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Surprise and error: common neuronal architecture for the processing of errors and novelty
Journal article   Open access   Peer reviewed

Surprise and error: common neuronal architecture for the processing of errors and novelty

Jan R Wessel, Claudia Danielmeier, J Bruce Morton and Markus Ullsperger
The Journal of neuroscience, Vol.32(22), pp.7528-7537
05/30/2012
DOI: 10.1523/jneurosci.6352-11.2012
PMCID: PMC6703591
PMID: 22649231
url
https://doi.org/10.1523/jneurosci.6352-11.2012View
Published (Version of record) Open Access

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.
 Electroencephalography Magnetic Resonance Imaging Cerebral Cortex - blood supply Humans Male Reaction Time Oxygen - blood Young Adult Evoked Potentials, Visual - physiology Image Processing, Computer-Assisted Brain Mapping Conflict (Psychology) Adult Cerebral Cortex - physiology Female Photic Stimulation Inhibition (Psychology)

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