Early Action Error Processing Is Due to Domain-General Surprise, Whereas Later Processing Is Error Specific.

Abstract

The ability to adapt behavior after erroneous actions is one of the key aspects of cognitive control. Error commission typically causes people to slow down their subsequent actions [post-error slowing (PES)]. Recent work has challenged the notion that PES reflects adaptive, controlled processing and instead suggests that it is a side effect of the surprising nature of errors. Indeed, human neuroimaging suggests that the brain networks involved in processing errors overlap with those processing error-unrelated surprise, calling into question whether there is a specific system for error processing in the brain at all. In the current study, we used EEG decoding and a novel behavioral paradigm to test whether there are indeed unique, error-specific processes that contribute to PES beyond domain-general surprise. Across two experiments in male and female humans (N = 76), we found that both errors and error-unrelated surprise were followed by slower responses when response-stimulus intervals were short. Furthermore, the early neural processes following error-specific and domain-general surprise showed significant cross-decoding. However, at longer intervals, which provided additional processing time, only errors were still followed by post-trial slowing. Furthermore, this error-specific PES effect was reflected in sustained neural activity that could be decoded from that associated with domain-general surprise, with the strongest contributions found at lateral frontal, occipital, and sensorimotor scalp sites. These findings suggest that errors and surprise initially share common processes, but that after additional processing time, unique, genuinely error-specific processes take over and contribute to behavioral adaptation.SIGNIFICANCE STATEMENT Humans typically slow their actions after errors (PES). Some suggest that PES is a side effect of the unexpected, surprising nature of errors, challenging the notion of a genuine error processing system in the human brain. Here, we used multivariate EEG decoding to identify behavioral and neural processes uniquely related to error processing. Action slowing occurred following both action errors and error-unrelated surprise when time to prepare the next response was short. However, when there was more time to react, only errors were followed by slowing, further reflected in sustained neural activity. This suggests that errors and surprise initially share common processing, but that after additional time, error-specific, adaptive processes take over.