COGNITION AND BEHAVIOR particular the dorsal ACC,is involved in the with pre-response conflict clustering slightly tradeoff between speed and accuracy of monitoring of response conflict (/8).Re- more dorsally than foci activated during responding that place the cognitive system n sponse conflict occurs when a task concur- error and feedback monitoring (2/,22). in a more cautious(as opposed to impulsive) IAL rently activates more than one response Second,single-cell recordings in monkeys response mode,and (ii)increases in control n tendency;for example,when the stimulus suggest that different (neighboring)neurons that improve the efficiency of information primes a prepotent but incorrect response or within specific pMFC regions can be in- processing.Speed/accuracy tradeoffs may be EC when the correct response is underdeter- volved in different aspects of performance expressed in“post-error slowing,”the ob- mined.Often,incorrect response tendencies monitoring (4).Thus,the overlap between servation that reaction times typically slow 。 are overridden in time by the overt correct the activation foci identified in human down after errors and correct,high-conflict response,resulting in high response conflict neuroimaging studies does not necessarily trials (18).Changes in control,induced by before the correct response (pre-response imply identical functions for all neurons or such trials,can become evident in improved conflict).In contrast.occasional errors neuronal ensembles within the pMFC. performance due to reduced interference resulting from premature responding are A potential link between the outlined from distracting information.For example, characterized by response conflict after the theories of pMFC functions is that pre- the increase in reaction times normally response:The correct response tendency response conflict and decision uncertainty observed for incongruent stimuli (where resulting from continued stimulus processing signal a reduced probability of obtaining target and distractor stimuli call for opposing conflicts with the already executed incorrect reward,whereas errors and unexpected responses)as compared to congruent stimuli response.In underdetermined responding negative feedback signal the loss of antici- (when distractors elicit the same action as (that is,under conditions requiring choosing pated reward.The pMFC,particularly thethe target stimulus)is typically reduced on from a set of responses,none of which is RCZ,is engaged when the need for adjust- trials after errors (30). more compelling than the others),decision ments to achieve action goals becomes Several observations are consistent with a uncertainty occurs.Thus,decision uncertain- evident.Interestingly,the monitoring pro- close link between modulations of pMFC ty involves conflict similar to response cesses examined here cluster primarily in the activity and subsequent changes in perform- conflict observed in tasks in which a transition zone between the cingulate and ance.One study categorized trials in terms of prepotent response is overridden (18). paracingulate (areas 24 and 32),association their ERN amplitudes and found that the The conflict-monitoring theory is consist- (area 8),and premotor cortices (area 6),an reaction time on the subsequent trial slowed ent with the neuroimaging evidence for area that has extensive connections with progressively with increasing ERN ampli- pMFC activation in response to errors, brain areas involved in the control of tude on the current trial (/4).In a similar reviewed above,and with the timing of the cognitive and motor processes and has been vein,response errors on a two-alternative response ERN,indicating post-response con- implicated in the regulation of autonomic forced-choice task are foreshadowed by flict.In addition,the theory predicts that the arousal (23,24).This presumably places the modulation of this pMFC activity during pMFC should be active in correct trials pMFC in a strategically located position for the immediately preceding (correct)re- characterized by high pre-response conflict, signaling the need for performance adjust- sponse.Error-preceding trials were charac- a prediction that has been confirmed by a ments and for interacting with brain areas terized by increased positivity in the time large number of studies(Fig.1B).Moreover, involved in motor and cognitive,as well as window typically associated with the ERN the predicted timing of such conflict-related autonomic and motivational,functions. (③I).This“error--preceding positivity”may activity is consistent with the occurrence of reflect a transient disengagement of the an ERN-like component,the N2,just before Performance Adjustments monitoring system,resulting in occasional the response (19).Finally,the detection of Although the pMFC is consistently impli- failures to implement appropriate control high post-response conflict may be used as a cated in action monitoring,the mechanisms adjustments and hence in errors.Experimen- reliable basis for internal error detection, underlying the implementation of subsequent tal factors that affect ERN amplitude may thereby obviating the need for an explicit performance adjustments are less well un- also affect subsequent performance adjust- error detection mechanism (/9). derstood.Two important questions are:(i)Is ments.For example,alcohol consumption The theory further holds that,upon the there a link between pMFC activation led to a reduction in the ERN amplitude and detection of response conflict,the pMFC associated with performance monitoring and eliminated the post-error reduction of inter- signals other brain structures that the level of subsequent performance adjustments?(ii) ference observed in a control condition (30). cognitive control needs to be increased. What brain structures may be involved in The relation between these findings and the Convergence and divergence in perform- the implementation of such control adjust- associated neural circuitry was captured ance monitoring.The findings reviewed ments?In neuroimaging and neuropsycho- more directly in recent neuroimaging studies above suggest that the detection of unfavor- logical studies,the LPFC has been broadly of Stroop task and response-inhibition per- able outcomes,response errors,response implicated in the coordination of adaptive formance (32,33):Post-hoc reaction time conflict,and decision uncertainty elicits goal-directed behavior(25-29).We review analyses revealed that greater ACC activity largely overlapping clusters of activation studies that address the first question,and during error trials was associated with foci in the pMFC.This assumption is we briefly evaluate the scant literature on greater post-error slowing. consistent with a meta-analysis of the human functional interactions between the pMFC The latter studies also addressed the role neuroimaging literature (table S1),focusing and LPFC in the service of adaptive control. of the LPFC in implementing control adjust- on pMFC activations in response to these pMFC activity and immediate control ments and its interaction with the pMFC. types of events (Fig.1B)(20).The high adjustments.When stimuli elicit conflicting Trials exhibiting the greatest behavioral degree of overlap should not be taken. response tendencies or overt response errors, adjustments after errors and correct,high- however,as direct evidence for a generic appropriate performance adjustments may be conflict trials were associated with increased role of neurons (or neuronal populations)in aimed not only at immediate correction of activity in the LPFC.Further,the degree of this brain area in monitoring various aspects these tendencies but also at preventing errors pMFC activity on conflict and error trials of performance.First,although there is on subsequent trials.A distinction can be accurately predicted activity in the LPFC on considerable overlap,there are some appar- made between two types of trial-to-trial the next trial.These and other findings are ent differences as well.with foci associated performance adjustments:(i)shifts in the consistent with the idea that the pMFC,as a www.sciencemag.org SCIENCE VOL 306 15 OCTOBER 2004 445particular the dorsal ACC, is involved in the monitoring of response conflict (18). Re￾sponse conflict occurs when a task concur￾rently activates more than one response tendency; for example, when the stimulus primes a prepotent but incorrect response or when the correct response is underdeter￾mined. Often, incorrect response tendencies are overridden in time by the overt correct response, resulting in high response conflict before the correct response (pre-response conflict). In contrast, occasional errors resulting from premature responding are characterized by response conflict after the response: The correct response tendency resulting from continued stimulus processing conflicts with the already executed incorrect response. In underdetermined responding (that is, under conditions requiring choosing from a set of responses, none of which is more compelling than the others), decision uncertainty occurs. Thus, decision uncertain￾ty involves conflict similar to response conflict observed in tasks in which a prepotent response is overridden (18). The conflict-monitoring theory is consist￾ent with the neuroimaging evidence for pMFC activation in response to errors, reviewed above, and with the timing of the response ERN, indicating post-response con￾flict. In addition, the theory predicts that the pMFC should be active in correct trials characterized by high pre-response conflict, a prediction that has been confirmed by a large number of studies (Fig. 1B). Moreover, the predicted timing of such conflict-related activity is consistent with the occurrence of an ERN-like component, the N2, just before the response (19). Finally, the detection of high post-response conflict may be used as a reliable basis for internal error detection, thereby obviating the need for an explicit error detection mechanism (19). The theory further holds that, upon the detection of response conflict, the pMFC signals other brain structures that the level of cognitive control needs to be increased. Convergence and divergence in perform￾ance monitoring. The findings reviewed above suggest that the detection of unfavor￾able outcomes, response errors, response conflict, and decision uncertainty elicits largely overlapping clusters of activation foci in the pMFC. This assumption is consistent with a meta-analysis of the human neuroimaging literature (table S1), focusing on pMFC activations in response to these types of events (Fig. 1B) (20). The high degree of overlap should not be taken, however, as direct evidence for a generic role of neurons (or neuronal populations) in this brain area in monitoring various aspects of performance. First, although there is considerable overlap, there are some appar￾ent differences as well, with foci associated with pre-response conflict clustering slightly more dorsally than foci activated during error and feedback monitoring (21, 22). Second, single-cell recordings in monkeys suggest that different (neighboring) neurons within specific pMFC regions can be in￾volved in different aspects of performance monitoring (4). Thus, the overlap between the activation foci identified in human neuroimaging studies does not necessarily imply identical functions for all neurons or neuronal ensembles within the pMFC. A potential link between the outlined theories of pMFC functions is that pre￾response conflict and decision uncertainty signal a reduced probability of obtaining reward, whereas errors and unexpected negative feedback signal the loss of antici￾pated reward. The pMFC, particularly the RCZ, is engaged when the need for adjust￾ments to achieve action goals becomes evident. Interestingly, the monitoring pro￾cesses examined here cluster primarily in the transition zone between the cingulate and paracingulate (areas 24 and 32), association (area 8), and premotor cortices (area 6), an area that has extensive connections with brain areas involved in the control of cognitive and motor processes and has been implicated in the regulation of autonomic arousal (23, 24). This presumably places the pMFC in a strategically located position for signaling the need for performance adjust￾ments and for interacting with brain areas involved in motor and cognitive, as well as autonomic and motivational, functions. Performance Adjustments Although the pMFC is consistently impli￾cated in action monitoring, the mechanisms underlying the implementation of subsequent performance adjustments are less well un￾derstood. Two important questions are: (i) Is there a link between pMFC activation associated with performance monitoring and subsequent performance adjustments? (ii) What brain structures may be involved in the implementation of such control adjust￾ments? In neuroimaging and neuropsycho￾logical studies, the LPFC has been broadly implicated in the coordination of adaptive goal-directed behavior (25–29). We review studies that address the first question, and we briefly evaluate the scant literature on functional interactions between the pMFC and LPFC in the service of adaptive control. pMFC activity and immediate control adjustments. When stimuli elicit conflicting response tendencies or overt response errors, appropriate performance adjustments may be aimed not only at immediate correction of these tendencies but also at preventing errors on subsequent trials. A distinction can be made between two types of trial-to-trial performance adjustments: (i) shifts in the tradeoff between speed and accuracy of responding that place the cognitive system in a more cautious (as opposed to impulsive) response mode, and (ii) increases in control that improve the efficiency of information processing. Speed/accuracy tradeoffs may be expressed in ‘‘post-error slowing,’’ the ob￾servation that reaction times typically slow down after errors and correct, high-conflict trials (18). Changes in control, induced by such trials, can become evident in improved performance due to reduced interference from distracting information. For example, the increase in reaction times normally observed for incongruent stimuli (where target and distractor stimuli call for opposing responses) as compared to congruent stimuli (when distractors elicit the same action as the target stimulus) is typically reduced on trials after errors (30). Several observations are consistent with a close link between modulations of pMFC activity and subsequent changes in perform￾ance. One study categorized trials in terms of their ERN amplitudes and found that the reaction time on the subsequent trial slowed progressively with increasing ERN ampli￾tude on the current trial (14). In a similar vein, response errors on a two-alternative forced-choice task are foreshadowed by modulation of this pMFC activity during the immediately preceding (correct) re￾sponse. Error-preceding trials were charac￾terized by increased positivity in the time window typically associated with the ERN (31). This ‘‘error-preceding positivity’’ may reflect a transient disengagement of the monitoring system, resulting in occasional failures to implement appropriate control adjustments and hence in errors. Experimen￾tal factors that affect ERN amplitude may also affect subsequent performance adjust￾ments. For example, alcohol consumption led to a reduction in the ERN amplitude and eliminated the post-error reduction of inter￾ference observed in a control condition (30). The relation between these findings and the associated neural circuitry was captured more directly in recent neuroimaging studies of Stroop task and response-inhibition per￾formance (32, 33): Post-hoc reaction time analyses revealed that greater ACC activity during error trials was associated with greater post-error slowing. The latter studies also addressed the role of the LPFC in implementing control adjust￾ments and its interaction with the pMFC. Trials exhibiting the greatest behavioral adjustments after errors and correct, high￾conflict trials were associated with increased activity in the LPFC. Further, the degree of pMFC activity on conflict and error trials accurately predicted activity in the LPFC on the next trial. These and other findings are consistent with the idea that the pMFC, as a C OGNITION AND B EHAVIOR www.sciencemag.org SCIENCE VOL 306 15 OCTOBER 2004 445 S PECIAL S ECTION