Frontal midline theta and the error-related negativity: neurophysiological mechanisms of action regulation

Objective: The error-related negativity (ERN) is an event-related potential (ERP) peak occurring between 50 and 100 ms after the commission of a speeded motor response that the subject immediately realizes to be in error. The ERN is believed to index brain processes that monitor action outcomes. Our previous analyses of ERP and EEG data suggested that the ERN is dominated by partial phase-locking of intermittent theta-band EEG activity. In this paper, this possibility is further evaluated. Methods: The possibility that the ERN is produced by phase-locking of theta-band EEG activity was examined by analyzing the single-trial EEG traces from a forced-choice speeded response paradigm before and after applying theta-band (4–7 Hz) filtering and by comparing the averaged and single-trial phase-locked (ERP) and non-phase-locked (other) EEG data. Electrical source analyses were used to estimate the brain sources involved in the generation of the ERN. Results: Beginning just before incorrect button presses in a speeded choice response paradigm, midfrontal theta-band activity increased in amplitude and became partially and transiently phase-locked to the subjectʹs motor response, accounting for 57% of ERN peak amplitude. The portion of the theta-EEG activity increase remaining after subtracting the response-locked ERP from each trial was larger and longer lasting after error responses than after correct responses, extending on average 400 ms beyond the ERN peak. Multiple equivalent-dipole source analysis suggested 3 possible equivalent dipole sources of the theta-bandpassed ERN, while the scalp distribution of non-phase-locked theta amplitude suggested the presence of additional frontal theta-EEG sources. Conclusions: These results appear consistent with a body of research that demonstrates a relationship between limbic theta activity and action regulation, including error monitoring and learning.