Associations Between Cortical Structure and Reading Skills in Beginning Readers

The acquisition of literacy is a challenging task that engages multiple processing systems to integrate multimodal information. As a result, children exhibit wide variability in reading ability, with the lowest performers classified as having Specific Reading Disability (SRD). Functional and structural magnetic resonance imaging (MRI) research has identified a reading network in the brain consisting primarily of left hemisphere temporo-parietal, occipito-temporal, and inferior frontal regions, but the structural neural substrates that support skilled reading during the formative years of reading acquisition remain underspecified. The present study applied a continuous analytic approach to investigate distinct surface-based properties of cortical structure (cortical thickness and surface area) in association with individual differences in reading-related skills in a sample of children ages 5-8 years. Brain structure was examined in relation to reading-related skills measured at concurrent and lagged follow-up time points in order to assess the stability of these relationships over time. Significant positive correlations with cortical structure were observed in the analysis of reading skills measured 8-12 months after MRI. Cortical surface area in left occipito-temporal, left prefrontal, and right superior temporal regions was associated with sight-word reading performance; Cortical thickness in the right postcentral cortex was associated with phonological awareness performance. These findings indicate that distinct properties of cortical structure are independently related to reading skills and may be salient predictors of reading outcomes over time. Running head: ASSOCIATIONS BETWEEN CORTICAL STRUCTURE AND READING 1 Associations Between Cortical Structure and Reading Skills in Beginning Readers Introduction “The whole world opened up to me when I learned to read. ” − Mary McLeod Bethune Literacy is a defining feature of modern society, and the ability to read has become crucial for day-to-day functioning in much of the world. Reading is a complex behavior that requires engagement of multiple cognitive and perceptual systems, from basic visual and auditory processing to working memory and executive function. Because reading evolved relatively recently in human phylogeny, the brain has not developed a specialized “reading apparatus”, but instead recruits multiple neural systems that serve various functions related to reading. Thus, successful acquisition of reading skills relies on adequate development of the various perceptual, cognitive, and neural systems that support reading, as well as responsiveness of these systems to reading instruction. Early language and cognitive development lay the foundation of literacy acquisition long before formal reading instruction begins. During the formative years of reading instruction in alphabetic languages (usually kindergarten through grade 3 in the United States), children progress through phases of learning from establishing the alphabetic principle, the knowledge that letters represent the sounds of language, through applying this rule to sound out words and build a repertoire of automatically recognizable sight-words, and ultimately attaining the ability to fluently read and comprehend text. Given this complex process of learning to read, children exhibit a high degree of variability in their reading outcomes that may affect their abilities at levels of word reading, fluent text reading, and/or reading comprehension. Establishing strong word-level reading skills is critical for subsequent development of reading ASSOCIATIONS BETWEEN CORTICAL STRUCTURE AND READING 2 fluency and comprehension, which become fundamental skills as schooling transitions from a focus on learning to read to reading to learn. Children who persistently fail to acquire adequate word-level reading skills despite access to instruction, sufficient motivation, and absence of gross sensory, intellectual, or neurological impairments are diagnosed with Specific Reading Disability (SRD; also called developmental dyslexia), a learning disability characterized by poor word recognition and decoding abilities (Lyon, Shaywitz, & Shaywitz, 2003). SRD affects approximately seven percent of school-age children (Peterson & Pennington, 2015), placing it among the most common learning disabilities. Furthermore, substantial heritability of SRD has been observed through family and twin studies (Grigorenko, 2004), which have led to genetic investigations of this disorder and the identification of candidate genes that confer elevated risk for SRD. Nine of these genes have been replicated in a least one independent sample, giving credence to a potential role in reading (DYX1C1, DCDC2, KIAA0319, C2ORF3, MRPL19, ROBO1, GRIN2B, FOXP2 and CNTNAP2; Mascheretti et al., 2017). Broadly, these genes are thought to regulate aspects of neurodevelopment, including processes such as neuronal migration, neurite branching and synapse function (Eicher & Gruen, 2013; Mascheretti et al., 2017). Based on these roles, researchers have proposed that variations on candidate genes contribute to reading disability by setting up atypical neural architecture and functioning early in prenatal development (Bates et al., 2010; Meng et al., 2005). The proposed genetic effects on neurobiology fit well with evidence from functional and structural magnetic resonance imaging (MRI), which suggests that language-related regions adjacent to the sylvian fissure, along with left occipito-temporal regions are altered in individuals with SRD relative to their typically reading peers (Maisog, Einbinder, Flowers, Turkeltaub, & Eden, ASSOCIATIONS BETWEEN CORTICAL STRUCTURE AND READING 3 2008; Richlan, Kronbichler, & Wimmer, 2009, 2013). These regions are thought to be involved in aspects of phonological processing and recoding, integration of orthographic, phonologic, and lexico-semantic information, and automatic word recognition (Pugh et al., 2001). Studies in prereading children at familial risk of SRD suggest that atypical structure and function observed in posterior brain regions, particularly in the left temporo-parietal and occipito-temporal cortices, predate reading onset, and may thus represent a cause, rather than a consequence, of poor reading (see Vandermosten, Hoeft, & Norton, 2016 for a review and meta-analysis). These findings point toward the potential identification of neural traits that may supplement behavioral measures as predictors of reading outcomes. In the sections that follow, I will provide an overview of behavioral and neural correlates of reading ability, address limitations of methods commonly applied to examine brain-behavior relationships in reading, and propose alternative methods to build upon the findings in the existing literature. Behavioral predictors of reading ability Early identification of children most likely to struggle with reading is key to best serve the educational needs of children as they learn to read. Several early language skills that can be tested prior to reading acquisition have been identified as strong predictors of reading outcomes, namely letter knowledge, phonological awareness, and rapid naming (for a review, see OzernovPalchik & Gaab, 2016). Schatschneider and colleagues (2004) found that these three skills measured at kindergarten served as robust predictors of word identification, reading fluency, and reading comprehension skills at grades 1-2, while vocabulary, oral language (syntax), and visual perceptual skills were weak predictors of the same skills. ASSOCIATIONS BETWEEN CORTICAL STRUCTURE AND READING 4 Letter knowledge (LK) encompasses the skills of letter naming and knowledge of letter sounds. Letter naming, the ability to identify visually presented letters, provides the foundation of orthographic knowledge upon which reading is built. Letter sound knowledge is a somewhat more complex skill that requires an understanding that letters represent sound units independent of their own names, and thus a greater reliance on phonological skills. Both of these letter knowledge sub-skills uniquely predict subsequent word recognition performance (Hulme, Bowyer-Crane, Carroll, Duff, & Snowling, 2012; Leppänen, Aunola, Niemi, & Nurmi, 2008; McBride-Chang, 1999; Schatschneider et al., 2004). Phonological awareness (PA), the ability to accurately perceive and manipulate the structural units of speech sounds (Melby-Lervåg, Lyster, & Hulme, 2012), is a critical building block for decoding text (orthographic information) and mapping it to its corresponding spoken form (phonological information). Accordingly, this skill is particularly important in the early stages of reading acquisition in which children rely heavily on sounding out words that they do not automatically recognize. Several studies corroborate evidence that PA skills predict later reading ability, especially at the word-reading level (Hulme et al., 2002; Kirby, Parrila, & Pfeiffer, 2003; Muter, Hulme, Snowling, & Stevenson, 2004). Notably, Kirby and colleagues (2003) reported a strong relationship between kindergarten PA skills and word reading outcomes in grades 1-2, but the strength of the relationship diminished in grades 3-5. The diminishing effects likely indicate that as children become more proficient readers, they rely more on rapid recognition of familiar words (sight-word reading) rather than phonological decoding. Rapid automatized naming (RAN) is the ability to quickly and accurately identify items presented in a visual array (Araújo, 2015). RAN assessments may include objects, colors, letters, ASSOCIATIONS BETWEEN CORTICAL STRUCTURE AND READING 5 digits, or some combination of these (called rapid alternating stimulus). RAN performance is thought to reflect aspects of attention, processing speed, automatic retrieval of phonological information, and integration of visual and phonological representations, skills that are important for a