Motor oscillations reveal new correlates of error processing in the human brain

Abstract

Abstract It has been demonstrated that during motor responses, the activation of the motor cortical regions emerges in close association with the activation of the medial frontal cortex implicated with performance monitoring and cognitive control. The present study explored the oscillatory neurodynamics of response-related potentials during correct and error responses to test the hypothesis that such continuous communication would modify the characteristics of motor potentials during performance errors. Electroencephalogram (EEG) was recorded at 64 electrodes in a four-choice reaction task and response-related potentials (RRPs) of correct and error responses were analysed. Oscillatory RRP components at extended motor areas were analysed in the theta (3.5-7 Hz) and delta (1-3 Hz) frequency bands with respect to power, temporal synchronization (phase-locking factor, PLF), and spatial synchronization (phase-locking value, PLV). Major results demonstrated that motor oscillations differed between correct and error responses. Error-related changes (1) were frequency-specific, engaging delta and theta frequency bands, (2) emerged already before response production, and (3) had specific regional topographies at posterior sensorimotor and anterior (pre-motor and medial frontal) areas. Specifically, the connectedness of motor and sensorimotor areas contra-lateral to the response supported by delta networks was substantially reduced during errors. Also, there was an error-related suppression of the phase stability of delta and theta oscillations at these areas. This synchronization reduction was accompanied by increased temporal synchronization of motor theta oscillations at bi-lateral pre-motor regions and by two distinctive error-related effects at medial frontal regions: (1) a focused fronto-central enhancement of theta power and (2) a separable enhancement of the temporal synchronization of delta oscillations with a localized medial frontal focus. Together, these observations indicate that the electrophysiological signatures of performance errors are not limited to the medial frontal signals, but they also involve the dynamics of oscillatory motor networks at extended cortical regions generating the movement. Also, they provide a more detailed picture of the medial frontal processes activated in relation to error processing.