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.