Clay B. Holroyd

The feedback-related negativity reflects the binary evaluation of good versus bad outcomes

Electrophysiological studies have utilized event-related brain potentials to study neural processes related to the evaluation of environmental feedback. In particular, the feedback-related negativity (FRN) has been shown to reflect the evaluation of monetary losses and negative performance feedback. Two experiments were conducted to examine whether or not the FRN is sensitive to the magnitude of negative feedback. In both experiments, participants performed simple gambling tasks in which they could receive a range of potential outcomes on each trial. Relative to feedback indicating monetary gain, feedback indicating non-rewards was associated with a FRN in both experiments; however, the magnitude of the FRN did not demonstrate sensitivity to the magnitude of non-reward in either experiment. These data suggest that the FRN reflects the early appraisal of feedback based on a binary classification of good versus bad outcomes. These data are discussed in terms of contemporary theories of the FRN, as well as appraisal processes implicated in emotional processing.

Dorsal anterior cingulate cortex shows fMRI response to internal and external error signals.

In our event-related functional magnetic resonance imaging (fMRI) experiment, participants learned to select between two response options by trial-and-error, using feedback stimuli that indicated monetary gains and losses. The results of the experiment indicate that error responses and error feedback activate the same region of dorsal anterior cingulate cortex, suggesting that this region is sensitive to both internal and external sources of error information.

Why is there an ERN/Ne on correct trials? Response representations, stimulus-related components, and the theory of error-processing

The ERN or Ne is a component of the event-related brain potential that occurs when human subjects make errors in reaction time tasks. It is observed in response-locked averages, time-locked to the execution of the incorrect response. Recent research has reported that this component is present on correct response trials, thereby challenging the idea that the component is specifically related to error-processing. In this paper, we argue that the ERN or Ne observed on correct trials can be attributed to one or both of two factors: either there is error-processing on correct trials, and/or the response-locked averages used to derive the ERN/Ne are contaminated by negative components evoked by the stimulus. For this reason, there is no reason to abandon theories that relate the ERN/Ne to error-processing.

The feedback correct-related positivity: Sensitivity of the event-related brain potential to unexpected positive feedback

The N200 and the feedback error-related negativity (fERN) are two components of the event-related brain potential (ERP) that share similar scalp distributions, time courses, morphologies, and functional dependencies, which raises the question as to whether they are actually the same phenomenon. To investigate this issue, we recorded the ERP from participants engaged in two tasks that independently elicited the N200 and fERN. Our results indicate that they are, in fact, the same ERP component and further suggest that positive feedback elicits a positive-going deflection in the time range of the fERN. Taken together, these results indicate that negative feedback elicits a common N200 and that modulation of fERN amplitude results from the superposition on correct trials of a positive-going deflection that we term the feedback correct-related positivity.

Errors in reward prediction are reflected in the event-related brain potential.

The error-related negativity (ERN) is a negative deflection in the event-related brain potential associated with error processing. A recent theory holds that the ERN is elicited by the impact of a reward prediction error signal carried by the mesencephalic dopamine system on anterior cingulate cortex. The theory predicts that larger ERNs should be elicited by unexpected unfavorable outcomes than by expected unfavorable outcomes. We tested the theory in an experiment in which the frequency of occurrence of reward was varied by condition, reasoning that the system that produces the ERN would come to expect non-reward when rewards were infrequent. Consistent with the theory, we found that larger ERNs were elicited by unexpected absences of reward.

Error-related scalp potentials elicited by hand and foot movements: evidence for an output-independent error-processing system in humans

The error-related negativity (ERN) is a fronto-centrally distributed component of the event-related brain potential (ERP) that occurs when human subjects make errors in a variety of experimental tasks. In the present study, we recorded ERPs from 128 scalp electrodes while subjects performed a choice reaction time task using either their hands or feet. We applied the brain electric source analysis technique to compare ERNs elicited by hand and foot errors. The scalp distributions of these error potentials suggest that they share the same neural generator and, therefore, that the ERN process is output-independent. Together with other findings, the results are consistent with the hypothesis that the ERN is generated within the anterior cingulate cortex and is elicited by the activation of a generic error-processing system.

A computational account of altered error processing in older age: Dopamine and the error-related negativity

When participants commit errors or receive feedback signaling that they have made an error, a negative brain potential is elicited. According to Holroyd and Coles’s (in press) neurocomputational model of error processing, this error-related negativity (ERN) is elicited when the brain first detects that the consequences of an action are worse than expected. To study age-related changes in error processing, we obtained performance and ERN measures of younger and high-functioning older adults. Experiment 1 demonstrated reduced ERN amplitudes in older adults in the context of otherwise intact brain potentials. This result could not be attributed to uncertainty about the required response in older adults. Experiment 2 revealed impaired performance and reduced response- and feedback-related ERNs of older adults in a probabilistic learning task. These age changes could be simulated by manipulation of a single parameter of the neurocomputational model, this manipulation corresponding to weakened phasic activity of the mesencephalic dopamine system.

The good, the bad and the neutral: electrophysiological responses to feedback stimuli.

The feedback error-related negativity (fERN) is a component of the event-related brain potential elicited in gambling and trial-and-error learning tasks by negative, but not positive, feedback stimuli. Here, we present the results of a series of five experiments that investigated the response of the fERN to the presentation of neutral feedback stimuli. In three of the experiments, the neutral feedback stimuli indicated that the participants did not receive a potential reward nor incur a potential penalty (i.e., they received nothing); and in the remaining two experiments, the neutral feedback stimuli did not convey any meaningful information (i.e., the participants were either successful or unsuccessful on those trials, but the feedback stimuli were uninformative about the outcomes). Across the five experiments, we found that neutral feedback stimuli elicited a fERN about as large as that elicited by negative feedback stimuli. This result is consistent with recent proposals that the evaluative system that produces the fERN classifies outcomes into two categories: those outcomes that indicate that a goal has been satisfied and those that do not.

Knowing good from bad : differential activation of human cortical areas by positive and negative outcomes

Previous research has identified a component of the event‐related brain potential (ERP), the feedback‐related negativity, that is elicited by feedback stimuli associated with unfavourable outcomes. In the present research we used event‐related functional magnetic resonance imaging (fMRI) and electroencephalographic (EEG) recordings to test the common hypothesis that this component is generated in the caudal anterior cingulate cortex. The EEG results indicated that our paradigm, a time estimation task with trial‐to‐trial performance feedback, elicited a large feedback‐related negativity (FRN). Nevertheless, the fMRI results did not reveal any area in the caudal anterior cingulate cortex that was differentially activated by positive and negative performance feedback, casting doubt on the notion that the FRN is generated in this brain region. In contrast, we found a number of brain areas outside the posterior medial frontal cortex that were activated more strongly by positive feedback than by negative feedback. These included areas in the rostral anterior cingulate cortex, posterior cingulate cortex, right superior frontal gyrus, and striatum. An anatomically constrained source model assuming equivalent dipole generators in the rostral anterior cingulate, posterior cingulate, and right superior frontal gyrus produced a simulated scalp distribution that corresponded closely to the observed scalp distribution of the FRN. These results support a new hypothesis regarding the neural generators of the FRN, and have important implications for the use of this component as an electrophysiological index of performance monitoring and reward processing.

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.