T M×T L× M × C L× C× T
1.66, 1, 1, 1.77, 1.87, 1.28, 2.62, 3.28, 1.62, 2.68,
13.30 8 8 14.16 15.00 10.25 21.00 26,25 12.96 21.41
F
P
9.76 7.19 7.71 15.55 7.69 5.81 6.00 5.83 11.99 3.88
0.0034 0.0279 0.0241 0.0004 0.0056 0.0302 0.0053 0.0028 0.0017 0.0267
(D) Fz
C
Cz
Pz
Oz
df
F
P
F
P
F
P
F
P
1, 8
1.62
0.2394
4.54
0.0656
9.93
0.0136
13.95
0.0057
of a comparable size in P300, N E, and RTs (left panel). However, after auditory stimuli, RT and N E were much more delayed than the P300 (right panel).
Discussion The main finding of the present paper is a characteristic difference in the ERP structure in correct and error trials in our choice reaction task: (i) the ERP amplitude in the P300 range was reduced in error as compared to correct trials, with maximum difference in the frontocentral leads; (ii) in the slow wave range (500-700 msec) the amplitude was enhanced in error trials, with a parieto-occipital maximum.
The differences are not likely to be caused by a larger latency variance of ERP components in error trials, since the effects were also seen in the single sweep data (Fig. 1). The possibility that the P300 effect is partly due to the shorter RTs in incorrect reactions can also be ruled out, since it is well known that shorter RTs are associated with an enhancement, and not a decrease, of the P300 (Kutas and Donchin 1978; Kok and Looren de Jong 1980; Pfefferbaum et al. 1983). It is not likely that the physiological process which is reflected by the P300 is attenuated in error trials. In this case, the N E, as a mere reflection of an amplitude decrease of the P300, should be maximal at Pz. However, the N E had a &onto-central maximum. Second, the peak latencies of the N~ and the P300 were differ-
ERROR PROCESSING AND ERPs
453
DA
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,,, ."1'.,. 600 ms
-200
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ms
Z~(INCORRECT CORRECT) -
Fig. 4. Grand means of the differences between the ERPs in incorrect and correct trials (incorrect minus correct). Upper panels: visual ERPs; lower panels: auditory ERPs. STA: stimulus-triggered averages; RTA: response-triggered averages. Thin lines: focused attention (FA); heavy lines: divided attention (DA).
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Fig. 5. Reaction time (RT; full circles), latency of the P300 (open rectangles) and latency of the error negativity (NE; open triangles) for the two attention conditions. FA: focused attention; DA: divided attention. Left panel: visual data: right panel: auditory data.
ent, and the N E latency was much more influenced by attention than the P300 latency. Third, not only a reduction of the P300, but a clear negativity was seen in the fronto-central leads, particularly in the responsetriggered ERPs. Therefore we propose an additional process occurring in error trials that is reflected in a fronto-central component, namely the N F. The Nv overlaps with the the P300, thereby reducing its amplitude. These results confirm the postulate of Donchin et al. (1988) of an additional process in error trials. The fact that the NF. was larger and less smeared in the responsethan in the stimulus-triggered averages indicates that it is time-locked more closely to the response than to the stimulus. This is further supported by the similarity of the attention effects on RT and N~ (cf., Fig. 5). The time-locking to the overt response, though, is not at all perfect, since, in the response-triggered averages after auditory stimuli, the N~ peaked later for divided than for focused attention. This argues against the N~ being a motor potential, since a motor potential should be time-locked to the overt response. The divergence of the attention effects on the latencies of the N~ and the P300 (which is assumed to vary with stimulus evaluation time) indicates that the N E is not time-locked to the stimulus evaluation process. Hence the most likely process to which the Nt~ could be time-locked is response selection. We define response selection as the cognitive mapping of the results obtained from the stimulus evaluation process to the appropriate response. Incorrect responses that are faster than the corresponding correct ones (as found in our results) are elicited prematurely before the end of this process, which nevertheless runs to its end. The response is executed "'aspecifically," i.e., not driven by the outcome of response selection. Rather, sequential expectations or guessing ("fast guesses": cf., Coles 1988) may trigger the response. Since several negative components that are described in the literature seem to reflect a mismatch process (N~i~it~inen et al. 1978; Kutas and Hillyard 1980: Courchesne 1983), we were led to the assumption that the N~: reflects an automatic mismatch between the overt response and the outcome of the response selection process. The N E is assumed to be elicited at the moment of the completion of the response selection process, since the postulated mismatch cannot occur earlier. The continuous-flow theory (Coles ev al. 1985, 1988: Smid et al. 1987) suggests that response selection is tikely to run partly in parallel to stimulus evaluation, especially under time pressure conditions as in our ~tudy. Hence response selection may be conducted beJore or during the P300 (cf. also, Ragot and Renault 1985; Renault et al. 1988). This suggests that the N~, peaking on average slightly after the P300, is not a real-time index of response selection, but rather a limemarker of its completion.
454
For auditory stimuli the N E was delayed by the division of attention. Given our interpretation of the N E as a time-marker of the completion of response selection, it follows that the process that is impaired by the division of attention is response selection. This impairment is responsible for the observed R T effects. The similarity of the attention effects on NE and R T is in accordance with this view. The c o m b i n e d R T and N E results support our conclusions drawn from our previous findings with correct-trial data (Hohnsbein et al., this issue). The second p h e n o m e n o n in our error trial ERPs was an enhanced positive activity in the slow wave range. Because of the polarity and t o p o g r a p h y of this slow wave we interpret it to be a second P300. A different interpretation was suggested by the data of D o n c h i n and colleagues ( M c C a r t h y et al. 1979; D o n c h i n 1984; D o n c h i n et al. 1988), who found a delay of the P300 in error compared to correct trials of about 60 msec in a visual oddball task. D o n c h i n et al. (1988) explained this delay by the extra time necessary for processing the error. As suggested by the visual divided attention data of Fig. 2, our slow wave in error trials could also be interpreted to be a severely delayed P300. However, this is improbable for several reasons. First, our slow wave occurs very late, which would imply a P300 latency shift of about 150 msec in error trials. Moreover, the slow wave appeared later for auditory than for visual stimuli, whereas the opposite was seen for the P300 latency. This would imply a P300 delay of about 250 msec for auditory stimuli. Second, a positive peak at Pz was seen in the error trial ERPs as well, with a latency similar to the P300 of the correct trials. This indicates that the stimulus-related P300 is present in error trials, in addition to the slow wave. The A N O V A revealed the P300 latencies not to be significantly different for incorrect compared to correct trials, i.e., stimulus evaluation time seems to be the same in error and correct trials. Third, the slow wave effect was only marginally significant (for Oz only) in the stimulus-triggered averages, whereas the F values were larger in the response-triggered averages. This indicates that the slow wave is related to the response rather than to the stimulus. The fact that Coles et al. (1985) as well as Smid et al. (1987) also found increased P300 latencies in trials with incorrect reaction tendencies can be explained by a different stimulus structure c o m p a r e d to our study. The incorrect reactions in those studies were induced by concurrent and incompatible stimuli. Coles et al. (1985) suggested that the incompatible stimuli produce a conflict in stimulus evaluation which slows the evaluation process. Since no concurrent stimuli were presented in our paradigm, the lack of a P300 delay in our data is not surprising. Hence there is evidence that our slow wave is in fact a second P300 that reflects in some way the processing of the error. The possibility of a second
M. F A L K E N S T E I N El" AL.
P300 was also considered by D o n c h i n et al. (1988). O u r interpretation for the slow wave is similar to a postulate of RSsler (1983), namely, that the processing of an error event should be accompanied by an additional P300. In contrast to the error negativity, this type of processing is assumed to be conscious and, as proposed by D o n c h i n et al. (1988), to be related to adjustments in the subject's strategy subsequent to the recognition of an error. The slow wave can thus be discussed in terms of context updating ( D o n c h i n and Coles 1988). The variability of lhe slow wave across trials and subjects was considerable. This makes sense in context with our interpretation, since the cognitive (and, perhaps, emotional) reactions to errors can be assumed to vary considerably across subjects. Indeed, one of our subjects exhibited no slow wave at all, whereas for two subjects it had an extreme amplitude. This m a y indicate different ways of coping with errors. The entire N E / s l o w wave complex in the difference wave shape reminds one strongly of a c o m m o n ERP. It can also be discussed in terms of an N2 and a P300 as a reaction to the subject's own response. This view is implicit in our interpretations, which are, however, more specific. In sum, our two difference-wave c o m p o n e n t s are interpreted as reflecting different stages of error processing. We assume that the error negativity (NE) reflects a (perhaps unconscious) mismatch between response selection and "aspecific" response execution, whereas the slow wave reflects the conscious evaluation of the error. With this interpretation the Nv2 can be seen as a time-marker of the completion of the responseselection process. The attention effects on the N E suggest that the response selection process is impaired after auditory, but not after visual, stimuli in our divided attention condition. This supports nicely our previous conclusions drawn from correct trial data (Hohnsbein et al., this issue). Like the P300 for stimulus evaluation, the NE may prove to be a useful tool for assessing the timing of response selection in error trials. Since even a few sweeps yield a clear error negativity, its evaluation in choice reaction paradigms is recommended. We would like to thank Prof. C.R. Cavonius, Dortmund, and 4 a n o n y m o u s referees for valuable comments on earlier versions of the manuscript. We are indebted to Christiane Westedt for her committed technical assistance.
References Campbell, K.B., Courchesne, E., Picton. T.W. and Squires, K.C. Evoked potential correlates of h u m a n information processing. Biol. Psychol., 1979, 8 : 4 5 68. Coles, M.G.H. Modern mind-brain reading: psychophysiology, physiology and cognition. Psychophysiology, 1988, 26: 251-269.
E R R O R PROCESSING A N D ERPs Coles, M.G.H., Gratton, G.. Bashore, T.R., Eriksen, C.W. and Donchin, E. A psychophysiological investigation of the continuous flow model of h u m a n information processing. J. Exp. Psychol: Hum. Percept. Perform., 1985, l l : 529-553. Coles, M.G., Gratton, G. and Donchin, E. Detecting early communication: using measures of movement-related potentials to illuminate h u m a n information processing. Biol. Psychol., 1988, 26: 69-89. Courchesne. E. Cognitive components in the event-related brain potential: changes associated with development. In: A.W.K. Gaillard and W. Ritter (Eds.), Tutorials in ERP Research: Endogenous Components. North-Holland, Amsterdam, 1983: 329-344. Dixon, W.J. BMDP Statistical Software. University of California Press, Berkeley, CA, 1983. Donchin, E. (Ed.). Cognitive Psychophysiology: Event-Related Potentials and the Study of Cognition (Vol. 1). The Carmel Conferences. Lawrence Erlhaum, Hillsdale, N J, 1984. Donchin, E. and Coles. M.G.H. Is the P300 component a manifestation of context updating? Behav. Brain Sci., 1988. l l : 357-374. Donchin, E., Gratton, G., Dupree, D. and Coles, M. After a rash action: latency and amplitude of the P300 following fast guesses. In: G.C. Galbraith, M.L. Kietzman and E. Donchin (Eds.), Neurophysiology and Psychophysiology: Experimental and Clinical Applications. Lawrence Erlbaum, Hillsdale, N J, 1988: 173-188. Horst, R.L.. Johnson. R. and Donchin, E. Event-related brain potentials and subjective probability in a learning task. Mere. Cogn., 1980, 8 : 4 7 6 488. Kok, A. and Looren de Jong, H. Components of the event-related potential following degraded and undegraded visual stimuli. Biol. Psychol., 1980, 11: 117-133. Kutas, M. and Donchin, E, Variations in the latency of P300 as a function of variations in semantic categorization. In: D.A. Otto (Ed.), Multidisciplinary Perspectives in Event-Related Brain Potential Research. U.S. Government Printing Office, Washington, DC, 1978: 198-201. Kutas, M. and Hillyard, S. Reading senseless sentences: brain potentials reflect semantic incongruity. Science, 1980, 207: 203-204. Kutas, M.. McCarthy, G. and Donchin, E. Augmenting mental chro-
455 nometry: the P300 as a measure of stimulus evaluation time. Science, 1977, 197:792 795. Lindman, H.R. Analysis of Variance in Complex Experimental Designs. Freeman. San Francisco, CA, 1974. McCarthy, G., Kutas, M. and Donchin, E. Detecting errors with P300 latency. Psychophysiology, 1979, 16: 175. N~it~inen, R., Galliard. A.W.K. and Mfintysalo. S. Early selective attention effect on evoked potential reinterpreted. Acta Psvchol. (Amst.), 1 9 7 8 . 4 2 : 3 1 3 329. Pfefferbaum, A., Ford, J., Johnson, R.. Wenegrat, B. and Kopell, B.S. Manipulation of P3 latency: speed vs. accuracy instructions. Electroenceph, olin. Neurophysiol., 1983, 55:188 197. Ragot, R. and Renault. B. P300 and S-R compatibility: a reply to Magliero et al. Psychophysiology, 1985, 22: 349-352. Renault, B., Ragot, R. and LesOvre, N. Correct and incorrect responses in a choice reaction time task and the endogenous components of the evoked potential. In: H.It. Kornhuher and L. I)eecke (Eds.), Motivation, Motor and Sensory Processes of the Brain; Electrical Potentials, Behaviour and ('linical / s e . El,~cvier, Amsterdam, 1980: 647-654. Renault, B., Fiori, N. and Giami, S. I,atencies of event related potentials as a tool for studying motor processing organization. Biol. Psychol.. 1988, 26:217 230. ROsier, F. Endogenous E R " P s " and cognition: probes, prospects and pitfalls in matching pieces of the mincl-body puzzle. In: A.W.K. Galliard and W. Ritter (Eds.), Tutorials in ERP Research: Endogenous Components. North-Holland, Amsterdam, 1983: 9-35. Ruchkin, D.S. and (}laser, E.M. Simple digital filters for examining CNV and P300 on a single trial basis. In: D.A. Otto (Ed.), Multidisciplinary Perspectives in Event-Relamd Brain Potential Research. U.S. Government Printing Office Washington, DC, 1978: 579-584. Staid, H.G.O.M., Mulder, G. and Mulder, I..J.M. The continuous flow model revisited: perceptual and central motor aspects. In: R. Johnson, J.W. Rohrbaugh and R. Parasuraman IEds.), ('urrent Trends in Event-Related Potential Research (EEG Suppl. 40). Elsevier, Amsterdam, 1987 270 278.
Electroencephah)graphy and clinical Neurophysiology, 1991, 7 8 : 4 4 7 - 4 5 5 '~ t991 Elsevier Scientific Publishers Ireland, Ltd. 0013-4649/91/$03.50 A D O N I S 0013464991001012
EEG 89609
Effects of crossmodal divided attention on late E R P components. II. Error processing in choice reaction tasks M. Falkenstein, J. Hohnsbein, J. Hoormann and L. Blanke lnstitut fi;tr A rbeitsphysiologie, A bt. Sinnes- und Neurophysiologie, D-4600 Dortmund ( F. R. G.) (Accepted for publication: 6 August 1990)
Summary Reaction times and event-related potentials in correct and incorrect trials were studied in a bimanual choice reaction task. In a focused attention (FA) condition, the stimulus modality was constant (visual or auditory); in a divided attention (DA) condition, the modality was varied at random from trial to trial. Stimulus- and response-triggered averages were computed from the midline EEG leads. In error trials, the ERP amplitude was reduced in the P300 range (300-500 msec) and enhanced in the slow wave range (500-700 msec) compared to correct reaction trials. Difference plots between the ERPs (incorrect minus correct reaction trials) revealed a large fronto-central negativity ( " N ~ " ) and a parieto-occipital "'slow wave." These components appeared larger in the response-triggered averages. We believe that they reflect two different stages of error processing. After auditory stimuli the N E peaked m u c h later for D A than for FA, which supports the idea of an asymmetrical allocation of processing resources to the disadvantage of the auditory modality in our D A condition. Key words: Error processing; Divided attention; Choice reaction; Event-related potentials
Relatively little is known about error processing, i.e., the cognitive processes leading to, or following, incorrect responses. Moreover, the influence of attentional mechanisms on information processing stages may be different in trials that yield correct and incorrect responses. We propose that the event-related potential (ERP) may be a valuable tool for analyzing such differences. Surprisingly, very few studies explicitly focus upon ERP differences between correct and incorrect reactions in choice reaction tasks. Renault et al. (1980) found larger N200-P300 amplitudes in erroneous trials as compared to correct ones in a bimodal choice reaction task. Two studies applied feedback stimuli following "correct" or "incorrect" trials in a time-estimation task (Campbell et al. 1979; Horst et al. 1980). The main findings were larger P300 amplitudes following feedback stimuli with low (as opposed to high) subjective probability. However, the meaning of the feedback stimulus ("correct" or "incorrect" trial) did not influence the feedback-elicited P300. Kutas et al. (1977) found in an oddball task that incorrect responses occurred earlier than correct ones, whereas the latency of P300 remained constant. However, no quantitative ERP data for the incorrect trials were reported. Donchin et al. (1988) repeated and ex-
Correspondence to: Dr. M. Falkenstein, Institut ftir Arbeitsphysiologie, Abt. Sinnes- und Neurophysiologie, Ardeystr. 67. D-4600 Dortmund (F.R.G.).
tended the Kutas et al. study. In error trials they found a P300-1ike positivity which peaked later than the P300 in correct trials. This finding was interpreted by postulating a delay of the P300 in error trials, caused by the processing of the error. However, other interpretations, such as a second P300 in error trials, were also considered by the authors (see also Donchin 1984, p. 254-285). Coles et al. (1985, 1988) presented resuhs of a bimanual choice reaction task paradigm in which they differentiated not only between correct and incorrect responses but also between levels of incorrect response tendencies, revealed by E M G and hand squeeze measurements. The incorrect reaction tendencies were induced mainly by incompatible distractors, i.e., incorrect responses were induced by presenting the competing stimulus at the same time as the target. Among other results, the authors found prolonged P300 latencies with rising incorrect response tendency. This is in accordance with the Donchin et al. study. However, Coles et al. interpret their P300 delay as a prolongation of stimulus evaluation time caused by the distractors. Since some of the cited studies are not aimed at the error issue or their results and, more important, their interpretations seem to be controversial, the main aim of the present study was to elucidate the effects of errors on the ERP in a choice reaction task, and to discuss them in terms of error processing. It is very likely that an error, which is an important event, is reflected also in the ERP of error trials. This possibility of an additional process in error trials was also consid-
448 ered by Donchin et al. (1988). These authors postulated a "process that occurs when the subject processes the commitment of an error (a recognition that need not reach the subject's awareness)." However, such a process is not clearly seen in the results of Donchin et al. In order to decide whether possible error effects are related to the stimulus or to the (incorrect) response, we thought that the computation of both stimulus-triggered and response-triggered averages would be helpful, To overcome the problem that the number of trials in which an error occurs is too low to yield usable averages, the error rate was enhanced by a time-pressure regimen. A second question addressed in the present study was whether error processing can be influenced by attention. In the companion paper (Hohnsbein et al., this issue) we reported results from correct trials in a paradigm in which the subjects were forced to divide their attention because stimuli were presented randomly to the visual and auditory systems. Results in that study revealed (i) that response-related processes were impaired by the division of attention, and (ii) that this effect was larger following auditory stimuli. This was interpreted as supporting the idea of an asymmetrical allocation of attention in favor of the visual modality in the divided-attention condition. In the present study we asked whether these conclusions drawn from "correct" trials are confirmed by the RT and ERP results from incorrect trials.
Methods
Procedure The procedure has been described in full detail in the companion paper (Hohnsbein et al., this issue). Eleven right-handed healthy paid subjects participated in the study. The data of 2 females had to be discarded because of alpha activity. The remaining 9 subjects (4 males and 5 females) had a mean age of 24.3 years (range: 15-43). In 4 sessions, single letter stimuli ( " F " or " J " ) were presented to the subjects in r a n d o m order with equal probability. The ISI was randomized in the range of 750-2250 msec. In the focused-attention condition 100 letters were either presented visually (on a TV monitor), or auditorily (via headphones) within one block. In the divided-attention condition 100 visual and 100 auditory stimuli were presented within one block, with the modality varying at r a n d o m with equal probability. The task was to respond to each letter by pressing the appropriate key of a keyboard ( " F " left, " J " right index finger). Time pressure (TP) was induced by a feedback stimulus (a 60 dB SPL tone), which was given when the subject's response did not occur within 550 msec after stimulus onset. The subjects were instructed to react fast enough to avoid the feedback tone, even at the risk of committing errors.
M. FALKENSTEIN ET AL.
Data collection and analysis" The first 2 sessions were practice sessions in which the subjects reached a rather stable performance level. Only the ERP and R T data of the last 2 sessions were pooled across sessions and letters and evaluated. The E E G was recorded from Fz, Cz, Pz, and Oz against linked mastoids, the E O G from the left eye. All data were filtered (0.03-60 Hz) and digitized with 200 samples/sec. The artifact rejection (cf., Hohnsbein et al., this issue) was performed during the off-line averaging. Correct and incorrect trial ERPs were averaged separately. Averaging was performed by using either the stimulus (stimulus-triggered averaging, STA) or the key-press (reaction-triggered averaging, RTA) as trigger. The averaging epochs had a length of 750 msec, of which 400 msec were pre-trigger in the RTA mode. The averaged data were digitally low-pass filtered (cut-off: 17 Hz; Ruchkin and Glaser 1978). Since the number of available trials was about 6 times as large in the "correct" as in the "error" condition, the signal-to-noise ratio was estimated to be a factor f 6 - = 2.45 smaller, and the variance correspondingly larger in the error trials as compared to the correct trials. This variance inhomogeneity may cause problems in amplitude estimation and statistical analysis. The A N O V A is known to be robust against violations of variance homogeneity up to variance ratios of 1 : 1 0 (Lindman 1974, p. 33). Nevertheless, we considered only effects that yielded P < 0.03 to be significant, which we feel is conservative. However, the higher noise levels in error trial ERPs are likely to introduce systematic errors in peak amplitude (but not in latency) estimation, in such a way that the absolute amplitude is overestimated in error-related ERPs. Therefore, the ERP amplitudes were evaluated by a window analysis. The idea was to define ERP windows of fixed length which included certain components and to enter equidistant sample points covering the entire window into A N O V A with sample time (T) in the window as additional factor. Compared to integral measures the window analysis has the advantage of being sensitive not only to mean amplitude differences in the window (main effect of a factor, F), but also to differences between curve shapes (F × T interactions). In our case, the 10-to-10 msec samples of certain E R P windows of 200 msec length (2 windows for each averaging mode) were subjected to 5-way A N O V A s (BMDP4V, Dixon 1983), with the factors electrode (L; levels: Fz, Cz, Pz, Oz). stimulus modality (M; visual, auditory), attention (A; focused, divided), response correctness (C; correct, incorrect) and sample time (T; 20 levels). In addition to the window analysis, the latency of the largest relative m a x i m u m at Pz in the window 300-500 msec of the stimulus-triggered averages was measured as the P300 latency. The latency values were subjected to a 3-way A N O V A (design: M, A, C). Difference
ERROR PROCESSING A N D ERPs
449 VIS
waves between correct and incorrect ERPs were also computed. The peak latency values at Cz of the negative component of the difference wave (see below) were subjected to A N O V A (design: M, A). Reaction time (RT) was recorded in each trial. The mean RTs were subjected to a 3-way A N O V A (design: M, A, C). The error rates were likewise subjected to an A N O V A (design: M, A). For all ANOVAs the degrees of freedom were corrected by using the GreenhouseGeisser procedure, which is included in BMDP4V.
0
Results
Behavioral data Table I presents the reaction time (RT) results and the error rates. The mean RT was about 20 msec shorter in error than in correct trials ( P = 0.0003). Moreover, it was longer for divided than for focused attention ( P = 0.0003). This difference was larger for auditory (68 msec) than for visual stimuli (17 msec) which was reflected in the modality x attention interaction ( P = 0.0004). This asymmetry was not different for correct and error trials (the modality x attention x correctness interaction was not significant). The error rate was about 15%. It did not differ significantly across conditions.
200
g.O0
AUD
600
ms
0
200
&O0
600
ms
Fig. l. Stimulus-triggered single trial (upper panel) and averaged ERPs (lower panel) for correct (thin lines) and error trials (heavy lines) for one representative subject (focused-attention condition; the averaged ERPs are from the two recording sessions). Left panel: visual ERPs; right panel: auditory FRPs.
E R P data Fig. 1 gives typical examples for single sweep and stimulus-triggered averages (STA) for one representative subject, showing large differences between correct and incorrect trials for both modalities. In general, an amplitude reduction in the range of about 300--500 msec and a late positive wave in the range of about 500-700 msec was seen in error compared to correct trials.
"FABLE 1 (A) Mean reaction times (in msec) and (interindividual) S.D.s (in parentheses) to visual and auditory stimuli for incorrect and correct responses. e = percentage of errors; FA = focused attention; DA = divided attention. (B) ANOVA results for the RTs. Incorrect
e
Correct
Mean
Visual FA DA
347 (30) 367 (21)
16.0 15.4
378 (28) 392 (17)
363 380
Mean DA FA
357 20
385 14
371 17
Auditory FA DA
323 (40) 387 (35)
332 (29) 403 (27)
328 395
Mean D A - FA
355 64
368 71
362 68
(A)
16.5 14.9
(B) Source
af
F
P
Modality (M) Attention (A) Correctness (C) MxA MxC AxC MxAxC
1,8 1, 8 1, 8 1, 8 1, 8 1,8 1,8
1.98 36.78 36.68 32.72 5.27 0.06 1.64
ns 0.0003 0.0003 0.0004 0.0508 ns ns
450
M. F A L K E N S T E I N
Figs. 2 and 3 show the grand means of the visual and the auditory ERPs. The stimulus-triggered averages (STA) are given in the left panels of both figures, the A N O V A results in Table II. In correct trials a clear P300 was seen, In error trials the ERP structure was quite different. In the window including the P300 (300500 msec), the amplitude of the ERP was severely reduced compared to "correct" trials ( P = 0.0009). The significant lead × correctness interaction ( P = 0.0003) and the subsequent simple tests for the 4 leads revealed this effect to be maximal at Fz ( P = 0.0002). Despite the amplitude reduction, a positive peak was seen with Pz maximum in the latency range of the correct trial P300. In the window 500-700 msec a positive complex without a distinct peak was seen; the amplitude in the window appeared larger for error than for correct trials, which was significant for Oz only ( P = 0.0122). The positive complex appeared to be later and smaller in the auditory than in the visual ERPs, which was reflected in
VISUAL STA
ET AL.
AUDITORY STA
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Fig, 3. G r a n d m e a n s of the ERPs to auditory stimuli. Refer to legend of Fig. 2 for details.
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oz
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-
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-
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Fig. 2. Grand means of the ERPs to visual stimuli (n = 9). Upper panels: focused attention (FA; constant stimulus modality). Lower panels: divided attention (DA; stimulus modality is varied at random from trial to trial). STA: stimulus-triggered averages; RTA: responsetriggered averages. Heavy lines: incorrect trials; thin lines: correct trials. The associated reaction times are given as vertical thin and heavy bars in the STAs (Oz lead).
the modality main effect and the interactions with modality. The P300 latency was clearly different across modalities ( P = 0.0003). (This was also re,flected in the significant modality effect and the lead x modality interaction in the window analysis (300-500 msec), cf., Table II.) No P300 latency difference was found between correct and error trials, but a strong tendency for a modality × correctness interaction ( P = 0.0513). However, the test of simple effects (modality fixed) revealed no significant P300 latency difference between correct and error trials in both modalities. The reaction-triggered averages (RTA) are given in the right panels of Figs. 2 and 3, the A N O V A results in Table III. These data reveal similar differences between correct and error trials, which proved to be highly significant in the windows - 5 0 to +150 msec and +150 to +350 msec (relative to the key-press). Both effects appeared to be stronger in the reaction- than in the stimulus-triggered averages, which was also reflected in the larger F values of Table Ill compared to Table II.
ERROR PROCESSING A N D ERPs
451
To isolate the correctness effects, the differences between incorrect and correct trial ERPs were computed for both triggering modes. The grand means of these difference waves are shown in Fig. 4. For both averaging modes, a marked negativity with fronto-central maximum, and a subsequent positivity with parieto-occipital maximum, can be seen. The negativity is referred to as "error negativity" (NE), the positivity as "slow wave" in the following. In the response-trigger mode the N E appeared larger and less smeared than in the stimulus-trigger mode. In the stimulus-trigger mode the peak of the N L at Cz was delayed for divided compared to focused attention by
about 60 msec ( P = 0.0004). Because oF the significant modality × attention interaction ( P = 0.0040), tests for simple effects (modality fixed) were run for each modality. They revealed the delay to be only significant for auditory (P = 0.0001), but not for visual ( P = 0.2972) stimuli. A similar asymmetrical delay was seen in the response-trigger mode. In this data set the peak of the N E at Cz was delayed by 39 msec for auditory stimuli (P = 0.0230), whereas again no effect was found for visual stimuli ( P = 0.2159). Fig. 5 gives an overview of RTs and P300, as well as N E latencies (stimulus-triggered averages). After visual stimuli, the division of attention caused a latency shift
TABLE I1 ANOVA results of the window analysis for the stimulus-triggered averages (STA). To save space, only significant effects ( P < 0.03) are given. (A) Time window 300--500 msec (including the P300). (B) The simple effect (leads fixed) in the window 300-500 msec for corectness (C). (C) Time window 500-700 msec (including the slow wave). (D) The simple effect (leads fixed) in the window 500-700 msec for correcmess (C).
Source
df
F
P
7.42 12.70 26.07 8.78 10.82 23.92 7.83 12.67 9.11 8.20
0.0190 0.0074 0.0009 0.0029 0.0019 0.0003 0.0232 0.0008 0.0002 0.0058
(A) Electrode (L) Modality (M) Correctness (C) L× M L×A L× C A×C M ×T L× M ×T AxC×T
1.19, 1, 1, 1.35, 1.74, 1.30, 1, 1.84, 3.35, 1.79,
9.56 8 8 10.79 13.92 10.43 8 14.68 26.80 13.80
(B) Fz
C
Cz
Pz
Oz
df
F
P
F
P
F
P
F
P
1,8
44.12
0.0002
37.71
0.0003
15.51
0.0043
1.15
0.3149
(c)
df
F
P
Electrode (L) Modality (M) Time (T) L×M L×C M×C M×T LxMxC AxC×T
1.60,12.80 1, 8 1.40,11.23 1.64, 13,14 1.31, 10.49 1, 8 2.19, 17.54 1.51, 12.04 2.69, 21.50
9.56 18.93 20.13 11.28 6.20 8.09 8.58 5.39 5.70
0.0042 0.0024 0.0004 0.0021 0.0249 0.0217 0.0021 0.0279 0.0061
(D) Fz
C
Cz
Pz
Oz
df
F
P
F
P
F
P
F
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1, 8
0.12
0.7378
0.65
0.4429
3.65
0.0925
10.39
0.0122
452
M. FALKENSTEIN ET AL.
TABLE Ill ANOVA results of the window analysis for the response-triggered averages (RTA). To save space, only significant effects ( P < 0.03) are given. (A) Time window - 5 0 to + 150 msec. (B) The simple effect (leads fixed) in the window - 5 0 to + 150 msec for correctness (C). (C) Time window + 150 to + 350 msec. (D) The simple effect (leads fixed) in the window + 150 to + 350 msec for correctness (C).
Source
df
F
P
9.75 25.77 30.70 5.95 33.94 10.38 4.12 21.70 5.24 6.83
0.0085 0.0010 0.0005 0.0140 0.0000 0.0004 0.0263 0.0000 0.0040 0.0022
(A) Electrode (L) Modality (M) Correctness (C) L× A L× C L× T A×T C×T L× A× T L× C ×T
1.24, 1, 1, 1.50, 1.85, 2.59, 2.42, 2.84, 3.24, 2.82,
9.89 8 8 11.98 14.83 20.68 19.39 22.71 27.65 22.56
(B) Fz
C
Cz
Pz
Oz
df
F
P
F
P
F
P
F
P
1,8
41.22
0.0002
42.25
0.0002
28.70
0.0007
1.15
0.3 149
(c) df
Electrode (L) Modality (M) Correctness (C) Time (T) L× M L× C L×T M×T L× M × C L× C× T
1.66, 1, 1, 1.77, 1.87, 1.28, 2.62, 3.28, 1.62, 2.68,
13.30 8 8 14.16 15.00 10.25 21.00 26,25 12.96 21.41
F
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of a comparable size in P300, N E, and RTs (left panel). However, after auditory stimuli, RT and N E were much more delayed than the P300 (right panel).
Discussion The main finding of the present paper is a characteristic difference in the ERP structure in correct and error trials in our choice reaction task: (i) the ERP amplitude in the P300 range was reduced in error as compared to correct trials, with maximum difference in the frontocentral leads; (ii) in the slow wave range (500-700 msec) the amplitude was enhanced in error trials, with a parieto-occipital maximum.
The differences are not likely to be caused by a larger latency variance of ERP components in error trials, since the effects were also seen in the single sweep data (Fig. 1). The possibility that the P300 effect is partly due to the shorter RTs in incorrect reactions can also be ruled out, since it is well known that shorter RTs are associated with an enhancement, and not a decrease, of the P300 (Kutas and Donchin 1978; Kok and Looren de Jong 1980; Pfefferbaum et al. 1983). It is not likely that the physiological process which is reflected by the P300 is attenuated in error trials. In this case, the N E, as a mere reflection of an amplitude decrease of the P300, should be maximal at Pz. However, the N E had a &onto-central maximum. Second, the peak latencies of the N~ and the P300 were differ-
ERROR PROCESSING AND ERPs
453
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Fig. 4. Grand means of the differences between the ERPs in incorrect and correct trials (incorrect minus correct). Upper panels: visual ERPs; lower panels: auditory ERPs. STA: stimulus-triggered averages; RTA: response-triggered averages. Thin lines: focused attention (FA); heavy lines: divided attention (DA).
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Fig. 5. Reaction time (RT; full circles), latency of the P300 (open rectangles) and latency of the error negativity (NE; open triangles) for the two attention conditions. FA: focused attention; DA: divided attention. Left panel: visual data: right panel: auditory data.
ent, and the N E latency was much more influenced by attention than the P300 latency. Third, not only a reduction of the P300, but a clear negativity was seen in the fronto-central leads, particularly in the responsetriggered ERPs. Therefore we propose an additional process occurring in error trials that is reflected in a fronto-central component, namely the N F. The Nv overlaps with the the P300, thereby reducing its amplitude. These results confirm the postulate of Donchin et al. (1988) of an additional process in error trials. The fact that the NF. was larger and less smeared in the responsethan in the stimulus-triggered averages indicates that it is time-locked more closely to the response than to the stimulus. This is further supported by the similarity of the attention effects on RT and N~ (cf., Fig. 5). The time-locking to the overt response, though, is not at all perfect, since, in the response-triggered averages after auditory stimuli, the N~ peaked later for divided than for focused attention. This argues against the N~ being a motor potential, since a motor potential should be time-locked to the overt response. The divergence of the attention effects on the latencies of the N~ and the P300 (which is assumed to vary with stimulus evaluation time) indicates that the N E is not time-locked to the stimulus evaluation process. Hence the most likely process to which the Nt~ could be time-locked is response selection. We define response selection as the cognitive mapping of the results obtained from the stimulus evaluation process to the appropriate response. Incorrect responses that are faster than the corresponding correct ones (as found in our results) are elicited prematurely before the end of this process, which nevertheless runs to its end. The response is executed "'aspecifically," i.e., not driven by the outcome of response selection. Rather, sequential expectations or guessing ("fast guesses": cf., Coles 1988) may trigger the response. Since several negative components that are described in the literature seem to reflect a mismatch process (N~i~it~inen et al. 1978; Kutas and Hillyard 1980: Courchesne 1983), we were led to the assumption that the N~: reflects an automatic mismatch between the overt response and the outcome of the response selection process. The N E is assumed to be elicited at the moment of the completion of the response selection process, since the postulated mismatch cannot occur earlier. The continuous-flow theory (Coles ev al. 1985, 1988: Smid et al. 1987) suggests that response selection is tikely to run partly in parallel to stimulus evaluation, especially under time pressure conditions as in our ~tudy. Hence response selection may be conducted beJore or during the P300 (cf. also, Ragot and Renault 1985; Renault et al. 1988). This suggests that the N~, peaking on average slightly after the P300, is not a real-time index of response selection, but rather a limemarker of its completion.
454
For auditory stimuli the N E was delayed by the division of attention. Given our interpretation of the N E as a time-marker of the completion of response selection, it follows that the process that is impaired by the division of attention is response selection. This impairment is responsible for the observed R T effects. The similarity of the attention effects on NE and R T is in accordance with this view. The c o m b i n e d R T and N E results support our conclusions drawn from our previous findings with correct-trial data (Hohnsbein et al., this issue). The second p h e n o m e n o n in our error trial ERPs was an enhanced positive activity in the slow wave range. Because of the polarity and t o p o g r a p h y of this slow wave we interpret it to be a second P300. A different interpretation was suggested by the data of D o n c h i n and colleagues ( M c C a r t h y et al. 1979; D o n c h i n 1984; D o n c h i n et al. 1988), who found a delay of the P300 in error compared to correct trials of about 60 msec in a visual oddball task. D o n c h i n et al. (1988) explained this delay by the extra time necessary for processing the error. As suggested by the visual divided attention data of Fig. 2, our slow wave in error trials could also be interpreted to be a severely delayed P300. However, this is improbable for several reasons. First, our slow wave occurs very late, which would imply a P300 latency shift of about 150 msec in error trials. Moreover, the slow wave appeared later for auditory than for visual stimuli, whereas the opposite was seen for the P300 latency. This would imply a P300 delay of about 250 msec for auditory stimuli. Second, a positive peak at Pz was seen in the error trial ERPs as well, with a latency similar to the P300 of the correct trials. This indicates that the stimulus-related P300 is present in error trials, in addition to the slow wave. The A N O V A revealed the P300 latencies not to be significantly different for incorrect compared to correct trials, i.e., stimulus evaluation time seems to be the same in error and correct trials. Third, the slow wave effect was only marginally significant (for Oz only) in the stimulus-triggered averages, whereas the F values were larger in the response-triggered averages. This indicates that the slow wave is related to the response rather than to the stimulus. The fact that Coles et al. (1985) as well as Smid et al. (1987) also found increased P300 latencies in trials with incorrect reaction tendencies can be explained by a different stimulus structure c o m p a r e d to our study. The incorrect reactions in those studies were induced by concurrent and incompatible stimuli. Coles et al. (1985) suggested that the incompatible stimuli produce a conflict in stimulus evaluation which slows the evaluation process. Since no concurrent stimuli were presented in our paradigm, the lack of a P300 delay in our data is not surprising. Hence there is evidence that our slow wave is in fact a second P300 that reflects in some way the processing of the error. The possibility of a second
M. F A L K E N S T E I N El" AL.
P300 was also considered by D o n c h i n et al. (1988). O u r interpretation for the slow wave is similar to a postulate of RSsler (1983), namely, that the processing of an error event should be accompanied by an additional P300. In contrast to the error negativity, this type of processing is assumed to be conscious and, as proposed by D o n c h i n et al. (1988), to be related to adjustments in the subject's strategy subsequent to the recognition of an error. The slow wave can thus be discussed in terms of context updating ( D o n c h i n and Coles 1988). The variability of lhe slow wave across trials and subjects was considerable. This makes sense in context with our interpretation, since the cognitive (and, perhaps, emotional) reactions to errors can be assumed to vary considerably across subjects. Indeed, one of our subjects exhibited no slow wave at all, whereas for two subjects it had an extreme amplitude. This m a y indicate different ways of coping with errors. The entire N E / s l o w wave complex in the difference wave shape reminds one strongly of a c o m m o n ERP. It can also be discussed in terms of an N2 and a P300 as a reaction to the subject's own response. This view is implicit in our interpretations, which are, however, more specific. In sum, our two difference-wave c o m p o n e n t s are interpreted as reflecting different stages of error processing. We assume that the error negativity (NE) reflects a (perhaps unconscious) mismatch between response selection and "aspecific" response execution, whereas the slow wave reflects the conscious evaluation of the error. With this interpretation the Nv2 can be seen as a time-marker of the completion of the responseselection process. The attention effects on the N E suggest that the response selection process is impaired after auditory, but not after visual, stimuli in our divided attention condition. This supports nicely our previous conclusions drawn from correct trial data (Hohnsbein et al., this issue). Like the P300 for stimulus evaluation, the NE may prove to be a useful tool for assessing the timing of response selection in error trials. Since even a few sweeps yield a clear error negativity, its evaluation in choice reaction paradigms is recommended. We would like to thank Prof. C.R. Cavonius, Dortmund, and 4 a n o n y m o u s referees for valuable comments on earlier versions of the manuscript. We are indebted to Christiane Westedt for her committed technical assistance.
References Campbell, K.B., Courchesne, E., Picton. T.W. and Squires, K.C. Evoked potential correlates of h u m a n information processing. Biol. Psychol., 1979, 8 : 4 5 68. Coles, M.G.H. Modern mind-brain reading: psychophysiology, physiology and cognition. Psychophysiology, 1988, 26: 251-269.
E R R O R PROCESSING A N D ERPs Coles, M.G.H., Gratton, G.. Bashore, T.R., Eriksen, C.W. and Donchin, E. A psychophysiological investigation of the continuous flow model of h u m a n information processing. J. Exp. Psychol: Hum. Percept. Perform., 1985, l l : 529-553. Coles, M.G., Gratton, G. and Donchin, E. Detecting early communication: using measures of movement-related potentials to illuminate h u m a n information processing. Biol. Psychol., 1988, 26: 69-89. Courchesne. E. Cognitive components in the event-related brain potential: changes associated with development. In: A.W.K. Gaillard and W. Ritter (Eds.), Tutorials in ERP Research: Endogenous Components. North-Holland, Amsterdam, 1983: 329-344. Dixon, W.J. BMDP Statistical Software. University of California Press, Berkeley, CA, 1983. Donchin, E. (Ed.). Cognitive Psychophysiology: Event-Related Potentials and the Study of Cognition (Vol. 1). The Carmel Conferences. Lawrence Erlhaum, Hillsdale, N J, 1984. Donchin, E. and Coles. M.G.H. Is the P300 component a manifestation of context updating? Behav. Brain Sci., 1988. l l : 357-374. Donchin, E., Gratton, G., Dupree, D. and Coles, M. After a rash action: latency and amplitude of the P300 following fast guesses. In: G.C. Galbraith, M.L. Kietzman and E. Donchin (Eds.), Neurophysiology and Psychophysiology: Experimental and Clinical Applications. Lawrence Erlbaum, Hillsdale, N J, 1988: 173-188. Horst, R.L.. Johnson. R. and Donchin, E. Event-related brain potentials and subjective probability in a learning task. Mere. Cogn., 1980, 8 : 4 7 6 488. Kok, A. and Looren de Jong, H. Components of the event-related potential following degraded and undegraded visual stimuli. Biol. Psychol., 1980, 11: 117-133. Kutas, M. and Donchin, E, Variations in the latency of P300 as a function of variations in semantic categorization. In: D.A. Otto (Ed.), Multidisciplinary Perspectives in Event-Related Brain Potential Research. U.S. Government Printing Office, Washington, DC, 1978: 198-201. Kutas, M. and Hillyard, S. Reading senseless sentences: brain potentials reflect semantic incongruity. Science, 1980, 207: 203-204. Kutas, M.. McCarthy, G. and Donchin, E. Augmenting mental chro-
455 nometry: the P300 as a measure of stimulus evaluation time. Science, 1977, 197:792 795. Lindman, H.R. Analysis of Variance in Complex Experimental Designs. Freeman. San Francisco, CA, 1974. McCarthy, G., Kutas, M. and Donchin, E. Detecting errors with P300 latency. Psychophysiology, 1979, 16: 175. N~it~inen, R., Galliard. A.W.K. and Mfintysalo. S. Early selective attention effect on evoked potential reinterpreted. Acta Psvchol. (Amst.), 1 9 7 8 . 4 2 : 3 1 3 329. Pfefferbaum, A., Ford, J., Johnson, R.. Wenegrat, B. and Kopell, B.S. Manipulation of P3 latency: speed vs. accuracy instructions. Electroenceph, olin. Neurophysiol., 1983, 55:188 197. Ragot, R. and Renault. B. P300 and S-R compatibility: a reply to Magliero et al. Psychophysiology, 1985, 22: 349-352. Renault, B., Ragot, R. and LesOvre, N. Correct and incorrect responses in a choice reaction time task and the endogenous components of the evoked potential. In: H.It. Kornhuher and L. I)eecke (Eds.), Motivation, Motor and Sensory Processes of the Brain; Electrical Potentials, Behaviour and ('linical / s e . El,~cvier, Amsterdam, 1980: 647-654. Renault, B., Fiori, N. and Giami, S. I,atencies of event related potentials as a tool for studying motor processing organization. Biol. Psychol.. 1988, 26:217 230. ROsier, F. Endogenous E R " P s " and cognition: probes, prospects and pitfalls in matching pieces of the mincl-body puzzle. In: A.W.K. Galliard and W. Ritter (Eds.), Tutorials in ERP Research: Endogenous Components. North-Holland, Amsterdam, 1983: 9-35. Ruchkin, D.S. and (}laser, E.M. Simple digital filters for examining CNV and P300 on a single trial basis. In: D.A. Otto (Ed.), Multidisciplinary Perspectives in Event-Relamd Brain Potential Research. U.S. Government Printing Office Washington, DC, 1978: 579-584. Staid, H.G.O.M., Mulder, G. and Mulder, I..J.M. The continuous flow model revisited: perceptual and central motor aspects. In: R. Johnson, J.W. Rohrbaugh and R. Parasuraman IEds.), ('urrent Trends in Event-Related Potential Research (EEG Suppl. 40). Elsevier, Amsterdam, 1987 270 278.
