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

Smadar Z. Patael, Emily A. Farris, Jessica M. Black, Roeland Hancock, John D.E. Gabrieli, Laurie E. Cutting, Fumiko Hoeft

Research output: Contribution to journalArticlepeer-review

24 Scopus citations

Abstract

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.

Original languageEnglish
Article numbere0198791
JournalPLoS ONE
Volume13
Issue number6
DOIs
StatePublished - Jun 2018
Externally publishedYes

Bibliographical note

Publisher Copyright:
© 2018 Patael et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding

Research was funded by the National Institute of Child Health and Human Development (NICHD) K23HD054720. FH was funded by NICHD R01HD086168, R01HD078351, R01HD065794 (PI: K. Pugh), P01HD001994 (PI: J. Rueckl), P50HD052120 (PI: R. Wagner), National Science Foundation NSF-1540854, University of California Office of the President Multicampus Research Programs and Initiatives Award MRP-17-454925, Oak Foundation ORIO-16-012, UCSF Dyslexia Center, Ray & Lori dePole, Dyslexia Training Institute, The Potter Family, and Currey Ingram Academy. LC was funded by NICHD R01HD067254, R01HD044073, U54HD083211, R21HD087088 and R01HD089474. SP was supported by the CCC-UCSF Neuroscience of Creativity Fellowship Award and the Tel Aviv University post-doctoral fellowship. JB was funded by the Boston College Ignite Grant and Boston College Research Incentive Grant. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

FundersFunder number
National Institute of Child Health and Human DevelopmentP50HD052120, R01HD044073, R01HD065794, P01HD001994, R01HD086168, R01HD067254, R01HD078351, R21HD087088, R01HD089474, U54HD083211, K23HD054720
University of CaliforniaORIO-16-012, MRP-17-454925
National Science FoundationNSF-1540854

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