Altered topology of the functional speech production network in non-fluent/agrammatic variant of PPA

Non-fluent/agrammatic primary progressive aphasia (nfvPPA) is caused by neuro-degeneration within the left fronto-insular speech and language production network (SPN). Graph theory is a branch of mathematics that studies network architecture (topology) by quantifying features based on its elements (...

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Autores: Mandelli, Maria Luisa, Welch, Ariane E., Vilaplana, Eduard, Watson, Christa, Battistella, Giovanni, Brown, Jesse A., Possin, Katherine L., Hubbard, Honey I., Miller, Zachary A., Henry, Maya L., Marx, Gabe A., Santos Santos, Miguel A., Bajorek, Lynn P., Fortea Ormaechea, Juan, Boxer, Adam, Rabinovici, Gil D., Lee, Suzee, Deleon, Jessica, Rosen, Howard J., Miller, Bruce L., Seeley, William W., Gorno Tempini, Maria Luisa
Tipo de recurso: artículo
Estado:Versión aceptada para publicación
Fecha de publicación:2018
País:España
Institución:Universidad de Barcelona
Repositorio:Dipòsit Digital de la UB
OAI Identifier:oai:diposit.ub.edu:2445/172121
Acceso en línea:https://hdl.handle.net/2445/172121
Access Level:acceso abierto
Palabra clave:Afàsia
Malalties neurodegeneratives
Aphasia
Neurodegenerative Diseases
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spelling Altered topology of the functional speech production network in non-fluent/agrammatic variant of PPAMandelli, Maria LuisaWelch, Ariane E.Vilaplana, EduardWatson, ChristaBattistella, GiovanniBrown, Jesse A.Possin, Katherine L.Hubbard, Honey I.Miller, Zachary A.Henry, Maya L.Marx, Gabe A.Santos Santos, Miguel A.Bajorek, Lynn P.Fortea Ormaechea, JuanBoxer, AdamRabinovici, Gil D.Lee, SuzeeDeleon, JessicaRosen, Howard J.Miller, Bruce L.Seeley, William W.Gorno Tempini, Maria LuisaAfàsiaMalalties neurodegenerativesAphasiaNeurodegenerative DiseasesNon-fluent/agrammatic primary progressive aphasia (nfvPPA) is caused by neuro-degeneration within the left fronto-insular speech and language production network (SPN). Graph theory is a branch of mathematics that studies network architecture (topology) by quantifying features based on its elements (nodes and connections). This approach has been recently applied to neuroimaging data to explore the complex architecture of the brain connectome, though few studies have exploited this technique in PPA. Here, we used graph theory on functional MRI resting state data from a group of 20 nfvPPA patients and 20 matched controls to investigate topological changes in response to focal neuro-degeneration. We hypothesized that changes in the network architecture would be specific to the affected SPN in nfvPPA, while preserved in the spared default mode network (DMN). Topological configuration was quantified by hub location and global network metrics. Our findings showed a less efficiently wired and less optimally clustered SPN, while no changes were detected in the DMN. The SPN in the nfvPPA group showed a loss of hubs in the left fronto-parietal-temporal area and new critical nodes in the anterior left inferior-frontal and right frontal regions. Behaviorally, speech production score and rule violation errors correlated with the strength of functional connectivity of the left (lost) and right (new) regions respectively. This study shows that focal neurodegeneration within the SPN in nfvPPA is associated with network-specific topological alterations, with the loss and gain of crucial hubs and decreased global efficiency that were better accounted for through functional rather than structural changes. These findings support the hypothesis of selective network vulnerability in nfvPPA and may offer biomarkers for future behavioral intervention.Elsevier Masson2018info:eu-repo/semantics/articleinfo:eu-repo/semantics/acceptedVersionapplication/pdfhttps://hdl.handle.net/2445/172121Articles publicats en revistes (Institut d'lnvestigació Biomèdica de Bellvitge (IDIBELL))reponame:Dipòsit Digital de la UBinstname:Universidad de BarcelonaInglésVersió postprint del document publicat a: https://doi.org/10.1016/j.cortex.2018.08.002Cortex, 2018, vol. 108, p. 252-264https://doi.org/10.1016/j.cortex.2018.08.002(c) Elsevier Ltd., 2018info:eu-repo/semantics/openAccessoai:diposit.ub.edu:2445/1721212026-05-27T06:46:51Z
dc.title.none.fl_str_mv Altered topology of the functional speech production network in non-fluent/agrammatic variant of PPA
title Altered topology of the functional speech production network in non-fluent/agrammatic variant of PPA
spellingShingle Altered topology of the functional speech production network in non-fluent/agrammatic variant of PPA
Mandelli, Maria Luisa
Afàsia
Malalties neurodegeneratives
Aphasia
Neurodegenerative Diseases
title_short Altered topology of the functional speech production network in non-fluent/agrammatic variant of PPA
title_full Altered topology of the functional speech production network in non-fluent/agrammatic variant of PPA
title_fullStr Altered topology of the functional speech production network in non-fluent/agrammatic variant of PPA
title_full_unstemmed Altered topology of the functional speech production network in non-fluent/agrammatic variant of PPA
title_sort Altered topology of the functional speech production network in non-fluent/agrammatic variant of PPA
dc.creator.none.fl_str_mv Mandelli, Maria Luisa
Welch, Ariane E.
Vilaplana, Eduard
Watson, Christa
Battistella, Giovanni
Brown, Jesse A.
Possin, Katherine L.
Hubbard, Honey I.
Miller, Zachary A.
Henry, Maya L.
Marx, Gabe A.
Santos Santos, Miguel A.
Bajorek, Lynn P.
Fortea Ormaechea, Juan
Boxer, Adam
Rabinovici, Gil D.
Lee, Suzee
Deleon, Jessica
Rosen, Howard J.
Miller, Bruce L.
Seeley, William W.
Gorno Tempini, Maria Luisa
author Mandelli, Maria Luisa
author_facet Mandelli, Maria Luisa
Welch, Ariane E.
Vilaplana, Eduard
Watson, Christa
Battistella, Giovanni
Brown, Jesse A.
Possin, Katherine L.
Hubbard, Honey I.
Miller, Zachary A.
Henry, Maya L.
Marx, Gabe A.
Santos Santos, Miguel A.
Bajorek, Lynn P.
Fortea Ormaechea, Juan
Boxer, Adam
Rabinovici, Gil D.
Lee, Suzee
Deleon, Jessica
Rosen, Howard J.
Miller, Bruce L.
Seeley, William W.
Gorno Tempini, Maria Luisa
author_role author
author2 Welch, Ariane E.
Vilaplana, Eduard
Watson, Christa
Battistella, Giovanni
Brown, Jesse A.
Possin, Katherine L.
Hubbard, Honey I.
Miller, Zachary A.
Henry, Maya L.
Marx, Gabe A.
Santos Santos, Miguel A.
Bajorek, Lynn P.
Fortea Ormaechea, Juan
Boxer, Adam
Rabinovici, Gil D.
Lee, Suzee
Deleon, Jessica
Rosen, Howard J.
Miller, Bruce L.
Seeley, William W.
Gorno Tempini, Maria Luisa
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Afàsia
Malalties neurodegeneratives
Aphasia
Neurodegenerative Diseases
topic Afàsia
Malalties neurodegeneratives
Aphasia
Neurodegenerative Diseases
description Non-fluent/agrammatic primary progressive aphasia (nfvPPA) is caused by neuro-degeneration within the left fronto-insular speech and language production network (SPN). Graph theory is a branch of mathematics that studies network architecture (topology) by quantifying features based on its elements (nodes and connections). This approach has been recently applied to neuroimaging data to explore the complex architecture of the brain connectome, though few studies have exploited this technique in PPA. Here, we used graph theory on functional MRI resting state data from a group of 20 nfvPPA patients and 20 matched controls to investigate topological changes in response to focal neuro-degeneration. We hypothesized that changes in the network architecture would be specific to the affected SPN in nfvPPA, while preserved in the spared default mode network (DMN). Topological configuration was quantified by hub location and global network metrics. Our findings showed a less efficiently wired and less optimally clustered SPN, while no changes were detected in the DMN. The SPN in the nfvPPA group showed a loss of hubs in the left fronto-parietal-temporal area and new critical nodes in the anterior left inferior-frontal and right frontal regions. Behaviorally, speech production score and rule violation errors correlated with the strength of functional connectivity of the left (lost) and right (new) regions respectively. This study shows that focal neurodegeneration within the SPN in nfvPPA is associated with network-specific topological alterations, with the loss and gain of crucial hubs and decreased global efficiency that were better accounted for through functional rather than structural changes. These findings support the hypothesis of selective network vulnerability in nfvPPA and may offer biomarkers for future behavioral intervention.
publishDate 2018
dc.date.none.fl_str_mv 2018
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/acceptedVersion
format article
status_str acceptedVersion
dc.identifier.none.fl_str_mv https://hdl.handle.net/2445/172121
url https://hdl.handle.net/2445/172121
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Versió postprint del document publicat a: https://doi.org/10.1016/j.cortex.2018.08.002
Cortex, 2018, vol. 108, p. 252-264
https://doi.org/10.1016/j.cortex.2018.08.002
dc.rights.none.fl_str_mv (c) Elsevier Ltd., 2018
info:eu-repo/semantics/openAccess
rights_invalid_str_mv (c) Elsevier Ltd., 2018
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Elsevier Masson
publisher.none.fl_str_mv Elsevier Masson
dc.source.none.fl_str_mv Articles publicats en revistes (Institut d'lnvestigació Biomèdica de Bellvitge (IDIBELL))
reponame:Dipòsit Digital de la UB
instname:Universidad de Barcelona
instname_str Universidad de Barcelona
reponame_str Dipòsit Digital de la UB
collection Dipòsit Digital de la UB
repository.name.fl_str_mv
repository.mail.fl_str_mv
_version_ 1869420105850421248
score 15,300719

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