The Error-Related Negativity.

We look back on the events surrounding the genesis of our 1993 article on the error-related negativity (ERN), a component of the event-related brain potential that accompanies errors in the performance of speeded-response tasks. Our reminiscences focus on the personal friendships, intellectual influences, and chance occurrences that shaped the article. To put our work in historical context, we consider subsequent trends in neuroimaging, computational modeling, and psychiatry that gave the ERN high visibility and contributed to the longevity of its scientific interest.

Smiling faces, sometimes they don't tell the truth: facial expression in the ultimatum game impacts decision making and event-related potentials.

Facial expressions are an important aspect of social interaction, conveying not only information regarding emotional states, but also regarding intentions, personality, and complex social characteristics. The present research investigates how a smiling, compared to a nonsmiling, expression impacts decision making and underlying cognitive and emotional processes in economic bargaining. Our results using the ultimatum game show that facial expressions have an impact on decision making as well as the feedback-related negativity following the offer. Furthermore, a moderating effect of sex on decision making was observed, with differential effects of facial expressions from male compared to female proposers. It is concluded that predictions of bargaining behavior must account for aspects of social interactions as well as sex effects to obtain more precise estimates of behavior.

How bad was it? Differences in the time course of sensitivity to the magnitude of loss in problem gamblers and controls.

Previous research has shown that pathological gamblers show various cognitive distortions, especially in interpreting near losses. Using a modified blackjack task, we investigated the electrophysiological responses to near and full losses in problem gamblers and controls. We assessed the event-related brain potentials (ERPs) of 20 problem gamblers and 21 controls at two time points following negative game outcomes. We also studied the behavioral changes after near and full loss experiences. Between 270 and 320 ms following a loss, controls but not gamblers showed a differential ERP response to near and full losses suggesting that a near loss is evaluated more negatively than a full loss. However, between 430 and 480 ms after a loss, the ERPs of both, gamblers and controls, showed a differential response as a function of the type of loss. Both groups became more cautious in their subsequent gambling behavior following near loss. The present study revealed differences in the time course of processing negative feedback in problem gamblers and normal controls, which might be due to gamblers preoccupation with gains rather than with losses.

The influence of the magnitude, probability, and valence of potential wins and losses on the amplitude of the feedback negativity.

We assessed the influence of the variables outcome potential, feedback valence, magnitude, and probability on the amplitude of the feedback negativity (FN). Outcome potential was defined as the a priori valence of an upcoming feedback, that is, is there a potential win or potential loss? All these variables have been studied previously, although never together, but the findings have been contradictory. We analyzed the event-related potential (ERP) after feedback presentation in a reinforcement-learning task to examine the effects of all the variables on feedback negativity. Our results show that outcome potential, feedback valence, probability, and magnitude all influence feedback related ERPs. Taken together, the findings suggest that ERPs in the time range of the feedback negativity are primarily driven by positive outcomes (reinforcement) rather than negative outcomes (punishment).

Your mistake is my mistake . . . or is it? Behavioural adjustments following own and observed actions in cooperative and competitive contexts.

A social speeded choice-reaction-time task was used to study adaptive behaviours following own and observed actions (errors and correct responses) in cooperative and competitive contexts. After making an erroneous response, the appropriate remedial action to avoid future errors in speeded reaction tasks is to slow down. Consistent with previous results, people indeed slow down following their own errors. Importantly, people who slow down most following own errors also slow down following observed errors in a cooperative situation. In a competitive context, a different pattern was found. People accelerated after errors from their opponent. The current findings demonstrate that the social context determines the way people respond to the errors of others, indicating that the neural systems that control remedial actions are highly flexible. These systems may underlie social adaptive behaviour, enabling people to respond flexibly to other people's actions in a wide variety of social contexts.

Dissociation of Pe and ERN/Ne in the conscious recognition of an error.

We evaluated the relationship between conscious awareness and the ERN/Ne and Pe in a digit entering task. On each trial, participants rated the accuracy of their responses on a three-point scale (incorrect, unsure, correct). The ERN/Ne was present on incorrect trials judged as incorrect. The Pe was evident on the same trials but also on correct and incorrect trials judged as unsure. We propose that the ERN/Ne occurs when there is an incorrect execution of a correct motor plan and the representation of the correct response is available for comparison with the actual response. The mismatch information that results from this comparison can be transferred to the Pe process and conscious awareness. However, the Pe process and conscious awareness do not only depend on this transfer of information from the ERN/Ne process. The Pe also occurs when there is uncertainty about the correctness of the motor plan, whether or not the plan is, in fact, correct.

Why humans deviate from rational choice.

Rational choice theory predicts that humans always optimize the expected utility of options when making decisions. However, in decision-making games, humans often punish their opponents even when doing so reduces their own reward. We used the Ultimatum and Dictator games to examine the affective correlates of decision-making. We show that the feedback negativity, an event-related brain potential that originates in the anterior cingulate cortex that has been related to reinforcement learning, predicts the decision to reject unfair offers in the Ultimatum game. Furthermore, the decision to reject is positively related to more negative emotional reactions and to increased autonomic nervous system activity. These findings support the idea that subjective emotional markers guide decision-making and that the anterior cingulate cortex integrates instances of reinforcement and punishment to provide such affective markers.

Hypersensitivity to reward in problem gamblers.

BACKGROUND: Recent research has begun to examine the neurophysiologic basis of pathological gambling. However, direct evidence of a behavioral deficit and an accompanying neurofunctional deviation in a realistic gambling context such as Black Jack has not yet been reported. METHODS: Electroencephalogram was recorded while 20 problem gamblers and 21 control participants played a computerized version of Black Jack. Participants were asked to decide at point scores between 11 and 21 whether they wanted to take another card ("hit") to arrive closer to 21 than the opponent (simulated by computer) or not to take another card ("sit") to avoid going over 21 ("bust"). RESULTS: At a critical point score of 16, problem gamblers decided more often to hit despite losses due to a bust on the preceding trial, whereas control participants decided more often to sit under these conditions. Furthermore, problem gamblers showed more reward-related positive amplitudes in the event-related brain potential than control participants after successful hit decisions at 16. CONCLUSIONS: Here we provide experimental evidence for high-risk taking behavior in gamblers and its correlate in event-related brain potentials. Our results suggest that high-risk-taking behavior in problem gamblers is associated with an increased reward-related neural response to infrequent successes of this behavior.

Decision-making under risk: an fMRI study.

Recent research has focused on decision-making under risk and its neural bases. Two kinds of bad decisions under risk may be defined: too risky decisions and too cautious decisions. Here we show that suboptimal decisions of both kinds lead to increased activity in the anterior cingulate cortex in a Blackjack gambling task. Moreover, this increased activity is related to the avoidance of the negatively evaluated decision under risk. These findings complement other results suggesting an important role of the dorsal anterior cingulate cortex in reward-based decision-making and conflict resolution.

An electrophysiological analysis of coaching in Blackjack.

Recent research has demonstrated that a negative deflection in the event-related potential (ERP) that is usually elicited by errors, negative performance feedback, and monetary losses, and which has been associated with response monitoring and reinforcement learning, is also present when we observe others. In the present study we aimed to extend these findings to the domain of coaching behavior. In many contexts of human social life, advice is given by experts to novices, e.g., teachers or parents to scholars or children. However, their advice is sometimes rejected. Here we show that a rejection of one's advice elicits the same negative potential as when one receives negative feedback about one's own behavior.

Delay-related cerebral activity and motor preparation.

Flexible goal-oriented behavior requires the ability to carry information across temporal delays. This ability is associated with sustained neural firing. In cognitive terms, this ability has often been associated with the maintenance of sensory material online, as during short-term memory tasks, or with the retention of a motor code, as during movement preparation tasks. The general issue addressed in this paper is whether short-term storage of sensory information and preparation of motor responses rely on different anatomical substrates. We used functional magnetic resonance imaging (fMRI) to measure sustained and time-varying delay-related cerebral activity evoked during performance of a delay non-match to sample (DNMS) task, where task contingencies rather than explicit instructions ensured that either sensory or motor representations were used to cross the delay period on each trial. This approach allowed us to distinguish sensory from motor characteristics of delay-related activity evoked by task contingencies, rather than differences in the control of short-term storage driven by verbal instructions. Holding sensory material online evoked both sustained and time-varying delay-related activity in prefrontal regions, whereas movement preparation evoked delay-related responses in precentral areas. Intraparietal cortex was sensitive to the presence of memoranda, but indifferent to the type of information that was retained in memory. Our findings indicate that short-term storage of sensory information and preparation of motor responses rely on partially segregated cerebral circuits. In the frontal lobe, these circuits are organized along a rostro-caudal dimension, corresponding to the sensory or motor nature of the stored material.

Dorsal anterior cingulate cortex integrates reinforcement history to guide voluntary behavior.

Two competing types of theory have been proposed about the function of dorsal anterior cingulate cortex (dACC): evaluative theories hold that dACC monitors ongoing behavior to detect errors or conflict, whereas response selection theories hold that dACC is directly involved in the decision making process. In particular, one response selection theory proposes that dACC utilizes reward prediction error signals carried by the midbrain dopamine system to decide which of several competing motor control systems should be given control over the motor system (Holroyd and Coles, 2002). The theory further proposes that the impact of these dopamine signals on dACC determines the amplitude of a component of the event-related brain potential called the error-related negativity (ERN). In the present study, we applied this theory to a decision making problem that requires participants to select between two response options in which an erroneous choice is not clearly defined. Rather, the reward received for a particular response evolves in relation to the individual's previous behavior. We adapted a computational model associated with the theory to simulate human performance and the ERN in the task, and tested the predictions of the model against empirical ERP data. Our results indicate that ERN amplitude reflects the subjective value attributed by each participant to their response options as derived from their recent reward history. This finding is consistent with the position that dACC integrates the recent history of reinforcements to guide voluntary choice behavior, as opposed to evaluating behaviors per se.

On the programming and reprogramming of actions.

Actions are often selected in the context of ongoing movement plans. Most studies of action selection have overlooked this fact, implicitly assuming that the motor system is passive prior to presentation of instructions triggering movement selection. Other studies addressed action planning in the context of an already present motor plan, but focused mostly on inhibition of a prepotent response under fierce time pressure. Under these circumstances, inhibition of previous motor plans and selection of a new response become temporally intermingled. Here, we explore how the presence of earlier motor plans influences cerebral effects associated with action selection, separating in time movement programming, reprogramming, and execution. We show that portions of parietofrontal circuits, including intraparietal sulcus and left dorsal premotor cortex, are systematically involved in programming motor responses, their activity being indifferent to the presence of earlier motor plans. We identify additional regions recruited when a motor response is programmed in the context of an existing motor program. We found that several right-hemisphere regions, previously associated with response inhibition, might be better characterized as involved in response selection. Finally, we detail the specific role of a right precentral region in movement reprogramming that is involved in inhibiting not only actual responses but also motor representations.

Decision-making in Blackjack: an electrophysiological analysis.

Previous studies have identified a negative potential in the event-related potential (ERP), the error-related negativity (ERN), which is claimed to be triggered by a deviation from a reward expectation. Furthermore, this negativity is related to shifts in risk taking, strategic behavioral adjustments, and inhibition. We used a computer Blackjack gambling task to further examine the process associated with the ERN. Our findings are in line with the view that the ERN process is related to the degree of reward expectation. Furthermore, increased ERN amplitude is associated with the negative evaluation of ongoing decisions, and the amplitude of the ERN is directly related to risk-taking and decision-making behavior. However, the findings suggest that an explanation exclusively based on the deviation from a reward expectation may be insufficient and that the intention of the participants and the importance of a negative event for learning and behavioral change are crucial to the understanding of ERN phenomena.

Anterior cingulate cortex activity can be independent of response conflict in Stroop-like tasks.

Cognitive control includes the ability to formulate goals and plans of action and to follow these while facing distraction. Previous neuroimaging studies have shown that the presence of conflicting response alternatives in Stroop-like tasks increases activity in dorsal anterior cingulate cortex (ACC), suggesting that the ACC is involved in cognitive control. However, the exact nature of ACC function is still under debate. The prevailing conflict detection hypothesis maintains that the ACC is involved in performance monitoring. According to this view, ACC activity reflects the detection of response conflict and acts as a signal that engages regulative processes subserved by lateral prefrontal brain regions. Here, we provide evidence from functional MRI that challenges this view and favors an alternative view, according to which the ACC has a role in regulation itself. Using an arrow-word Stroop task, subjects responded to incongruent, congruent, and neutral stimuli. A critical prediction made by the conflict detection hypothesis is that ACC activity should be increased only when conflicting response alternatives are present. Our data show that ACC responses are larger for neutral than for congruent stimuli, in the absence of response conflict. This result demonstrates the engagement of the ACC in regulation itself. A computational model of Stroop-like performance instantiating a version of the regulative hypothesis is shown to account for our findings.

Neural dynamics of error processing in medial frontal cortex.

Adaptive behavior requires an organism to evaluate the outcome of its actions, such that future behavior can be adjusted accordingly and the appropriate response selected. During associative learning, the time at which such evaluative information is available changes as learning progresses, from the delivery of performance feedback early in learning to the execution of the response itself during learned performance. Here, we report a learning-dependent shift in the timing of activation in the rostral cingulate zone of the anterior cingulate cortex from external error feedback to internal error detection. This pattern of activity is seen only in the anterior cingulate, not in the pre-supplementary motor area. The dynamics of these reciprocal changes are consistent with the claim that the rostral cingulate zone is involved in response selection on the basis of the expected outcome of an action. Specifically, these data illustrate how the anterior cingulate receives evaluative information, indicating that an action has not produced the desired result.

A mechanism for error detection in speeded response time tasks.

The concept of error detection plays a central role in theories of executive control. In this article, the authors present a mechanism that can rapidly detect errors in speeded response time tasks. This error monitor assigns values to the output of cognitive processes involved in stimulus categorization and response generation and detects errors by identifying states of the system associated with negative value. The mechanism is formalized in a computational model based on a recent theoretical framework for understanding error processing in humans (C. B. Holroyd & M. G. H. Coles, 2002). The model is used to simulate behavioral and event-related brain potential data in a speeded response time task, and the results of the simulation are compared with empirical data.

Reinforcement-related brain potentials from medial frontal cortex: origins and functional significance.

The development of the field of cognitive neuroscience has inspired a revival of interest in the brain mechanisms involved in the processing of rewards, punishments, and abstract performance feedback. One fruitful line of research in this area was initiated by the report of an electrophysiological brain potential in humans that was differentially sensitive to negative and positive performance feedback [J. Cogn. Neurosci. 9 (1997) 788]. Here we review current knowledge regarding the neural basis and functional significance of this feedback-evoked 'error-related negativity' (ERN). Our review is organized around a set of predictions derived from a recent theory, which holds that the ERN is associated with the arrival of a negative reward prediction error signal in anterior cingulate cortex.

Modulation of activity in medial frontal and motor cortices during error observation.

We used measures of the human event-related brain potential (ERP) to investigate the neural mechanisms underlying error processing during action observation. Participants took part in two conditions, a task execution condition and a task observation condition. We found that activity in both the medial frontal cortex and the motor cortices, as measured via the error-related negativity and the lateralized readiness potential, respectively, was modulated by the correctness of observed behavior. These data suggest that similar neural mechanisms are involved in monitoring one's own actions and the actions of others.