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

Date Published: June 14, 2018

Publisher: Public Library of Science

Author(s): Smadar Z. Patael, Emily A. Farris, Jessica M. Black, Roeland Hancock, John D. E. Gabrieli, Laurie E. Cutting, Fumiko Hoeft, Bert De Smedt.

http://doi.org/10.1371/journal.pone.0198791

Abstract

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.

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 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).

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.

Partial Text

Becoming proficient in reading comprehension relies on mastering decoding [1], a skill that enables a child to map letters to their corresponding speech sounds and meaning. Indeed, seminal frameworks in reading and its development indicate that reading comprehension is highly dependent on a reader’s ability to decode words accurately, fluently and effortlessly [2]. Neuroimaging studies indicated that reading comprehension and decoding activated overlapping regions [3, 4]. Yet, there are exceptions. Some readers show a discrepancy between reading comprehension and decoding skills. While the term “discrepancy” has often been used to reflect differences between cognitive abilities (or aptitude such as IQ) and reading skills arising from a historical definition of dyslexia using the “discrepancy criteria” [5, 6], these readers have also been known as discrepant readers. While potentially confusing, for the purpose of consistency, we use the term discrepant readers to describe individuals with large differences between reading comprehension and decoding with possible discrepancy in either direction (either comprehension better than decoding or decoding better than comprehension). There are two profiles that anchor the spectrum of discrepant readers: those who have low decoding, but relatively good comprehension skills, known as resilient dyslexia [7–10], and those who have low comprehension skills but relative good decoding known as specific reading comprehension disorder, S-RCD [11–14]. The aim of this study was twofold; first, to characterize the neurobiological structural of discrepant readers in children with a wide range of reading abilities; and second, to examine in an independent dataset whether the brain regions associated with reading discrepancy are a consequence of learned compensatory strategies that develop over time or whether these regions are in place prior to reading acquisition and predictive of later discrepancy.

A large number of studies have investigated the neural correlates of developmental reading disorders. Nevertheless, only few studies examined the neural basis of readers that show a discrepancy between two important reading skills: decoding and reading comprehension. While these skills are highly related, the existence of discrepant readers suggests that there are additional skills important to becoming proficient at reading comprehension. Our main goal was to fill this gap and examine the neural basis that underlie the discrepancy between decoding skills and reading comprehension in children with a wide range of reading abilities.

 

Source:

http://doi.org/10.1371/journal.pone.0198791

 

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