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The Journal of Neuroscience, January 1, 2000, 20(1):464-469
Medial Frontal Cortex in Action Monitoring
Phan
Luu1, 2,
Tobias
Flaisch3, and
Don M.
Tucker1, 2
1 Department of Psychology, University of Oregon,
Eugene, Oregon 97403, 2 Electrical Geodesics, Inc., Eugene,
Oregon 97403 and 3 University of Konstanz, 78457 Konstanz, Germany
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ABSTRACT |
Effective behavior requires continuous action monitoring.
Electrophysiological studies in both monkeys and humans have shown activity in the medial frontal cortex that reflects dynamic control and
monitoring of behavioral acts. In humans, the centromedial frontal
cortex shows an electrical response within 100 msec of an error, the
error-related negativity (ERN). The ERN occurs only when subjects are
aware of making an error, suggesting that a critical factor may be
self-monitoring of the action process. In the present study, we
examined late responses in a deadline reaction time task, in which the
subject becomes increasingly aware of making an error as the response
becomes increasingly late. We found evidence of response conflict
before errors defined by late responses but not before errors defined
by incorrect responses. The results also show a linear increase in the
amplitude of the ERN with increasingly late responses. These data
suggest that frontal networks provide dynamic representations that
monitor and evaluate the unfolding action plan.
Key words:
anterior cingulate; error-related negativity; action
monitoring; awareness; response conflict; event-related potential
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INTRODUCTION |
Action monitoring is an important
component of self-regulation. This component is best appreciated when
self-monitoring is defective, as in patients with the alien-hand
syndrome. With lesions to the centromedial aspect of the prefrontal
lobe, including the supplementary motor area (SMA), these patients feel
as if certain self-initiated actions have a foreign source, i.e., as if
some of their actions are not volitional (Goldberg, 1985 ). In recent years, scalp electrophysiological studies in humans have provided insight into the neurophysiological processes of action monitoring and
error detection. Falkenstein et al. (1991) identified a negative deflection in the event-related potential (ERP) that is associated with
an error response [the NE or the N2c by Kopp et
al. (1996) ]. This negativity can be observed in both stimulus-locked
and response-locked ERPs. It has a frontocentral distribution and peaks
within 80-110 msec after the response in response-locked averages.
Other researchers independently observed this effect (Gehring et al.,
1993 ) and termed it the error-related negativity (ERN). Dipole modeling of a 64-channel recording showed that the neural source of the ERN lies
in the vicinity of the anterior cingulate gyrus (Dehaene et al., 1994 ).
However, because of inaccuracies of dipole models, contributions from
other areas of the medial prefrontal cortex, including the SMA, cannot
be ruled out.
The amplitude of the ERN does not seem to be influenced by stimulus
differences (Bernstein et al., 1995 ), nor does it seem to be involved
in attempts to inhibit or correct erroneous responses (Scheffers et
al., 1996 ) or in making response selections (Badgaiyan and Posner,
1998 ). It can be observed in error responses during both auditory and
visual tasks (Falkenstein et al., 1991 ). Although error feedback can be
sufficient (Miltner et al., 1998 ), it is not required to produce the
ERN (Gehring et al., 1993 ).
In the anterior cingulate cortex, single-cell recordings in monkeys
have revealed cells that track the commission of an error (Niki and
Watanabe, 1979 ). Importantly, these same cells also respond to the
omission of a reward for a correct response. Motivational factors also
influence the amplitude of the ERN in human studies. Tucker et al.
(1999) observed a centromedial frontal negativity (stimulus-locked, at ~480 msec) in response to task feedback, with a
more negative deflection for negative than for positive feedback. This
effect was larger for subjects who reported either pleasant or
unpleasant arousal during the task, suggesting that it may have
reflected the subject's level of motivation.
Gehring et al. (1993) originally observed that the amplitude of the ERN
was larger when task instructions emphasized accuracy rather than speed
of responding. More recently, Gehring et al. (2000) showed that the
amplitude of the ERN was larger in obsessive-compulsive patients than
in normal controls, and within the patients it was larger for those
with more severe symptoms. Luu et al. (2000) also found that in the
initial stages of the experiment high-negative affect subjects
(characterized as subjects who experience high levels of subjective
distress) initially exhibited larger ERN amplitudes compared with the
low-negative affect subjects. Dikman and Allen (2000) found that
individuals with low-trait socialization exhibit smaller ERN
amplitudes in tasks that penalize error responses when compared with
high-trait socialization individuals. No differences in ERN amplitude
were observed between these two groups when error responses prevented
the earning of rewards. Thus, subjects who are characterized as being
high or low on the dimension of subjective distress and who engage in
excessive self-monitoring show exaggerated ERNs.
Despite the increasing amount of evidence from these experiments, the
psychological nature of the ERN remains unclear. Some authors have
suggested that it indexes error-related monitoring (Gehring et al.,
1993 ), whereas others have argued that it indexes response conflict
(Carter et al., 1998 ). More recently, Carter et al. (1999) have
emphasized an evaluative role for the anterior cingulate. In this
model, the anterior cingulate specifically evaluates (i.e., detects)
processing conflicts that may lead to a decrement in behavioral
performance. Because of the centromedial frontal distribution of the
ERN, a response-conflict interpretation is consistent with the many
findings of anterior cingulate activity under conditions of both
cognitive and response conflict (Pardo et al., 1990 ; Posner and
DiGirolamo, 1998 ). Another important issue is whether awareness is
required to generate the ERN. Dehaene et al. (1994) showed that when
subjects were unaware of making an error, no ERN was observed.
In a speeded task, subjects can commit two types of errors. The first
type of error is the error of commission. This type of error is a
response hand error. Given a particular response deadline, not all
correct responses will occur before the imposed time limit. These late
responses make up the second class of errors: errors of speed. Both
types of error responses (incorrect responses and errors of speed) are
defined as erroneous by the parameters of the task because points are
deducted in both cases. In the present study, errors of speed are
similar to the errors defined in time estimation tasks used by Miltner
et al. (1998) and Badgaiyan and Posner (1998) . In other words, in these
two studies, responses must be generated within a particular time
interval for them to qualify as correct. What these researchers find
are that errors in these tasks are not obvious to subjects and that an
error feedback signal is required to generate the ERN.
Errors of speed are particularly interesting. As a response becomes
increasingly late, subjects become increasingly aware that the response
is past the deadline and thus in error. Explicit awareness of the error
may not be the critical factor, of course. Significant increases in
self-monitoring may be underway before subjects are able to report that
they are aware of being late.
In the present study, we sorted responses in a speeded task into those
that were slightly, moderately, and very late. To examine the role of
response conflict as subjects were attempting to decide these late
responses, we analyzed the lateralized readiness potential (LRP). The first hypothesis was that greater response conflict as evidenced by the LRP would be associated with greater motor preparation of the incorrect response and that this index of response conflict would correlate with the magnitude of the ERN. The second hypothesis was that increasing lateness would be associated with increasing self-monitoring and with increasing amplitude of the ERN,
even though the response was the correct choice.
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MATERIALS AND METHODS |
Subjects. Twenty-one subjects participated in the
experiment. Subjects were recruited from the Department of
Psychology's subject pool. All subjects participated to fulfill
a course requirement. Subjects also had opportunities to earn a
monetary reward as described in Procedure. All subjects had normal or
corrected-to-normal vision and were fluent in English. They ranged in
age from 18 to 26 years (19.4 ± 1.9, mean ± SD). Eight
subjects were male, and 19 subjects were right-handed. None of the
subjects was currently taking prescription medications. These subjects
are a random subset of the subjects reported in Luu et al. (2000) .
Task. The task used is known as the Eriksen flanker
task (Eriksen and Eriksen, 1979 ). It was used originally to
study stages of information processing. Important for our purposes,
this task also requires subjects to monitor their responses as they
make speeded decisions. It has been used by Gehring et al. (1993) to study the ERN. In this task, subjects were presented with a warning cue, an asterisk, at the center of a screen above a fixation mark, which was present for the entire experiment. The warning cue was presented for 804 msec, after which it was replaced with one of the
following strings of target letters: HHHHH, SSHSS, SSSSS, or
HHSHH. The bottom of the letter strings was presented 0.1° above the
fixation mark, and each letter subtended 0.5°. The probability of
each string of letters was 0.25. The target letter string was presented
for 107 msec.
The subject's task was to indicate as quickly and as accurately as
possible which letter was in the center by pressing a key with one hand
if the center letter of the target string was an H and another key with
the opposite hand if the center letter was an S (keys were
counterbalanced across subjects). The timing of the reaction time
(RT) began with the presentation of the target.
The criterion for RT deadline for each subject was based on his or her
median RT on practice trials. During the practice trials, subjects were
informed that the deadline was set at 400 msec. Subjects were presented
with practice trials in blocks of 40. The median RT was only determined
for the last 30 trials of each block, because the first 10 trials were
used to orient the subjects to the task. Subjects were allowed to
practice as much as they wanted. However, most subjects only chose to
complete one block of practice trials (40). Subjects were not informed
that their median RT from the practice trials would be used to
determine their RT deadline for the task; however, they were instructed regarding the new deadline value that would be used during the formal
task run that followed. The range of the RT deadline across subjects,
as determined from the practice trials, was 343-651 msec (408 ± 96 msec, mean ± SD). The response interval was 1005 msec from the
time of target onset. If subjects did not respond by this time for a
particular trial, no response time was recorded, and the trial was
marked as having no response.
After the response interval, a feedback signal informing the subject of
the status of the response was presented above the fixation mark. The
feedback could indicate that the response was correct and on time (a
plus sign), correct but too late (an exclamation point), or incorrect
or no response (a minus sign). The feedback signal was presented for
1099 msec. The recording of the EEG began 201 msec before cue onset and
terminated with the removal of the feedback signal. The intertrial
interval varied between 1525 and 2505 msec.
EEG recording. EEG was recorded from 128 scalp sites using
the 128-channel Geodesic Sensor Net (Tucker, 1993 ). The impedance of
all electrodes was between 10 and 40 k . All recordings were initially referenced to Cz. EEG was recorded using a 0.1-50 Hz bandpass (3 dB attenuation). The signals were sampled at 125 samples/sec and were digitized with a 12-bit analog-to-digital converter.
Because of volume conduction, no site on the head, including
traditional reference sites such as the mastoids or earlobes, can be
regarded as being an "inactive" reference site (Tucker et al.,
1994 ). Therefore the EEG was rereferenced against an average reference
(Bertrand et al., 1985 ). Editing of the EEG for movement, eye movement,
blink artifacts, and noise was performed by a computer algorithm. The
artifact-free EEG was then averaged locked to the response for each
subject according to the different types of responses: correct, Early
late, Mid late, Late late, and error.
EEG averaging. Correct responses were those responses that
consisted of the correct hand and occurred before the deadline. Error
responses were defined as responses with the incorrect hand, regardless
of speed. Late responses were defined as responses with the correct
response hand but whose latency exceeded the response deadline. Because
we are interested in response conflict, only incompatible trials (i.e.,
HHSHH and SSHSS) were included in the averages and in the analyses of
the late responses (for both the lateralized readiness potential and
late ERN measures). Late responses were separated into three categories
according to the following procedure: For each individual subject, his
or her late responses were rank-ordered and divided into three even intervals (i.e., bins). The intervals were labeled Early late, Mid
late, and Late late. The Early late interval contained responses that
barely exceeded the RT deadline, and the Late late interval contained
responses that were the latest, with the Mid late interval in between.
The RT values for each of these intervals were computed separately for
each subject.
After the EEG was averaged according to the five different response
types, it was baseline-corrected using the 400 msec window before the
response and digitally filtered with a 30 Hz low-pass filter (using a
600-400 msec preresponse baseline did not affect the results).
Lateralized readiness potential. The bereitschaftspotential
(BP) or motor readiness potential is a negative-going deflection in the
EEG centered around the dorsal motor and mediodorsal areas before a
motor response. It is believed to reflect the preparatory set and
intention to act (Lang et al., 1988 ). This potential can begin up to a
second or more before a self-paced act. When the BP is taken as a
difference between the contralateral and ipsilateral sites, it is
referred to as the LRP and is used as a measure of motor priming
by stimulus events (see Coles et al., 1988 ). By using the LRP, we can
measure response competition directly.
Procedure. After being prepared for the EEG recording by
application of the Geodesic Sensor Net (Tucker, 1993 ), subjects were seated in front of a monitor in an EEG recording booth, with distance and alignment to the screen controlled by use of a chin rest. After
completion of recording of the resting EEG, subjects were given
instructions on how to perform the task.
Each subject started the experiment with 3200 points. Subjects were
informed that if they responded correctly and before a predetermined
time limit no points would be lost. Subjects were also told that
correct but late responses (errors of speed) were penalized 1 point for
every 100 msec that they were tardy and that response errors (errors of
commission) would result in a loss of 8 points. To increase motivation
to perform well on the task, we told the subjects that the total amount
of points that they managed to retain by the end of the task would be
rewarded at a rate of 0.5 cent for every point. It was emphasized that this monetary reward was in addition to the course credits that they
would receive for participating.
As a further manipulation of motivation levels, subjects were informed
that at the end of the study they would be given feedback about their
overall performance relative to others who had performed the task. (All
subjects exerted adequate effort on the task and were told that they
had done well.) Subjects then proceeded to practice the task. After
subjects were comfortable with the task, they completed 800 trials,
broken down into 200-trial blocks. Between blocks, subjects were
allowed to rest and move about. The time spent on the task took between
1 and 1.5 hr.
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RESULTS |
Behavioral data
First, we analyzed the distribution of stimulus type (compatible
vs incompatible) according to late responses. As expected, lateness of
response interacted with stimulus compatibility
[F(2,40) = 12.4; p < 0.001]. This interaction indicated that more incompatible trials were
associated with the Late late than with the Early late responses and
conversely that fewer compatible trials were associated with the Late
late than with the Early late responses. All subsequent analyses that
include late responses will only contain data from incompatible trials,
because we are specifically interested in response competition.
The median RT of each late interval was obtained and entered into an
ANOVA model with response type (correct, Early late, Mid late, Late
late, and error) as the only factor. The analysis revealed that there
was a significant difference in median RT between response types
[F(4,80) = 227.3; Geisser-Greenhouse
corrected p < 0.001]. Means comparisons revealed that
the correct and error responses did not differ in median reaction time.
In contrast, the correct RTs were significantly faster than Late late
RTs [F(1,80) = 646.4;
p < 0.001]. These results are not surprising because the reaction times themselves were the basis of response-type separation for the late responses.
Response-locked ERP data
Lateralized readiness potential
In the present study, we averaged the EEG to correct, Early late,
Mid late, Late late, and error responses separately for left- and
right-hand responses. The LRP was then defined for each response type
as the average of the difference between the EEG over the contralateral
motor cortex (to the response hand) minus the EEG over the ipsilateral
motor cortex. In other words, the LRP is defined as: [(C4' C3') + (C3' C4')]/2. Within this formula, the average should be
zero, or close to zero, when there is no (or equal) activity observed
over the motor cortex. However, as motor cortices are activated
asymmetrically according to the response hand, the value departs from
zero. Because appropriate motor priming is observed over the
contralateral motor cortex as a developing negativity before a
response, correct motor priming should be observed as a negative
deflection in the LRP according to the above formula.
Because the LRP is a difference wave, interpretation of the difference
should rely on careful inspection of the original waveforms to
determine the source of the difference. Figure
1 presents the raw voltage waveforms for
three representative conditions. It can clearly be seen that when
subjects make a correct right-hand response there is minimal difference
between the electrodes overlying the motor cortex. In contrast, when
subjects make a right-hand response that is late, the voltage over the
ipsilateral motor area is more negative. Conversely, when subjects
respond with the right hand and it is an error, the contralateral motor
area is more negative. Thus, in the present study the LRP over all the
conditions (Fig. 2) does appropriately
reflect asymmetric motor activation.

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Figure 1.
Raw voltage waveforms at C3' and C4' for three
representative conditions. Right-hand key presses for correct
(top), Late late (middle), and error
(bottom) responses. Time 0 marks the time of
response.
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Figure 2.
The lateralized readiness potentials for the five
response types. Time 0 marks the time of response.
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It can be observed in Figure 2 that ~300 msec before response onset,
the LRPs for the five response types begin to diverge from each other.
The amplitudes of the LRPs associated with correct and Early late
responses are smallest. Next, in order of positive LRP amplitudes, are
the Mid late and Late late responses. These LRPs indicate that the
later the response, the more likely it was that subjects were preparing
to respond with the incorrect hand. The error responses, in contrast,
are associated with a negative deflection in the LRP, indicating that
there was no ambivalence, and only preparation of the motor cortex
contralateral to the hand that actually responded (which was in this
case the wrong response).
We took the average amplitude of the LRP between 280 and 160 msec
before response onset for all five types of responses. These values
were entered into an ANOVA model with response type as the single
factor. The analysis revealed a significant effect of response type
[F(4,80) = 7.7; G-G
p < 0.001]. A means comparison confirmed the above
differences between the correct and Late late responses
[F(1,80) = 9.1; p < 0.01] and the error and Late late responses
[F(1,80) = 26.6; p < 0.001].
Error-related negativity
Figure 3 shows the response-locked
ERP for each type of response at the centromedial frontal ERN maximum
site (channel 6, ~3 cm rostral to Cz). The ERN can be clearly
observed for error responses, peaking ~80 msec after response onset.
However, ERNs also can be seen for late responses (errors of speed but
not of action). Moreover, the amplitude of the ERN varies linearly with the lateness of the response.

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Figure 3.
The error-related negativity, shown at a channel
~3 cm rostral to Cz, can be observed in all types of responses, but
its amplitude is largest for error responses. The time of response is
marked by the vertical line.
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To verify that the late ERNs are similar to the ERN observed for error
responses, topographic maps of the correct, late (collapsed across all
three late types), and error responses are displayed in Figure
4. In Figure 4 the data were filtered
with a 4 Hz high-pass filter to remove the slow, parietal positivity
associated with response onset. This parietal positivity possibly
reflects the P3 associated with the stimulus, because most
reaction times fall within the P3 interval (Luu et al., 2000 ). Removing
the large positivity that overlaps with the ERN allows for the
grayscale palette to cover the range of the ERNs associated with the
correct and late responses (which are of much smaller amplitude) and
thus to bring out the topography of the negativity. Figure 4 shows that
the negativity associated with the correct and late responses has the
same topographic distribution as that of the ERN for error responses.

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Figure 4.
Topographic map of the error-related negativity at
80 msec after response for correct, late, and error responses.
Darker colors indicate greater
negativity. The orientation of the map is top looking
down and nose toward the front. See Results for
details.
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We measured the average potential of the ERN over a 40-144 msec
postresponse epoch from channel 6 for the five response types and
entered the values into an ANOVA model. Response type was entered as
the single factor into the model. The results revealed a significant
main effect [F(4,80) = 10.6; G-G
p < 0.001]. Means comparisons confirm that the ERP
associated with the Late late response type was significantly less
positive than the ERP associated with the Early late response type
[F(1,80) = 6.0; p < 0.04]. The error response type was significantly more negative than
all of the other types [F(1,80) = 22.7; p < 0.001 (correct);
F(1,80) = 36.1; p < 0.001 (Early late); F(1,80) = 22.3;
p < 0.001 (Mid late);
F(1,80) = 12.6; p < 0.005 (Late late)]. We also tested whether there were latency
differences between the different response types but found no
significant differences.
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DISCUSSION |
In this study, we examined human frontal lobe electrical activity
in relation to errors of inaction (taking too long to respond) as well
as errors of incorrect action (pressing the wrong button). ERNs over
the centromedial frontal lobe were seen within 100 msec of the response
in both cases. In this speeded task, subjects knew that they had to
respond within a target interval or the response would be considered
late and scored as an error. The late responses varied from those
barely missing the deadline to ones that were made much later. We
hypothesized that as responses become increasingly late, the
self-monitoring of these responses should become increasingly strong
and the ERNs should increase linearly. By comparing the ERP associated
with different degrees of response lateness, we tested this hypothesis
and confirmed that increasingly late responses were associated with
increasingly large ERNs.
We interpret these findings to indicate that self-monitoring is
integral to the ERN. For an early response, there are only moderate
demands on self-monitoring. For an increasingly late response, as
subjects try to avoid the error of responding past the deadline, there
are increasing demands for attentional self-monitoring that appear to
be reflected in increasing activity in the centromedial frontal cortex.
Analysis of the LRP suggested that the late responses were also
associated with response conflict. The LRP is a measure of asymmetric
motor preparation, and it has been used as a measure of motor
preparation in response to task demands (Coles et al., 1988 ; Hackley
and Valle-Inclan, 1998 ). The LRP has also been used to study the
effects of response competition arising from incongruent primes that
are presented subconsciously (Dehaene et al., 1998 ). Dehaene et al.
(1998) found that the response competition indexed by the LRP can be
validated using functional magnetic resonance-imaging (fMRI) methods.
These researchers used a lateralized measure of the BOLD
response in motor cortices and found the effect to be identical to the
effect using the LRP (i.e., incongruent primes activated the wrong
motor areas). Finally, the LRP has been used to study early response
activation in classical conflict paradigms, such as the Eriksen flanker
task and the Stroop task, and to study incompatible response priming
induced by incompatible noise (Coles et al., 1988 ).
In the present study, the late responses were associated with
inappropriate priming of the motor cortex ipsilateral to the eventual
response hand. By looking at just the incompatible trials, it could be
seen that the degree of response lateness is related to the degree of
priming of the inappropriate response hand. The LRP that is observed is
likely caused by the effects of the incompatible stimuli, because the
onset of the LRP occurs ~100 msec after stimulus onset. That is, the
asymmetric motor priming begins ~300 msec before the response (the
responses range between 300 and 700 msec after stimulus onset).
Although increasing response conflict was associated with the increased
ERN for late responses, there was no LRP evidence of response
competition for the incorrect response errors. Rather, the subjects
appeared to make the wrong response without any (conflicted) preparation of the correct response. Because the LRP is a difference measure, it is possible that high levels of conflict (i.e., high levels
of simultaneous activation of both left and right motor cortices) can
result in near-zero LRP values. Figure 1 shows, however, that the
condition in which equal activity is observed over the motor cortices
is the correct response condition. For responses in which the most
response conflict is expected (i.e., Late late and error responses),
the motor activation is maximally asymmetric. The wrong hand is primed
in both cases. For the Late late responses, the motor activation
eventually switches to the side contralateral to the correct hand. For
the error responses, it remains with the wrong hand, and the wrong
response key is pressed. Although Figure 1 shows the data for the right
hand, identical effects were observed for the left-hand responses.
Therefore, we conclude from the present data that response conflict was
associated with the ERN for one kind of error in this experiment (the
late responses) but not another (the incorrect responses).
There was a brief inversion of the LRP after the response was made
(Fig. 2 at ~60 msec after the response), and this effect was greater
for incorrect response errors than for late errors. Thus, judging from
the LRP, one might think that a brief period of response conflict, or
perhaps response correction (activating the motor area for the correct
hand), could have occurred immediately after the incorrect response (at
~60 msec after the response), just before the ERN (at ~80 msec
after the response). However, inspection of the waveforms from both
left- and right-hand errors shows that this postresponse inversion of
the LRP was caused by a brief negative deflection over the
contralateral motor cortex (C3') of the correct, nonresponding, right
hand only for the left-hand error response. It would be expected that
if this was an index of a response correction, then this negativity
would be observed over C4' (contralateral to the correct, nonresponding
hand) for the right-hand errors, but in fact, the pattern was the same
as that of the left-hand errors. In debriefing, subjects in fact reported that they experienced little or no response conflict on the
incorrect response trials. Several subjects reported that the error
responses felt impulsive and that they had to slow down deliberately to
avoid committing consecutive errors.
According to the response-conflict monitoring hypothesis proposed by
Carter et al. (1998) , error responses are made under conditions of high
response conflict. Although this explanation fits well with the late
responses of the present study, it does not fit the data from incorrect
responses. The response-conflict hypothesis also has difficulty
explaining the studies using error feedback to elicit the ERN
(Badgaiyan and Posner, 1998 ; Miltner et al., 1998 ). It was argued by
Badgaiyan and Posner that error feedback does not require a generation
of a response, and therefore, the ERN is not associated with motor or
premotor events. This suggestion has been confirmed recently by
Leuthold and Sommer (1999) using response-locked ERNs. These
researchers were able to show that the ERN is not part of the
stimulus-response pathway. Rather, they argue that the ERN reflects a
general error-processing mechanism.
Although the response-conflict hypothesis remains an important one for
explaining anterior cingulate and medial frontal activation during
errors, we favor an interpretation that emphasizes the more general
function of self-monitoring of the motor plan. Conflicting responses
inherently engage self-monitoring, but self-monitoring often occurs in
the absence of conflicting responses.
Results from animal studies imply that self-monitoring of the error is
required for the appearance of error-related cortical potentials
(Brooks, 1986 ; Gemba et al., 1986 ). Brooks et al. observed cortical potentials in monkeys that were related to errors in task
performance. These potentials were similar to the human ERN in several
ways. First, they were recorded in the anterior cingulate cortex.
Second, they were surface-negative. Finally, the time course was very
similar to that of the ERN. Importantly, before the monkey had gained
an effective representation of the correct response for the task, the
error responses did not elicit error potentials. Thus, the current
awareness of the difference between correct and error responses (or at
least the working memory substrate of monkey awareness) appears
essential to the formation of error-related potentials.
The present results provide further evidence that activity in the
medial frontal lobe closely parallels the control of attention (Posner
and Rothbart, 1998 ). Because ERN-like centromedial negativities are
seen in stimulus-locked ERPs when subjects discriminate good from bad
targets in a video game (Tucker et al., 1999 ), or in other
experiments when a feedback signal is given (Miltner et al., 1998 ),
motivational evaluation appears integral to this class of frontal lobe
responses. Similarly, when subjects make decisions on whether
emotionally significant trait words (e.g., stingy, bold, or geek) apply
to them, a centromedial effect at 350 msec after the stimulus
discriminates both endorsement and the emotional valence (good/bad) of
the words (D. M. Tucker, A. Hartry-Speiser, R. Desmond, L. McDougal, T. Flaisch, and P. Luu, unpublished observations). These
reports are consistent with the well known effects of medial prefrontal
lesions, which cause patients to be apathetic and unconcerned about the
consequences of their actions (Rylander, 1947 ; Tucker et al., 1995 ).
Considering the evidence in its entirety, we propose that the core
contribution to attention from the anterior cingulate gyrus and
associated medial frontal cortex is evaluative self-monitoring along an
affective dimension. When subjects are concerned with the outcome of an
action, the cingulate gyrus and associated centromedial frontal lobe
provide a dynamic monitoring of that action and its effects. As
evidenced in the present findings of progressively larger ERNs to
responses increasingly past the deadline, this self-monitoring process
appears to be a dynamic operation, providing continuous motivational
evaluation, and presumably continuous executive guidance, to direct the
neural mechanisms of behavior.
 |
FOOTNOTES |
Received July 21, 1999; revised Oct. 12, 1999; accepted Oct. 14, 1999.
This research was supported by the National Institute of Mental Health
Grants MH42129 (Depression and Anxiety as Neural Control Processes) and
MH42669 (Depression and Spatial Orienting) to D.M.T. We thank Michael
Posner for his careful reviews.
Correspondence should be addressed to Dr. Phan Luu, Department of
Psychology, University of Oregon, Eugene, OR 97403. E-mail address:
pluu{at}oregon.uoregon.edu.
 |
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