Surprise and Error: Common Neuronal Architecture for the Processing of Errors and Novelty

Abstract

According to recent accounts, the processing of errors and generally infrequent, surprising (novel) events share a common neuroanatomical substrate. Direct empirical evidence for this common processing network in humans is, however, scarce. To test this hypothesis, we administered a hybrid error-monitoring/novelty-oddball task in which the frequency of novel, surprising trials was dynamically matched to the frequency of errors. Using scalp electroencephalographic recordings and event-related functional magnetic resonance imaging (fMRI), we compared neural responses to errors with neural responses to novel events. In Experiment 1, independent component analysis of scalp ERP data revealed a common neural generator implicated in the generation of both the error-related negativity (ERN) and the novelty-related frontocentral N2. In Experiment 2, this pattern was confirmed by a conjunction analysis of event-related fMRI, which showed significantly elevated BOLD activity following both types of trials in the posterior medial frontal cortex, including the anterior midcingulate cortex (aMCC), the neuronal generator of the ERN. Together, these findings provide direct evidence of a common neural system underlying the processing of errors and novel events. This appears to be at odds with prominent theories of the ERN and aMCC. In particular, the reinforcement learning theory of the ERN may need to be modified because it may not suffice as a fully integrative model of aMCC function. Whenever course and outcome of an action violates expectancies (not necessarily related to reward), the aMCC seems to be engaged in evaluating the necessity of behavioral adaptation.

Plastic modifications within inhibitory control networks induced by practicing a stop-signal task: An electrical neuroimaging study

“…Another limitation of the current study is that because the SSDs tended to decrease between the beginning and the end of the session, our contrast was possibly contaminated by a differential anticipation of the stop cues. Frontoecentral N2 components manifesting over our period of topographic modulation are indeed sensitive to the formation of temporal expectations and to their violations (e.g., Rimmele et al, 2011;Wessel et al, 2012). While the resetting of the SSD to 300 msec at the beginning of each block likely minimized the potential influence of temporal expectations, it possibly induced another confound: Since participants became more proficient with SST practice and that the SSD were reset to the same value at the beginning and at the end of the task, stopping their responses was likely easier at the end than at the beginning of the session.…”

Frontal theta band oscillations predict error correction and posterror slowing in typing.

“…Hewig et al, 2011;Navarro-Cebrian & Kayser, 2013;Roger, Benar, Vidal, Hasbroucq, & Burle, 2010;Scheffers & Coles, 2000;Shalgi & Deouell, 2012;Wessel, Danielmeier, Morton, & Ullsperger, 2012), it contradicts the traditional view that ERN is related to implicit but not to explicit error awareness (e.g. Ehlis, Herrmann, Bernhard, & Fallgatter, 2005;Endrass et al, 2005Endrass et al, , 2007Hester, Foxe, Molholm, Shpaner, & Garavana, 2005;Hughes & Yeung, 2011;Nieuwenhuis et al, 2001;O'Connell et al, 2007;Overbeek et al, 2005;Steinhauser & Yeung, 2010).…”

Brain systems underlying the affective and social monitoring of actions: An integrative review

“…longer RTs on the (correct) trial following errors due to adjustments in response tendencies King et al, 2010) or as a reflection of attentional orienting to these deviant and worse than expected events (Notebaert et al, 2009;Wessel et al, 2012). Errors can lead to increased post-error accuracy , indicating a potential shift in speed/accuracy trade-off.…”

“…Second, event-related potentials (ERPs) have revealed several phasic components of conflict, error, and outcome monitoring, which have specific temporal and topographical properties, such as the N2, error-related negativity (ERN), and feedback-related negativity (FRN). These ERP components may partially reflect a common underlying process Wessel et al, 2012;Yeung et al, 2004) that is characterized by phasic bursts in theta band activity (Cavanagh et al, 2012;Cohen, 2011).…”