Theta EEG dynamics of the error-related negativity

Objective: The error-related negativity (ERN) is a response-locked brain potential (ERP) occurring 80-100 ms following response errors. This report contrasts three views of the genesis of the ERN, testing the classic view that time-locked phasic bursts give rise to the ERN against the view that the ERN arises from a pure phase-resetting of ongoing theta (4-7 Hz) EEG activity and the view that the ERN is generated - at least in part - by a phase-resetting and amplitude enhancement of ongoing theta EEG activity. Methods: Time-domain ERP analyses were augmented with time-frequency investigations of phase-locked and non-phase-locked spectral power, and inter-trial phase coherence (ITPC) computed from individual EEG trials, examining time courses and scalp topographies. Simulations based on the assumptions of the classic, pure phase-resetting, and phase-resetting plus enhancement views, using parameters from each subject's empirical data, were used to contrast the time-frequency findings that could be expected if one or more of these hypotheses adequately modeled the data. Results: Error responses produced larger amplitude activity than correct responses in time-domain ERPs immediately following responses, as expected. Time-frequency analyses revealed that significant error-related post-response increases in total spectral power (phase- and non-phase-locked), phase-locked power, and ITPC were primarily restricted to the theta range, with this effect located over midfrontocentral sites, with a temporal distribution from ≈150-200 ms prior to the button press and persisting up to 400 ms post-button press. The increase in non-phase-locked power (total power minus phase-locked power) was larger than phase-locked power, indicating that the bulk of the theta event-related dynamics were not phase-locked to response. Results of the simulations revealed a good fit for data simulated according to the phase-locking with amplitude enhancement perspective, and a poor fit for data simulated according to the classic view and the pure phase-resetting view. Conclusions: Error responses produce not only phase-locked increases in theta EEG activity, but also increases in non-phase-locked theta, both of which share a similar topography. Significance: The findings are thus consistent with the notion advanced by Luu et al. [Luu P, Tucker DM, Makeig S. Frontal midline theta and the error-related negativity; neurophysiological mechanisms of action regulation. Clin Neurophysiol 2004;115:1821-35] that the ERN emerges, at least in part, from a phase-resetting and phase-locking of ongoing theta-band activity, in the context of a general increase in theta power following errors.