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PSYCHOLOGICAL SCIENCE

Research Report
A NEURAL SYSTEM FOR ERROR DETECTION
AND COMPENSATION
William J. Gehring,l Brian GOSS,l Michael G.H. Coles, 1 David E., Meyer,2 and
Emanuel Donchin 1
lUniversity of Illinois and 2 University of Michigan

Abstract-Humans can monitor actions & Brooks, 1986, for an exception). Much ~hen response accuracy is important to
and compensate for errors. Analysis of of the work investigating the issue has the subject. We predicted that the ampli-
the human event-related brain potentials inferred the existence of a monitoring tude of the ERN will vary with the rela-
(ERPs) accompanying errors provides and compensation apparatus from be- tive weight the subject's task assigns to
evidence for a neural process whose ac- havior that appears to be compensatory, accuracy and speed. Furthermore, if the
tivity is specifically associated with mon- as when subjects execute an error and ERN is a manifestation of an error-
itoring and compensating for erroneous then quickly execute the correct re- compensation mechanism, there ought
behavior. This error-related activity is sponse (Rabbitt, 1966, 1968) or slow to be a relationship between its ampli-
enhanced when subjects strive for accu- down subsequent to errors (Laming, tude and the dynamics of the erroneous
rate performance but is diminished when 1968; Rabbitt, 1966). These phenomena, responses. We varied, therefore, the
response speed is emphasized at the ex- while consistent with the existence of an speed and accuracy requirements placed
pense of accuracy. The activity is also error-monitoring system, are not conclu- upon the subject, and we measured sev-
related to attempts to compensate for sive, however, because they could occur eral performance parameters that may
the erroneous behavior. without the presence of an error- reflect compensatory activity, including
detection system: The apparent correc- the force with which the subject exe-
tion could simply be a correct response cutes a response, the probability of cor-
A fundamental characteristic of hu- produced in parallel with, but more recting the error, and the speed of re-
man cognition is its fallibility. People slowly than, the error. Furthermore, a sponses following the error. We embed-
rarely perform tasks perfectly, even response on a trial after an error could be ded these manipulations and measures in
though the costs of imperfection can be slow because of a persistence of the pro- a task known from previous research to
devastating (Norman, 1988; Reason, cessing problem that caused the error. produce erroneous response activation
1990). It is plausible to assume that the More direct evidence for an error- (see Coles, Gratton, Bashore, Eriksen,
prevalence of errors, and their high cost, monitoring mechanism comes from de- & Donchin, 1985; Gratton, Coles,
has led to the evolution of mechanisms scriptions of an event-related brain pro- Sirevaag, Eriksen, & Donchin, 1988).
that monitor the accuracy of actions and cess that appears to be evoked contem-
attempt to correct, or compensate for, poraneously with the commission of
errors. That such mechanisms exist is, erroneous responses. We (Gehring, METHOD
indeed, assumed explicitly or implicitly Coles, Meyer, & Donchin, 1990) have re-
in many theories of cognition. For exam- ported that an error-related negativity Subjects
ple, concepts of error monitoring are in- (ERN) appears selectively on error trials
cluded in theories of action (MacKay, in choice reaction time experiments. The Six University of IIIinoisstudents (4
1987), learning (Adams, 1971; Rumel- ERN takes the form ofa sharp, negative- men and 2 women) between the ages of
hart, Hinton, & Williams, 1986), speak- 18 and 26 served as subjects. All were
going deflection of up to 10 J.LV in ampli-
ing (LeveIt, 1989), and consciousness tude and is largest at electrodes placed right-handed and had normal or cor-
(Kosslyn & Koenig, 1992). Monitoring over the front and middle ofthe scalp. Its rected-to-normal vision. They received
mechanisms are also implied by theories onset is shortly after the onset of elec- $3.50 per hour plus bonuses for partici-
of executive or supervisory cognitive tromyographic (EMG) activity detected pation.
control systems (Logan, 1985; Shallice, in the limb that is about to make an error,
1988; Stuss & Benson, 1986). and it peaks about 100 ms following its
Given the frequency with which the Stimuli
onset. A similar observation was made,
concept of error monitoring is invoked, it independently, by Falkenstein, Hohns- Stimuli were presented on a Hewlett-
is remarkable that there is little direct bein; Hoormann, and Blanke (1990). Packard computer display (#1310A).
neurophysiological evidence for the ex- In this report, we present evidence Subjects sat 1 m from the screen, such
istence of error-detection and -compen- that the ERN is a manifestation of the that each letter subtended approximately
sation systems (but see Gemba, Sasaki, activity of a system associated with mon- OS of visual angle. One of four arrays
itoring the accuracy of the response sys- occurred on each trial: The two compat-
Address correspondence to William J. tem and with compensating for errors. ible arrays were HHHHH and SSSSS,
Gehring, who is now at the Center for Neu- Our test is predicated on the assumption and the two incompatible arrays were
roscience, University of California, Davis, that if the ERN manifests the activity of SSHSS and HHSHH. The probability of
Davis, CA 95616. such a system, it will be more active each of these arrays was .25. A fixation

VOL. 4, NO.6, NOVEMBER 1993 Copyright © 1993 American Psychological Society 385
PSYCHOLOGICAL SCIENCE

Error Detection and Compensation

dot, visible throughout the experiment, occurred in the other arm, to identify er- submitted to separate 3 (Speed Condi-
appeared 0.1 0 below the central letter of rors that were corrected. EMG onset la- tion) x 2 (Compatibility) repeated mea-
the array. An asterisk appeared as a tency was defined as the first point, fol- sures analyses of variance (ANOVAs).
warning stimulus 1,000 ms prior to the lowing the stimulus, that exceeded 4 For correct EMG onsets, the main effect
onset of each stimulus array. standard deviations of the baseline, pre- of speed condition was statistically sig-
stimulus activity. nificant, F(2, 10) = 57.21, p < .0001,
MS e = 239.01, as was the planned anal-
Procedure ysis oflinear trend, F(I, 5) = 65.589, p <
Psychophysiological Recording .0005, MSe = 416.8. For proportion cor-
Subjects were required to respond rect, the same effects were evident (main
with the left or right hand according to The electroencephalogram (EEG) effect of speed condition: F[2, 10] =
the identity (H or S) of the letter at the was recorded from midline and lateral 69.62, p < .0001, MSe = 0.014; linear
center of the letter array. Subjects re" scalp electrode sites: Fz ' Cz ' Pz ' C3' (4 trend: F[I, 5] = 126.73, P < .0001, MS e
sponded by squeezing zero-displacement cm to the left ofC z ), and C4' (4 cm to the = 0.016).
dynamometers (as in Gratton et aL, right of Cz ) according to the 10/20 sys-
1988). (For details of the effects of the tem, referenced to linked mastoids. Hor-
compatibility manipulation-the flanking izontal and vertical eye movements and Error-Related Negativity
letters-see Coles et aI., 1985.) forearm flexor EMG activity were re-
Subjects received financial penalties corded from standard locations (see The event-related potential (ERP)
for errors and bonuses for responses Gratton et aI., 1988). All electrodes were data confirmed the presence of error-
faster than a particular deadline. These Medical Associates disposable Ag/AgCI related brain electrical activity. Re-
values were varied such that in the speed electrodes affixed with Grass EC2 elec- sponse-locked EEG activity was ob-
condition subjects responded quickly trode cream. Impedance for EEG and tained by extracting an epoch of 1,000
with little regard for errors, in the accu- electrooculogram (EOG) electrodes was ms in duration that began 400 ms before
racy condition subjects responded below 10 KOhm; EMG electrode imped- the first detectable EMG on each trial.
slowly and accurately, and in the neutral ance was less than 20 KOhm. The EEG records for correct and incor-
condition subjects responded at an inter- EEG, EOG, and EMG signals were rect responses were then averaged sepa-
mediate level of speed and accuracy. In amplified and conditioned, and eye rately to yield the waveforms for the Cz
each of three experimental sessions, sub- movement artifacts were corrected, as in electrode (located at the center of the
jects had to perform 520 trials under each Gratton et al. (1988). The derived Volt- scalp), shown in Figure 1. The ERP as-
of the three speed-accuracy conditions. age x Time functions were digitized at sociated with an incorrect response was
The order of conditions was counterbal- 100 Hz for 2,100 ms, starting 100 ms characterized by a negative-going deflec-
anced. prior to the presentation of each warning tion (the ERN) that began at around the
stimulus. time of the incorrect response and
peaked about 100 ms later. The deflec-
Responses tion was not evident in the averages
based on trials in which the subjects re-
A criterion overt response was de- RESULTS AND DISCUSSION 1 sponded correctly.
fined as a squeeze that exceeded 25% of To quantify this activity, we filtered
maximum squeeze force (determined for Pedormance Data the EEG using a 59-point equal-ripple,
each subject and each hand separately), zero-phase-shift, optimal finite impulse
and reaction time (used to compute bo- response low-pass filter with a passband
EMG data revealed that the speed-
nuses) was defined as the time at which accuracy instructions were effective. cutoff frequency of 8 Hz and a stopband
the force exceeded this criterion. Several cutoff frequency of 10 Hz (cf. Farwell,
EMG onset latency on correct trials and
hundred initial trials were deemed Martinerie, Bashore, Rapp, & Goddard,
accuracy (percentage correct) were as
"practice" trials, and on these trials 1993). The amplitude of the ERN was
follows: for the speed condition, 236.9
only, subjects received feedback, in the ms, 67.6%; for the neutral condition, defined as the difference between the av-
form of an auditory click, whenever their 271.8 ms, 78.8%; for the accuracy con- erage amplitude of the waveform within
squeeze response exceeded the crite- a 50-ms window centered at 100 ms post-
dition, 304.4 ms, 89.4%. These values
rion. EMG onset and the average amplitude of
. (proportion correct values were trans-
For the analyses in this article, we a baseline for the 50 ms immediately pre-
formed with the arc sine transform;
used the latency and side of the first de- ceding EMG onset. We submitted the
Neter, Wasserman, & Kutner, 1985) were
tectable EMG activity to classify the re- data to a 5 (Electrode) x 3 (Speed Con-
sponse as .correct or incorrect on each dition) x 2 (Response Accuracy) x 2
trial. This classification allowed us to 1. The Greenhouse-Geisser correction was
(Compatibility) ANOVA. The main ef-
subdivide the error category according applied when appropriate to correct for pos- fect of accuracy was F(I, 5) = 120.58, p
to the level of squeeze amplitude at- sible violations of the analysis of variance as- < .0001, MS e = 5,236.69.
tained on each. trial (see below). We also sumption of sphericity. The text lists cor- To evaluate the relationship between
noted whether a second EMG response rected p values. the ERN and the importance of errors to

386 VOL. 4, NO.6, NOVEMBER 1993


PSYCHOLOGICAL SCIENCE

W.J. Gehring et at.

discriminant function procedure and the


-2.5 resulting posterior probability measures
-correct
were sensitive to the distinctive wave-
o ---incorrect
shape seen in Figures I and 2.
2.5 We found the amplitude of the ERN
to be related to three measures of the
5.0 subjects' compensatory behavior. Figure
3 (right panel, top) shows the mean am-
JlV 7.5 ',plitude of the error response squeeze for
~ach posterior probability quartile. The
10.0 figure suggests that the larger the ERN,
the smaller the error squeeze. To con-
12.5 firm this pattern, we submitted these
measures to a 3 (Speed Condition) x 4
15.0 (Quartile) repeated measures ANDYA.
17.5 L -_ _--J..-_ _---1. l . -_ _-l...-_ _---J A main effect of quartile (F[3, 15] =
-400 -200 0 200 400 600 11.66, p < .01, MS<! = 831.63) and a sig-

t
EMG Onset
msec
nificant analysis of linear trend (F[I, 5]
= 19.22, p < .01, MS e = 1,505.12)
both support the observation that large
ERNs were associated with small error
squeezes, suggesting that the ERN might
Fig. 1. Comparison of response-locked event-related potential activity, recorded at
the Cz electrode, for correct and incorrect trials.

the subject, we compared the ERNs de- amplitude derived from stepwise dis- --c:onod
__inCOtreCt

rived from the three accuracy condi- criminant analysis (SWDA) of the ERP
tions. Because any effect of speed- data. SWDA produces a discriminant
accuracy emphasis could be attributed to function-vector of weights-that when JiV:
the overall difference in response speed cross-multiplied with the actual ERP
9
between conditions, we selected from waveforms produces scores whose val- 12
each condition trials whose reaction ues optimally distinguish correct from in-
1~·I:-:OO,.-1.-:.2~OO:---l---,Oi,-L...,200~J--::!400~~600
times fell within the same 50-ms reaction correct trials. To build the functions, we
time window. For each subject, the re- used a randomly chosen subset of cor- Neutral
-6
action time bin was either 250 to 300 ms rect and incorrect trials in the accuracy
-3
or 200 to 250 ms. As can be seen in Fig- condition. We limited the analysis to the
ure 2, the ERN was largest for the accu- epoch from 100 ms prior to EMG onset
3
racy condition and smallest for the speed to 200 ms following EMG onset for the JiV 6
condition, with the neutral condition in- F z (frontal) and Cz (central) channels
9
termediate. We submitted the mean am- (relative to a loo-ms prestimulus base-
12
plitude measures (at Cz) from error trials line). For most subjects, the major con-
1~4':-OO:--'--:_20:±-O....L--O~.1.--:200::!:::---'---~40~O-'--:::!600
to a single-factor (speed condition) re- tribution to the discrimination between
peated measures ANDYA. A significant correct and incorrect trials was provided Accuracy
effect of speed condition (F[2, 10] = by activity at the Cz electrode in the -6
-3
6.19, p < .05, MSe = 371.48) and a sig- postresponse portion of the epoch.
nificant analysis of linear trend (F[l, 5] For each trial in the experiment, the
= 8.44, p < .05, MS e = 507.7) con- SWDA computed the posterior probabil- JiV
3
6
firmed that the ERN increased in ampli- ity that the response on a trial was in fact
9
tude from speed to neutral to accuracy an error. We used these posterior prob- 12
conditions. These data· are consistent ability values as estimates of the ampli-
1~·':-OO:--'--_2",!OO~l...-O~.L.....,200::!:::---'----,J400~J......':":!600
with the view that the ERN is associated tude of the ERN on each trial. For the
with an error-related processing mecha- analyses below, we partitioned the data t
EMGOnset
msec
nism, whose activity is modulated by the according to four quartiles of the distri-
degree to which accuracy is important to bution of posterior probabilities, which
Fig. 2. The effects of different speed-
the subject. yielded four different levels of ERN am- accuracy instructions on the error-
We now turn to additional data that plitude. Figure 3 (left panel) shows the related negativity recorded at Czo For
suggest the ERN is related to attempts to average ERPs (at the Cz electrode) for each of the three conditions, trials with
compensate for .errors. To analyze this these four levels of ERN amplitude on the same reaction time were used (see-
relationship, we used a measure of ERN error trials. These data confirm that the text).

VOL. 4, NO.6, NOVEMBER 1993 387


PSYCHOLOGICAL SCIENCE

Error Detection and Compen-sation

The ERN 12

10
Error Force

-8 ERN Size (quartile) Kg 6

··..
••••• - ( 1 ) small 4
• • - - (2) medium
-4
·• .•
2
•• •• _.- (3) large
•••••• (4) X-large 0
•• •••
o •· .
• •
....
: 1\ : 0.8
Probability
of Error-Correction

.... ..,...
:/
./'
\: "0
Ql
13
4 ....
Ql
.... 0.7

'/\1\.
0

JlV 0
0
c

8 t
0
C-
0.6
o
....
0-
0.5
12
300 Correct RT on Next Trial

16 U
Ql
290

.s
(J)

280
I-
a:
13 270
200 400 600 ....
Ql
.... 260
0
0
msec 250
2 3
EMG Onset small medium large X·large
ERN Quartile

Fig. 3. Relationship between error-related negativity (ERN) amplitude and three measures of compensatory behavior. Left panel:
Average event-related potentials at the Cz electrode as a function of the four levels of the posterior probability measure of ERN
amplitude. Right panel, top: Error squeeze force in Kg as a function of the four ERN levels. Right panel, middle: Probability of
error correction as a function of the four ERN levels. Right panel, bottom: Correct reaction time on the trial following an error
as a function of the four ERN levels. .

reflect an attempt to brake the erroneous 0.059, and a subsequent analysis of


response. linear trend, F(l, 5) = 6.54, p < .06, MSe monitoring and compensation. This interpre-
Figure 3 (right panel, center) further = 0.15, confrrmed that the probability tation is, however, clouded by the possibility
suggests that the larger the ERN, the that a response was corrected increased that the ERNs on these trials could be elicited
greater the probability that the error with the size of the ERN. 2 by the second, erroneous response. The close
would be followed by a correct response temporal proximity of the correct response
on the same trial. We submitted the and the subsequent error on these trials
probability that a response was cor- 2. We included correct trials in this analy- makes it difficult to determine which response
sis because we found the ERN to be present elicited the ERN. Indeed, our attempts to'dis-
rected (converted with the arc sine trans-
on correct trials in which the correct response ambiguate these interpretations (e.g., by ex-
form) to a 3 (Speed Condition) x 2 (Re- was followed by an error. If such correct re- amining trials in which the interval between
sponse Accuracy) x 4 (Posterior Proba- sponses were themselves "corrected," then th~ correct response and the subsequent error
bility Quartile) repeated measures the presence of the ERN on these trials is was relatively large) were not successful, in
ANDVA. A significant main effect of consistent with our hypothesis that the ERN part because of the small number of trials'-
quartile, F(3, 15} = 5.94, p < .05, MSe manifests the operation of a system for error available for such an analysis.

388 VOL. 4, NO.6, NOVEMBER 1993


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W.J. Gehring et al.

Finally, the larger the ERN, the (e.g., Angel, 1976) postulating that the served in monkeys performing go/no-go
slower the subjects' response on the im- brain retains a neural record of the motor tasks: No-go trials elicit field potential
mediately following correct trial (Fig. 3, commands it sends to the effectors-an activity in the prefrontal cortex that
right panel, bottom). We examined the efference copy-that is used to judge the may be involved in response inhibition
correct reaction times on trials subse- accuracy of the movement. (Sasaki & Gemba, 1986; Sasaki, Gemba,
quent to the error trials, submitting these ERN amplitude measures provide ad- & Tsujimoto, 1989). Gemba and Sasaki
reaction times to a 3 (Speed Condition) ditional constraints. The relationship be- (1989) observed analogous scalp-re-
x 4 (Previous Trial's ERN Amplitude tween the speed-accuracy manipulation corded potentials in humans.
Quartile) repeated measures ANDVA. and ERN activity suggests that the pro- : Whatever its neural substrate, the
The main effect of amplitude quartile, cess manifested by the ERN is influ- ERN provides a way to assess the be-
F(3, 15) = 5.58, p < .05, MSe = 39.78, enced by the importance of errors to the havior of the error-detection and -com-
and a planned test oflinear trend, F(l, 5) subject: The more costly the error, the pensation system. This measure should
= 11.14, P < .025, MS e = 59.15, were greater the likelihood or strength of the enable further development and refine-
both significant. These results suggest activity manifested by the ERN. The as- ment of a comprehensive theory of error
that the tendency to adopt a more con- sociation between the ERN and a variety detection and compensation and, more
servative strategy following an error of compensatory behaviors suggests that generally, of the executive control of in-
(originally described by Rabbitt, 1966, the error-detection system provides in- formation processing.
and Laming, 1968) is related to the size put to different compensatory systems.
of the ERN on the error trial. These mechanisms appear to include Acknowledgments-This research was
fast-acting systems that can inhibit and supported by Grant MH 41445 from the
correct the error as it occurs, as well as National Institute of Mental Health and by
CONCLUSIONS systems that control response strategies, a National Science Foundation graduate
fellowship to the first author. Portions of
whose effects are evident on future tri- this work were presented at the 30th
Taken together, these data are consis- als. Meeting of the Society for Psychophysio-
tent with the existence of a brain system It is important to note that our data logical Research, Boston, October 1990.
for error detection and compensation, are consistent with an "active" error- William Gehring presented the work re-
whose behavior is manifested at the compensation process that is invoked ported in this article in partial fulfillment
of the requirements for the doctoral de-
scalp in a measure of brain potential ac- when an error is detected. Theories can gree in psychology at the University of Il-
tivity, the ERN. We confirmed our pre- often account for behavior that seems linois at Urbana-Champaign. The authors
vious observation that the ERN occurs compensatory without having to postu- gratefully acknowledge the critical com-
at around the time that subjects make er- late error-detection mechanisms (e.g., ments of Marie Banich, Neal Cohen, Gary
Dell, Susan Garnsey, Timothy Harpur,
roneous responses. In addition, we Dell, 1986). In this particular experi- Wendy Heller, Art Kramer, and Greg
found that the magnitude of the ERN ment, subjects might generate a weak er- Miller.
was affected by the degree to which ac- ror response or a response that appears
curate performance was emphasized (see to correct the error without actually de-
Falkenstein et aI., 1990, for a similar ob- tecting the error. It is not clear, how-
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