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Alcohol Consumption Impairs Detection of Performance Errors in Mediofrontal Cortex

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Science  13 Dec 2002:
Vol. 298, Issue 5601, pp. 2209-2211
DOI: 10.1126/science.1076929

Abstract

The anterior cingulate cortex (ACC) is a critical component of the human mediofrontal neural circuit that monitors ongoing processing in the cognitive system for signs of erroneous outcomes. Here, we show that the consumption of alcohol in moderate doses induces a significant deterioration of the ability to detect the activation of erroneous responses as reflected in the amplitude of brain electrical activity associated with the ACC. This impairment was accompanied by failures to instigate performance adjustments after these errors. These findings offer insights into how the effects of alcohol on mediofrontal brain function may result in compromised performance.

Alcohol consumption gives rise to a diffuse pattern of neurochemical changes (1) that lead to subtle impairments in cognitive operations (2). These effects modulate, for instance, the competence to drive a car (3, 4). Adequate driving performance requires that cognitive operations can be adapted rapidly and flexibly in response to environmental cues (5). Behavioral adjustments may be prompted by external cues (e.g., traffic signs or a child suddenly crossing the street) or by the outcome of internal action monitoring. Adaptive control of behavior involves the ability to monitor ongoing processing in the cognitive system for signs of conflict or erroneous outcome (6). Psychophysiological and neuroimaging studies concluded that the anterior cingulate cortex (ACC) is a central component of the neural circuit for action monitoring (7, 8). This control system (9–12) is involved in detecting the activation of erroneous or conflicting responses (11).

An important psychophysiological index of action monitoring is the error-related negativity (ERN) (13) or error negativity (14), an event-related brain potential (ERP) component most likely originating from the ACC (10–12, 15). The recording of this component at the scalp reflects the detection of action errors and response conflicts (6, 16). ERN is observed after errors of choice as well as failures to inhibit an action (16) and after action slips that are recognized as such by the subject as well as after errors that elude the subject's awareness (17). Thus, ERN reflects the activity of a preconscious action-monitoring system. The efficiency of other preconscious processes (such as the perceptual detection of acoustic deviance) is attenuated by alcohol (18). Here, we examine whether alcohol impairs the detection of action slips as expressed by ERN.

Subjects completed a version of the so-called “flanker task,” chosen because of its demonstrated efficacy in eliciting ERNs after performance errors as induced by distractors (11,15, 16). In the flanker task, a target arrow could be flanked by congruent or incongruent distractors (pointing in the same or opposite direction as the target, respectively); subjects were to respond to the direction of the target and to ignore distractor arrows. Subjects performed the task after a placebo and two different doses of alcohol that corresponded to blood alcohol concentrations of 0.0, 0.4, and 1.0 per mil (‰), respectively (19).

Adequate performance in the flanker task relies on effective engagement of interference control processes, such as response inhibition (20). If alcohol consumption were to induce a reduction in the efficiency of control processes in general, then impairments in both interference control and error detection could result. In that case, effects of alcohol on ERN amplitude would result indirectly from the more general effect, not from a direct effect on ACC. Although the proficiency of response inhibition can be reduced by alcohol consumption (21, 22), this effect can be countered by strengthening motivation through instruction or reward (23). To prevent alcohol-induced changes in interference control from influencing the error monitoring results, subjects were instructed and trained to attain constant levels of flanker interference in reaction time (RT) across alcohol conditions. Likewise, instruction and practice kept response accuracy constant at a predesignated level to circumvent confounding effects of alcohol on the speed-accuracy tradeoff (24–26).

Processing speed was reduced by alcohol consumption [mean valueM = 352, 360, and 382 ms in placebo, low-dose, and high-dose conditions, respectively; F(2,26) = 7.51;P = 0.007], whereas accuracy remained unaffected [F(2,26) = 0.18]. Helmert contrasts indicated that RT was shorter in placebo conditions than in the alcohol conditions [F(1,13) = 11.18, P = 0.005] and that RT was longer after the high-alcohol dose than after the low dose [F(1,13) = 5.69, P = 0.033]. This pattern of performance (detailed in table S1) justified an examination of the effects of alcohol on error monitoring and interference control without potentially confounding effects in terms of the speed-accuracy tradeoff or in terms of alcohol-induced stimulus misperception (which would also affect accuracy).

Compared to congruent trials, incongruent arrays were associated with slower responses [M = 348 versus 380 ms,F(1,13) = 128.93, P < 0.001] and more errors [M = 4.8 versus 19.8%, F(1,13) = 125.94, P < 0.001]. The magnitude of these typical congruity effects was not modulated by alcohol (table S1) [F(2,26) = 0.08 and 0.03 for RT and accuracy, respectively]. We further examined two measures of the inhibition of incorrect responses (19). First, the reduction of flanker interference effects that is typically observed in the RTs of slow, as compared to fast, responses provides a sensitive behavioral index of selective suppression of incorrect responses in conflict tasks (20, 27). Alcohol failed to moderate this reduction of flanker interference (fig. S1) [F(2,26) = 1.43]. Second, the amplitude of the N2 component of the ERP provides an electrocortical expression of the engagement of response inhibition processes in conflict tasks (28) that is diminished by alcohol (29). The N2 is typically larger after incongruent as compared to congruent trials. Although this effect was replicated in the present data [F(1,13) = 10.04, P = 0.007], N2 amplitude was not modulated by alcohol [F(2,26) = 2.24]. Moreover, alcohol failed to influence the effect of congruence on N2 [F(2,26) = 0.57] (Fig. 1). Taken together, these results indicate that subjects successfully prevented the detrimental effects of incongruent distractors from being magnified by the effects of alcohol. Any effects of alcohol on error detection, which was examined next, are therefore not contaminated by effects on interference control. In addition to reflecting prefrontal response inhibition, N2 amplitude has recently been argued to represent contributions from ACC in monitoring conflicting activations during correct responses to incongruent stimuli (15). The absence of alcohol effects on N2, in that case, may suggest that the susceptibility of conflict monitoring in ACC to alcohol effects is prevented from being expressed in N2 amplitude, for instance because the relatively small effects on N2 are absorbed by noise or by simultaneous inhibition-related contributions to N2 (that are not modulated by alcohol in this study). We then turned to an analysis of a less equivocal index of error monitoring in ACC, the ERN.

Figure 1

Stimulus-locked grand-average ERPs recorded from the medial frontocentral electrode position FCz during correct responses to congruent (thin lines) and incongruent (thick lines) stimuli at placebo, low dose, and high dose (top, middle, and bottom, respectively). S denotes the time of the stimulus presentation. Relative to congruent trials, incongruent trials are characterized by an enhancement in the negative component identified as N2 (peaking between 200 and 300 ms poststimulus).

Apparent in the ERPs associated with incorrect responses under placebo was a distinct ERN that was largest in amplitude at frontocentral scalp sites proximal to ACC and that attained its maximum amplitude shortly after response initiation (Fig. 2). The ERN was attenuated significantly by alcohol consumption [F(2,26) = 6.61,P = 0.005] (Fig. 3). Helmert contrasts confirmed that placebo conditions differed from the alcohol conditions [F(1,13) = 13.32, P = 0.003] whereas low- and high-dose conditions did not differ [F(1,13) = 0.12]. Like ERN, the effect of alcohol on ERN had a frontocentral scalp distribution (fig. S2). Thus, alcohol selectively affected the amplitude of ERN, an effect that was not confounded with alcohol-induced changes in accuracy levels or in the sensitivity to flanker interference.

Figure 2

Response-locked grand-average ERPs recorded from FCz during correct responses (thin lines) and during errors (thick lines), pooled across congruent and incongruent trials, at placebo, low dose, and high dose (top, middle, and bottom, respectively). Rdenotes the time of the response. Relative to correct responses, erroneous responses are characterized by a negative component identified as the ERN (peaking about 50 ms after the response). The ERN is followed by a positive deflection, typically identified as the error positivity (16).

Figure 3

(Left) Amplitude of the ERN component identified in the ERPs at FCz associated with incorrect responses under various doses of alcohol. Error bars reflect standard errors. ERN amplitude is reduced after alcohol consumption.

If alcohol consumption impairs action monitoring in the brain, then some measurable and meaningful consequence of such failure should be evident. To the extent that the ACC fails to detect errors, it should fail also in signaling the need to instigate performance adjustments after these errors. Thus, under alcohol conditions subjects may fail to display the reduction in congruity effects typically observed after error commission (27,30). Indeed, although flanker interference effects were reduced after errors in placebo conditions [F(1,13) = 5.01,P = 0.043], no such reduction was observed in low- or high-dose alcohol conditions [F(1,13) = 0.21 and 0.40, respectively] (Fig. 4; details in table S2).

Figure 4

(Right) Performance adjustments after error commission. Interference effects on RT are reduced after errors (relative to the effects after correct responses) under placebo but not under alcohol conditions. Error bars as in Fig. 3.

Although alcohol-induced detriments have been documented across a wide array of cognitive processes (2–4,18, 21–25), the relation between effects on the brain and those on behavioral performance are still poorly understood (1). The present study documents that the consumption of alcohol (even in moderate doses) compromises performance by attenuating the brain's capacity to detect action slips. The ability to monitor ongoing processing in the cognitive system for signs of erroneous outcome is a prerequisite for adequate performance (involving flexible executive control to adapt cognitive operations in response to environmental prompts, such as when driving a car or when operating machinery). On the basis of the present data we cannot decide whether alcohol induces a pervasive reduction in action monitoring or rather an increase in the incidence of lapses in this ACC function. Both effects could potentially elicit the observed reduction in ERN amplitude.

Beyond the demonstration of ethanol- induced effects on ERP correlates of performance, the present ERP findings offer new empirical insights into how the effects of alcohol consumption on the mediofrontal brain may result in compromised performance. Even modest impairments in the detection of action slips by the ACC may result in deficits in signaling the need to instigate performance adjustments, as evidenced by adjustment failures in posterror performance.

Supporting Online Material

www.sciencemag.org/cgi/content/full/1076929/DC1

Materials and Methods

Figs. S1 and S2

Tables S1 and S2

  • * To whom correspondence should be addressed. E-mail: richard{at}psy.uva.nl

REFERENCES AND NOTES

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