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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Altered hierarchical auditory predictive processing after lesions to the orbitofrontal cortex

Abstract:

Orbitofrontal cortex (OFC) is classically linked to inhibitory control, emotion regulation, and reward processing. Recent perspectives propose that the OFC also generates predictions about perceptual events, actions, and their outcomes. We tested the role of the OFC in detecting violations of prediction at two levels of abstraction (i.e., hierarchical predictive processing) by studying the event-related potentials (ERPs) of patients with focal OFC lesions (n = 12) and healthy controls (n = 14) while they detected deviant sequences of tones in a local–global paradigm. The structural regularities of the tones were controlled at two hierarchical levels by rules defined at a local (i.e., between tones within sequences) and at a global (i.e., between sequences) level. In OFC patients, ERPs elicited by standard tones were unaffected at both local and global levels compared to controls. However, patients showed an attenuated mismatch negativity (MMN) and P3a to local prediction violation, as well as a diminished MMN followed by a delayed P3a to the combined local and global level prediction violation. The subsequent P3b component to conditions involving violations of prediction at the level of global rules was preserved in the OFC group. Comparable effects were absent in patients with lesions restricted to the lateral PFC, which lends a degree of anatomical specificity to the altered predictive processing resulting from OFC lesion. Overall, the altered magnitudes and time courses of MMN/P3a responses after lesions to the OFC indicate that the neural correlates of detection of auditory regularity violation are impacted at two hierarchical levels of rule abstraction.

Authors:

• Olgerta Asko

• Alejandro Omar Blenkmann

• Sabine Liliana Leske

• Maja Dyhre Foldal

• Anais Llorens

• Ingrid Funderud

• Torstein R Meling

• Robert T Knight

• Tor Endestad

• Anne-Kristin Solbakk

Date: 2024

DOI: https://doi.org/10.7554/eLife.86386

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Predictable and unpredictable deviance detection in the human hippocampus and amygdala

Abstract:

Our brains extract structure from the environment and form predictions given past experience. Predictive circuits have been identified in wide-spread cortical regions. However, the contribution of medial temporal structures in predictions remains under-explored. The hippocampus underlies sequence detection and is sensitive to novel stimuli, sufficient to gain access to memory, while the amygdala to novelty. Yet, their electrophysiological profiles in detecting predictable and unpredictable deviant auditory events remain unknown. Here, we hypothesized that the hippocampus would be sensitive to predictability, while the amygdala to unexpected deviance. We presented epileptic patients undergoing presurgical monitoring with standard and deviant sounds, in predictable or unpredictable contexts. Onsets of auditory responses and unpredictable deviance effects were detected earlier in the temporal cortex compared with the amygdala and hippocampus. Deviance effects in 1–20 Hz local field potentials were detected in the lateral temporal cortex, irrespective of predictability. The amygdala showed stronger deviance in the unpredictable context. Low-frequency deviance responses in the hippocampus (1–8 Hz) were observed in the predictable but not in the unpredictable context. Our results reveal a distributed network underlying the generation of auditory predictions and suggest that the neural basis of sensory predictions and prediction error signals needs to be extended.

Authors:

• Athina Tzovara

• Tommaso Fedele

• Johannes Sarnthein

• Debora Ledergerber

• Jack J. Lin

• Robert T. Knight

Date: 2024

DOI: https://doi.org/10.1093/cercor/bhad532

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Ramping dynamics and theta oscillations reflect dissociable signatures during rule-guided human behavior

abstract:

Contextual cues and prior evidence guide human goal-directed behavior. The neurophysiological mechanisms that implement contextual priors to guide subsequent actions in the human brain remain unclear. Using intracranial electroencephalography (iEEG), we demonstrate that increasing uncertainty introduces a shift from a purely oscillatory to a mixed processing regime with an additional ramping component. Oscillatory and ramping dynamics reflect dissociable signatures, which likely differentially contribute to the encoding and transfer of different cognitive variables in a cue-guided motor task. The results support the idea that prefrontal activity encodes rules and ensuing actions in distinct coding subspaces, while theta oscillations synchronize the prefrontal-motor network, possibly to guide action execution. Collectively, our results reveal how two key features of large-scale neural population activity, namely continuous ramping dynamics and oscillatory synchrony, jointly support rule-guided human behavior.

Authors:

• Jan Weber

• Anne-Kristin Solbakk

• Alejandro O. Blenkmann

• Anais Llorens

• Ingrid Funderud

• Sabine Leske

• Pål Gunnar Larsson

• Lugoslav Ivanovic

• Robert T. Knight

• Tor Endestad

• Randolph F. Helfrich

Date: 2024

DOI: https://doi.org/10.1038/s41467-023-44571-7

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Awake ripples enhance emotional memory encoding in the human brain

Abstract:

Enhanced memory for emotional experiences is hypothesized to depend on amygdala-hippocampal interactions during memory consolidation. Here we show using intracranial recordings from the human amygdala and the hippocampus during an emotional memory encoding and discrimination task increased awake ripples after encoding of emotional, compared to neutrally-valenced stimuli. Further, post-encoding ripple-locked stimulus similarity is predictive of later memory discrimination. Ripple-locked stimulus similarity appears earlier in the amygdala than in hippocampus and mutual information analysis confirms amygdala influence on hippocampal activity. Finally, the joint ripple-locked stimulus similarity in the amygdala and hippocampus is predictive of correct memory discrimination. These findings provide electrophysiological evidence that post-encoding ripples enhance memory for emotional events.

Authors:

• Haoxin Zhang

• Ivan Skelin

• Shiting Ma

• Michelle Paff

• Lilit Mnatsakanyan

• Michael A. Yassa

• Robert T. Knight

• Jack J. Lin

Date: 2024

DOI: https://doi.org/10.1038/s41467-023-44295-8

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