Subspace partitioning in the human prefrontal cortex resolves cognitive interference

Abstract:

The human prefrontal cortex (PFC) constitutes the structural basis underlying flexible cognitive control, where mixed-selective neural populations encode multiple task features to guide subsequent behavior. The mechanisms by which the brain simultaneously encodes multiple task–relevant variables while minimizing interference from task-irrelevant features remain unknown. Leveraging intracranial recordings from the human PFC, we first demonstrate that competition between coexisting representations of past and present task variables incurs a behavioral switch cost. Our results reveal that this interference between past and present states in the PFC is resolved through coding partitioning into distinct low-dimensional neural states; thereby strongly attenuating behavioral switch costs. In sum, these findings uncover a fundamental coding mechanism that constitutes a central building block of flexible cognitive control.

Authors:

• Jan Weber

• Gabriela Iwama

• Anne-Kristin Solbakk

• Alejandro O. Blenkmann

• Pal G. Larsson

• Jugoslav Ivanovic

• Robert T. Knight

• Tor Endestad

• Randolph Helfrich

Date: 2023

DOI: https://doi.org/10.1073/pnas.2220523120

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A rapid theta network mechanism for flexible information encoding

Abstract:

Flexible behavior requires gating mechanisms that encode only task-relevant information in working memory. Extant literature supports a theoretical division of labor whereby lateral frontoparietal interactions underlie information maintenance and the striatum enacts the gate. Here, we reveal neocortical gating mechanisms in intracranial EEG patients by identifying rapid, within-trial changes in regional and inter-regional activities that predict subsequent behavioral outputs. Results first demonstrate information accumulation mechanisms that extend prior fMRI (i.e., regional high-frequency activity) and EEG evidence (inter-regional theta synchrony) of distributed neocortical networks in working memory. Second, results demonstrate that rapid changes in theta synchrony, reflected in changing patterns of default mode network connectivity, support filtering. Graph theoretical analyses further linked filtering in task-relevant information and filtering out irrelevant information to dorsal and ventral attention networks, respectively. Results establish a rapid neocortical theta network mechanism for flexible information encoding, a role previously attributed to the striatum.

Authors:

• Elizabeth L. Johnson

• Jack J. Lin

• David King-Stephens

• Peter B. Weber

• Kenneth D. Laxer

• Ignacio Saez

• Fady Girgis

• Mark D’Esposito

• Robert T. Knight

• David Badre

Date: 2023

DOI: https://doi.org/10.1038/s41467-023-38574-7

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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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Left hemisphere dominance for bilateral kinematic encoding in the human brain

Abstract:

Neurophysiological studies in humans and nonhuman primates have revealed movement representations in both the contralateral and ipsilateral hemispheres. Inspired by clinical observations, we ask if this bilateral representation differs for the left and right hemispheres. Electrocorticography was recorded in human participants during an instructed-delay reaching task, with movements produced with either the contralateral or ipsilateral arm. Using a cross-validated kinematic encoding model, we found stronger bilateral encoding in the left hemisphere, an effect that was present during preparation and was amplified during execution. Consistent with this asymmetry, we also observed better across-arm generalization in the left hemisphere, indicating similar neural representations for right and left arm movements. Notably, these left hemisphere electrodes were centered over premotor and parietal regions. The more extensive bilateral encoding in the left hemisphere adds a new perspective to the pervasive neuropsychological finding that the left hemisphere plays a dominant role in praxis.

authors:

• Christina M Merrick

• Tanner C Dixon

• Assaf Breska

• Jack Lin

• Edward F Chang

• David King-Stephens

• Kenneth D Laxer

• Peter B Weber

• Jose Carmena

• Robert Thomas Knight

• Richard B Ivry

Date: 2022

DOI: : https://doi.org/10.7554/eLife.69977

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Encoding and decoding analysis of music perception using intracranial EEG

Abstract:

Music perception engages multiple brain regions, however the neural dynamics of this core human experience remains elusive. We applied predictive models to intracranial EEG data from 29 patients listening to a Pink Floyd song. We investigated the relationship between the song spectrogram and the elicited high-frequency activity (70-150Hz), a marker of local neural activity. Encoding models characterized the spectrotemporal receptive fields (STRFs) of each electrode and decoding models estimated the population-level song representation. Both methods confirmed a crucial role of the right superior temporal gyri (STG) in music perception. A component analysis on STRF coefficients highlighted overlapping neural populations tuned to specific musical elements (vocals, lead guitar, rhythm). An ablation analysis on decoding models revealed the presence of unique musical information concentrated in the right STG and more spatially distributed in the left hemisphere. Lastly, we provided the first song reconstruction decoded from human neural activity.

Authors:

• Ludovic Bellier

• Anaïs Llorens

• Déborah Marciano

• Gerwin Schalk

• Peter Brunner

• Robert T. Knight

• Brian N. Pasley

Date: 2022

DOI: https://doi.org/10.1101/2022.01.27.478085

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Event segmentation reveals working memory forgetting rate

Abstract:

We encounter the world as a continuous flow and effortlessly segment sequences of events into episodes. This process of event segmentation engages working memory (WM) for tracking the flow of events and impacts subsequent memory accuracy. WM is limited in how much information (i.e., WM capacity) and for how long the information is retained (i.e., forgetting rate). In this study, across multiple tasks, we estimated participants’ WM capacity and forgetting rate in a dynamic context and evaluated their relationship to event segmentation. A Ushaped relationship across tasks shows that individuals who segmented the movie more finely or coarsely than the average have a faster WM forgetting rate. A separate task assessing long-term memory retrieval revealed that the coarse-segmenters have better recognition of temporal order of events compared to the fine-segmenters. These findings show that event segmentation employs dissociable memory strategies and correlates with how long information is retained in WM

Authors:

• Anna Jafarpour

• Elizabeth A. Buffalo

• Robert T. Knight

• Anne G.E. Collins

Date: 2022

DOI: https://doi.org/10.1016/j.isci.2022.103902

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Mind-wandering: mechanistic insights from lesion, tDCS, and iEEG

Abstract:

Cognitive neuroscience has witnessed a surge of interest in investigating the neural correlates of the mind when it drifts away from an ongoing task and the external environment. To that end, functional neuroimaging research has consistently implicated the default mode network (DMN) and frontoparietal control network (FPCN) in mind-wandering. Yet, it remains unknown which subregions within these networks are necessary and how they facilitate mind-wandering. In this review, we synthesize evidence from lesion, transcranial direct current stimulation (tDCS), and intracranial electroencephalogram (iEEG) studies demonstrating the causal relevance of brain regions, and providing insights into the neuronal mechanism underlying mind-wandering. We propose that the integration of complementary approaches is the optimal strategy to establish a comprehensive understanding of the neural basis of mindwandering.

Authors:

• Julia W.Y. Kam

• Matthias Mittner

• Robert T. Knight

Date: 2022

DOI: https://doi.org/10.1016/j.tics.2021.12.005

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Consciousness is supported by near-critical slow cortical electrodynamics

Abstract:

Mounting evidence suggests that during conscious states, the electrodynamics of the cortex are poised near a critical point or phase transition and that this near-critical behavior supports the vast flow of information through cortical networks during conscious states. Here, we empirically identify a mathematically specific critical point near which waking cortical oscillatory dynamics operate, which is known as the edge-of-chaos critical point, or the boundary between stability and chaos. We do so by applying the recently developed modified 0-1 chaos test to electrocorticography (ECoG) and magnetoencephalography (MEG) recordings from the cortices of humans and macaques across normal waking, generalized seizure, anesthesia, and psychedelic states. Our evidence suggests that cortical information processing is disrupted during unconscious states because of a transition of low-frequency cortical electric oscillations away from this critical point; conversely, we show that psychedelics may increase the information richness of cortical activity by tuning low-frequency cortical oscillations closer to this critical point. Finally, we analyze clinical electroencephalography (EEG) recordings from patients with disorders of consciousness (DOC) and show that assessing the proximity of slow cortical oscillatory electrodynamics to the edge-of-chaos critical point may be useful as an index of consciousness in the clinical setting.

Authors:

• Daniel Toker

• Ioannis Pappas

• Janna D. Lendner

• Joel Frohlich

• Diego M. Mateos

• Suresh Muthukumaraswamy

• Robin Carhart-Harris

• Michelle Paff

• Paul M. Vespa

• Martin M. Monti

• Friedrich T. Sommer

• Robert T. Knight

• Mark D’Esposito

Date: 2022

DOI: https://doi.org/10.1073/pnas.2024455119

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Investigating the Link Between Linguistic and Non-Linguistic Cognitive Control in Bilinguals Using Laplacian-Transformed Event Related Potentials

Abstract:

Bilinguals’ need to suppress the activation of their other language while speaking has been proposed to result in enhanced cognitive control abilities outside of language. Several studies therefore suggest shared cognitive control processes across linguistic and non-linguistic tasks. Here we investigate this potential overlap using scalp electroencephalographic recordings and the Laplacian transformation, providing an estimation of the current source density and enabling the separation of EEG components in space. Fourteen Spanish-English bilinguals performed a picture-word matching task contrasting incongruent trials using cross-linguistic false cognates (e.g., a picture – foot, overlaid with distractor text: the English word PIE, i.e., the false cognate for the Spanish pie meaning “foot”) with congruent trials (matching English picture names and words, i.e., a picture – foot, with overlaid text: the English word FOOT), and an unrelated control condition. In addition, participants performed an arrow-version of the Eriksen flanker task. Worse behavioral performance was observed in incongruent compared to congruent trials in both tasks. In the non-linguistic task, we replicated the previously observed congruency effect on a medial-frontal event-related potential (ERP) peaking around 50 ms before electromyography (EMG) onset. A similar ERP was present in the linguistic task, was sensitive to congruency, and peaked earlier, around 150 ms before EMG onset. In addition, another component was found in the linguistic task at a left lateralized anterior frontal site peaking around 200 ms before EMG onset, but was absent in the non-linguistic task. Our results suggest a partial overlap between linguistic and non-linguistic cognitive control processes and that linguistic conflict resolution may engage additional left anterior frontal control processes.

Authors:

• Martha Mendoza

• Henrike K. Blumenfeld

• Robert T. Knight

• Stephanie K. Ries

Date: 2021

DOI: https://doi.org/10.1162/nol_a_00056

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