Cargando…

Neuroanatomical and cellular degeneration associated with a social disorder characterized by new ritualistic belief systems in a TDP-C patient vs. a Pick patient

Frontotemporal dementia (FTD) is a spectrum of clinically and pathologically heterogenous neurodegenerative dementias. Clinical and anatomical variants of FTD have been described and associated with underlying frontotemporal lobar degeneration (FTLD) pathology, including tauopathies (FTLD-tau) or TD...

Descripción completa

Detalles Bibliográficos
Autores principales: Ohm, Daniel T., Rhodes, Emma, Bahena, Alejandra, Capp, Noah, Lowe, MaKayla, Sabatini, Philip, Trotman, Winifred, Olm, Christopher A., Phillips, Jeffrey, Prabhakaran, Karthik, Rascovsky, Katya, Massimo, Lauren, McMillan, Corey, Gee, James, Tisdall, M. Dylan, Yushkevich, Paul A., Lee, Edward B., Grossman, Murray, Irwin, David J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10600461/
https://www.ncbi.nlm.nih.gov/pubmed/37900607
http://dx.doi.org/10.3389/fneur.2023.1245886
_version_ 1785125991348174848
author Ohm, Daniel T.
Rhodes, Emma
Bahena, Alejandra
Capp, Noah
Lowe, MaKayla
Sabatini, Philip
Trotman, Winifred
Olm, Christopher A.
Phillips, Jeffrey
Prabhakaran, Karthik
Rascovsky, Katya
Massimo, Lauren
McMillan, Corey
Gee, James
Tisdall, M. Dylan
Yushkevich, Paul A.
Lee, Edward B.
Grossman, Murray
Irwin, David J.
author_facet Ohm, Daniel T.
Rhodes, Emma
Bahena, Alejandra
Capp, Noah
Lowe, MaKayla
Sabatini, Philip
Trotman, Winifred
Olm, Christopher A.
Phillips, Jeffrey
Prabhakaran, Karthik
Rascovsky, Katya
Massimo, Lauren
McMillan, Corey
Gee, James
Tisdall, M. Dylan
Yushkevich, Paul A.
Lee, Edward B.
Grossman, Murray
Irwin, David J.
author_sort Ohm, Daniel T.
collection PubMed
description Frontotemporal dementia (FTD) is a spectrum of clinically and pathologically heterogenous neurodegenerative dementias. Clinical and anatomical variants of FTD have been described and associated with underlying frontotemporal lobar degeneration (FTLD) pathology, including tauopathies (FTLD-tau) or TDP-43 proteinopathies (FTLD-TDP). FTD patients with predominant degeneration of anterior temporal cortices often develop a language disorder of semantic knowledge loss and/or a social disorder often characterized by compulsive rituals and belief systems corresponding to predominant left or right hemisphere involvement, respectively. The neural substrates of these complex social disorders remain unclear. Here, we present a comparative imaging and postmortem study of two patients, one with FTLD-TDP (subtype C) and one with FTLD-tau (subtype Pick disease), who both developed new rigid belief systems. The FTLD-TDP patient developed a complex set of values centered on positivity and associated with specific physical and behavioral features of pigs, while the FTLD-tau patient developed compulsive, goal-directed behaviors related to general themes of positivity and spirituality. Neuroimaging showed left-predominant temporal atrophy in the FTLD-TDP patient and right-predominant frontotemporal atrophy in the FTLD-tau patient. Consistent with antemortem cortical atrophy, histopathologic examinations revealed severe loss of neurons and myelin predominantly in the anterior temporal lobes of both patients, but the FTLD-tau patient showed more bilateral, dorsolateral involvement featuring greater pathology and loss of projection neurons and deep white matter. These findings highlight that the regions within and connected to anterior temporal lobes may have differential vulnerability to distinct FTLD proteinopathies and serve important roles in human belief systems.
format Online
Article
Text
id pubmed-10600461
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-106004612023-10-27 Neuroanatomical and cellular degeneration associated with a social disorder characterized by new ritualistic belief systems in a TDP-C patient vs. a Pick patient Ohm, Daniel T. Rhodes, Emma Bahena, Alejandra Capp, Noah Lowe, MaKayla Sabatini, Philip Trotman, Winifred Olm, Christopher A. Phillips, Jeffrey Prabhakaran, Karthik Rascovsky, Katya Massimo, Lauren McMillan, Corey Gee, James Tisdall, M. Dylan Yushkevich, Paul A. Lee, Edward B. Grossman, Murray Irwin, David J. Front Neurol Neurology Frontotemporal dementia (FTD) is a spectrum of clinically and pathologically heterogenous neurodegenerative dementias. Clinical and anatomical variants of FTD have been described and associated with underlying frontotemporal lobar degeneration (FTLD) pathology, including tauopathies (FTLD-tau) or TDP-43 proteinopathies (FTLD-TDP). FTD patients with predominant degeneration of anterior temporal cortices often develop a language disorder of semantic knowledge loss and/or a social disorder often characterized by compulsive rituals and belief systems corresponding to predominant left or right hemisphere involvement, respectively. The neural substrates of these complex social disorders remain unclear. Here, we present a comparative imaging and postmortem study of two patients, one with FTLD-TDP (subtype C) and one with FTLD-tau (subtype Pick disease), who both developed new rigid belief systems. The FTLD-TDP patient developed a complex set of values centered on positivity and associated with specific physical and behavioral features of pigs, while the FTLD-tau patient developed compulsive, goal-directed behaviors related to general themes of positivity and spirituality. Neuroimaging showed left-predominant temporal atrophy in the FTLD-TDP patient and right-predominant frontotemporal atrophy in the FTLD-tau patient. Consistent with antemortem cortical atrophy, histopathologic examinations revealed severe loss of neurons and myelin predominantly in the anterior temporal lobes of both patients, but the FTLD-tau patient showed more bilateral, dorsolateral involvement featuring greater pathology and loss of projection neurons and deep white matter. These findings highlight that the regions within and connected to anterior temporal lobes may have differential vulnerability to distinct FTLD proteinopathies and serve important roles in human belief systems. Frontiers Media S.A. 2023-10-11 /pmc/articles/PMC10600461/ /pubmed/37900607 http://dx.doi.org/10.3389/fneur.2023.1245886 Text en Copyright © 2023 Ohm, Rhodes, Bahena, Capp, Lowe, Sabatini, Trotman, Olm, Phillips, Prabhakaran, Rascovsky, Massimo, McMillan, Gee, Tisdall, Yushkevich, Lee, Grossman and Irwin. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neurology
Ohm, Daniel T.
Rhodes, Emma
Bahena, Alejandra
Capp, Noah
Lowe, MaKayla
Sabatini, Philip
Trotman, Winifred
Olm, Christopher A.
Phillips, Jeffrey
Prabhakaran, Karthik
Rascovsky, Katya
Massimo, Lauren
McMillan, Corey
Gee, James
Tisdall, M. Dylan
Yushkevich, Paul A.
Lee, Edward B.
Grossman, Murray
Irwin, David J.
Neuroanatomical and cellular degeneration associated with a social disorder characterized by new ritualistic belief systems in a TDP-C patient vs. a Pick patient
title Neuroanatomical and cellular degeneration associated with a social disorder characterized by new ritualistic belief systems in a TDP-C patient vs. a Pick patient
title_full Neuroanatomical and cellular degeneration associated with a social disorder characterized by new ritualistic belief systems in a TDP-C patient vs. a Pick patient
title_fullStr Neuroanatomical and cellular degeneration associated with a social disorder characterized by new ritualistic belief systems in a TDP-C patient vs. a Pick patient
title_full_unstemmed Neuroanatomical and cellular degeneration associated with a social disorder characterized by new ritualistic belief systems in a TDP-C patient vs. a Pick patient
title_short Neuroanatomical and cellular degeneration associated with a social disorder characterized by new ritualistic belief systems in a TDP-C patient vs. a Pick patient
title_sort neuroanatomical and cellular degeneration associated with a social disorder characterized by new ritualistic belief systems in a tdp-c patient vs. a pick patient
topic Neurology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10600461/
https://www.ncbi.nlm.nih.gov/pubmed/37900607
http://dx.doi.org/10.3389/fneur.2023.1245886
work_keys_str_mv AT ohmdanielt neuroanatomicalandcellulardegenerationassociatedwithasocialdisordercharacterizedbynewritualisticbeliefsystemsinatdpcpatientvsapickpatient
AT rhodesemma neuroanatomicalandcellulardegenerationassociatedwithasocialdisordercharacterizedbynewritualisticbeliefsystemsinatdpcpatientvsapickpatient
AT bahenaalejandra neuroanatomicalandcellulardegenerationassociatedwithasocialdisordercharacterizedbynewritualisticbeliefsystemsinatdpcpatientvsapickpatient
AT cappnoah neuroanatomicalandcellulardegenerationassociatedwithasocialdisordercharacterizedbynewritualisticbeliefsystemsinatdpcpatientvsapickpatient
AT lowemakayla neuroanatomicalandcellulardegenerationassociatedwithasocialdisordercharacterizedbynewritualisticbeliefsystemsinatdpcpatientvsapickpatient
AT sabatiniphilip neuroanatomicalandcellulardegenerationassociatedwithasocialdisordercharacterizedbynewritualisticbeliefsystemsinatdpcpatientvsapickpatient
AT trotmanwinifred neuroanatomicalandcellulardegenerationassociatedwithasocialdisordercharacterizedbynewritualisticbeliefsystemsinatdpcpatientvsapickpatient
AT olmchristophera neuroanatomicalandcellulardegenerationassociatedwithasocialdisordercharacterizedbynewritualisticbeliefsystemsinatdpcpatientvsapickpatient
AT phillipsjeffrey neuroanatomicalandcellulardegenerationassociatedwithasocialdisordercharacterizedbynewritualisticbeliefsystemsinatdpcpatientvsapickpatient
AT prabhakarankarthik neuroanatomicalandcellulardegenerationassociatedwithasocialdisordercharacterizedbynewritualisticbeliefsystemsinatdpcpatientvsapickpatient
AT rascovskykatya neuroanatomicalandcellulardegenerationassociatedwithasocialdisordercharacterizedbynewritualisticbeliefsystemsinatdpcpatientvsapickpatient
AT massimolauren neuroanatomicalandcellulardegenerationassociatedwithasocialdisordercharacterizedbynewritualisticbeliefsystemsinatdpcpatientvsapickpatient
AT mcmillancorey neuroanatomicalandcellulardegenerationassociatedwithasocialdisordercharacterizedbynewritualisticbeliefsystemsinatdpcpatientvsapickpatient
AT geejames neuroanatomicalandcellulardegenerationassociatedwithasocialdisordercharacterizedbynewritualisticbeliefsystemsinatdpcpatientvsapickpatient
AT tisdallmdylan neuroanatomicalandcellulardegenerationassociatedwithasocialdisordercharacterizedbynewritualisticbeliefsystemsinatdpcpatientvsapickpatient
AT yushkevichpaula neuroanatomicalandcellulardegenerationassociatedwithasocialdisordercharacterizedbynewritualisticbeliefsystemsinatdpcpatientvsapickpatient
AT leeedwardb neuroanatomicalandcellulardegenerationassociatedwithasocialdisordercharacterizedbynewritualisticbeliefsystemsinatdpcpatientvsapickpatient
AT grossmanmurray neuroanatomicalandcellulardegenerationassociatedwithasocialdisordercharacterizedbynewritualisticbeliefsystemsinatdpcpatientvsapickpatient
AT irwindavidj neuroanatomicalandcellulardegenerationassociatedwithasocialdisordercharacterizedbynewritualisticbeliefsystemsinatdpcpatientvsapickpatient