Advances in human intracranial electroencephalography research, guidelines and good practices

Abstract:

Since the second half of the twentieth century, intracranial electroencephalography (iEEG), including both electrocorticography (ECoG) and stereo-electroencephalography (sEEG), has provided an intimate view into the human brain. At the interface between fundamental research and the clinic, iEEG provides both high temporal resolution and high spatial specificity but comes with constraints, such as the individual's tailored sparsity of electrode sampling. Over the years, researchers in neuroscience developed their practices to make the most of the iEEG approach. Here we offer a critical review of iEEG research practices in a didactic framework for newcomers, as well addressing issues encountered by proficient researchers. The scope is threefold: (i) review common practices in iEEG research, (ii) suggest potential guidelines for working with iEEG data and answer frequently asked questions based on the most widespread practices, and (iii) based on current neurophysiological knowledge and methodologies, pave the way to good practice standards in iEEG research. The organization of this paper follows the steps of iEEG data processing. The first section contextualizes iEEG data collection. The second section focuses on localization of intracranial electrodes. The third section highlights the main pre-processing steps. The fourth section presents iEEG signal analysis methods. The fifth section discusses statistical approaches. The sixth section draws some unique perspectives on iEEG research. Finally, to ensure a consistent nomenclature throughout the manuscript and to align with other guidelines, e.g., Brain Imaging Data Structure (BIDS) and the OHBM Committee on Best Practices in Data Analysis and Sharing (COBIDAS), we provide a glossary to disambiguate terms related to iEEG research.

Authors:

• Manuel R. Mercier

• Anne-Sophie Dubarry

• François Tadel

• Pietro Avanzini

• Nikolai Axmacher

• Dillan Cellier

• Maria Del Vecchio

• Liberty S. Hamilton

• Dora Hermes

• Michael J. Kahana

• Robert T. Knight

• Anais Llorens

• Pierre Megevand

• Lucia Melloni

• Kai J. Miller

• Vitória Piai

• Aina Puce

• Nick F. Ramsey

• Caspar M. Schwiedrzik

• Sydney E. Smith

• Arjen Stolk

• Nicole C. Swann

• Mariska J Vansteensel

• Bradley Voytek

• Liang Wang

• Jean-Philippe Lachaux

• Robert Oostenveld

Date: 2022

DOI: https://doi.org/10.1016/j.neuroimage.2022.119438

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Parameterizing neural power spectra into periodic and aperiodic components

Abstract:

Electrophysiological signals exhibit both periodic and aperiodic properties. Periodic oscillations have been linked to numerous physiological, cognitive, behavioral and disease states. Emerging evidence demonstrates that the aperiodic component has putative physiological interpretations and that it dynamically changes with age, task demands and cognitive states. Electrophysiological neural activity is typically analyzed using canonically defined frequency bands, without consideration of the aperiodic (1/f-like) component. We show that standard analytic approaches can conflate periodic parameters (center frequency, power, bandwidth) with aperiodic ones (offset, exponent), compromising physiological interpretations. To overcome these limitations, we introduce an algorithm to parameterize neural power spectra as a combination of an aperiodic component and putative periodic oscillatory peaks. This algorithm requires no a priori specification of frequency bands. We validate this algorithm on simulated data, and demonstrate how it can be used in applications ranging from analyzing age-related changes in working memory to large-scale data exploration and analysis.

Authors:

• Thomas Donoghue

• Matar Haller

• Erik J Peterson

• Paroma Varma

• Priyadarshini Sebastian

• Richard Gao

• Torben Noto

• Antonio H Lara

• Joni D Wallis

• Robert T Knight

• Avgusta Shestyuk

• Bradley Voytek

Date: 2020

DOI: https://doi.org/10.1038/s41593-020-00744-x

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iEEG-BIDS, extending the Brain Imaging Data Structure specification to human intracranial electrophysiology

Description:

The Brain Imaging Data Structure (BIDS) is a community-driven specification for organizing neuroscience data and metadata with the aim to make datasets more transparent, reusable, and reproducible. Intracranial electroencephalography (iEEG) data offer a unique combination of high spatial and temporal resolution measurements of the living human brain. To improve internal (re) use and external sharing of these unique data, we present a specification for storing and sharing iEEG data: iEEG-BIDS.

Authors:

• Christopher Holdgraf

• Stefan Appelhoff

• Stephan Bickel

• Kristofer Bouchard

• Sasha D’Ambrosio

• Olivier David

• Orrin Devinsky

• Benjamin Dichter

• Adeen Flinker

• Brett L. Foster

• Krzysztof J. Gorgolewski

• Iris Groen

• David Groppe

• Aysegul Gunduz

• Liberty Hamilton

• Christopher J. Honey

• Mainak Jas

• Robert T. Knight

• Jean-Philippe Lachaux

• Jonathan C. Lau

• Christopher Lee-Messer

• Brian N. Lundstrom

• Kai J. Miller

• Jeffrey G. Ojemann

• Robert Oostenveld

• Natalia Petridou

• Gio Piantoni

• Andrea Pigorini

• Nader Pouratian

• Nick F. Ramsey

• Arjen Stolk

• Nicole C. Swann

• François Tadel

• Bradley Voytek

• Brian A . Wandell

• Jonathan Winawer

• Kirstie Whitaker

• Lyuba Zehl

• Dora Hermes

Date: 2019

DOI: https://doi.org/10.1038/s41597-019-0105-7

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Age-Related Changes in 1/f Neural Electrophysiological Noise

ABSTRACT

Aging is associated with performance decrements across multiple cognitive domains. The neural noise hypothesis, a dominant view of the basis of this decline, posits that aging is accompanied by an increase in spontaneous, noisy baseline neural activity. Here we analyze data from two different groups of human subjects: intracranial electrocorticography from 15 participants over a 38 year age range (15–53 years) and scalp EEG data from healthy younger (20 –30 years) and older (60 –70 years) adults to test the neural noise hypothesis from a 1/f noise perspective. Many natural phenomena, including electrophysiology, are characterized by 1/f noise. The defining characteristic of 1/f is that the power of the signal frequency content decreases rapidly as a function of the frequency ( f ) itself. The slope of this decay, the noise exponent (), is often1 for electrophysiological data and has been shown to approach white noise (defined as  0) with increasing task difficulty.Weobserved, in both electrophysiological datasets, that aging is associated with a flatter (more noisy) 1/f power spectral density, even at rest, and that visual cortical 1/f noise statistically mediates age-related impairments in visual working memory. These results provide electrophysiological support for the neural noise hypothesis of aging.

AUTHORS

• Bradley Voytek

• Mark A. Kramer

• John Case

• Kyle Q. Lepage

• Zachary Tempesta

• Robert T. Knight

• Adam Gazzaley

Date: 2015

DOI: 10.1523/JNEUROSCI.2332-14.2015

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Oscillatory dynamics coordinating human frontal networks in support of goal maintenance

Abstract:

Humans have a capacity for hierarchical cognitive control—the ability to simultaneously control immediate actions while holding more abstract goals in mind. Neuropsychological and neuroimaging evidence suggests that hierarchical cognitive control emerges from a frontal architecture whereby prefrontal cortex coordinates neural activity in the motor cortices when abstract rules are needed to govern motor outcomes. We utilized the improved temporal resolution of human intracranial electrocorticography to investigate the mechanisms by which frontal cortical oscillatory networks communicate in support of hierarchical cognitive control. Responding according to progressively more abstract rules resulted in greater frontal network theta phase encoding (4–8 Hz) and increased prefrontal local neuronal population activity (high gamma amplitude, 80–150 Hz), which predicts trial-by-trial response times. Theta phase encoding coupled with high gamma amplitude during inter-regional information encoding, suggesting that inter-regional phase encoding is a mechanism for the dynamic instantiation of complex cognitive functions by frontal cortical subnetworks.

Authors:

• Bradley Voytek

• Andrew S. Kayser

• David Badre

• David Fegen

• Edward F. Chang

• Nathan E. Crone

• Josef Parvizi

• Robert T. Knight

• Mark D'Esposito

Date: 2015

DOI: 10.1038/nn.4071

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Proceedings of the Third International Workshop on Advances in Electrocorticography

Authors:

• Anthony Ritaccio

• Michael Beauchamp

• Conrado Bosman

• Peter Brunner

• Edward F. Chang

• Nathan E. Crone

• Ayesegul Gunduz

• Disha Gupta

• Robert T. Knight

• Eric Leuthardt

• Brian Litt

• Daniel Moran

• Jeffrey G. Ojemann

• Josef Parvizi

• Nick F. Ramsey

• Jochem W. Rieger

• Jonathan Viventi

• Bradley Voytek

• Justin Williams

• Gerwin Schalk

Date: 2012

DOI: 10.1016/j.yebeh.2012.09.016

PubMed: 23160096

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Abstract:

The Third International Workshop on Advances in Electrocorticography (ECoG) was convened in Washington, DC, on November 10–11, 2011. As in prior meetings, a true multidisciplinary fusion of clinicians, scientists, and engineers from many disciplines gathered to summarize contemporary experiences in brain surface recordings. The proceedings of this meeting serve as evidence of a very robust and transformative field but will yet again require revision to incorporate the advances that the following year will surely bring.

Differential Go/NoGo activity in both contingent negative variation and spectral power

Authors:

• Ingrid Funderud

• Magnus Lindgren

• Marianne Lovstad

• Tor Endestad

• Bradley Voytek

• Robert T. Knight

• Anne-Kristin Solbakk

Date: 2012

DOI: 10.1371/journal.pone.0048504

PubMed: 23119040

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Abstract:

We investigated whether both the contingent negative variation (CNV), an event-related potential index of preparatory brain activity, and event-related oscillatory EEG activity differentiated Go and NoGo trials in a delayed response task. CNV and spectral power (4-100 Hz) were calculated from EEG activity in the preparatory interval in 16 healthy adult participants. As previously reported, CNV amplitudes were higher in Go compared to NoGo trials. In addition, event-related spectral power of the Go condition was reduced in the theta to low gamma range compared to the NoGo condition, confirming that preparing to respond is associated with modulation of event-related spectral activity as well as the CNV. Altogether, the impact of the experimental manipulation on both slow event-related potentials and oscillatory EEG activity may reflect coordinated dynamic changes in the excitability of distributed neural networks involved in preparation.

A method for event-related phase/amplitude coupling

Authors:

• Bradley Voytek

• Mark D'Esposito

• Nathan E. Crone

• Robert T. Knight

Date: 2012

DOI: 10.1016/j.neuroimage.2012.09.023

PubMed: 22986076

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Abstract:

Phase/amplitude coupling (PAC) is emerging as an important electrophysiological measure of local and long-distance neuronal communication. Current techniques for calculating PAC provide a numerical index that represents an average value across an arbitrarily long time period. This requires researchers to rely on block design experiments and temporal concatenation at the cost of the sub-second temporal resolution afforded by electrophysiological recordings. Here we present a method for calculating event-related phase/amplitude coupling (ERPAC) designed to capture the temporal evolution of task-related changes in PAC across events or between distant brain regions that is applicable to human or animal electromagnetic recording.

Anterior Cingulate Cortex and Cognitive Control: Neuropsychological and Electrophysiological Findings in Two Patients with Lesions to Dorsomedial Prefrontal Cortex

Authors:

• Marianne Lovstad

• Ingrid Funderud

• Torstein Meling

• Ulrike M. Krämer

• Bradley Voytek

• Paulina Due-Tønnesse

• Tor Endestad

• Magnus Lindgren

• Robert T. Knight

• Anne-Kristin Solbakk

Date: 2012

DOI: 10.1016/j.bandc.2012.07.008

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Abstract:

Whereas neuroimaging studies of healthy subjects have demonstrated an association between the anterior cingulate cortex (ACC) and cognitive control functions, including response monitoring and error detection, lesion studies are sparse and have produced mixed results. Due to largely normal behavioral test results in two patients with medial prefrontal lesions, a hypothesis has been advanced claiming that the ACC is not involved in cognitive operations. In the current study, two comparably rare patients with unilateral lesions to dorsal medial prefrontal cortex (MPFC) encompassing the ACC were assessed with neuropsychological tests as well as Event-Related Potentials in two experimental paradigms known to engage prefrontal cortex (PFC). These included an auditory Novelty Oddball task and a visual Stop-signal task. Both patients performed normally on the Stroop test but showed reduced performance on tests of learning and memory. Moreover, altered attentional control was reflected in a diminished Novelty P3, whereas the posterior P3b to target stimuli was present in both patients. The error-related negativity, which has been hypothesized to be generated in the ACC, was present in both patients, but alterations of inhibitory behavior were observed. Although interpretative caution is generally called for in single case studies, and the fact that the lesions extended outside the ACC, the findings nevertheless suggest a role for MPFC in cognitive control that is not restricted to error monitoring.

Contribution of Subregions of Human Frontal Cortex to Novelty Processing

Authors:

• Marianne Lovstad

• Ingrid Funderud

• Magnus Lindgren

• Tor Endestad

• Paulina Due-Tønnesse

• Torstein Meling

• Bradley Voytek

• Robert T. Knight

• Anne-Kristin Solbakk

Date: 2012

DOI: 10.1162/jocn_a_00099

PubMed: 21812562

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Abstract:

Novelty processing was studied in patients with lesions centered in either OFC or lateral pFC (LPFC). An auditory novelty oddball ERP paradigm was applied with environmental sounds serving as task irrelevant novel stimuli. Lesions to the LPFC as well as the OFC resulted in a reduction of the frontal Novelty P3 response, supporting a key role of both frontal subdivisions in novelty processing. The posterior P3b to target sounds was unaffected in patients with frontal lobe lesions in either location, indicating intact posterior cortical target detection mechanisms. LPFC patients displayed an enhanced sustained negative slow wave (NSW) to novel sounds not observed in OFC patients, indicating prolonged resource allocation to task-irrelevant stimuli after LPFC damage. Both patient groups displayed an enhanced NSW to targets relative to controls. However, there was no difference in behavior between patients and controls suggesting that the enhanced NSW to targets may index an increased resource allocation to response requirements enabling comparable performance in the frontal lesioned patients. The current findings indicate that the LPFC and OFC have partly shared and partly differential contributions to the cognitive subcomponents of novelty processing.

Prefrontal lesions impair object-spatial integration.

Authors:

• Bradley Voytek

• Maryam Soltani

• Natasha Pickard

• Mark M. Kishiyama

• Robert T. Knight

Date: 2012

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Abstract:

How and where object and spatial information are perceptually integrated in the brain is a central question in visual cognition. Single-unit physiology, scalp EEG, and fMRI research suggests that the prefrontal cortex (PFC) is a critical locus for object-spatial integration. To test the causal participation of the PFC in an object-spatial integration network, we studied ten patients with unilateral PFC damage performing a lateralized object-spatial integration task. Consistent with single-unit and neuroimaging studies, we found that PFC lesions result in a significant behavioral impairment in object-spatial integration. Furthermore, by manipulating inter-hemispheric transfer of object-spatial information, we found that masking of visual transfer impairs performance in the contralesional visual field in the PFC patients. Our results provide the first evidence that the PFC plays a key, causal role in an object-spatial integration network. Patient performance is also discussed within the context of compensation by the non-lesioned PFC.

Dynamic communication and connectivity in frontal networks

Authors:

• Bradley Voytek

• Robert T. Knight

Date: 2011

DOI: 10.1093/acprof:oso/9780199791569.003.0028

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Abstract:

How do we maintain a stable percept of the world in the face of the powerful drive of neuroplasticity in both health and disease? This dichotomy forms one of the most fundamental unanswered questions in neuroscience concerning the balance between the dynamic, plastic underpinnings of our neurobiology and the relative stability of our cognition. Th e brain undergoes massive changes in size, morphology, and connectivity during normal development and aging as well as in response to brain injury, yet we can maintain a relatively stable sense of cognition and self during the lifespan. Human brains, each with over 100 billion neurons, develop similarly despite the wide variations in environment and experience. However, within the bounds of this stability there exists a wide range of variability and capacity for change. Here we will discuss the role of neuroplasticity in frontal lobe-dependent cognition by examining the localization of attention and memory functions in the brain and how these seemingly fixed locations may reflect flexible neural networks that change communication properties as required by behavior.

Shifts in gamma phase-amplitude coupling frequency from theta to alpha over posterior cortex during visual tasks

Authors:

• Bradley Voytek

• Ryan T. Canolty

• Avgusta Shestyuk

• Nathan E. Crone

• Josef Parvizi

• Robert T. Knight

Date: 2010

DOI: 10.3389/fnhum.2010.00191

PubMed: 21060716

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Abstract:

The phase of ongoing theta (4–8 Hz) and alpha (8–12 Hz) electrophysiological oscillations is coupled to high gamma (80–150 Hz) amplitude, which suggests that low-frequency oscillations modulate local cortical activity. While this phase–amplitude coupling (PAC) has been demonstrated in a variety of tasks and cortical regions, it has not been shown whether task demands differentially affect the regional distribution of the preferred low-frequency coupling to high gamma. To address this issue we investigated multiple-rhythm theta/alpha to high gamma PAC in two subjects with implanted subdural electrocorticographic grids. We show that high gamma amplitude couples to the theta and alpha troughs and demonstrate that, during visual tasks, alpha/high gamma coupling preferentially increases in visual cortical regions. These results suggest that low-frequency phase to high-frequency amplitude coupling is modulated by behavioral task and may reflect a mechanism for selection between communicating neuronal networks.

Dynamic neuroplacticity after human prefrontal cortex damage

Authors:

• Bradley Voytek

• Matar Davis

• Elena Yago

• Francisco Barceló

• Edward K. Vogel

• Robert T. Knight

Date: 2010

DOI: 10.1016/j.neuron.2010.09.018

PubMed: 21040843

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Abstract:

Memory and attention deficits are common after prefrontal cortex (PFC) damage, yet people generally recover some function over time. Recovery is thought to be dependent upon undamaged brain regions, but the temporal dynamics underlying cognitive recovery are poorly understood. Here, we provide evidence that the intact PFC compensates for damage in the lesioned PFC on a trial-by-trial basis dependent on cognitive load. The extent of this rapid functional compensation is indexed by transient increases in electrophysiological measures of attention and memory in the intact PFC, detectable within a second after stimulus presentation and only when the lesioned hemisphere is challenged. These observations provide evidence supporting a dynamic and flexible model of compensatory neural plasticity.

Prefrontal and basal ganglia contributions to visual working memory

Authors:

• Bradley Voytek

• Robert T. Knight

Date: 2010

DOI: 10.1073/pnas.1007277107

PubMed: 20921401

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Abstract:

Visual working memory (VWM) is a remarkable skill dependent on the brain’s ability to construct and hold an internal representation of the world for later comparison with an external stimulus. The prefrontal cortex (PFC) and basal ganglia (BG) interact within a cortical and subcortical network supporting VWM. We used scalp electroencephalography in groups of patients with unilateral PFC or BG lesions to provide evidence that these regions play complementary but dissociable roles in VWM. PFC patients show behavioral and electrophysiological deficits manifested by attenuation of extrastriate attention and VWM-related neural activity only for stimuli presented to the contralesional visual field. In contrast, patients with BG lesions show behavioral and electrophysiological VWM deficits independent of the hemifield of stimulus presentation but have intact extrastriate attention activity. The results support a model wherein the PFC is critical for top-down intrahemispheric modulation of attention and VWM with the BG involved in global support of VWM processes.

Hemicraniectomy: A New Model for Human Electrophysiology with High Spatio-temporal Resolution

Authors:

• Bradley Voytek

• Lavi Secundo

• Aurélie Bidet-Caulet

• Shirley I. Stiver

• Alisa D. Gean

• Geoffrey T. Manley

• Robert T. Knight

Date: 2010

DOI: 10.1162/jocn.2009.21384

PubMed: 19925193

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Abstract:

Human electrophysiological research is generally restricted to scalp EEG, magneto-encephalography, and intracranial electrophysiology. Here we examine a unique patient cohort that has undergone decompressive hemicraniectomy, a surgical procedure wherein a portion of the calvaria is removed for several months during which time the scalp overlies the brain without intervening bone. We quantify the differences in signals between electrodes over areas with no underlying skull and scalp EEG electrodes over the intact skull in the same subjects. Signals over the hemicraniectomy have enhanced amplitude and greater task-related power at higher frequencies (60–115 Hz) compared with signals over skull. We also provide evidence of a metric for trial-by-trial EMG/EEG coupling that is effective over the hemicraniectomy but not intact skull at frequencies >60 Hz. Taken together, these results provide evidence that the hemicraniectomy model provides a means for studying neural dynamics in humans with enhanced spatial and temporal resolution.