The dynamics of error processing in the human brain as reflected by high-gamma activity in noninvasive and intracranial EEG

AbstractError 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.Significance 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.

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Dynamic Spectral Imaging: Online and Offline Functional Brain Mapping Using High-Frequency Activity [50–150 Hz] in SEEG

Invasive Studies of the Human Epileptic Brain ◽

10.1093/med/9780198714668.003.0033 ◽

2018 ◽

pp. 453-464

Author(s):

Jean-Philippe Lachaux

Keyword(s):

High Frequency ◽

Large Scale ◽

Human Cognition ◽

Gamma Activity ◽

Intracranial Eeg ◽

Cortical Dynamics ◽

Functional Brain Mapping ◽

High Gamma ◽

High Frequency Activity ◽

Eeg Recordings

At the end of the twentieth century, a handful of research groups discovered that neural processing leaves a characteristic signature in intracranial EEG recordings: an increase of power in a broad frequency range above 50 Hz, dubbed ‘high-gamma’ of high-frequency activity ([50–150 Hz]). Since then, intracranial EEG research on human cognition has focused primarily on high-gamma activity to reveal the large-scale cortical dynamics of most major cognitive functions, not only offline in well-controlled paradigms, but also online, while patients freely interact with their environment. This chapter introduces that approach, including its recent extension to task-induced neural activity suppressions and functional connectivity mapping, and its clinical application to minimize cognitive deficits induced by epilepsy surgery.

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Intracranial-EEG evidence for medial temporal pole driving amygdala activity induced by multi-modal emotional stimuli

10.1101/2020.02.24.963801 ◽

2020 ◽

Author(s):

Saurabh Sonkusare ◽

Vinh Thai Nguyen ◽

Rosalyn Moran ◽

Johan van der Meer ◽

Yudan Ren ◽

...

Keyword(s):

Low Frequency ◽

Gamma Activity ◽

Cortical Region ◽

Frequency Range ◽

Intracranial Eeg ◽

Social And Emotional ◽

Temporal Pole ◽

High Gamma ◽

Amygdala Activity ◽

Computational Analyses

AbstractThe temporal pole (TP) is an associative cortical region required for complex cognitive functions such as social and emotional cognition. However, functional mapping of the TP with functional magnetic resonance imaging is technically challenging and thus understanding of its interaction with other key emotional circuitry, such as the amygdala, remain elusive. We exploited the unique advantages of stereo-electroencephalography (SEEG) to assess the responses of the TP and the amygdala during the perception of emotionally salient stimuli of pictures, music and movies. These stimuli consistently elicited high gamma responses (70-140 Hz) in both the TP and the amygdala, accompanied by functional connectivity in the low frequency range (2-12 Hz). Computational analyses suggested the TP driving this effect in the theta-alpha frequency range and which was modulated by the emotional salience of the stimuli. Of note, cross-frequency analysis indicated the phase of theta-alpha oscillations in the TP modulated the amplitude of high gamma activity in the amygdala. These results were reproducible with three types of stimuli including naturalistic stimuli suggesting a hierarchical influence of the TP over the amygdala in non-threatening stimuli.

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Measurement of the mapping between intracranial EEG and fMRI recordings in the human brain

10.1101/237198 ◽

2017 ◽

Cited By ~ 1

Author(s):

DW Carmichael ◽

S Vulliemoz ◽

T Murta ◽

U. Chaudhary ◽

S Perani ◽

...

Keyword(s):

Human Brain ◽

Sensorimotor Cortex ◽

Brain Activity ◽

Spatial Scales ◽

Electrophysiological Response ◽

Intracranial Eeg ◽

Eeg Activity ◽

High Gamma ◽

Gamma Power ◽

Patients With Epilepsy

AbstractThere are considerable gaps in our understanding of the relationship between human brain activity measured at different temporal and spatial scales by intracranial electroencephalography and fMRI. By comparing individual features and summary descriptions of intracranial EEG activity we determined which best predict fMRI changes in the sensorimotor cortex in two brain states: at rest and during motor performance. We also then examine the specificity of this relationship to spatial colocalisation of the two signals.We acquired electrocorticography and fMRI simultaneously (ECoG-fMRI) in the sensorimotor cortex of 3 patients with epilepsy. During motor activity, high gamma power was the only frequency band where the electrophysiological response was colocalised with fMRI measures across all subjects. The best model of fMRI changes was its principal components, a parsimonious description of the entire ECoG spectrogram. This model performed much better than a model based on the classical frequency bands both during task and rest periods or models derived on a summary of cross spectral changes (e.g. ‘root mean squared EEG frequency’). This suggests that the region specific fMRI signal is reflected in spatially and spectrally distributed EEG activity.

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Long range, high-gamma phase coherence in the human brain during overt and covert speech

10.1101/2021.01.23.427916 ◽

2021 ◽

Author(s):

Taufik A. Valiante ◽

Bojan Garic

Keyword(s):

Human Brain ◽

Large Scale ◽

Gamma Activity ◽

Optimal Time ◽

The Novel ◽

Axonal Conduction ◽

High Gamma ◽

Large Scale Integration ◽

Scale Integration ◽

Intracranial Electroencephalography

AbstractUsing intracranial electroencephalography (iEEG) in patients undergoing diagnostic workup for epilepsy, we show that during reading, phase coherent high-gamma activity emerges between spatially distant regions of proven involvement in vocalization. Using the novel metric of “phase-dependent power-causal correlations”, causal interactions were shown to be maximal at high-gamma frequencies, and displayed stronger correlations to power fluctuations near the optimal time delay, with this delay potentially accounted for by axonal conduction. We conclude that high-gamma activity may represents propagated, directed, large-scale integration between task related regions of the human brain.

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Direct electrical stimulation of human cortex evokes high gamma activity that predicts conscious somatosensory perception

Journal of Neural Engineering ◽

10.1088/1741-2552/aa9bf9 ◽

2018 ◽

Vol 15 (2) ◽

pp. 026015 ◽

Cited By ~ 2

Author(s):

Leah Muller ◽

John D Rolston ◽

Neal P Fox ◽

Robert Knowlton ◽

Vikram R Rao ◽

...

Keyword(s):

Electrical Stimulation ◽

Gamma Activity ◽

Direct Electrical Stimulation ◽

Human Cortex ◽

High Gamma ◽

Stimulation Of

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Comparison of subdural and subgaleal recordings of cortical high-gamma activity in humans

Clinical Neurophysiology ◽

10.1016/j.clinph.2015.03.014 ◽

2016 ◽

Vol 127 (1) ◽

pp. 277-284 ◽

Cited By ~ 8

Author(s):

Jared D. Olson ◽

Jeremiah D. Wander ◽

Lise Johnson ◽

Devapratim Sarma ◽

Kurt Weaver ◽

...

Keyword(s):

Gamma Activity ◽

High Gamma

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Prefrontal High Gamma in ECoG tags periodicity of musical rhythms in perception and imagination

10.1101/784991 ◽

2019 ◽

Author(s):

S. A. Herff ◽

C. Herff ◽

A. J. Milne ◽

G. D. Johnson ◽

J. J. Shih ◽

...

Keyword(s):

Auditory Processing ◽

Right Hemisphere ◽

Brain Activity ◽

Activity Patterns ◽

Superior Temporal Gyrus ◽

Gamma Activity ◽

Rhythm Perception ◽

High Gamma ◽

The Right ◽

Musical Rhythms

AbstractRhythmic auditory stimuli are known to elicit matching activity patterns in neural populations. Furthermore, recent research has established the particular importance of high-gamma brain activity in auditory processing by showing its involvement in auditory phrase segmentation and envelope-tracking. Here, we use electrocorticographic (ECoG) recordings from eight human listeners, to see whether periodicities in high-gamma activity track the periodicities in the envelope of musical rhythms during rhythm perception and imagination. Rhythm imagination was elicited by instructing participants to imagine the rhythm to continue during pauses of several repetitions. To identify electrodes whose periodicities in high-gamma activity track the periodicities in the musical rhythms, we compute the correlation between the autocorrelations (ACC) of both the musical rhythms and the neural signals. A condition in which participants listened to white noise was used to establish a baseline. High-gamma autocorrelations in auditory areas in the superior temporal gyrus and in frontal areas on both hemispheres significantly matched the autocorrelation of the musical rhythms. Overall, numerous significant electrodes are observed on the right hemisphere. Of particular interest is a large cluster of electrodes in the right prefrontal cortex that is active during both rhythm perception and imagination. This indicates conscious processing of the rhythms’ structure as opposed to mere auditory phenomena. The ACC approach clearly highlights that high-gamma activity measured from cortical electrodes tracks both attended and imagined rhythms.

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