Global and Local Dynamics of High-Gamma Activity Underlying Error Processing in the Human Brain Revealed by Noninvasive and Intracranial EEG

Abstract

Error detection in motor behavior is a fundamental cognitive function heavily relying on cortical information processing. Neural activity in the high-gamma frequency band (HGB) closely reflects such local cortical processing, but little is known about its role in error processing, particularly in the healthy human brain. Here we characterize the error-related response of the human brain based on data obtained with noninvasive EEG optimized for HGB mapping in 31 healthy subjects (15 females, 16 males), and additional intracranial EEG data from 9 epilepsy patients (4 females, 5 males). Our findings reveal a comprehensive picture of the global and local dynamics of error-related HGB activity in the human brain. On the global level as reflected in the noninvasive EEG, the error-related response started with an early component dominated by anterior brain regions, followed by a shift to parietal regions, and a subsequent phase characterized by sustained parietal HGB activity. This phase lasted for more than 1 s after the error onset. On the local level reflected in the intracranial EEG, a cascade of both transient and sustained error-related responses involved an even more extended network, spanning beyond frontal and parietal regions to the insula and the hippocampus. HGB mapping appeared especially well suited to investigate late, sustained components of the error response, possibly linked to downstream functional stages such as error-related learning and behavioral adaptation. Our findings establish the basic spatio-temporal properties of HGB activity as a neural correlate of error processing, complementing traditional error-related potential studies.\n\nSignificance StatementThere is great interest to understand how the human brain reacts to errors in goal-directed behavior. An important index of cortical and subcortical information processing is fast oscillatory brain activity, particularly in the high-gamma band (above 50 Hz). Here we show that it is possible to detect signatures of errors in event-related high-gamma responses with noninvasive techniques, characterize these responses comprehensively, and validate the EEG procedure for the detection of such signals. In addition, we demonstrate the added value of intracranial recordings pinpointing the fine-grained spatio-temporal patterns in error-related brain networks. We anticipate that the optimized noninvasive EEG techniques as described here will be helpful in many areas of cognitive neuroscience where fast oscillatory brain activity is of interest.