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A review examining the relationship between individual differences in the error-related negativity and cognitive control.

A. Meyer,G. Hajcak

Published 2019 in International Journal of Psychophysiology

ABSTRACT

Almost 30 years ago, two independent groups discovered the errorrelated negativity (ERN, or Ne; Falkenstein et al., 1991; Gehring et al., 1993), an event-related brain potential (ERP) evident as a large negative deflection that peaks approximately 50ms after error commission in speeded reaction time tasks. Although it is clear that the ERN is elicited by performance failures, the specific functional significance of the ERN continues to be debated. The ERN is often discussed within the broader context of performance monitoring: how the detection of errors and subsequent adjustments in performance are critical for successful goal-directed actions (Ridderinkhof et al., 2004). From this perspective, the ERN reflects the evaluation of actions that require corrective action. Indeed, early computational models proposed that the ERN reflected neural activity in the anterior cingulate cortex (ACC) that improved the subsequent selection of appropriate information and actions (Holroyd and Coles, 2002; Yeung et al., 2004). Many researchers argued that there was a direct link between error-monitoring activity of the ACC and subsequent adjustments in performance (Carter et al., 1998; Van Veen and Carter, 2006)—the ERN was viewed as a signal that engaged cognitive control processes. Gehring's original paper on the ERN provided the first empirical support linking ERN amplitude and cognitive control: within-subjects, the ERN was larger when performance instructions emphasized accuracy over speed, when post-error slowing was also increased; thus, the ERN was potentiated under conditions characterized by greater cognitive control (Gehring et al., 1993). Since then, additional research has linked the ERN to within-subject post-error slowing (for a review of these studies, see: Cavanagh and Shackman, 2015). It is important to note that the work and theories described above focus on the functional significance of the ERN from a within-participants perspective—e.g., how does variability in the ERN across types of trials relate to behavioral measures following those trial types? The vast majority of cognitive neuroscience research takes a within-subjects perspective to understanding human brain function (Hajcak et al., 2017). However, researchers frequently interpret between-subjects differences in neural activity in terms of insights derived from withinsubject comparisons. For example, many researchers have interpreted variability in the ERN across individuals as reflecting individual differences in cognitive control (Compton et al., 2013; Grammer et al., 2018; Lo et al., 2015; McDermott et al., 2012; Pontifex et al., 2009). Indeed, the ERN is currently included in the NIMH Research Domain Criteria (RDoC) – a matrix intended to explain variability across people – as a measure of “Cognitive Control”. In terms of evidence that the ERN “indexes cognitive control”, studies most often cite either within-subjects studies (for example, Cavanagh and Frank, 2014; Cavanagh and Shackman, 2015; Cavanagh et al., 2012) or theories that link the ERN to control within individuals (Botvinick et al., 2001; Falkenstein et al., 1991; Gehring et al., 1993; Holroyd and Coles, 2002). However, the logic of automatically translating within-subject associations to between-subject effects is flawed. Consider a classic example: accuracy and typing. It is certainly true that typing speed and accuracy are inversely correlated within subjects: the faster an individual types, the more mistakes they are likely to make. However, it is not the case that typing speed is negatively correlated with accuracy across subjects—rather, individuals who are more experienced and skilled typists are likely to be both faster and more accurate. In this way, the within-subject effect (↑ speed= ↓ accuracy) would be the opposite of a between-subject effect (↑ speed= ↑ accuracy). Thus, a within-subject effect (i.e., ERN relates to increased cognitive control) does not imply the same between-subject effect (i.e., people with a larger ERN are characterized by greater cognitive control)—though this error in logic is pervasive in clinical neuroscience.

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