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Evidence supporting a time-limited hippocampal role in retrieving autobiographical memories

The necessity of the human hippocampus for remote autobiographical recall remains fiercely debated. The standard model of consolidation predicts a time-limited role for the hippocampus, but the competing multiple trace/trace transformation theories posit indefinite involvement. Lesion evidence remai...

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Autores principales: Gilmore, Adrian W., Quach, Alina, Kalinowski, Sarah E., González-Araya, Estefanía I., Gotts, Stephen J., Schacter, Daniel L., Martin, Alex
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8000197/
https://www.ncbi.nlm.nih.gov/pubmed/33723070
http://dx.doi.org/10.1073/pnas.2023069118
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author Gilmore, Adrian W.
Quach, Alina
Kalinowski, Sarah E.
González-Araya, Estefanía I.
Gotts, Stephen J.
Schacter, Daniel L.
Martin, Alex
author_facet Gilmore, Adrian W.
Quach, Alina
Kalinowski, Sarah E.
González-Araya, Estefanía I.
Gotts, Stephen J.
Schacter, Daniel L.
Martin, Alex
author_sort Gilmore, Adrian W.
collection PubMed
description The necessity of the human hippocampus for remote autobiographical recall remains fiercely debated. The standard model of consolidation predicts a time-limited role for the hippocampus, but the competing multiple trace/trace transformation theories posit indefinite involvement. Lesion evidence remains inconclusive, and the inferences one can draw from functional MRI (fMRI) have been limited by reliance on covert (silent) recall, which obscures dynamic, moment-to-moment content of retrieved memories. Here, we capitalized on advances in fMRI denoising to employ overtly spoken recall. Forty participants retrieved recent and remote memories, describing each for approximately 2 min. Details associated with each memory were identified and modeled in the fMRI time-series data using a variant of the Autobiographical Interview procedure, and activity associated with the recall of recent and remote memories was then compared. Posterior hippocampal regions exhibited temporally graded activity patterns (recent events > remote events), as did several regions of frontal and parietal cortex. Consistent with predictions of the standard model, recall-related hippocampal activity differed from a non-autobiographical control task only for recent, and not remote, events. Task-based connectivity between posterior hippocampal regions and others associated with mental scene construction also exhibited a temporal gradient, with greater connectivity accompanying the recall of recent events. These findings support predictions of the standard model of consolidation and demonstrate the potential benefits of overt recall in neuroimaging experiments.
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spelling pubmed-80001972021-04-01 Evidence supporting a time-limited hippocampal role in retrieving autobiographical memories Gilmore, Adrian W. Quach, Alina Kalinowski, Sarah E. González-Araya, Estefanía I. Gotts, Stephen J. Schacter, Daniel L. Martin, Alex Proc Natl Acad Sci U S A Biological Sciences The necessity of the human hippocampus for remote autobiographical recall remains fiercely debated. The standard model of consolidation predicts a time-limited role for the hippocampus, but the competing multiple trace/trace transformation theories posit indefinite involvement. Lesion evidence remains inconclusive, and the inferences one can draw from functional MRI (fMRI) have been limited by reliance on covert (silent) recall, which obscures dynamic, moment-to-moment content of retrieved memories. Here, we capitalized on advances in fMRI denoising to employ overtly spoken recall. Forty participants retrieved recent and remote memories, describing each for approximately 2 min. Details associated with each memory were identified and modeled in the fMRI time-series data using a variant of the Autobiographical Interview procedure, and activity associated with the recall of recent and remote memories was then compared. Posterior hippocampal regions exhibited temporally graded activity patterns (recent events > remote events), as did several regions of frontal and parietal cortex. Consistent with predictions of the standard model, recall-related hippocampal activity differed from a non-autobiographical control task only for recent, and not remote, events. Task-based connectivity between posterior hippocampal regions and others associated with mental scene construction also exhibited a temporal gradient, with greater connectivity accompanying the recall of recent events. These findings support predictions of the standard model of consolidation and demonstrate the potential benefits of overt recall in neuroimaging experiments. National Academy of Sciences 2021-03-23 2021-03-15 /pmc/articles/PMC8000197/ /pubmed/33723070 http://dx.doi.org/10.1073/pnas.2023069118 Text en Copyright © 2021 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Gilmore, Adrian W.
Quach, Alina
Kalinowski, Sarah E.
González-Araya, Estefanía I.
Gotts, Stephen J.
Schacter, Daniel L.
Martin, Alex
Evidence supporting a time-limited hippocampal role in retrieving autobiographical memories
title Evidence supporting a time-limited hippocampal role in retrieving autobiographical memories
title_full Evidence supporting a time-limited hippocampal role in retrieving autobiographical memories
title_fullStr Evidence supporting a time-limited hippocampal role in retrieving autobiographical memories
title_full_unstemmed Evidence supporting a time-limited hippocampal role in retrieving autobiographical memories
title_short Evidence supporting a time-limited hippocampal role in retrieving autobiographical memories
title_sort evidence supporting a time-limited hippocampal role in retrieving autobiographical memories
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8000197/
https://www.ncbi.nlm.nih.gov/pubmed/33723070
http://dx.doi.org/10.1073/pnas.2023069118
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