Lesions to the prefrontal performance-monitoring network disrupt neural processing and adaptive behaviors after both errors and novelty

Unexpected events can have internal causes (action errors) as well as external causes (perceptual novelty). Both events call for adaptations of ongoing behavior, resulting, amongst other things, in post-error and post-novelty slowing (PES/PNS) of reaction times (RT). Both types of events are processed in prefrontal brain areas, indexed by event-related potentials (ERPs): Errors are followed by a complex of ERPs comprised of the error-related negativity (ERN) and error positivity (Pe), whereas novels are followed by a N2/P3 complex. However, despite those overlapping properties, past neuroscientific studies of both types of events resulted in largely separate branches of research. Only recently have theoretical efforts proposed overlapping neuronal networks for the computation of 'unexpectedness' in general. Crucially, in a recent study, we have shown that both errors and novelty are indeed processed in the same neuronal network in the human brain: the prefrontal-cingulate performance-monitoring network (PCMN) underlying the ERN also explained significant parts of the N2/P3 complex. Here, we attempt to take this research further by investigating the causal role of the PCMN in both error and novelty processing. Eight patients with ischemic lesions to the PCMN and eight control participants performed a version of the flanker task in which they made errors, while also being presented with unexpected action effects on a subset of otherwise correct trials. In line with our predictions, lesions to the PCMN lead to significant reductions in ERP amplitude following both errors and perceptual novelty. Also, while the age-matched control participants showed the expected pattern of adaptive RT slowing to both errors and novelty, patients did not exhibit adaptive slowing behaviors following either event. These results support recent theoretical accounts according to which a general PCMN reacts to surprising events, regardless of valence and/or source of the unexpectedness. (C) 2013 Elsevier Ltd. All rights reserved.