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Brain basis of cognitive resilience: Prefrontal cortex predicts better reading comprehension in relation to decoding

OBJECTIVE: The ultimate goal of reading is to understand written text. To accomplish this, children must first master decoding, the ability to translate printed words into sounds. Although decoding and reading comprehension are highly interdependent, some children struggle to decode but comprehend w...

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Autores principales: Patael, Smadar Z., Farris, Emily A., Black, Jessica M., Hancock, Roeland, Gabrieli, John D. E., Cutting, Laurie E., Hoeft, Fumiko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6002103/
https://www.ncbi.nlm.nih.gov/pubmed/29902208
http://dx.doi.org/10.1371/journal.pone.0198791
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author Patael, Smadar Z.
Farris, Emily A.
Black, Jessica M.
Hancock, Roeland
Gabrieli, John D. E.
Cutting, Laurie E.
Hoeft, Fumiko
author_facet Patael, Smadar Z.
Farris, Emily A.
Black, Jessica M.
Hancock, Roeland
Gabrieli, John D. E.
Cutting, Laurie E.
Hoeft, Fumiko
author_sort Patael, Smadar Z.
collection PubMed
description OBJECTIVE: The ultimate goal of reading is to understand written text. To accomplish this, children must first master decoding, the ability to translate printed words into sounds. Although decoding and reading comprehension are highly interdependent, some children struggle to decode but comprehend well, whereas others with good decoding skills fail to comprehend. The neural basis underlying individual differences in this discrepancy between decoding and comprehension abilities is virtually unknown. METHODS: We investigated the neural basis underlying reading discrepancy, defined as the difference between reading comprehension and decoding skills, in a three-part study: 1) The neuroanatomical basis of reading discrepancy in a cross-sectional sample of school-age children with a wide range of reading abilities (Experiment-1; n = 55); 2) Whether a discrepancy-related neural signature is present in beginning readers and predictive of future discrepancy (Experiment-2; n = 43); and 3) Whether discrepancy-related regions are part of a domain-general or a language specialized network, utilizing the 1000 Functional Connectome data and large-scale reverse inference from Neurosynth.org (Experiment-3). RESULTS: Results converged onto the left dorsolateral prefrontal cortex (DLPFC), as related to having discrepantly higher reading comprehension relative to decoding ability. Increased gray matter volume (GMV) was associated with greater discrepancy (Experiment-1). Region-of-interest (ROI) analyses based on the left DLPFC cluster identified in Experiment-1 revealed that regional GMV within this ROI in beginning readers predicted discrepancy three years later (Experiment-2). This region was associated with the fronto-parietal network that is considered fundamental for working memory and cognitive control (Experiment-3). INTERPRETATION: Processes related to the prefrontal cortex might be linked to reading discrepancy. The findings may be important for understanding cognitive resilience, which we operationalize as those individuals with greater higher-order reading skills such as reading comprehension compared to lower-order reading skills such as decoding skills. Our study provides insights into reading development, existing theories of reading, and cognitive processes that are potentially significant to a wide range of reading disorders.
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spelling pubmed-60021032018-06-25 Brain basis of cognitive resilience: Prefrontal cortex predicts better reading comprehension in relation to decoding Patael, Smadar Z. Farris, Emily A. Black, Jessica M. Hancock, Roeland Gabrieli, John D. E. Cutting, Laurie E. Hoeft, Fumiko PLoS One Research Article OBJECTIVE: The ultimate goal of reading is to understand written text. To accomplish this, children must first master decoding, the ability to translate printed words into sounds. Although decoding and reading comprehension are highly interdependent, some children struggle to decode but comprehend well, whereas others with good decoding skills fail to comprehend. The neural basis underlying individual differences in this discrepancy between decoding and comprehension abilities is virtually unknown. METHODS: We investigated the neural basis underlying reading discrepancy, defined as the difference between reading comprehension and decoding skills, in a three-part study: 1) The neuroanatomical basis of reading discrepancy in a cross-sectional sample of school-age children with a wide range of reading abilities (Experiment-1; n = 55); 2) Whether a discrepancy-related neural signature is present in beginning readers and predictive of future discrepancy (Experiment-2; n = 43); and 3) Whether discrepancy-related regions are part of a domain-general or a language specialized network, utilizing the 1000 Functional Connectome data and large-scale reverse inference from Neurosynth.org (Experiment-3). RESULTS: Results converged onto the left dorsolateral prefrontal cortex (DLPFC), as related to having discrepantly higher reading comprehension relative to decoding ability. Increased gray matter volume (GMV) was associated with greater discrepancy (Experiment-1). Region-of-interest (ROI) analyses based on the left DLPFC cluster identified in Experiment-1 revealed that regional GMV within this ROI in beginning readers predicted discrepancy three years later (Experiment-2). This region was associated with the fronto-parietal network that is considered fundamental for working memory and cognitive control (Experiment-3). INTERPRETATION: Processes related to the prefrontal cortex might be linked to reading discrepancy. The findings may be important for understanding cognitive resilience, which we operationalize as those individuals with greater higher-order reading skills such as reading comprehension compared to lower-order reading skills such as decoding skills. Our study provides insights into reading development, existing theories of reading, and cognitive processes that are potentially significant to a wide range of reading disorders. Public Library of Science 2018-06-14 /pmc/articles/PMC6002103/ /pubmed/29902208 http://dx.doi.org/10.1371/journal.pone.0198791 Text en © 2018 Patael 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
Patael, Smadar Z.
Farris, Emily A.
Black, Jessica M.
Hancock, Roeland
Gabrieli, John D. E.
Cutting, Laurie E.
Hoeft, Fumiko
Brain basis of cognitive resilience: Prefrontal cortex predicts better reading comprehension in relation to decoding
title Brain basis of cognitive resilience: Prefrontal cortex predicts better reading comprehension in relation to decoding
title_full Brain basis of cognitive resilience: Prefrontal cortex predicts better reading comprehension in relation to decoding
title_fullStr Brain basis of cognitive resilience: Prefrontal cortex predicts better reading comprehension in relation to decoding
title_full_unstemmed Brain basis of cognitive resilience: Prefrontal cortex predicts better reading comprehension in relation to decoding
title_short Brain basis of cognitive resilience: Prefrontal cortex predicts better reading comprehension in relation to decoding
title_sort brain basis of cognitive resilience: prefrontal cortex predicts better reading comprehension in relation to decoding
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6002103/
https://www.ncbi.nlm.nih.gov/pubmed/29902208
http://dx.doi.org/10.1371/journal.pone.0198791
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