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Neuroanatomy of Dyslexia: an Allometric Approach

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Neuroanatomy of Dyslexia: an Allometric Approach Received: 21 October 2019 | Revised: 4 January 2020 | Accepted: 17 January 2020 DOI: 10.1111/ejn.14690 RESEARCH REPORT Neuroanatomy of dyslexia: An allometric approach Hugo Peyre1,2,3 | Neha Mohanpuria1 | Katarzyna Jednoróg4 | Stefan Heim5,6 | Marion Grande7 | Muna van Ermingen-Marbach5,7 | Irene Altarelli8 | Karla Monzalvo9 | Camille Michèle Williams1 | David Germanaud2,9,10,11 | Roberto Toro12 | Franck Ramus1 1Laboratoire de Sciences Cognitives et Psycholinguistique (ENS, EHESS, CNRS), Ecole Normale Supérieure, PSL University, Paris, France 2Neurodiderot, INSERM UMR 1141, Paris Diderot University, Paris, France 3Department of Child and Adolescent Psychiatry, Robert Debré Hospital, APHP, Paris, France 4Laboratory of Language Neurobiology, Nencki Institute of Experimental Biology, Polish Academy of Sciences (PAS), Warsaw, Poland 5Department of Psychiatry, Psychotherapy and Psychosomatics, Medical Faculty, RWTH Aachen University, Aachen, Germany 6Institute of Neuroscience and Medicine (INM-1), Helmholtz-Gemeinschaft Deutscher Forschungszentren (HZ), Jülich, Germany 7Department of Neurology, Medical Faculty, RWTH Aachen University, Aachen, Germany 8Laboratory for the Psychology of Child Development and Education, CNRS UMR 8240, Université de Paris, Paris, France 9INSERM, UMR992, CEA, NeuroSpin Center, University Paris Saclay, Gif-sur-Yvette, France 10Department of Pediatric Neurology and Metabolic Diseases, Robert Debré Hospital, APHP, Paris, France 11INSERM, CEA, UMR 1129, Sorbonne Paris Cité University (USPC), Paris, France 12Human Genetics and Cognitive Functions, Institut Pasteur, Paris, France Correspondence Hugo Peyre, Département d’Etudes Abstract Cognitives, Ecole Normale Supérieure, 29 Despite evidence for a difference in total brain volume between dyslexic and good read- rue d'Ulm, 75005 Paris, France. ers, no previous neuroimaging study examined differences in allometric scaling (i.e. Email: [email protected] differences in the relationship between regional and total brain volumes) between dys- Funding information lexic and good readers. The present study aims to fill this gap by testing differences in Agence Nationale de la Recherche, Grant/ allometric scaling and regional brain volume differences in dyslexic and good read- Award Number: ANR-06-NEURO-019-01, ANR-11-BSV4-014-01, ANR-17- ers. Object-based morphometry analysis was used to determine grey and white matter EURE-0017 and ANR-10-IDEX-0001-02 volumes of the four lobes, the cerebellum and limbic structures in 130 dyslexic and PSL; Ecole des Neurosciences de Paris; the 106 good readers aged 8–14 years. Data were collected across three countries (France, Bettencourt-Schueller Foundation; Polish Ministry of Science and Higher Education; Poland and Germany). Three methodological approaches were used as follows: princi- Ministry of Science and Higher Education, pal component analysis (PCA), linear regression and multiple-group confirmatory factor Grant/Award Number: IP2010 015170 and IP2011 020271; National Science analysis (MGCFA). Difference in total brain volume between good and dyslexic readers Center, Grant/Award Number: 2011/03/D/ was Cohen's d = 0.39. We found no difference in allometric scaling, nor in regional HS6/05584, 2016/22/E/HS6/00119 and brain volume between dyslexic and good readers. Results of our three methodological DEC-2011/03/D/HS6/05584; German Abbreviations: ADHD, Attention Hyperactivity Deficit Disorder; IQ, Intelligence Quotient; MGCFA, Multiple-group Confirmatory Factor Analysis; MRI, Magnetic Resonance Imaging; OBM, Object-Based Morphometry; PCA, Principal Component Analysis; VBM, Voxel-Based Morphometry; WISC, Wechsler Intelligence Scale for Children. Edited by Susan Rossell. The peer review history for this article is available at https://publo ns.com/publo n/10.1111/EJN.14690 [Correction added on 13 March 2020, after first online publication: URL for peer review history has been corrected.] © 2020 Federation of European Neuroscience Societies and John Wiley & Sons Ltd Eur J Neurosci. 2020;52:3595–3609. wileyonlinelibrary.com/journal/ejn | 3595 3596 | PEYRE ET AL. Bundesministerium für Bildung und Forschung, Grant/Award Number: approaches (PCA, linear regression and MGCFA) were consistent. This study provides BMBF 01GJ0613, 01GJ0614 and evidence for total brain volume differences between dyslexic and control children, but 01GJ0804; Swiss National Science no evidence for differences in the volumes of the four lobes, the cerebellum or limbic Foundation, Grant/Award Number: 320030_135679 structures, once allometry is taken into account. It also finds no evidence for a difference in allometric relationships between the groups. We highlight the methodological interest of the MGCFA approach to investigate such research issues. KEYWORDS allometry, brain volume, dyslexia, sex 1 | INTRODUCTION For instance, previous findings suggest that sex differences and sex by age interactions in local brain volumes practically Dyslexia is characterized by persistent difficulties in learning disappeared when taking into account brain size (Jäncke, the written language code that cannot be accounted for by Mérillat, Liem, & Hänggi, 2015; Sanchis-Segura et al., another disorder and by lack of education or sensory deficits 2019). Brain size should thus be considered when examining (American Psychiatric Association, 2013). Like other neuro- volumetric differences across brain regions, as it accounts for developmental disorders, the aetiology of dyslexia involves more interindividual differences than sex or age. complex interactions between multiple genetic and environ- Given that dyslexic and normal readers are thought to dif- mental risk factors (Bishop, 2015; Mascheretti et al., 2013; fer in terms of total brain volumes, the question now arises Oliver & Plomin, 2007). At the cognitive level, deficits in whether they also differ in the relationship between any given phonological processes are thought to be central to the de- regional volume and total brain volume. This scaling rela- velopment of dyslexia in most cases (Ramus et al., 2003; tionship between a regional volume (y) and total brain vol- Saksida et al., 2016). ume (x) can be investigated with the commonly used power There is a vast literature on the neuroanatomical correlates equation y = b xa (Finlay, Darlington, & Nicastro, 2001). If of dyslexia, most of them relying on voxel-based morphom- a = 1, the volumes x and y are directly proportional (iso- etry (VBM) and reporting regional brain volume differences metric). If a ≠ 1, they are not (they are allometric). The al- between dyslexic and good readers. However, meta-analyses lometric scaling coefficient “a” can be easily estimated in a of those studies reported remarkably few consistent findings linear regression using a log–log transformation {log(y) = a after proper statistical corrections (Eckert, Berninger, Vaden, log(x) + log(b)}. When the regional volume grows dispro- Gebregziabher, & Tsu, 2016; Linkersdörfer, Lonnemann, portionately with total brain volume (a > 1), this is called Lindberg, Hasselhorn, & Fiebach, 2012; Richlan, positive allometry or hyperallometry. When the regional vol- Kronbichler, & Wimmer, 2013). Indeed, the validity of these ume grows more slowly than total brain volume (a < 1), this results has been questioned due to several methodological is called negative allometry or hypoallometry. In many cases, limitations (Ramus, Altarelli, Jednoróg, Zhao, & Scotto di “a” has been shown to differ from 1, non-linear relationships Covella, 2018). The problem of multiple testing is particu- being the rule more than the exception between regional and larly acute in cluster-based VBM studies with small samples, total brain volumes (Jäncke et al., 2015; de Jong et al., 2017; as it is the case for most studies on dyslexia. Comparatively, Reardon et al., 2018). Therefore, linearly adjusting for total neuroanatomical studies using predefined segmentations, brain volume when comparing regional volumes is theoret- which reduce the number of multiple comparisons (known as ically inappropriate. Indeed, recent studies have shown that Object-Based Morphometry [OBM] (Mangin et al., 2004)) of omitting brain allometry can lead to overestimating or un- tissues and lobes, are less concerned by false-positive results derestimating regional volumetric group differences and rec- (Scarpazza, Sartori, Simone, & Mechelli, 2013). Ramus and ommend that studies adjust for total brain volume differences colleagues (2018) argued that the only robust result emerg- using allometric scaling (Germanaud et al., 2014; Jäncke, ing from this literature was a smaller total brain volume in Liem, & Merillat, 2019; de Jong et al., 2017; Mankiw et al., dyslexics compared to good readers (Cohen's d = −0.58 [CI- 2017; Reardon et al., 2016; Sanchis-Segura et al., 2019). 95%: −0.32; −0.85]) (Ramus et al., 2018). Yet, these global In the present study, we examined differences in al- differences are only taken into account when investigating lometric scaling and regional brain volume differences of regional differences in about half of the studies. This is in dyslexic and good readers. Our analyses focused on particularly problematic when examining cerebral differ- 24 regional brain volumes (two hemispheres × six re- ences between groups with differing total brain volumes. gions (frontal, temporal, parietal, cerebellum, limbic and PEYRE ET AL. | 3597 occipital) × two tissue compartments (grey and white Dyslexic readers were either identified in school, through matter))
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