Regulating action: alternating activation of midline frontal and motor cortical networks

Focal electrical fields recorded over the midline prefrontal cortex have been found to index rapid evaluative decisions, including the recognition of having made an error in a speeded response task. The nature of these electrical fields and how they are related to cortical areas involved in response execution remains to be clarified. As subjects performed a speeded response task the EEG was recorded with a 128-channel sensor array. By filtering out the large slow waves of the event-related potential, we found that the error-related negativity (Ne/ERN) arises from a midline frontal oscillation that alternates with oscillations over lateral sensorimotor cortex. Electrical source analyses were used to determine the brain sources involved in the generation of these oscillations. The results show that the midline and lateral oscillations have a period of about 200 ms (theta), and they are present for both correct and error responses. When an error is made, the midline error oscillation is recruited strongly, and it becomes correlated with the motor oscillation. Source analyses localized the midline error oscillation to centromedial frontal cortex and the lateral oscillation to sensorimotor cortices. Because of the similarity between the midline oscillation observed in the present study and frontal midline theta, the nature of the Ne/ERN may be clarified by the frontal midline theta literature. The correlation between the midline and sensorimotor oscillations suggests a possible mechanism for how midline frontal evaluative and monitoring networks contribute to action regulation.