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Age-Related Changes in the Functional Network Underlying Specific and General Autobiographical Memory Retrieval: A Pivotal Role for the Anterior Cingulate Cortex

Age-related changes in autobiographical memory (AM) recall are characterized by a decline in episodic details, while semantic aspects are spared. This deleterious effect is supposed to be mediated by an inefficient recruitment of executive processes during AM retrieval. To date, contrasting evidence...

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Autores principales: Martinelli, Pénélope, Sperduti, Marco, Devauchelle, Anne-Dominique, Kalenzaga, Sandrine, Gallarda, Thierry, Lion, Stéphanie, Delhommeau, Marion, Anssens, Adèle, Amado, Isabelle, Meder, Jean François, Krebs, Marie-Odile, Oppenheim, Catherine, Piolino, Pascale
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3867357/
https://www.ncbi.nlm.nih.gov/pubmed/24367516
http://dx.doi.org/10.1371/journal.pone.0082385
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author Martinelli, Pénélope
Sperduti, Marco
Devauchelle, Anne-Dominique
Kalenzaga, Sandrine
Gallarda, Thierry
Lion, Stéphanie
Delhommeau, Marion
Anssens, Adèle
Amado, Isabelle
Meder, Jean François
Krebs, Marie-Odile
Oppenheim, Catherine
Piolino, Pascale
author_facet Martinelli, Pénélope
Sperduti, Marco
Devauchelle, Anne-Dominique
Kalenzaga, Sandrine
Gallarda, Thierry
Lion, Stéphanie
Delhommeau, Marion
Anssens, Adèle
Amado, Isabelle
Meder, Jean François
Krebs, Marie-Odile
Oppenheim, Catherine
Piolino, Pascale
author_sort Martinelli, Pénélope
collection PubMed
description Age-related changes in autobiographical memory (AM) recall are characterized by a decline in episodic details, while semantic aspects are spared. This deleterious effect is supposed to be mediated by an inefficient recruitment of executive processes during AM retrieval. To date, contrasting evidence has been reported on the neural underpinning of this decline, and none of the previous studies has directly compared the episodic and semantic aspects of AM in elderly. We asked 20 young and 17 older participants to recall specific and general autobiographical events (i.e., episodic and semantic AM) elicited by personalized cues while recording their brain activity by means of fMRI. At the behavioral level, we confirmed that the richness of episodic AM retrieval is specifically impoverished in aging and that this decline is related to the reduction of executive functions. At the neural level, in both age groups, we showed the recruitment of a large network during episodic AM retrieval encompassing prefrontal, cortical midline and posterior regions, and medial temporal structures, including the hippocampus. This network was very similar, but less extended, during semantic AM retrieval. Nevertheless, a greater activity was evidenced in the dorsal anterior cingulate cortex (dACC) during episodic, compared to semantic AM retrieval in young participants, and a reversed pattern in the elderly. Moreover, activity in dACC during episodic AM retrieval was correlated with inhibition and richness of memories in both groups. Our findings shed light on the direct link between episodic AM retrieval, executive control, and their decline in aging, proposing a possible neuronal signature. They also suggest that increased activity in dACC during semantic AM retrieval in the elderly could be seen as a compensatory mechanism underpinning successful AM performance observed in aging. These results are discussed in the framework of recently proposed models of neural reorganization in aging.
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spelling pubmed-38673572013-12-23 Age-Related Changes in the Functional Network Underlying Specific and General Autobiographical Memory Retrieval: A Pivotal Role for the Anterior Cingulate Cortex Martinelli, Pénélope Sperduti, Marco Devauchelle, Anne-Dominique Kalenzaga, Sandrine Gallarda, Thierry Lion, Stéphanie Delhommeau, Marion Anssens, Adèle Amado, Isabelle Meder, Jean François Krebs, Marie-Odile Oppenheim, Catherine Piolino, Pascale PLoS One Research Article Age-related changes in autobiographical memory (AM) recall are characterized by a decline in episodic details, while semantic aspects are spared. This deleterious effect is supposed to be mediated by an inefficient recruitment of executive processes during AM retrieval. To date, contrasting evidence has been reported on the neural underpinning of this decline, and none of the previous studies has directly compared the episodic and semantic aspects of AM in elderly. We asked 20 young and 17 older participants to recall specific and general autobiographical events (i.e., episodic and semantic AM) elicited by personalized cues while recording their brain activity by means of fMRI. At the behavioral level, we confirmed that the richness of episodic AM retrieval is specifically impoverished in aging and that this decline is related to the reduction of executive functions. At the neural level, in both age groups, we showed the recruitment of a large network during episodic AM retrieval encompassing prefrontal, cortical midline and posterior regions, and medial temporal structures, including the hippocampus. This network was very similar, but less extended, during semantic AM retrieval. Nevertheless, a greater activity was evidenced in the dorsal anterior cingulate cortex (dACC) during episodic, compared to semantic AM retrieval in young participants, and a reversed pattern in the elderly. Moreover, activity in dACC during episodic AM retrieval was correlated with inhibition and richness of memories in both groups. Our findings shed light on the direct link between episodic AM retrieval, executive control, and their decline in aging, proposing a possible neuronal signature. They also suggest that increased activity in dACC during semantic AM retrieval in the elderly could be seen as a compensatory mechanism underpinning successful AM performance observed in aging. These results are discussed in the framework of recently proposed models of neural reorganization in aging. Public Library of Science 2013-12-18 /pmc/articles/PMC3867357/ /pubmed/24367516 http://dx.doi.org/10.1371/journal.pone.0082385 Text en © 2013 Martinelli et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Martinelli, Pénélope
Sperduti, Marco
Devauchelle, Anne-Dominique
Kalenzaga, Sandrine
Gallarda, Thierry
Lion, Stéphanie
Delhommeau, Marion
Anssens, Adèle
Amado, Isabelle
Meder, Jean François
Krebs, Marie-Odile
Oppenheim, Catherine
Piolino, Pascale
Age-Related Changes in the Functional Network Underlying Specific and General Autobiographical Memory Retrieval: A Pivotal Role for the Anterior Cingulate Cortex
title Age-Related Changes in the Functional Network Underlying Specific and General Autobiographical Memory Retrieval: A Pivotal Role for the Anterior Cingulate Cortex
title_full Age-Related Changes in the Functional Network Underlying Specific and General Autobiographical Memory Retrieval: A Pivotal Role for the Anterior Cingulate Cortex
title_fullStr Age-Related Changes in the Functional Network Underlying Specific and General Autobiographical Memory Retrieval: A Pivotal Role for the Anterior Cingulate Cortex
title_full_unstemmed Age-Related Changes in the Functional Network Underlying Specific and General Autobiographical Memory Retrieval: A Pivotal Role for the Anterior Cingulate Cortex
title_short Age-Related Changes in the Functional Network Underlying Specific and General Autobiographical Memory Retrieval: A Pivotal Role for the Anterior Cingulate Cortex
title_sort age-related changes in the functional network underlying specific and general autobiographical memory retrieval: a pivotal role for the anterior cingulate cortex
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3867357/
https://www.ncbi.nlm.nih.gov/pubmed/24367516
http://dx.doi.org/10.1371/journal.pone.0082385
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