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A category-selective semantic memory deficit for animate objects in semantic variant primary progressive aphasia

Data are mixed on whether patients with semantic variant primary progressive aphasia exhibit a category-selective semantic deficit for animate objects. Moreover, there is little consensus regarding the neural substrates of this category-selective semantic deficit, though prior literature has suggest...

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Autores principales: Henderson, Shalom K, Dev, Sheena I, Ezzo, Rania, Quimby, Megan, Wong, Bonnie, Brickhouse, Michael, Hochberg, Daisy, Touroutoglou, Alexandra, Dickerson, Bradford C, Cordella, Claire, Collins, Jessica A
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8493104/
https://www.ncbi.nlm.nih.gov/pubmed/34622208
http://dx.doi.org/10.1093/braincomms/fcab210
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author Henderson, Shalom K
Dev, Sheena I
Ezzo, Rania
Quimby, Megan
Wong, Bonnie
Brickhouse, Michael
Hochberg, Daisy
Touroutoglou, Alexandra
Dickerson, Bradford C
Cordella, Claire
Collins, Jessica A
author_facet Henderson, Shalom K
Dev, Sheena I
Ezzo, Rania
Quimby, Megan
Wong, Bonnie
Brickhouse, Michael
Hochberg, Daisy
Touroutoglou, Alexandra
Dickerson, Bradford C
Cordella, Claire
Collins, Jessica A
author_sort Henderson, Shalom K
collection PubMed
description Data are mixed on whether patients with semantic variant primary progressive aphasia exhibit a category-selective semantic deficit for animate objects. Moreover, there is little consensus regarding the neural substrates of this category-selective semantic deficit, though prior literature has suggested that the perirhinal cortex and the lateral posterior fusiform gyrus may support semantic memory functions important for processing animate objects. In this study, we investigated whether patients with semantic variant primary progressive aphasia exhibited a category-selective semantic deficit for animate objects in a word-picture matching task, controlling for psycholinguistic features of the stimuli, including frequency, familiarity, typicality and age of acquisition. We investigated the neural bases of this category selectivity by examining its relationship with cortical atrophy in two primary regions of interest: bilateral perirhinal cortex and lateral posterior fusiform gyri. We analysed data from 20 patients with semantic variant primary progressive aphasia (mean age = 64 years, S.D. = 6.94). For each participant, we calculated an animacy index score to denote the magnitude of the category-selective semantic deficit for animate objects. Multivariate regression analysis revealed a main effect of animacy (β = 0.52, t = 4.03, P < 0.001) even after including all psycholinguistic variables in the model, such that animate objects were less likely to be identified correctly relative to inanimate objects. Inspection of each individual patient’s data indicated the presence of a disproportionate impairment in animate objects in most patients. A linear regression analysis revealed a relationship between the right perirhinal cortex thickness and animacy index scores (β = −0.57, t = −2.74, P = 0.015) such that patients who were more disproportionally impaired for animate relative to inanimate objects exhibited thinner right perirhinal cortex. A vertex-wise general linear model analysis restricted to the temporal lobes revealed additional associations between positive animacy index scores (i.e. a disproportionately poorer performance on animate objects) and cortical atrophy in the right perirhinal and entorhinal cortex, superior, middle, and inferior temporal gyri, and the anterior fusiform gyrus, as well as the left anterior fusiform gyrus. Taken together, our results indicate that a category-selective semantic deficit for animate objects is a characteristic feature of semantic variant primary progressive aphasia that is detectable in most individuals. Our imaging findings provide further support for the role of the right perirhinal cortex and other temporal lobe regions in the semantic processing of animate objects.
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spelling pubmed-84931042021-10-06 A category-selective semantic memory deficit for animate objects in semantic variant primary progressive aphasia Henderson, Shalom K Dev, Sheena I Ezzo, Rania Quimby, Megan Wong, Bonnie Brickhouse, Michael Hochberg, Daisy Touroutoglou, Alexandra Dickerson, Bradford C Cordella, Claire Collins, Jessica A Brain Commun Original Article Data are mixed on whether patients with semantic variant primary progressive aphasia exhibit a category-selective semantic deficit for animate objects. Moreover, there is little consensus regarding the neural substrates of this category-selective semantic deficit, though prior literature has suggested that the perirhinal cortex and the lateral posterior fusiform gyrus may support semantic memory functions important for processing animate objects. In this study, we investigated whether patients with semantic variant primary progressive aphasia exhibited a category-selective semantic deficit for animate objects in a word-picture matching task, controlling for psycholinguistic features of the stimuli, including frequency, familiarity, typicality and age of acquisition. We investigated the neural bases of this category selectivity by examining its relationship with cortical atrophy in two primary regions of interest: bilateral perirhinal cortex and lateral posterior fusiform gyri. We analysed data from 20 patients with semantic variant primary progressive aphasia (mean age = 64 years, S.D. = 6.94). For each participant, we calculated an animacy index score to denote the magnitude of the category-selective semantic deficit for animate objects. Multivariate regression analysis revealed a main effect of animacy (β = 0.52, t = 4.03, P < 0.001) even after including all psycholinguistic variables in the model, such that animate objects were less likely to be identified correctly relative to inanimate objects. Inspection of each individual patient’s data indicated the presence of a disproportionate impairment in animate objects in most patients. A linear regression analysis revealed a relationship between the right perirhinal cortex thickness and animacy index scores (β = −0.57, t = −2.74, P = 0.015) such that patients who were more disproportionally impaired for animate relative to inanimate objects exhibited thinner right perirhinal cortex. A vertex-wise general linear model analysis restricted to the temporal lobes revealed additional associations between positive animacy index scores (i.e. a disproportionately poorer performance on animate objects) and cortical atrophy in the right perirhinal and entorhinal cortex, superior, middle, and inferior temporal gyri, and the anterior fusiform gyrus, as well as the left anterior fusiform gyrus. Taken together, our results indicate that a category-selective semantic deficit for animate objects is a characteristic feature of semantic variant primary progressive aphasia that is detectable in most individuals. Our imaging findings provide further support for the role of the right perirhinal cortex and other temporal lobe regions in the semantic processing of animate objects. Oxford University Press 2021-09-14 /pmc/articles/PMC8493104/ /pubmed/34622208 http://dx.doi.org/10.1093/braincomms/fcab210 Text en © The Author(s) (2021). Published by Oxford University Press on behalf of the Guarantors of Brain. https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Original Article
Henderson, Shalom K
Dev, Sheena I
Ezzo, Rania
Quimby, Megan
Wong, Bonnie
Brickhouse, Michael
Hochberg, Daisy
Touroutoglou, Alexandra
Dickerson, Bradford C
Cordella, Claire
Collins, Jessica A
A category-selective semantic memory deficit for animate objects in semantic variant primary progressive aphasia
title A category-selective semantic memory deficit for animate objects in semantic variant primary progressive aphasia
title_full A category-selective semantic memory deficit for animate objects in semantic variant primary progressive aphasia
title_fullStr A category-selective semantic memory deficit for animate objects in semantic variant primary progressive aphasia
title_full_unstemmed A category-selective semantic memory deficit for animate objects in semantic variant primary progressive aphasia
title_short A category-selective semantic memory deficit for animate objects in semantic variant primary progressive aphasia
title_sort category-selective semantic memory deficit for animate objects in semantic variant primary progressive aphasia
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8493104/
https://www.ncbi.nlm.nih.gov/pubmed/34622208
http://dx.doi.org/10.1093/braincomms/fcab210
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