Unavoidable errors: a spatio-temporal analysis of time-course and neural sources of evoked potentials associated with...

The detection of errors is known to be associated with two successive neurophysiological components in EEG, with an early time-course following motor execution: the error-related negativity (ERN/Ne) and late positivity (Pe). The exact cognitive and physiological processes contributing to these two EEG components, as well as their functional independence, are still partly unclear. Furthermore, these components are typically obtained in conditions where errors are rare events relative to correct trials, and thus presumably implicate other cognitive and motivational processes besides error monitoring. Here, we investigated error processing using high-density scalp ERPs and advanced topographical analyses in healthy participants, during a new Go/noGo task that led to many errors within a relatively short period of time, yet without generating frustration or insufficient motivation. ERP results showed the presence of two distinct electrophysiological markers of error monitoring (ERN/Ne and Pe) during this task, even though errors were practically as frequent as correct responses. Topographic mapping analyses showed for the first time that both the ERN/Ne and Pe elicited a specific distribution of electrical activity relative to correct responses (not just a change in the amplitude of electric signals), suggesting the activation of a distinct configuration of intracranial generators during error detection. This was confirmed by additional analyses using dipole source localization, showing generators in anterior cingulate cortex contributing to the ERN/Ne, but in more posterior cingulate regions for Pe. Moreover, we found that, across all participants, the magnitude of the ERN/Ne correlated with the level of state anxiety, even in the subclinical range, whereas the Pe was correlated negatively with the total number of errors and positively with the improvement of response speed on correct trials. By contrast, no significant relation was found between error monitoring ERPs and individual measures of impulsivity. Taken together, these data suggest that these two successive EEG components associated with errors reflect different monitoring processes, with distinct neural substrates in cingulate cortex. While ERN/Ne processes in anterior cingulate might primarily mediate error detection, Pe processes in posterior cingulate might be more directly related to behavioral adjustment based on the outcome of current actions.