Disentangling influences of dyslexia, development, and reading experience on effective brain connectivity in children

Altered brain connectivity between regions of the reading network has been associated with reading difficulties. However, it remains unclear whether connectivity differences between children with dyslexia (DYS) and those with typical reading skills (TR) are specific to reading impairments or to read...

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Main Authors: Sarah V. Di Pietro, David Willinger, Nada Frei, Christina Lutz, Seline Coraj, Chiara Schneider, Philipp Stämpfli, Silvia Brem
Format: Article
Language:English
Published: Elsevier 2023-03-01
Series:NeuroImage
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811923000186
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author Sarah V. Di Pietro
David Willinger
Nada Frei
Christina Lutz
Seline Coraj
Chiara Schneider
Philipp Stämpfli
Silvia Brem
author_facet Sarah V. Di Pietro
David Willinger
Nada Frei
Christina Lutz
Seline Coraj
Chiara Schneider
Philipp Stämpfli
Silvia Brem
author_sort Sarah V. Di Pietro
collection DOAJ
description Altered brain connectivity between regions of the reading network has been associated with reading difficulties. However, it remains unclear whether connectivity differences between children with dyslexia (DYS) and those with typical reading skills (TR) are specific to reading impairments or to reading experience. In this functional MRI study, 132 children (M = 10.06 y, SD = 1.46) performed a phonological lexical decision task. We aimed to disentangle (1) disorder-specific from (2) experience-related differences in effective connectivity and to (3) characterize the development of DYS and TR. We applied dynamic causal modeling to age-matched (ndys = 25, nTR = 35) and reading-level-matched (ndys = 25, nTR = 22) groups. Developmental effects were assessed in beginning and advanced readers (TR: nbeg = 48, nadv = 35, DYS: nbeg = 24, nadv = 25). We show that altered feedback connectivity between the inferior parietal lobule and the visual word form area (VWFA) during print processing can be specifically attributed to reading impairments, because these alterations were found in DYS compared to both the age-matched and reading-level-matched TR. In contrast, feedforward connectivity from the VWFA to parietal and frontal regions characterized experience in TR and increased with age and reading skill. These directed connectivity findings pinpoint disorder-specific and experience-dependent alterations in the brain's reading network.
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spelling doaj.art-ab3b18f07bc244b3b7f5807c1c9a98e32023-02-08T04:16:29ZengElsevierNeuroImage1095-95722023-03-01268119869Disentangling influences of dyslexia, development, and reading experience on effective brain connectivity in childrenSarah V. Di Pietro0David Willinger1Nada Frei2Christina Lutz3Seline Coraj4Chiara Schneider5Philipp Stämpfli6Silvia Brem7Department of Child and Adolescent Psychiatry and Psychotherapy, University Hospital of Psychiatry Zurich, University of Zurich, Switzerland; Neuroscience Center Zurich, University of Zurich and ETH Zurich, Switzerland; URPP Adaptive Brain Circuits in Development and Learning (AdaBD), University of Zurich, Zurich, SwitzerlandDepartment of Child and Adolescent Psychiatry and Psychotherapy, University Hospital of Psychiatry Zurich, University of Zurich, Switzerland; Neuroscience Center Zurich, University of Zurich and ETH Zurich, Switzerland; Department of Psychology and Psychodynamics, Karl Landsteiner University of Health Sciences, Krems an der Donau, AustriaDepartment of Child and Adolescent Psychiatry and Psychotherapy, University Hospital of Psychiatry Zurich, University of Zurich, Switzerland; Neuroscience Center Zurich, University of Zurich and ETH Zurich, SwitzerlandDepartment of Child and Adolescent Psychiatry and Psychotherapy, University Hospital of Psychiatry Zurich, University of Zurich, Switzerland; Neuroscience Center Zurich, University of Zurich and ETH Zurich, SwitzerlandDepartment of Child and Adolescent Psychiatry and Psychotherapy, University Hospital of Psychiatry Zurich, University of Zurich, Switzerland; Neuroscience Center Zurich, University of Zurich and ETH Zurich, SwitzerlandDepartment of Child and Adolescent Psychiatry and Psychotherapy, University Hospital of Psychiatry Zurich, University of Zurich, SwitzerlandMR-Center of the Department of Psychiatry, Psychotherapy and Psychosomatics and the Department of Child and Adolescent Psychiatry and Psychotherapy, Psychiatric Hospital, University of Zurich, Zurich, SwitzerlandDepartment of Child and Adolescent Psychiatry and Psychotherapy, University Hospital of Psychiatry Zurich, University of Zurich, Switzerland; Neuroscience Center Zurich, University of Zurich and ETH Zurich, Switzerland; URPP Adaptive Brain Circuits in Development and Learning (AdaBD), University of Zurich, Zurich, Switzerland; MR-Center of the Department of Psychiatry, Psychotherapy and Psychosomatics and the Department of Child and Adolescent Psychiatry and Psychotherapy, Psychiatric Hospital, University of Zurich, Zurich, Switzerland; Corresponding author at: Department of Child and Adolescent Psychiatry and Psychotherapy, University Hospital of Psychiatry Zurich, University of Zurich, Neumünsterallee 9, 8032 Zürich, Switzerland.Altered brain connectivity between regions of the reading network has been associated with reading difficulties. However, it remains unclear whether connectivity differences between children with dyslexia (DYS) and those with typical reading skills (TR) are specific to reading impairments or to reading experience. In this functional MRI study, 132 children (M = 10.06 y, SD = 1.46) performed a phonological lexical decision task. We aimed to disentangle (1) disorder-specific from (2) experience-related differences in effective connectivity and to (3) characterize the development of DYS and TR. We applied dynamic causal modeling to age-matched (ndys = 25, nTR = 35) and reading-level-matched (ndys = 25, nTR = 22) groups. Developmental effects were assessed in beginning and advanced readers (TR: nbeg = 48, nadv = 35, DYS: nbeg = 24, nadv = 25). We show that altered feedback connectivity between the inferior parietal lobule and the visual word form area (VWFA) during print processing can be specifically attributed to reading impairments, because these alterations were found in DYS compared to both the age-matched and reading-level-matched TR. In contrast, feedforward connectivity from the VWFA to parietal and frontal regions characterized experience in TR and increased with age and reading skill. These directed connectivity findings pinpoint disorder-specific and experience-dependent alterations in the brain's reading network.http://www.sciencedirect.com/science/article/pii/S1053811923000186Reading networkDevelopmental dyslexiaDynamic causal modeling (DCM)Effective connectivityfMRIVisual Word Forma Area (VWFA)
spellingShingle Sarah V. Di Pietro
David Willinger
Nada Frei
Christina Lutz
Seline Coraj
Chiara Schneider
Philipp Stämpfli
Silvia Brem
Disentangling influences of dyslexia, development, and reading experience on effective brain connectivity in children
NeuroImage
Reading network
Developmental dyslexia
Dynamic causal modeling (DCM)
Effective connectivity
fMRI
Visual Word Forma Area (VWFA)
title Disentangling influences of dyslexia, development, and reading experience on effective brain connectivity in children
title_full Disentangling influences of dyslexia, development, and reading experience on effective brain connectivity in children
title_fullStr Disentangling influences of dyslexia, development, and reading experience on effective brain connectivity in children
title_full_unstemmed Disentangling influences of dyslexia, development, and reading experience on effective brain connectivity in children
title_short Disentangling influences of dyslexia, development, and reading experience on effective brain connectivity in children
title_sort disentangling influences of dyslexia development and reading experience on effective brain connectivity in children
topic Reading network
Developmental dyslexia
Dynamic causal modeling (DCM)
Effective connectivity
fMRI
Visual Word Forma Area (VWFA)
url http://www.sciencedirect.com/science/article/pii/S1053811923000186
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