Cargando…

The Brain Network of Naming: A Lesson from Primary Progressive Aphasia

OBJECTIVE: Word finding depends on the processing of semantic and lexical information, and it involves an intermediate level for mapping semantic-to-lexical information which also subserves lexical-to-semantic mapping during word comprehension. However, the brain regions implementing these component...

Descripción completa

Detalles Bibliográficos
Autores principales: Migliaccio, Raffaella, Boutet, Claire, Valabregue, Romain, Ferrieux, Sophie, Nogues, Marie, Lehéricy, Stéphane, Dormont, Didier, Levy, Richard, Dubois, Bruno, Teichmann, Marc
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4764674/
https://www.ncbi.nlm.nih.gov/pubmed/26901052
http://dx.doi.org/10.1371/journal.pone.0148707
_version_ 1782417413269094400
author Migliaccio, Raffaella
Boutet, Claire
Valabregue, Romain
Ferrieux, Sophie
Nogues, Marie
Lehéricy, Stéphane
Dormont, Didier
Levy, Richard
Dubois, Bruno
Teichmann, Marc
author_facet Migliaccio, Raffaella
Boutet, Claire
Valabregue, Romain
Ferrieux, Sophie
Nogues, Marie
Lehéricy, Stéphane
Dormont, Didier
Levy, Richard
Dubois, Bruno
Teichmann, Marc
author_sort Migliaccio, Raffaella
collection PubMed
description OBJECTIVE: Word finding depends on the processing of semantic and lexical information, and it involves an intermediate level for mapping semantic-to-lexical information which also subserves lexical-to-semantic mapping during word comprehension. However, the brain regions implementing these components are still controversial and have not been clarified via a comprehensive lesion model encompassing the whole range of language-related cortices. Primary progressive aphasia (PPA), for which anomia is thought to be the most common sign, provides such a model, but the exploration of cortical areas impacting naming in its three main variants and the underlying processing mechanisms is still lacking. METHODS: We addressed this double issue, related to language structure and PPA, with thirty patients (11 semantic, 12 logopenic, 7 agrammatic variant) using a picture-naming task and voxel-based morphometry for anatomo-functional correlation. First, we analyzed correlations for each of the three variants to identify the regions impacting naming in PPA and to disentangle the core regions of word finding. We then combined the three variants and correlation analyses for naming (semantic-to-lexical mapping) and single-word comprehension (lexical-to-semantic mapping), predicting an overlap zone corresponding to a bidirectional lexical-semantic hub. RESULTS AND CONCLUSIONS: Our results showed that superior portions of the left temporal pole and left posterior temporal cortices impact semantic and lexical naming mechanisms in semantic and logopenic PPA, respectively. In agrammatic PPA naming deficits were rare, and did not correlate with any cortical region. Combined analyses revealed a cortical overlap zone in superior/middle mid-temporal cortices, distinct from the two former regions, impacting bidirectional binding of lexical and semantic information. Altogether, our findings indicate that lexical/semantic word processing depends on an anterior-posterior axis within lateral-temporal cortices, including an anatomically intermediate hub dedicated to lexical-semantic integration. Within this axis our data reveal the underpinnings of anomia in the PPA variants, which is of relevance for both diagnosis and future therapy strategies.
format Online
Article
Text
id pubmed-4764674
institution National Center for Biotechnology Information
language English
publishDate 2016
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-47646742016-03-07 The Brain Network of Naming: A Lesson from Primary Progressive Aphasia Migliaccio, Raffaella Boutet, Claire Valabregue, Romain Ferrieux, Sophie Nogues, Marie Lehéricy, Stéphane Dormont, Didier Levy, Richard Dubois, Bruno Teichmann, Marc PLoS One Research Article OBJECTIVE: Word finding depends on the processing of semantic and lexical information, and it involves an intermediate level for mapping semantic-to-lexical information which also subserves lexical-to-semantic mapping during word comprehension. However, the brain regions implementing these components are still controversial and have not been clarified via a comprehensive lesion model encompassing the whole range of language-related cortices. Primary progressive aphasia (PPA), for which anomia is thought to be the most common sign, provides such a model, but the exploration of cortical areas impacting naming in its three main variants and the underlying processing mechanisms is still lacking. METHODS: We addressed this double issue, related to language structure and PPA, with thirty patients (11 semantic, 12 logopenic, 7 agrammatic variant) using a picture-naming task and voxel-based morphometry for anatomo-functional correlation. First, we analyzed correlations for each of the three variants to identify the regions impacting naming in PPA and to disentangle the core regions of word finding. We then combined the three variants and correlation analyses for naming (semantic-to-lexical mapping) and single-word comprehension (lexical-to-semantic mapping), predicting an overlap zone corresponding to a bidirectional lexical-semantic hub. RESULTS AND CONCLUSIONS: Our results showed that superior portions of the left temporal pole and left posterior temporal cortices impact semantic and lexical naming mechanisms in semantic and logopenic PPA, respectively. In agrammatic PPA naming deficits were rare, and did not correlate with any cortical region. Combined analyses revealed a cortical overlap zone in superior/middle mid-temporal cortices, distinct from the two former regions, impacting bidirectional binding of lexical and semantic information. Altogether, our findings indicate that lexical/semantic word processing depends on an anterior-posterior axis within lateral-temporal cortices, including an anatomically intermediate hub dedicated to lexical-semantic integration. Within this axis our data reveal the underpinnings of anomia in the PPA variants, which is of relevance for both diagnosis and future therapy strategies. Public Library of Science 2016-02-22 /pmc/articles/PMC4764674/ /pubmed/26901052 http://dx.doi.org/10.1371/journal.pone.0148707 Text en © 2016 Migliaccio 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 (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Migliaccio, Raffaella
Boutet, Claire
Valabregue, Romain
Ferrieux, Sophie
Nogues, Marie
Lehéricy, Stéphane
Dormont, Didier
Levy, Richard
Dubois, Bruno
Teichmann, Marc
The Brain Network of Naming: A Lesson from Primary Progressive Aphasia
title The Brain Network of Naming: A Lesson from Primary Progressive Aphasia
title_full The Brain Network of Naming: A Lesson from Primary Progressive Aphasia
title_fullStr The Brain Network of Naming: A Lesson from Primary Progressive Aphasia
title_full_unstemmed The Brain Network of Naming: A Lesson from Primary Progressive Aphasia
title_short The Brain Network of Naming: A Lesson from Primary Progressive Aphasia
title_sort brain network of naming: a lesson from primary progressive aphasia
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4764674/
https://www.ncbi.nlm.nih.gov/pubmed/26901052
http://dx.doi.org/10.1371/journal.pone.0148707
work_keys_str_mv AT migliaccioraffaella thebrainnetworkofnamingalessonfromprimaryprogressiveaphasia
AT boutetclaire thebrainnetworkofnamingalessonfromprimaryprogressiveaphasia
AT valabregueromain thebrainnetworkofnamingalessonfromprimaryprogressiveaphasia
AT ferrieuxsophie thebrainnetworkofnamingalessonfromprimaryprogressiveaphasia
AT noguesmarie thebrainnetworkofnamingalessonfromprimaryprogressiveaphasia
AT lehericystephane thebrainnetworkofnamingalessonfromprimaryprogressiveaphasia
AT dormontdidier thebrainnetworkofnamingalessonfromprimaryprogressiveaphasia
AT levyrichard thebrainnetworkofnamingalessonfromprimaryprogressiveaphasia
AT duboisbruno thebrainnetworkofnamingalessonfromprimaryprogressiveaphasia
AT teichmannmarc thebrainnetworkofnamingalessonfromprimaryprogressiveaphasia
AT migliaccioraffaella brainnetworkofnamingalessonfromprimaryprogressiveaphasia
AT boutetclaire brainnetworkofnamingalessonfromprimaryprogressiveaphasia
AT valabregueromain brainnetworkofnamingalessonfromprimaryprogressiveaphasia
AT ferrieuxsophie brainnetworkofnamingalessonfromprimaryprogressiveaphasia
AT noguesmarie brainnetworkofnamingalessonfromprimaryprogressiveaphasia
AT lehericystephane brainnetworkofnamingalessonfromprimaryprogressiveaphasia
AT dormontdidier brainnetworkofnamingalessonfromprimaryprogressiveaphasia
AT levyrichard brainnetworkofnamingalessonfromprimaryprogressiveaphasia
AT duboisbruno brainnetworkofnamingalessonfromprimaryprogressiveaphasia
AT teichmannmarc brainnetworkofnamingalessonfromprimaryprogressiveaphasia