Neural dynamics of semantic categorization in semantic variant of Primary Progressive Aphasia
- University of California, San Francisco, United States
Abstract
Semantic representations are processed along a posterior-to-anterior gradient reflecting a shift from perceptual (e.g., it has eight legs) to conceptual (e.g., venomous spiders are rare) information. One critical region is the anterior temporal lobe (ATL): patients with semantic variant primary progressive aphasia (svPPA), a clinical syndrome associated with ATL neurodegeneration, manifest a deep loss of semantic knowledge. We test the hypothesis that svPPA patients perform semantic tasks by over-recruiting areas implicated in perceptual processing. We compared MEG recordings of svPPA patients and healthy controls during a categorization task. While behavioral performance did not differ, svPPA patients showed indications of greater activation over bilateral occipital cortices and superior temporal gyrus, and inconsistent engagement of frontal regions. These findings suggest a pervasive reorganization of brain networks in response to ATL neurodegeneration: the loss of this critical hub leads to a dysregulated (semantic) control system, and defective semantic representations are seemingly compensated via enhanced perceptual processing.
Data availability
The sensitive nature of patients' data and our current ethics protocol do not permit open data sharing. However, anonymized, pre-processed, group-level data used to generate the figures have been uploaded to NeuroVault [https://neurovault.org/collections/FTKQLDFP/]. The clinical and neuroimaging data used in the current paper are available from the Senior Author (S.N.), upon formal request indicating name and affiliation of the researcher as well as a brief description of the use that will be done of the data. All requests will undergo UCSF regulated procedure thus require submission of a Material Transfer Agreement (MTA) which can be found at https://icd.ucsf.edu/material-transfer-and-data-agreements No commercial use would be approved.
Article and author information
Author details
Valentina Borghesani
Funding
National Institute of Health (R01NS050915)
- Maria Luisa Gorno-Tempini
Global Brain Health Institute
- Maria Luisa Gorno-Tempini
University of California Office of the President (MRP-17-454755)
- Srikantan Nagarajan
National Institute of Health (K24DC015544)
- Maria Luisa Gorno-Tempini
National Institute of Health (R01NS100440)
- John F Houde
National Institute of Health (R01DC013979)
- Srikantan Nagarajan
National Institute of Health (R01DC176960)
- Srikantan Nagarajan
National Institute of Health (R01DC017091)
- Srikantan Nagarajan
National Institute of Health (R01EB022717)
- Srikantan Nagarajan
National Institute of Health (R01AG062196)
- Srikantan Nagarajan
Larry Hillblom Foundation
- Maria Luisa Gorno-Tempini
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Chris I Baker, National Institute of Mental Health, National Institutes of Health, United States
Ethics
Human subjects: The study was approved by the UCSF Committee on Human Research and all subjects provided written informed consent.(IRB # 11-05249).
Version history
- Received: October 10, 2020
- Accepted: June 21, 2021
- Accepted Manuscript published: June 22, 2021 (version 1)
- Version of Record published: June 29, 2021 (version 2)
Copyright
© 2021, Borghesani et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Neural dynamics of semantic categorization in semantic variant of Primary Progressive Aphasia
eLife 10:e63905.
https://doi.org/10.7554/eLife.63905
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