Anatomical registration of intracranial electrodes. Robust model-based localization and deformable smooth brain-shift compensation methods

Abstract:

Background: Intracranial electrodes are typically localized from post-implantation CT artifacts. Automatic algorithms localizing low signal-to-noise ratio artifacts and high-density electrode arrays are missing. Additionally, implantation of grids/strips introduces brain deformations, resulting in registration errors when fusing post- implantation CT and pre-implantation MR images. Brain-shift compensation methods project electrode coordinates to cortex, but either fail to produce smooth solutions or do not account for brain deformations. New methods: We first introduce GridFit, a model-based fitting approach that simultaneously localizes all electrodes’ CT artifacts in grids, strips, or depth arrays. Second, we present CEPA, a brain-shift compensation algorithm combining orthogonal-based projections, spring-mesh models, and spatial regularization constraints. Results: We tested GridFit on ~6000 simulated scenarios. The localization of CT artifacts showed robust performance under difficult scenarios, such as noise, overlaps, and high-density implants (<1 mm errors). Validation with data from 20 challenging patients showed 99% accurate localization of the electrodes (3160/3192). We tested CEPA brain-shift compensation with data from 15 patients. Projections accounted for simple mechanical deformation principles with <0.4 mm errors. The inter-electrode distances smoothly changed across neighbor electrodes, while changes in inter-electrode distances linearly increased with projection distance. Comparison with existing methods: GridFit succeeded in difficult scenarios that challenged available methods and outperformed visual localization by preserving the inter-electrode distance. CEPA registration errors were smaller than those obtained for well-established alternatives. Additionally, modeling resting-state high-frequency activity in five patients further supported CEPA.

Authors:

• Alejandro Omar Blenkmann

• Sabine Liliana Leske

• Anaïs Llorens

• Jack J. Lin

• Edward F. Chang

• Peter Brunner

• Gerwin Schalk

• Jugoslav Ivanovic

• Pål Gunnar Larsson

• Robert Thomas Knight

• Tor Endestad

• Anne-Kristin Solbakk

Date: 2024

DOI: https://doi.org/10.1016/j.jneumeth.2024.110056

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Decision and response monitoring during working memory are sequentially represented in the human insula

Abstract:

Emerging research supports a role of the insula in human cognition. Here, we used intracranial EEG to investigate the spatiotemporal dynamics in the insula during a verbal working memory (vWM) task. We found robust effects for theta, beta, and high frequency activity (HFA) during probe presentation requiring a decision. Theta band activity showed differential involvement across left and right insulae while sequential HFA modulations were observed along the anteroposterior axis. HFA in anterior insula tracked decision making and subsequent HFA was observed in posterior insula after the behavioral response. Our results provide electrophysiological evidence of engagement of different insula subregions in both decision-making and response monitoring during vWM and expand our knowledge of the role of the insula in complex human behavior.

Authors:

• Anaïs Llorens

• Ludovic Bellier

• Alejandro O. Blenkmann

• Jugoslav Ivanovic

• Pål G. Larsson

• Jack J. Lin

• Tor Endestad

• Anne-Kristin Solbakk

• Robert T. Knight

Date: 2023

DOI: https://doi.org/10.1016/j.isci.2023.107653

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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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Orbitofrontal cortex governs working memory for temporal order

abstract:

How do we think about time? Converging lesion and neuroimaging evidence indicates that orbitofrontal cortex (OFC) supports the encoding and retrieval of temporal context in long-term memory, which may contribute to confabulation in individuals with OFC damage. Here, we reveal that OFC damage diminishes working memory for temporal order, that is, the ability to disentangle the relative recency of events as they unfold. OFC lesions reduced working memory for temporal order but not spatial position, and individual deficits were commensurate with lesion size. Comparable effects were absent in patients with lesions restricted to lateral prefrontal cortex (PFC). Based on these findings, we propose that OFC supports understanding of the order of events. Well-documented behavioral changes in individuals with OFC damage may relate to impaired temporal-order understanding.

authors:

• Elizabeth L Johnson

• William K Chang

• Callum D Dewar

• Donna Sorensen

• Jack J Lin

• Anne-Kristin Solbakk

• Tor Endestad

• Pal G Larsson

• Jugoslav Ivanovic

• Torstein R Meling

• Donatella Scabini

• Robert T Knight

Date: 2022

DOI: https:// doi.org/10.1016/j.cub.2022.03.074.

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Orbitofrontal cortex governs working memory for temporal order

Abstract:

How do we think about time? Converging lesion and neuroimaging evidence indicates that orbitofrontal cortex (OFC) supports the encoding and retrieval of temporal context in long-term memory1, which may contribute to confabulation in individuals with OFC damage2. Here, we reveal that OFC damage diminishes working memory for temporal order, that is, the ability to disentangle the relative recency of events as they unfold. OFC lesions reduced working memory for temporal order but not spatial position, and individual deficits were commensurate with lesion size. Comparable effects were absent in patients with lesions restricted to lateral prefrontal cortex (PFC). Based on these findings, we propose that OFC supports understanding of the order of events. Well-documented behavioral changes in individuals with OFC damage2 may relate to impaired temporal-order understanding.

Authors:

• Elizabeth L. Johnson

• William K. Chang

• Callum D. Dewar

• Donna Sorensen

• Jack J. Lin

• Anne-Kristin Solbakk

• Tor Endestad

• Pal G. Larsson

• Jugoslav Ivanovic

• Torstein R. Meling

• Donatella Scabini

• Robert T. Knight

Date: 2022

DOI: https://doi.org/10.1016/j.cub.2022.03.074

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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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Dynamic frontotemporal systems process space and time in working memory

ABSTRACT

How do we rapidly process incoming streams of information in working memory, a cognitive mechanism central to human behavior? Dominant views of working memory focus on the prefrontal cortex (PFC), but human hippocampal recordings provide a neurophysiological signature distinct from the PFC. Are these regions independent, or do they interact in the service of working memory? We addressed this core issue in behavior by recording directly from frontotemporal sites in humans performing a visuospatial working memory task that operationalizes the types of identity and spatiotemporal information we encounter every day. Theta band oscillations drove bidirectional interactions between the PFC and medial temporal lobe (MTL; including the hippocampus). MTL theta oscillations directed the PFC preferentially during the processing of spatiotemporal information, while PFC theta oscillations directed the MTL for all types of information being processed in working memory. These findings reveal an MTL theta mechanism for processing space and time and a domain-general PFC theta mechanism, providing evidence that rapid, dynamic MTL–PFC interactions underlie working memory for everyday experiences.

AUTHORS

• Elizabeth L. Johnson

• Jenna N. Adams

• Anne-Kristin Solbakk

• Tor Endestad

• Pål G. Larsson

• Jugoslav Ivanovic

• Torstein R. Meling

• Jack J. Lin

• Robert T. Knight

Date: 2018

DOI: 10.1371/journal.pbio.2004274

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