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Human hippocampal responses to network intracranial stimulation vary with theta phase

Hippocampal-dependent memory is thought to be supported by distinct connectivity states, with strong input to the hippocampus benefitting encoding and weak input benefitting retrieval. Previous research in rodents suggests that the hippocampal theta oscillation orchestrates the transition between th...

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Autores principales: Lurie, Sarah M, Kragel, James E, Schuele, Stephan U, Voss, Joel L
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9733942/
https://www.ncbi.nlm.nih.gov/pubmed/36453717
http://dx.doi.org/10.7554/eLife.78395
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author Lurie, Sarah M
Kragel, James E
Schuele, Stephan U
Voss, Joel L
author_facet Lurie, Sarah M
Kragel, James E
Schuele, Stephan U
Voss, Joel L
author_sort Lurie, Sarah M
collection PubMed
description Hippocampal-dependent memory is thought to be supported by distinct connectivity states, with strong input to the hippocampus benefitting encoding and weak input benefitting retrieval. Previous research in rodents suggests that the hippocampal theta oscillation orchestrates the transition between these states, with opposite phase angles predicting minimal versus maximal input. We investigated whether this phase dependence exists in humans using network-targeted intracranial stimulation. Intracranial local field potentials were recorded from individuals with epilepsy undergoing medically necessary stereotactic electroencephalographic recording. In each subject, biphasic bipolar direct electrical stimulation was delivered to lateral temporal sites with demonstrated connectivity to hippocampus. Lateral temporal stimulation evoked ipsilateral hippocampal potentials with distinct early and late components. Using evoked component amplitude to measure functional connectivity, we assessed whether the phase of hippocampal theta predicted relatively high versus low connectivity. We observed an increase in the continuous phase–amplitude relationship selective to the early and late components of the response evoked by lateral temporal stimulation. The maximal difference in these evoked component amplitudes occurred across 180 degrees of separation in the hippocampal theta rhythm; that is, the greatest difference in component amplitude was observed when stimulation was delivered at theta peak versus trough. The pattern of theta-phase dependence observed for hippocampus was not identified for control locations. These findings demonstrate that hippocampal receptivity to input varies with theta phase, suggesting that theta phase reflects connectivity states of human hippocampal networks. These findings confirm a putative mechanism by which neural oscillations modulate human hippocampal function.
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spelling pubmed-97339422022-12-10 Human hippocampal responses to network intracranial stimulation vary with theta phase Lurie, Sarah M Kragel, James E Schuele, Stephan U Voss, Joel L eLife Neuroscience Hippocampal-dependent memory is thought to be supported by distinct connectivity states, with strong input to the hippocampus benefitting encoding and weak input benefitting retrieval. Previous research in rodents suggests that the hippocampal theta oscillation orchestrates the transition between these states, with opposite phase angles predicting minimal versus maximal input. We investigated whether this phase dependence exists in humans using network-targeted intracranial stimulation. Intracranial local field potentials were recorded from individuals with epilepsy undergoing medically necessary stereotactic electroencephalographic recording. In each subject, biphasic bipolar direct electrical stimulation was delivered to lateral temporal sites with demonstrated connectivity to hippocampus. Lateral temporal stimulation evoked ipsilateral hippocampal potentials with distinct early and late components. Using evoked component amplitude to measure functional connectivity, we assessed whether the phase of hippocampal theta predicted relatively high versus low connectivity. We observed an increase in the continuous phase–amplitude relationship selective to the early and late components of the response evoked by lateral temporal stimulation. The maximal difference in these evoked component amplitudes occurred across 180 degrees of separation in the hippocampal theta rhythm; that is, the greatest difference in component amplitude was observed when stimulation was delivered at theta peak versus trough. The pattern of theta-phase dependence observed for hippocampus was not identified for control locations. These findings demonstrate that hippocampal receptivity to input varies with theta phase, suggesting that theta phase reflects connectivity states of human hippocampal networks. These findings confirm a putative mechanism by which neural oscillations modulate human hippocampal function. eLife Sciences Publications, Ltd 2022-12-01 /pmc/articles/PMC9733942/ /pubmed/36453717 http://dx.doi.org/10.7554/eLife.78395 Text en © 2022, Lurie et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Lurie, Sarah M
Kragel, James E
Schuele, Stephan U
Voss, Joel L
Human hippocampal responses to network intracranial stimulation vary with theta phase
title Human hippocampal responses to network intracranial stimulation vary with theta phase
title_full Human hippocampal responses to network intracranial stimulation vary with theta phase
title_fullStr Human hippocampal responses to network intracranial stimulation vary with theta phase
title_full_unstemmed Human hippocampal responses to network intracranial stimulation vary with theta phase
title_short Human hippocampal responses to network intracranial stimulation vary with theta phase
title_sort human hippocampal responses to network intracranial stimulation vary with theta phase
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9733942/
https://www.ncbi.nlm.nih.gov/pubmed/36453717
http://dx.doi.org/10.7554/eLife.78395
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