Default network and frontoparietal control network theta connectivity supports internal attention

Abstract:

Attending to our inner world is a fundamental cognitive phenomenon, yet its neural underpinnings remain largely unknown. Neuroimaging evidence implicates the default network (DN) and frontoparietal control network (FPCN); however, the electrophysiological basis for the interaction between these networks is unclear. Here we recorded intracranial electroencephalogram from DN and FPCN electrodes implanted in individuals undergoing presurgical monitoring for refractory epilepsy. Subjects performed an attention task during which they attended to tones (that is, externally directed attention) or ignored the tones and thought about whatever came to mind (that is, internally directed attention). Given the emerging role of theta band connectivity in attentional processes, we examined the theta power correlation between DN and two subsystems of the FPCN as a function of attention states. We found increased connectivity between DN and FPCNA during internally directed attention compared to externally directed attention, which positively correlated with attention ratings. There was no statistically significant difference between attention states in the connectivity between DN and FPCNB. Our results indicate that enhanced theta band connectivity between the DN and FPCNA is a core electrophysiological mechanism that underlies internally directed attention.

Authors:

• Julia WY Kam

• Jack J Lin

• Anne-Kristin Solbakk

• Tor Endestad

• Pål G Larsson

• Robert T Knight

Date: 2019

DOI: https://doi.org/10.1038/s41562-019-0717-0

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Auditory deviance detection in the human insula: An intracranial EEG study

Abstract:

The human insula is known to be involved in auditory processing, but knowledge about its precise functional role and the underlying electrophysiology is limited. To assess its role in automatic auditory deviance detection we analyzed the EEG high frequency activity (HFA; 75–145 Hz) and ERPs from 90 intracranial insular channels across 16 patients undergoing pre-surgical intracranial monitoring for epilepsy treatment. Subjects passively listened to a stream of standard and deviant tones differing in four physical dimensions: intensity, frequency, location or time. HFA responses to auditory stimuli were found in the short and long gyri, and the anterior, superior, and inferior segments of the circular sulcus of the insular cortex. Only a subset of channels in the inferior segment of the circular sulcus of the insula showed HFA deviance detection responses, i.e., a greater and longer latency response to specific deviants relative to standards. Auditory deviancy processing was also later in the insula when compared with the superior temporal cortex. ERP results were more widespread and supported the HFA insular findings. These results provide evidence that the human insula is engaged during auditory deviance detection.

Authors:

• Alejandro O Blenkmann

• Santiago Collavini

• James Lubell

• Anaïs Llorens

• Ingrid Funderud

• Jugoslav Ivanovic

• Pål G Larsson

• Torstein R Meling

• Tristan Bekinschtein

• Silvia Kochen

• Tor Endestad

• Robert T Knight

• Anne-Kristin Solbakk

Date: 2019

DOI: https://doi.org/10.1016/j.cortex.2019.09.002

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Electrocorticographic dissociation of alpha and beta rhythmic activity in the human sensorimotor system

Abstract:

This study uses electrocorticography in humans to assess how alpha- and beta-band rhythms modulate excitability of the sensorimotor cortex during psychophysically-controlled movement imagery. Both rhythms displayed effector-specific modulations, tracked spectral markers of action potentials in the local neuronal population, and showed spatially systematic phase relationships (traveling waves). Yet, alpha- and beta-band rhythms differed in their anatomical and functional properties, were weakly correlated, and traveled along opposite directions across the sensorimotor cortex. Increased alpha-band power in the somatosensory cortex ipsilateral to the selected arm was associated with spatially-unspecific inhibition. Decreased beta-band power over contralateral motor cortex was associated with a focal shift from relative inhibition to excitation. These observations indicate the relevance of both inhibition and disinhibition mechanisms for precise spatiotemporal coordination of movement-related neuronal populations, and illustrate how those mechanisms are implemented through the substantially different neurophysiological properties of sensorimotor alpha- and beta-band rhythms.

Authors:

• Arjen Stolk

• Loek Brinkman

• Mariska J Vansteensel

• Erik Aarnoutse

• Frans SS Leijten

• Chris H Dijkerman

• Robert T Knight

• Floris P de Lange

• Ivan Toni

Date: 2019

DOI: https://doi.org/10.7554/eLife.48065

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Neural entrainment and network resonance in support of top-down guided attention

Abstract:

Which neural mechanisms provide the functional basis of top-down guided cognitive control? Here we review recent evidence that suggest that the neural basis of attention is inherently rhythmic. In particular, we discuss two physical properties of self-sustained networks, namely entrainment and resonance, and how these shape the timescale of attentional control. Several recent findings revealed theta-band (3-8 Hz) dynamics in top-down guided behavior. These reports were paralleled by intracranial recordings, which implicated theta oscillations in the organization of functional attention networks. We discuss how the intrinsic network architecture shapes covert attentional sampling as well as overt behavior. Taken together, we posit that theta rhythmicity is an inherent feature of the attention network in support of top-down guided goal-directed behavior.

Authors:

• Randolph F Helfrich

• Assaf Breska

• Robert T Knight

Date: 2019

DOI: 10.1016/j.copsyc.2018.12.016

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Bidirectional prefrontal-hippocampal dynamics organize information transfer during sleep in humans

Abstract:

How are memories transferred from short-term to long-term storage? Systems-level memory consolidation is thought to be dependent on the coordinated interplay of cortical slow waves, thalamo-cortical sleep spindles and hippocampal ripple oscillations. However, it is currently unclear how the selective interaction of these cardinal sleep oscillations is organized to support information reactivation and transfer. Here, using human intracranial recordings, we demonstrate that the prefrontal cortex plays a key role in organizing the ripple-mediated information transfer during non-rapid eye movement (NREM) sleep. We reveal a temporally precise form of coupling between prefrontal slow-wave and spindle oscillations, which actively dictates the hippocampal-neocortical dialogue and information transfer. Our results suggest a model of the human sleeping brain in which rapid bidirectional interactions, triggered by the prefrontal cortex, mediate hippocampal activation to optimally time subsequent information transfer to the neocortex during NREM sleep.

Authors:

• Randolph F Helfrich

• Janna D Lendner

• Bryce A Mander

• Heriberto Guillen

• Michelle Paff

• Lilit Mnatsakanyan

• Sumeet Vadera

• Matthew P Walker

• Jack J Lin

• Robert T Knight

Date: 2019

DOI: https://doi.org/10.1038/s41467-019-11444-x

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Sleep as a potential biomarker of tau and β-amyloid burden in the human brain

Abstract:

Recent proposals suggest that sleep may be a factor associated with accumulation of two core pathological features of Alzheimer's disease (AD): tau and β-amyloid (Aβ). Here we combined PET measures of Aβ and tau, electroencephalogram sleep recordings, and retrospective sleep evaluations to investigate the potential utility of sleep measures in predicting in vivo AD pathology in male and female older adults. Regression analyses revealed that the severity of impaired slow oscillation-sleep spindle coupling predicted greater medial temporal lobe tau burden. Aβ burden was not associated with coupling impairment but instead predicted the diminished amplitude of <1 Hz slow-wave-activity, results that were statistically dissociable from each other. Additionally, comparisons of AD pathology and retrospective, self-reported changes in sleep duration demonstrated that changes in sleep across the lifespan can predict late-life Aβ and tau burden. Thus, quantitative and qualitative features of human sleep represent potential noninvasive, cost-effective, and scalable biomarkers (current and future forecasting) of AD pathology, and carry both therapeutic and public health implications.

Authors:

• Joseph R Winer

• Bryce A Mander

• Randolph F Helfrich

• Anne Maass

• Theresa M Harrison

• Suzanne L Baker

• Robert T Knight

• William J Jagust

• Matthew P Walker

Date: 2019

DOI: https://doi.org/10.1523/JNEUROSCI.0503-19.2019

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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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A differential role for human hippocampus in novelty and contextual processing: Implications for P300

Abstract:

The role of the hippocampus in P300 has long been debated. Here, we present a theoretical framework that elucidates hippocampal contributions to scalp P300 based on intracranial and lesion research combined with emerging evidence on the role of the hippocampus in rapid statistical learning, memory, and novelty processing. The P300 has been divided in two subcomponents: a fronto‐central P3a related to novelty and distractor processing, and a parietal P3b related to target detection. Interest in a role for hippocampus in scalp P300 was sparked by P3‐like ERPs measured intracranially in human hippocampus. Subsequent medial temporal lobe lesion studies show intact scalp P3b, indicating that the hippocampus is not critical for P3b. This contrasts with the scalp P3a, which was significantly diminished in human patients with lesions in the posterior hippocampus. This suggests a differential role for hippocampus in P3a and P3b. Our framework purports that the hippocampus plays a central role in distractor processing that leads to P3a generation in cortical regions. We also propose that the hippocampus is involved at the end of the cognitive episode for both P3a and P3b implementing contextual updating. P3‐like ERPs measured in hippocampus may reflect input signals from cortical regions implementing updates based on the outcome of cognitive processes underlying scalp P3, enabling a model update of the environment facilitated by the hippocampus. Overall, this framework proposes an active role for the hippocampus in novelty processing leading up to P3a generation, followed by contextual updating of the outcome of both scalp P3a and P3b.

Authors:

• Yvonne M Fonken

• Julia WY Kam

• Robert T Knight

Date: 2019

DOI: https://doi.org/10.1111/psyp.13400

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Medial orbitofrontal cortex, dorsolateral prefrontal cortex, and hippocampus differentially represent the event saliency

Abstract:

Two primary functions attributed to the hippocampus and prefrontal cortex (PFC) network are retaining the temporal and spatial associations of events and detecting deviant events. It is unclear, however, how these two functions converge into one mechanism. Here, we tested whether increased activity with perceiving salient events is a deviant detection signal or contains information about the event associations by reflecting the magnitude of deviance (i.e., event saliency). We also tested how the deviant detection signal is affected by the degree of anticipation. We studied regional neural activity when people watched a movie that had varying saliency of a novel or an anticipated flow of salient events. Using intracranial electroencephalography from 10 patients, we observed that high-frequency activity (50–150 Hz) in the hippocampus, dorsolateral PFC, and medial OFC tracked event saliency. We also observed that medial OFC activity was stronger when the salient events were anticipated than when they were novel. These results suggest that dorsolateral PFC and medial OFC, as well as the hippocampus, signify the saliency magnitude of events, reflecting the hierarchical structure of event associations.

Authors:

• Anna Jafarpour

• Sandon Griffin

• Jack J Lin

• Robert T Knight

Date: 2019

DOI: https://doi.org/10.1162/jocn_a_01392

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The use of intracranial recordings to decode human language: Challenges and opportunities

Abstract:

Decoding speech from intracranial recordings serves two main purposes: understanding the neural correlates of speech processing and decoding speech features for targeting speech neuroprosthetic devices. Intracranial recordings have high spatial and temporal resolution, and thus offer a unique opportunity to investigate and decode the electrophysiological dynamics underlying speech processing. In this review article, we describe current approaches to decoding different features of speech perception and production – such as spectrotemporal, phonetic, phonotactic, semantic, and articulatory components – using intracranial recordings. A specific section is devoted to the decoding of imagined speech, and potential applications to speech prosthetic devices. We outline the challenges in decoding human language, as well as the opportunities in scientific and neuroengineering applications.

Authors:

• Stephanie Martin

• José del R. Millán

• Robert T. Knight

• Brian N. Pasley

Date: 2019

DOI: http://dx.doi.org/10.1016/j.bandl.2016.06.003

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Roles of ventral versus dorsal pathways in language production: An awake language mapping study

Abstract:

Human language is organized along two main processing streams connecting posterior temporal cortex and inferior frontal cortex in the left hemisphere, travelling dorsal and ventral to the Sylvian fissure. Some views propose a dorsal motor versus ventral semantic division. Others propose division by combinatorial mechanism, with the dorsal stream responsible for combining elements into a sequence and the ventral stream for forming semantic dependencies independent of sequential order. We acquired data from direct cortical stimulation in the left hemisphere in 17 neurosurgical patients and subcortical resection in a subset of 10 patients as part of awake language mapping. Two language tasks were employed: a sentence generation (SG) task tested the ability to form sequential and semantic dependencies, and a picture-word interference (PWI) task manipulated semantic interference. Results show increased error rates in the SG versus PWI task during subcortical testing in the dorsal stream territory, and high error rates in both tasks in the ventral stream territory. Connectivity maps derived from diffusion imaging and seeded in the tumor sites show that patients with more errors in the SG than in the PWI task had tumor locations associated with a dorsal stream connectivity pattern. Patients with the opposite pattern of results had tumor locations associated with a more ventral stream connectivity pattern. These findings provide initial evidence using fiber tract disruption with electrical stimulation that the dorsal pathways are critical for organizing words in a sequence necessary for sentence generation, and the ventral pathways are critical for processing semantic dependencies.

Authors:

• Stephanie K Ries

• Vitória Piai

• David Perry

• Sandon M Griffin

• Kesshi Jordan

• Roland Henry

• Robert T. Knight

• Mitchel S Berger

Date: 2019

DOI: https://doi.org/10.1016/j.bandl.2019.01.001

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Patients with basal ganglia damage show preserved learning in an economic game

Abstract:

Both basal ganglia (BG) and orbitofrontal cortex (OFC) have been widely implicated in social and non-social decision-making. However, unlike OFC damage, BG pathology is not typically associated with disturbances in social functioning. Here we studied the behavior of patients with focal lesions to either BG or OFC in a multi-strategy competitive game known to engage these regions. We find that whereas OFC patients are significantly impaired, BG patients show intact learning in the economic game. By contrast, when information about the strategic context is absent, both cohorts are significantly impaired. Computational modeling further shows a preserved ability in BG patients to learn by anticipating and responding to the behavior of others using the strategic context. These results suggest that apparently divergent findings on BG contribution to social decision-making may instead reflect a model where higher-order learning processes are dissociable from trial-and-error learning, and can be preserved despite BG damage.

Authors:

• Lusha Zhu

• Yaomin Jiang

• Donatella Scabini

• Robert T. Knight

• Ming Hsu

Date: 2019

DOI: https://doi.org/10.1038/s41467-019-08766-1

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Opportunities and challenges for a maturing science of consciousness

Description:

Scientific research on consciousness is critical to multiple scientific, clinical, and ethical issues. The growth of the field could also be beneficial to several areas including neurology and mental health research. To achieve this goal, we need to set funding priorities carefully and address problems such as job creation and potential media misrepresentation.

Authors:

• Matthias Michel

• Diane Beck

• Ned Block

• Hal Blumenfeld

• Richard Brown

• David Carmel

• Marisa Carrasco

• Mazviita Chirimuuta

• Marvin Chun

• Axel Cleeremans

• Stanislas Dehaene

• Stephen M. Fleming

• Chris Frith

• Patrick Haggard

• Biyu J. He

• Cecilia Heyes

• Melvyn A. Goodale

• Liz Irvine

• Mitsuo Kawato

• Robert Kentridge

• Jean-Remi King

• Robert T. Knight

• Sid Kouider

• Victor Lamme

• Dominique Lamy

• Hakwan Lau

• Steven Laureys

• Joseph LeDoux

• Ying-Tung Lin

• Kayuet Liu

• Stephen L. Macknik

• Susana Martinez-Conde

• George A. Mashour

• Lucia Melloni

• Lisa Miracchi

• Myrto Mylopoulos

• Lionel Naccache

• Adrian M. Owen

• Richard E. Passingham

• Luiz Pessoa

• Megan A. K. Peters

• Dobromir Rahnev

• Tony Ro

• David Rosenthal

• Yuka Sasaki

• Claire Sergent

• Guillermo Solovey

• Nicholas D. Schiff

• Anil Seth

• Catherine Tallon-Baudry

• Marco Tamietto

• Frank Tong

• Simon van Gaal

• Alexandra Vlassova

• Takeo Watanabe

• Josh Weisberg

• Karen Yan

• Masatoshi Yoshida

Date: 2019

DOI: 10.1038/s41562-019-0531-8

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Temporal dynamics and response modulation across the human visual system in a spatial attention task: an ECoG study

Abstract:

The selection of behaviorally relevant information from cluttered visual scenes (often referred to as “attention”) is mediated by a cortical large-scale network consisting of areas in occipital, temporal, parietal, and frontal cortex that is organized into a functional hierarchy of feedforward and feedback pathways. In the human brain, little is known about the temporal dynamics of attentional processing from studies at the mesoscopic level of electrocorticography (ECoG), that combines millisecond temporal resolution with precise anatomical localization of recording sites. We analyzed high-frequency broadband responses (HFB) responses from 626 electrodes implanted in 8 epilepsy patients who performed a spatial attention task. Electrode locations were reconstructed using a probabilistic atlas of the human visual system. HFB responses showed high spatial selectivity and tuning, constituting ECoG response fields (RFs), within and outside the topographic visual system. In accordance with monkey physiology studies, both RF widths and onset latencies increased systematically across the visual processing hierarchy. We used the spatial specificity of HFB responses to quantitatively study spatial attention effects and their temporal dynamics to probe a hierarchical top-down model suggesting that feedback signals back propagate the visual processing hierarchy. Consistent with such a model, the strengths of attentional modulation were found to be greater and modulation latencies to be shorter in posterior parietal cortex, middle temporal cortex and ventral extrastriate cortex compared with early visual cortex. However, inconsistent with such a model, attention effects were weaker and more delayed in anterior parietal and frontal cortex.

Authors:

• Anne B. Martin

• Xiaofang Yang

• Yuri B. Saalmann

• Liang Wang

• Avgusta Shestyuk

• Jack J. Lin

• Josef Parvizi

• Robert T. Knight

• Sabine Kastner

Date: 2019

DOI: 10.1523/JNEUROSCI.1889-18.2018

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Spectral imprints of working memory for everyday associations in the frontoparietal network

ABSTRACT

How does the human brain rapidly process incoming information in working memory? In growing divergence from a single-region focus on the prefrontal cortex (PFC), recent work argues for emphasis on how distributed neural networks are rapidly coordinated in support of this central neurocognitive function. Previously, we showed that working memory for everyday “what,” “where,” and “when” associations depends on multiplexed oscillatory systems, in which signals of different frequencies simultaneously link the PFC to parieto-occipital and medial temporal regions, pointing to a complex web of sub-second, bidirectional interactions. Here, we used direct brain recordings to delineate the frontoparietal oscillatory correlates of working memory with high spatiotemporal precision. Seven intracranial patients with electrodes simultaneously localized to prefrontal and parietal cortices performed a visuospatial working memory task that operationalizes the types of identity and spatiotemporal information we encounter every day. First, task-induced oscillations in the same delta-theta (2–7 Hz) and alpha-beta (9–24 Hz) frequency ranges previously identified using scalp electroencephalography (EEG) carried information about the contents of working memory. Second, maintenance was linked to directional connectivity from the parietal cortex to the PFC. However, presentation of the test prompt to cue identity, spatial, or temporal information changed delta-theta coordination from a unidirectional, parietal-led system to a bidirectional, frontoparietal system. Third, the processing of spatiotemporal information was more bidirectional in the delta-theta range than was the processing of identity information, where alpha-beta connectivity did not exhibit sensitivity to the contents of working memory. These findings implicate a bidirectional delta-theta mechanism for frontoparietal control over the contents of working memory.

AUTHORS

• Elizabeth L. Johnson

• David King-Stephens

• Peter B. Weber

• Kenneth D. Laxer

• Jack J. Lin

• Robert T. Knight

Date: 2019

DOI: 10.3389/fnsys.2018.00065

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Neural entrainment and network resonance in support of top-down guided attention

ABSTRACT

Which neural mechanisms provide the functional basis of top-down guided cognitive control? Here, we review recent evidence that suggest that the neural basis of attention is inherently rhythmic. In particular, we discuss two physical properties of self-sustained networks, namely entrainment and resonance, and how these shape the timescale of attentional control. Several recent findings revealed theta-band (3–8 Hz) dynamics in top-down guided behavior. These reports were paralleled by intracranial recordings, which implicated theta oscillations in the organization of functional attention networks. We discuss how the intrinsic network architecture shapes covert attentional sampling as well as overt behavior. Taken together, we posit that theta rhythmicity is an inherent feature of the attention network in support of top-down guided goal-directed behavior.

AUTHORS

• Randolph F. Helfrich

• Assaf Breska

• Robert T. Knight

Date: 2019

DOI: 10.1016/j.copsyc.2018.12.016

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Systematic comparison between a wireless EEG system with dry electrodes and a wired EEG system with wet electrodes

Abstract:

Recent advances in dry electrodes technology have facilitated the recording of EEG in situations not previously possible, thanks to the relatively swift electrode preparation and avoidance of applying gel to subject's hair. However, to become a true alternative, these systems should be compared to state-of-the-art wet EEG systems commonly used in clinical or research applications. In our study, we conducted a systematic comparison of electrodes application speed, subject comfort, and most critically electrophysiological signal quality between the conventional and wired Biosemi EEG system using wet active electrodes and the compact and wireless F1 EEG system consisting of dry passive electrodes. All subjects (n = 27) participated in two recording sessions on separate days, one with the wet EEG system and one with the dry EEG system, in which the session order was counterbalanced across subjects. In each session, we recorded their EEG during separate rest periods with eyes open and closed followed by two versions of a serial visual presentation target detection task. Each task component allows for a neural measure reflecting different characteristics of the data, including spectral power in canonical low frequency bands, event-related potential components (specifically, the P3b), and single trial classification based on machine learning. The performance across the two systems was similar in most measures, including the P3b amplitude and topography, as well as low frequency (theta, alpha, and beta) spectral power at rest. Both EEG systems performed well above chance in the classification analysis, with a marginal advantage of the wet system over the dry. Critically, all aforementioned electrophysiological metrics showed significant positive correlations (r = 0.54–0.89) between the two EEG systems. This multitude of measures provides a comprehensive comparison that captures different aspects of EEG data, including temporal precision, frequency domain as well as multivariate patterns of activity. Taken together, our results indicate that the dry EEG system used in this experiment can effectively record electrophysiological measures commonly used across the research and clinical contexts with comparable quality to the conventional wet EEG system.

Authors:

• Julia W.Y. Kam

• Sandon Griffin

• Alan Shen

• Shawn Patel

• Hermann Hinrichs

• Hans-Jochen Heinze

• Leon Y. Deouell

• Robert T. Knight

Date: 2019

DOI: 10.1016/j.neuroimage.2018.09.012

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