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

Anke Bletsch; Tim Schafer; Caroline Mann; Derek Sayre Andrews; Eileen M Daly; Maria Gudbrandsen; Amber N. V. Ruigrok; Robert Dallyn; Rafael Romero-Garcia; Meng-Chuan Lai; Michael V. Lombardo; Michael C. Craig; John Suckling; Edward T. Bullmore; Simon Baron-Cohen; Declan G. M. Murphy; Flavio Dell'Acqua; Christine Ecker

doi:10.1002/hbm.25237

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

Anke Bletsch, Tim Schafer, Caroline Mann, Derek Sayre Andrews, Eileen M Daly, Maria Gudbrandsen, Amber N. V. Ruigrok, Robert Dallyn, Rafael Romero-Garcia, Meng-Chuan Lai, Michael V. Lombardo, Michael C. Craig, John Suckling, Edward T. Bullmore, Simon Baron-Cohen, Declan G. M. Murphy, Flavio Dell'Acqua, Christine Ecker

Research output: Contribution to journal › Article › peer-review

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.

Original language	English
Pages (from-to)	467-484
Number of pages	18
Journal	HUMAN BRAIN MAPPING
Volume	42
Issue number	2
DOIs	https://doi.org/10.1002/hbm.25237
Publication status	Published - 1 Feb 2021

Keywords

diffusion tensor imaging
multimodal imaging
myelinated and unmyelinated gray matter
superficial white matter

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10.1002/hbm.25237

https://onlinelibrary.wiley.com/doi/10.1002/hbm.25237Licence: CC BY

Cite this

Bletsch, A., Schafer, T., Mann, C., Andrews, D. S., Daly, E. M., Gudbrandsen, M., Ruigrok, A. N. V., Dallyn, R., Romero-Garcia, R., Lai, M.-C., Lombardo, M. V., Craig, M. C., Suckling, J., Bullmore, E. T., Baron-Cohen, S., Murphy, D. G. M., Dell'Acqua, F., & Ecker, C. (2021). Atypical measures of diffusion at the gray-white matter boundary in autism spectrum disorder in adulthood. HUMAN BRAIN MAPPING, 42(2), 467-484. https://doi.org/10.1002/hbm.25237

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

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.",

keywords = "diffusion tensor imaging, multimodal imaging, myelinated and unmyelinated gray matter, superficial white matter",

author = "Anke Bletsch and Tim Schafer and Caroline Mann and Andrews, {Derek Sayre} and Daly, {Eileen M} and Maria Gudbrandsen and Ruigrok, {Amber N. V.} and Robert Dallyn and Rafael Romero-Garcia and Meng-Chuan Lai and Lombardo, {Michael V.} and Craig, {Michael C.} and John Suckling and Bullmore, {Edward T.} and Simon Baron-Cohen and Murphy, {Declan G. M.} and Flavio Dell'Acqua and Christine Ecker",

note = "{\textcopyright} 2020 The Authors. Human Brain Mapping published by Wiley Periodicals LLC.",

year = "2021",

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Bletsch, A, Schafer, T, Mann, C, Andrews, DS, Daly, EM, Gudbrandsen, M, Ruigrok, ANV, Dallyn, R, Romero-Garcia, R, Lai, M-C, Lombardo, MV, Craig, MC, Suckling, J, Bullmore, ET, Baron-Cohen, S, Murphy, DGM, Dell'Acqua, F & Ecker, C 2021, 'Atypical measures of diffusion at the gray-white matter boundary in autism spectrum disorder in adulthood', HUMAN BRAIN MAPPING, vol. 42, no. 2, pp. 467-484. https://doi.org/10.1002/hbm.25237

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T1 - Atypical measures of diffusion at the gray-white matter boundary in autism spectrum disorder in adulthood

AU - Bletsch, Anke

AU - Schafer, Tim

AU - Mann, Caroline

AU - Andrews, Derek Sayre

AU - Daly, Eileen M

AU - Gudbrandsen, Maria

AU - Ruigrok, Amber N. V.

AU - Dallyn, Robert

AU - Romero-Garcia, Rafael

AU - Lai, Meng-Chuan

AU - Lombardo, Michael V.

AU - Craig, Michael C.

AU - Suckling, John

AU - Bullmore, Edward T.

AU - Baron-Cohen, Simon

AU - Murphy, Declan G. M.

AU - Dell'Acqua, Flavio

AU - Ecker, Christine

PY - 2021/2/1

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N2 - 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.

AB - 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.

KW - diffusion tensor imaging

KW - multimodal imaging

KW - myelinated and unmyelinated gray matter

KW - superficial white matter

U2 - 10.1002/hbm.25237

DO - 10.1002/hbm.25237

M3 - Article

C2 - 33094897

SN - 1065-9471

VL - 42

SP - 467

EP - 484

JO - HUMAN BRAIN MAPPING

JF - HUMAN BRAIN MAPPING

IS - 2

ER -