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Atypical measures of diffusion at the gray-white matter boundary in autism spectrum disorder in adulthood

Research output: Contribution to journalArticlepeer-review

the MRC AIMS Consortium

Original languageEnglish
Pages (from-to)467-484
Number of pages18
JournalHuman Brain Mapping
Volume42
Issue number2
DOIs
Published1 Feb 2021

Bibliographical note

Funding Information: This project was generously supported by the National Institute for Health Research (NIHR) Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King's College London; the Medical Research Council UK (grant number G0400061); and the Innovative Medicines Initiative 2 Joint Undertaking under grant agreement No. 115300 (for EU‐AIMS) and No. 777394 (for AIMS‐2‐TRIALS). This Joint Undertaking receives support from the European Union's Horizon 2020 research and innovation programme and EFPIA and Autism Speaks, Autistica, and SFARI. C. E. gratefully acknowledges support from the German Research Foundation (DFG) under the Heisenberg programme (grant numbers EC480/1‐1 and EC480/2‐1). M.‐C. L. was supported by the Ontario Brain Institute via the Province of Ontario Neurodevelopmental Disorders Network (grant number IDS‐I 1‐02), the Academic Scholars Award from the Department of Psychiatry, University of Toronto, and the Canadian Institutes of Health Research (grant number PJT‐159578). The authors would like to thank all of the participants and their family members for partaking in this study. The Autism Imaging Multicentre Study Consortium, members in alphabetical order are as follows: Anthony J. Bailey (Oxford), S. B.‐C. (Cambridge), Patrick F. Bolton (IoP), E. T. B. (Cambridge), Sarah Carrington (Oxford), Marco Catani (IoPPN), Bhismadev Chakrabarti (Cambridge), M. C. C. (IoPPN), E. M. D. (IoPPN), Sean C. L. Deoni (IoPPN), C. E. (IoPPN), Francesca Happé (IoPPN), Julian Henty (Cambridge), Peter Jezzard (Oxford), Patrick Johnston (IoPPN), Derek K. Jones (IoPPN), M.‐C. L. (Cambridge), M. V. L. (Cambridge), Anya Madden (IoPPN), Diane Mullins (IoPPN), Clodagh M. Murphy (IoPPN), D. G. M. M. (IoPPN), Greg Pasco (Cambridge), A. N. V. R. (Cambridge), Susan A. Sadek (Cambridge), Debbie Spain (IoPPN), Rose Stewart (Oxford), J. S. (Cambridge), Sally J. Wheelwright (Cambridge), Steven C. Williams (IoPPN), and C. Ellie Wilson (IoPPN). Furthermore, the authors would like to thank the National Institute for Health Research Biomedical Research Centre for Mental Health, the Dr Mortimer and Theresa Sackler Foundation, and the German Research Foundation (DFG). Funding Information: This project was generously supported by the National Institute for Health Research (NIHR) Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King's College London; the Medical Research Council UK (grant number G0400061); and the Innovative Medicines Initiative 2 Joint Undertaking under grant agreement No. 115300 (for EU-AIMS) and No. 777394 (for AIMS-2-TRIALS). This Joint Undertaking receives support from the European Union's Horizon 2020 research and innovation programme and EFPIA and Autism Speaks, Autistica, and SFARI. C. E. gratefully acknowledges support from the German Research Foundation (DFG) under the Heisenberg programme (grant numbers EC480/1-1 and EC480/2-1). M.-C. L. was supported by the Ontario Brain Institute via the Province of Ontario Neurodevelopmental Disorders Network (grant number IDS-I 1-02), the Academic Scholars Award from the Department of Psychiatry, University of Toronto, and the Canadian Institutes of Health Research (grant number PJT-159578). The authors would like to thank all of the participants and their family members for partaking in this study. The Autism Imaging Multicentre Study Consortium, members in alphabetical order are as follows: Anthony J. Bailey (Oxford), S. B.-C. (Cambridge), Patrick F. Bolton (IoP), E. T. B. (Cambridge), Sarah Carrington (Oxford), Marco Catani (IoPPN), Bhismadev Chakrabarti (Cambridge), M. C. C. (IoPPN), E. M. D. (IoPPN), Sean C. L. Deoni (IoPPN), C. E. (IoPPN), Francesca Happ? (IoPPN), Julian Henty (Cambridge), Peter Jezzard (Oxford), Patrick Johnston (IoPPN), Derek K. Jones (IoPPN), M.-C. L. (Cambridge), M. V. L. (Cambridge), Anya Madden (IoPPN), Diane Mullins (IoPPN), Clodagh M. Murphy (IoPPN), D. G. M. M. (IoPPN), Greg Pasco (Cambridge), A. N. V. R. (Cambridge), Susan A. Sadek (Cambridge), Debbie Spain (IoPPN), Rose Stewart (Oxford), J. S. (Cambridge), Sally J. Wheelwright (Cambridge), Steven C. Williams (IoPPN), and C. Ellie Wilson (IoPPN). Furthermore, the authors would like to thank the National Institute for Health Research Biomedical Research Centre for Mental Health, the Dr Mortimer and Theresa Sackler Foundation, and the German Research Foundation (DFG). Funding Information: Academic Scholars Award from the Department of Psychiatry, University of Toronto, and the Canadian Institutes of Health Research, Grant/Award Number: PJT‐159578; German Research Foundation (DFG) under the Heisenberg Programme, Grant/Award Numbers: EC480/1‐1, EC480/2‐1; Innovative Medicines Initiative 2 Joint Undertaking, Grant/Award Numbers: 115300, 777394; Medical Research Council UK, Grant/Award Number: G0400061; National Institute for Health Research (NIHR) Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King's College London; Ontario Brain Institute via the Province of Ontario Neurodevelopmental Disorders Network, Grant/Award Number: IDS‐I 1‐02 Funding information Publisher Copyright: © 2020 The Authors. Human Brain Mapping published by Wiley Periodicals LLC. Copyright: Copyright 2021 Elsevier B.V., All rights reserved.

King's Authors

Abstract

Autism spectrum disorder (ASD) is a highly complex neurodevelopmental condition that is accompanied by neuroanatomical differences on the macroscopic and microscopic level. Findings from histological, genetic, and more recently in vivo neuroimaging studies converge in suggesting that neuroanatomical abnormalities, specifically around the gray-white matter (GWM) boundary, represent a crucial feature of ASD. However, no research has yet characterized the GWM boundary in ASD based on measures of diffusion. Here, we registered diffusion tensor imaging data to the structural T1-weighted images of 92 adults with ASD and 92 matched neurotypical controls in order to examine between-group differences and group-by-sex interactions in fractional anisotropy and mean diffusivity sampled at the GWM boundary, and at different sampling depths within the superficial white and into the gray matter. As hypothesized, we observed atypical diffusion at and around the GWM boundary in ASD, with between-group differences and group-by-sex interactions depending on tissue class and sampling depth. Furthermore, we identified that altered diffusion at the GWM boundary partially (i.e., ~50%) overlapped with atypical gray-white matter tissue contrast in ASD. Our study thus replicates and extends previous work highlighting the GWM boundary as a crucial target of neuropathology in ASD, and guides future work elucidating etiological mechanisms.

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