The anterior cingulate as a conflict monitor: fmri and ERP studies

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1 Physiology & Behavior 77 (2002) The anterior cingulate as a conflict monitor: fmri and ERP studies Vincent van Veen a,b, Cameron S. Carter a,b,c,d, * a Department of Psychology, University of Pittsburgh, Pittsburgh, PA 15213, USA b Center for the Neural Basis of Cognition, Pittsburgh, PA 15213, USA c Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA 15213, USA d Department of Neuroscience, University of Pittsburgh, Pittsburgh, PA 15213, USA Received 31 July 2002; accepted 22 September 2002 Abstract We propose that the anterior cingulate cortex (ACC) contributes to cognition by detecting the presence of conflict during information processing, and to alert systems involved in top-down control to resolve this conflict. Here, we review several functional magnetic resonance imaging (fmri) and event-related potential (ERP) studies that have used simple response interference tasks, and propose that ACC activity is activated prior to the response during correct conflict trials and reflected in the frontocentral N2, and immediately following error trials and reflected in the error-related negativity (ERN). Furthermore, we suggest that certain disturbances in cognition and behavior in common mental disorders such as schizophrenia and obsessive-compulsive disorder (OCD) can be understood as resulting from alteration in performance monitoring functions associated with this region of the brain. D 2002 Elsevier Science Inc. All rights reserved. Keywords: Cingulate; Attention; Conflict; Interference; Event-related potentials; Functional magnetic resonance imaging; N2; Error-related negativity; Schizophrenia; Obsessive-compulsive disorder 1. Introduction The anterior cingulate cortex (ACC), located on the medial surface of the frontal lobes, has been the subject of increasing interest during the previous decade. It is usually thought of as playing an important role in attentional and motivational processes [1]; however, its exact role in cognition has been the subject of debate. We have recently proposed a comprehensive theory of human ACC functioning that we believe accounts for most, if not all, of the neuroimaging and event-related potential (ERP) data available about this region of the brain [2,3]. According to this view, the ACC is activated in response to conflict occurring between incompatible streams of information processing. Following conflict detection, regions of the lateral prefrontal cortices and other areas associated with attentional control are engaged to resolve the conflict. The * Corresponding author. Western Psychiatric Institute and Clinic, 3811 O Hara Street, Pittsburgh, PA 15213, USA. Tel.: ; fax: address: (C.S. Carter). current review will focus on discussing evidence supporting the conflict theory. In particular, we focus on data obtained using two methodologies from modern cognitive neuroscience that we have used to test predictions of this theory: functional magnetic resonance imaging (fmri) and ERPs. fmri has excellent spatial resolution but relatively poor temporal resolution, while ERPs have excellent temporal resolution but relatively poor temporal resolution. The two methodologies are thus mutually complementary in developing a spatio-temporal map of human brain activity during cognition. 2. fmri studies of ACC functioning An earlier, popular view of ACC functioning maintained that it was involved in exerting attentional control and selection for action [4]. According to this view, the ACC guides the selection and processing of stimuli that need to be acted upon or are otherwise relevant to the currently active task or goal representation. In contrast, we maintain that ACC activity is often observed when control is engaged because a strong engagement of /02/$ see front matter D 2002 Elsevier Science Inc. All rights reserved. PII: S (02)

2 478 V. van Veen, C.S. Carter / Physiology & Behavior 77 (2002) control is needed in situations in which conflict is high [3], conflict and control being confounded in most studies. Two recent fmri studies from our lab have contrasted the control view with the conflict theory. One study [5] did so by analyzing between-trial reaction time (RT) adjustments and their relationship to ACC activity during a version of the Eriksen flanker interference paradigm [6]. In this paradigm, participants respond to a centrally presented target while trying to ignore simultaneously presented flanker stimuli, responding to the identity of the target with a left or right button press. It is usually found that RTs and error rates are smallest when these flankers are identical to the target (congruent), and highest when they are mapped onto the opposite response hand (incongruent), indicating that conflict, and thus the need for control, are high during such trials. In this paradigm, control is dynamically adjusted depending on the trial type, as reflected in between trial-rt adjustments; following high-conflict trials, control is more strongly engaged [7]. Thus, when an incongruent trial is preceded by an incongruent trial (ii trial), RT is shorter than when it is preceded by a congruent trial (ci). This phenomenon provided a way to dissociate between conflict and control: during ii trials, control is highly engaged and conflict is relatively low; during ci trials, control is lower and conflict is highest. The selection-for-action hypothesis of ACC functioning would thus have predicted stronger ACC activation during ii trials. However, fmri showed that the ACC was most strongly engaged in response to the ci trials, supporting the conflict theory [5]. A second experiment designed to critically distinguish between conflict and control-based explanations of ACC functioning manipulated participants expectancy about the frequency of high-conflict versus low-conflict trials [8]. It has been shown that, when most trials in a block are congruent, RT interference is very large. Since most trials are low-conflict in such a condition, control does not need to be strongly engaged, thereby making incongruent trials very high in conflict. In contrast, when most trials are incongruent, RTs interference is much smaller, presumably reflecting the fact that control is more strongly engaged [9]. As in the previous study, this study provided the opportunity to contrast conflict and control. Instead of the Eriksen flanker interference task, it used a version of the Stroop color-word naming interference paradigm. In this paradigm, participants have to name the color in which a word is written; the usual finding is that RTs and error rates are smallest when color and word are identical, and highest when the color and the word are incongruent (e.g., the word red written in green letters, the correct response being green ) [10]. Results, again, supported the conflict theory; fmri showed that ACC activity to incongruent trials was highest during blocks when these were relatively infrequent, rather than frequent [8]. When considering interference tasks, an important issue to address is to determine at what level of processing conflict takes place [10]. In the same vein, we might ask what levels of processing are monitored by the ACC for the presence of conflict. In the incongruent condition of tasks such as the Eriksen or Stroop tasks, one dimension of the stimulus is associated with the correct response and another dimension of the stimulus leads to an incorrect response. Thus, it has been argued that incongruent stimuli in the Eriksen or Stroop interference tasks not only elicit response conflict, but also conflict at the level of stimulus encoding or target detection, and a comparison between congruent and incongruent stimuli would confound these two sources of interference [11]. A first attempt to start addressing the issue regarding what kinds of conflict the ACC responds to was done using a version of the Eriksen flanker task [12]. In addition to a congruent condition (CO), in which flankers and target are identical, and a response-incongruent condition (RI), in which flankers and target are mapped onto opposite response fingers, we used a condition in which flankers are different than the target, but mapped onto the same hand as the target, simply by associating two letters with each response finger. This latter condition presumably reflects conflict at the level of stimulus encoding or target detection without response conflict (stimulus-incongruent, SI), and RTs in this condition have been found to be greater than RTs to CO stimuli, but smaller than RTs to RI stimuli [6]. Thus, comparing CO to SI trials presumably isolates stimulus conflict, whereas comparing SI to RI trials isolates response conflict. While RTs indeed showed both stimulus and response conflict (CO < SI < RI), comparing brain activity elicited by these three trial types revealed that the ACC did not distinguish between the CO and SI stimuli [12]. ACC activity was enhanced only to RI stimuli, suggesting that in this kind of interference task, the ACC only monitors for the presence of response conflict. The activation found in the Eriksen flanker study is in the same location as that in our earlier study using a different version of this paradigm [5]. Specifically, the ACC activation seen in these and many other interference tasks is located in the rostral cingulate motor zone [13]. From its strong connectivity to other parts of the motor system, it is not surprising that this area is most strongly activated to response conflict during these kinds of tasks (Fig. 1). Preliminary data from our lab, however, suggest that depending on the task, ACC activation might not be limited to response conflict, but might respond to other sources of conflict as well. This would be consistent with previous findings that suggest that ACC activity can be elicited in situations without motor requirements: ACC activity has been observed in response to conflict induced by unexpected error feedback in the Wisconsin Card Sorting Task [14], to conflict occurring at a conceptual level by having participants read stories that do not form an integrated narrative [15], or to conflict induced when

3 V. van Veen, C.S. Carter / Physiology & Behavior 77 (2002) Fig. 1. Area of the anterior cingulate cortex engaged by response conflict but not conflict at the stimulus level during the Eriksen flanker task during functional MRI (from [Ref. 12]). participants are instructed to inhibit sexual arousal while watching erotic films [16]. 3. ERP correlates of ACC activity Another popular theory of ACC functioning was based on research using ERPs. In the presence of response conflict, people are known to sometimes make fast, impulsive errors based on partial, incomplete analysis of the stimulus. Such impulsive errors are known as slips [17]. Research has shown that within ms following the commission of a slip, a large, negative deflection is observed in the ERP, with a maximum at frontal or central sites [18,19]. Subsequent dipole modeling of this so-called error-related negativity (ERN) suggested an ACC generator [2,20]. Later fmri studies confirmed that the ACC showed increased activity during error trials [21,22]. The discovery of the ERN led to the hypothesis that it might reflect the detection that an error was made, based on a comparison between the actual movement and the intended movement; a mismatch would give rise to the ERN [23]. However, a recent fmri study using a guilty knowledge task observed strong ACC activation during lies [24]. This is inconsistent with a comparison-based account of error detection, because there is no mismatch between the intended and the actual response; during lies, these are identical. We interpret the existence of the ERN as consistent with a conflict-based explanation of ACC functioning [2]. It is known that following error commission, stimulus processing continues, leading to fast activation of the correct response [25 27]. The moment at which the correct and incorrect responses are both maximally activated, thus, the moment of greatest conflict, occurs therefore immediately following the error, which is of course the moment that the ERN peaks. Evidence suggests that the timing of events during correct incongruent trials is somewhat similar. After trial onset, the incorrect response is prepared based on partial stimulus analysis; however, before its activation reaches response threshold, the correct response manages to override the incorrect response activation leading to a correct response [26,27]. Thus, during correct incongruent trials, ACC activation is expected prior to the response, whereas during error trials the ACC is activated immediately following the response (Fig. 2). We hypothesized that ACC activity during correct conflict trials is reflected in the frontocentral N2 component of the ERP [2]. We used the same version of the Eriksen task described earlier [12] using high-density EEG. Importantly, we found that the ERN and N2 had identical scalp distributions, and dipole source localization suggested the same caudal ACC generator for both peaks, strongly suggesting that these two components reflect the same process [2]. As we collected enough trials to analyze error rates, we found that accuracy was reduced in response to RI trials, but was similar to CO and SI trials, showing that only the RI trials elicited Fig. 2. Conflict-related (left, stimulus-locked) and error-related activity (right, response-locked) ERP waveforms observed as subjects performed the Eriksen flanker task (from Ref. [2]). CO: congruent condition in which targets and flankers are the same, SI: stimulus-incongruent condition in which targets and flankers are different but map to the same response hand, RI: response-incongruent condition in which targets and flankers are different and map to responses on opposite hands, ERN: error-related negativity.

4 480 V. van Veen, C.S. Carter / Physiology & Behavior 77 (2002) increased response conflict. Since fmri data had shown that the ACC is activated only to response conflict in this task, we expected the N2 too to be increased only to RI stimuli, but similar in amplitude to CO and SI stimuli. This was indeed what we found [2]. These data provide evidence that the ERN and N2 reflect conflict detection by the ACC. Indeed, in a variety of studies using different tasks, including Go/NoGo, target search and other conflict tasks, the frontal-central N2 is largest to those conditions that involved the most conflict (as reflected in increased error rates and/or RTs) [2,27 31]. For instance, much like in the fmri study described earlier [5], the N2 has been observed to be larger to conflict trials that followed low-conflict trials than to conflict trials that followed conflict trials [29]. Thus, we suggest that the ACC activation observed during correct conflict trials in fmri studies is the same as measured by the frontocentral N2 in ERP studies (Fig. 3). Interestingly, fmri research had previously indicated that the rostral ACC was engaged during error trials [22]. Our dipole analysis of the response-locked waveforms suggested that the rostral ACC was activated following the ERN, and reflected in the error positivity, the component that follows the ERN [2]. Both the error positivity [32] and the rostral ACC [1] have been associated with affective processes, and our dipole model is thus consistent with previous findings and theories, linking the two lines of research. One prediction that follows from the hypothesis that both the ERN and the frontocentral N2 reflect conflict detection by the ACC is that both should have the same cognitive properties. Interestingly, it has been shown that both the ERN and the N2 can be elicited unconsciously. During an anti-saccade task, in which participants have to make a saccade to the opposite side of a peripheral abrupt onset cue, participants are often unaware of their errors. The ERN, Fig. 3. Scalp topography and dipole source solutions of the N2 and ERN in the Eriksen flanker task. Note identical topographies and source locations in the caudal region of the ACC (from Ref. [2]).

5 V. van Veen, C.S. Carter / Physiology & Behavior 77 (2002) however, is still present following such unconscious errors [33]. Likewise, targets preceded by subliminally presented primes elicited enhanced RTs and error rates, and an increased N2, when the prime was incongruent with the target [34]. These findings thus suggest that conflict monitoring is a process that can occur outside of awareness. In neuroimaging studies, too, ACC activity has sometimes been found to be engaged by unconsciously occurring conflict [35]. Although the hypothesis that the (caudal) ACC monitoring system is an implicit one still has to be addressed more thoroughly, the findings so far are in sharp contrast to earlier views that regarded the ACC as a structure contributing in an important way to consciousness [36]. 4. Implications for neuropsychiatric disorders Disturbances in the function of the ACC have been reported in a number of psychiatric disorders, including schizophrenia and obsessive-compulsive disorder (OCD). In schizophrenia, cognitive control is impaired, and the level of cognitive dysfunction in the illness is correlated with behavioral disorganization and with social and occupational disability [37]. The conflict monitoring theory of schizophrenia would predict that if ACC dysfunction is contributing to these deficits, decreases in both error-related and conflict-related activity would be observed in the ACC, and these would be associated with decreases in trial-to-trial adjustments in performance. Many PET and fmri studies have shown decreased ACC activity in schizophrenia [38,39]. ERP studies of the N2 and ERN in this illness have shown decreases in these indices of ACC functioning, too [40]. Finally, using fmri, we observed a reduction of error-related activity in the ACC in schizophrenia, associated with decreases in post-error adjustments in performance in this illness [39]. These data suggest that a disruption of ACC functioning contributes to impaired cognitive control in schizophrenia through an impairment in its performance monitoring function. OCD is characterized by obsessive thoughts and repetitive behaviors accompanied by a persistent sense of doubt and dread. Functional imaging studies of OCD have often reported increased activity in the ACC in this illness [41]. An increased ERN has been reported in this illness, which has been interpreted as an overactive error monitoring system [42]. However, OCD patients are often observed to perform in the normal range, but to take a very cautious approach to task performance, suggesting that OCD patients are unusually sensitive to conflicts. Thus, we propose that hyperactivity in the ACC should be seen during both incorrect trials as well as correct conflict trials, indicative of an overactive conflict monitoring system. We tested this hypothesis using event-related fmri, and confirmed that both conflict-related and error-related activity were indeed increased in the caudal ACC of OCD patients, compared to healthy controls [41]. These two lines of research suggest a role for the ACC in both the lack of control in schizophrenia and the excess of control in OCD. We believe that the approach outlined in the studies described above is also likely to be a useful one in the investigation of neural mechanisms underlying a number of other neuropsychiatric disorders, including ADHD and substance abuse disorders, in which disturbances in cognitive control and internal monitoring are prominent features. References [1] Bush G, Luu P, Posner MI. Cognitive and emotional influences in anterior cingulate cortex. 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