The Association Between Gray Matter Volume and Reading Proficiency: a Longitudinal Study of Beginning Readers
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The Association between Gray Matter Volume and Reading Proficiency: A Longitudinal Study of Beginning Readers 1,2 1,3 1,2 Janosch Linkersdörfer , Alina Jurcoane , Sven Lindberg , Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/27/2/308/1823454/jocn_a_00710.pdf by MIT Libraries user on 17 May 2021 Jochen Kaiser3, Marcus Hasselhorn1,2,3, Christian J. Fiebach1,3,4, and Jan Lonnemann1,2 Abstract ■ Neural systems involved in the processing of written lan- baseline gray matter volume in the left superior temporal gyrus guage have been identified by a number of functional imaging and subsequent changes in reading proficiency. Furthermore, a studies. Structural changes in cortical anatomy that occur in the negative relationship was found between reading proficiency at course of literacy acquisition, however, remain largely unknown. the second measurement time point and intraindividual cortical Here, we follow elementary school children over their first volume development in the inferior parietal lobule and the pre- 2 years of formal reading instruction and use tensor-based mor- central and postcentral gyri of the left hemisphere. These results phometry to relate reading proficiency to cortical volume at are interpreted as evidence that reading acquisition is associated baseline and follow-up measurement as well as to intraindividual with preexisting structural differences as well as with experience- longitudinal volume development between the two measure- dependent structural changes involving dendritic and synaptic ment time points. A positive relationship was found between pruning. ■ INTRODUCTION a second system in the inferior frontal gyrus has been Reading is a relatively recent human cultural invention associated with articulatory processes and the active that has to be taught explicitly and practiced intensively analysis of phonological elements (e.g., Schlaggar & to be mastered. As a consequence, no genetically pre- McCandliss, 2007); and finally, a system in occipitotem- disposed neural systems for reading exist. Instead, learn- poral regions, including parts of the extrastriate fusiform ing to read is thought to involve the use of a distributed and inferior temporal gyri, is considered to facilitate the set of brain regions originally serving other purposes direct mapping between familiar visual words or frequent (Dehaene, 2004). letter combinations within words and corresponding se- The neural basis of reading has been investigated mantic and phonological representations (e.g., McCandliss, extensively in functional imaging studies (for meta- Cohen, & Dehaene, 2003; Cohen et al., 2000). analyses, see, e.g., Bolger, Perfetti, & Schneider, 2005; A common developmental hypothesis is that, in the Jobard, Crivello, & Tzourio-Mazoyer, 2003; Turkeltaub, beginning of formal reading instruction, children pri- Eden, Jones, & Zeffiro, 2002). Most consistently, these marily make use of the temporoparietal system to decode studies identified three neural systems in the left hemi- written words in a laborious letter-by-letter (or syllable- sphere to play an important role in the processing of by-syllable) manner. Through continuous practice and written language. The first system includes parts of the in tight coupling with the temporoparietal system, the posterior superior temporal gyrus and the inferior parie- occipitotemporal system is increasingly incorporated, tal lobule and is assumed to support the mapping of eventually resulting in automatic and fluent reading orthographic elements of written words (graphemes) performance (Pugh et al., 2001). These assumptions onto corresponding phonological elements (phonemes); have been supported by functional imaging studies showing greater activity in children relative to adults in the temporoparietal system (Church, Coalson, Lugar, 1Center for Individual Development and Adaptive Education of Petersen, & Schlaggar, 2008; Booth et al., 2001) and Children at Risk (IDeA), Frankfurt am Main, Germany, 2German longitudinal increases in activity over the first years of Institute for International Educational Research, Frankfurt am reading instruction in the occipitotemporal system in Main, Germany, 3Goethe University, Frankfurt am Main, Germany, reading or reading-related tasks (Ben-Shachar, Dougherty, 4Radboud University, Nijmegen, The Netherlands Deutsch, & Wandell, 2011). © 2014 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 27:2, pp. 308–318 doi:10.1162/jocn_a_00710 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn_a_00710 by guest on 01 October 2021 Despite the large body of functional imaging research, first 2 years of reading instruction. For this longitudinal only a few studies have examined neurostructural cor- sample, we collected both standardized reading tests relates of reading, that is, how different levels of reading and structural magnetic resonance imaging (MRI) data. skill relate to differences in cortical gray matter structure. To relate childrenʼs reading proficiency to cortical volume These studies have focused mainly on comparisons be- differences at the baseline and follow-up measurements as tween control participants and persons suffering from well as to differences in the intraindividual cortical volume developmental dyslexia, a severe difficulty in learning to development between the two measurement time points, read accurately and fluently. Although both reductions we used tensor-based morphometry (TBM; see, e.g., Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/27/2/308/1823454/jocn_a_00710.pdf by MIT Libraries user on 17 May 2021 and increases of gray matter properties have been reported Ashburner & Friston, 2003). In contrast to VBM, which in dyslexic readers, the results of two recent coordinate- identifies regional neurostructural differences by seg- based meta-analyses of voxel-based morphometry (VBM) mentation of tissue classes and statistical analysis of the studies point to gray matter reductions in bilateral tem- resulting tissue probability maps after nonlinear transfor- poroparietal (Richlan, Kronbichler, & Wimmer, 2013; mation to a common space, TBM derives information from Linkersdörfer, Lonnemann, Lindberg, Hasselhorn, & high-resolution deformation fields obtained from these Fiebach, 2012), left occipitotemporal, and bilateral cere- nonlinear transformations. In cross-sectional TBM studies, bellar (Linkersdörfer et al., 2012) regions as the most con- participantsʼ structural images are nonlinearly transformed sistent neurostructural correlates of dyslexia. to a common anatomical template; in longitudinal studies, Studies investigating neurostructural correlates of structural images of the same participant are nonlinearly reading in nonimpaired populations are even more transformed to each other. From the resulting deformation sparse and so far yielded mixed results. More specifically, tensor fields, the Jacobian matrix is computed for each a positive association between reading performance and voxel, whose determinant quantifies the fractional volume measures of gray matter volume, density, or thickness expansion and contraction needed to align the two images. has been demonstrated in bilateral (Blackmon et al., These relative local volume differences between a partici- 2010) or left (He et al., 2013; Steinbrink et al., 2008) pantʼs image and the template, that is, the group average, temporoparietal and left (Zhang et al., 2013) or right in a cross-sectional analysis or between images from the (Hoeft et al., 2007) occipitotemporal regions. In addi- same participant at different time points in a longitudinal tion, negative correlations have been reported for left analysis are then, after transformation to a common space, occipitotemporal and bilateral inferior frontal regions used in the statistical analysis. TBM is considered to offer (Blackmon et al., 2010) and the left posterior cingulate more precise and robust results than VBM, especially in cortex (He et al., 2013). Furthermore, as all of these longitudinal analyses (Anderson et al., 2012; Hua et al., studies employed a cross-sectional design (i.e., participants 2009; Lee et al., 2007). were studied at only one point in time), they cannot answer the question of whether reading-related differences in cortical anatomy arise in the course of reading instruc- METHODS tion and represent the result of different levels of reading proficiency or whether they can be regarded as a pre- Participants existing condition possibly causing differences in reading Twenty-eight normally developing children participated proficiency. One VBM study (Carreiras et al., 2009) found in the MRI procedure at both measurement time points. higher bilateral temporoparietal gray matter density in The study was approved by the ethics committee of the late-literates (persons who acquired literacy as adults) chamber of physicians of the state of Hessen, Germany, compared with illiterates, which supports the hypothesis and informed consent was obtained from all participating of experience-dependent structural changes. It remains children and their parents. Six children were excluded unclear, however, whether structural changes associated from the analysis because of movement artifacts (see with reading acquisition in adulthood resemble those that below), resulting in a final sample of 22 children (10 girls). occur when reading is learned in childhood. Cortical gray All children were in their first year of elementary school at matter structure has been shown to