Altered Connectivity Between Cerebellum, Visual, and Sensory-Motor Networks in Autism Spectrum Disorder: Results from the EU-AIMS Longitudinal European Autism Project

Marianne Oldehinkel, Maarten Mennes, Andre Marquand, Tony Charman, Julian Tillmann, Christine Ecker, Flavio Dell'Acqua, Daniel Brandeis, Tobias Banaschewski, Sarah Baumeister, Carolin Moessnang, Simon Baron-Cohen, Rosemary Holt, Sven Bölte, Sarah Durston, Prantik Kundu, Michael V. Lombardo, Will Spooren, Eva Loth, Declan G.M. Murphy & 2 others Christian F. Beckmann, Jan K. Buitelaar

Research output: Contribution to journalArticleResearchpeer-review

Abstract

Background: Resting-state functional magnetic resonance imaging–based studies on functional connectivity in autism spectrum disorder (ASD) have generated inconsistent results. Interpretation of findings is further hampered by small samples and a focus on a limited number of networks, with networks underlying sensory processing being largely underexamined. We aimed to comprehensively characterize ASD-related alterations within and between 20 well-characterized resting-state networks using baseline data from the EU-AIMS (European Autism Interventions—A Multicentre Study for Developing New Medications) Longitudinal European Autism Project. Methods: Resting-state functional magnetic resonance imaging data was available for 265 individuals with ASD (7.5–30.3 years; 73.2% male) and 218 typically developing individuals (6.9–29.8 years; 64.2% male), all with IQ > 70. We compared functional connectivity within 20 networks—obtained using independent component analysis—between the ASD and typically developing groups, and related functional connectivity within these networks to continuous (overall) autism trait severity scores derived from the Social Responsiveness Scale Second Edition across all participants. Furthermore, we investigated case-control differences and autism trait–related alterations in between-network connectivity. Results: Higher autism traits were associated with increased connectivity within salience, medial motor, and orbitofrontal networks. However, we did not replicate previously reported case-control differences within these networks. The between-network analysis did reveal case-control differences showing on average 1) decreased connectivity of the visual association network with somatosensory, medial, and lateral motor networks, and 2) increased connectivity of the cerebellum with these sensory and motor networks in ASD compared with typically developing subjects. Conclusions: We demonstrate ASD-related alterations in within- and between-network connectivity. The between-network alterations broadly affect connectivity between cerebellum, visual, and sensory-motor networks, potentially underlying impairments in multisensory and visual-motor integration frequently observed in ASD.

Original languageEnglish
Pages (from-to)260-270
Number of pages11
JournalBiological Psychiatry: Cognitive Neuroscience and Neuroimaging
Volume4
Issue number3
DOIs
Publication statusPublished - Mar 2019

Keywords

  • Autism
  • Cerebellum
  • Functional connectivity
  • Resting-state fMRI
  • Sensory networks
  • Visual-motor integration

Cite this

Oldehinkel, Marianne ; Mennes, Maarten ; Marquand, Andre ; Charman, Tony ; Tillmann, Julian ; Ecker, Christine ; Dell'Acqua, Flavio ; Brandeis, Daniel ; Banaschewski, Tobias ; Baumeister, Sarah ; Moessnang, Carolin ; Baron-Cohen, Simon ; Holt, Rosemary ; Bölte, Sven ; Durston, Sarah ; Kundu, Prantik ; Lombardo, Michael V. ; Spooren, Will ; Loth, Eva ; Murphy, Declan G.M. ; Beckmann, Christian F. ; Buitelaar, Jan K. / Altered Connectivity Between Cerebellum, Visual, and Sensory-Motor Networks in Autism Spectrum Disorder : Results from the EU-AIMS Longitudinal European Autism Project. In: Biological Psychiatry: Cognitive Neuroscience and Neuroimaging. 2019 ; Vol. 4, No. 3. pp. 260-270.
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abstract = "Background: Resting-state functional magnetic resonance imaging–based studies on functional connectivity in autism spectrum disorder (ASD) have generated inconsistent results. Interpretation of findings is further hampered by small samples and a focus on a limited number of networks, with networks underlying sensory processing being largely underexamined. We aimed to comprehensively characterize ASD-related alterations within and between 20 well-characterized resting-state networks using baseline data from the EU-AIMS (European Autism Interventions—A Multicentre Study for Developing New Medications) Longitudinal European Autism Project. Methods: Resting-state functional magnetic resonance imaging data was available for 265 individuals with ASD (7.5–30.3 years; 73.2{\%} male) and 218 typically developing individuals (6.9–29.8 years; 64.2{\%} male), all with IQ > 70. We compared functional connectivity within 20 networks—obtained using independent component analysis—between the ASD and typically developing groups, and related functional connectivity within these networks to continuous (overall) autism trait severity scores derived from the Social Responsiveness Scale Second Edition across all participants. Furthermore, we investigated case-control differences and autism trait–related alterations in between-network connectivity. Results: Higher autism traits were associated with increased connectivity within salience, medial motor, and orbitofrontal networks. However, we did not replicate previously reported case-control differences within these networks. The between-network analysis did reveal case-control differences showing on average 1) decreased connectivity of the visual association network with somatosensory, medial, and lateral motor networks, and 2) increased connectivity of the cerebellum with these sensory and motor networks in ASD compared with typically developing subjects. Conclusions: We demonstrate ASD-related alterations in within- and between-network connectivity. The between-network alterations broadly affect connectivity between cerebellum, visual, and sensory-motor networks, potentially underlying impairments in multisensory and visual-motor integration frequently observed in ASD.",
keywords = "Autism, Cerebellum, Functional connectivity, Resting-state fMRI, Sensory networks, Visual-motor integration",
author = "Marianne Oldehinkel and Maarten Mennes and Andre Marquand and Tony Charman and Julian Tillmann and Christine Ecker and Flavio Dell'Acqua and Daniel Brandeis and Tobias Banaschewski and Sarah Baumeister and Carolin Moessnang and Simon Baron-Cohen and Rosemary Holt and Sven B{\"o}lte and Sarah Durston and Prantik Kundu and Lombardo, {Michael V.} and Will Spooren and Eva Loth and Murphy, {Declan G.M.} and Beckmann, {Christian F.} and Buitelaar, {Jan K.}",
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Oldehinkel, M, Mennes, M, Marquand, A, Charman, T, Tillmann, J, Ecker, C, Dell'Acqua, F, Brandeis, D, Banaschewski, T, Baumeister, S, Moessnang, C, Baron-Cohen, S, Holt, R, Bölte, S, Durston, S, Kundu, P, Lombardo, MV, Spooren, W, Loth, E, Murphy, DGM, Beckmann, CF & Buitelaar, JK 2019, 'Altered Connectivity Between Cerebellum, Visual, and Sensory-Motor Networks in Autism Spectrum Disorder: Results from the EU-AIMS Longitudinal European Autism Project' Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, vol. 4, no. 3, pp. 260-270. https://doi.org/10.1016/j.bpsc.2018.11.010

Altered Connectivity Between Cerebellum, Visual, and Sensory-Motor Networks in Autism Spectrum Disorder : Results from the EU-AIMS Longitudinal European Autism Project. / Oldehinkel, Marianne; Mennes, Maarten; Marquand, Andre; Charman, Tony; Tillmann, Julian; Ecker, Christine; Dell'Acqua, Flavio; Brandeis, Daniel; Banaschewski, Tobias; Baumeister, Sarah; Moessnang, Carolin; Baron-Cohen, Simon; Holt, Rosemary; Bölte, Sven; Durston, Sarah; Kundu, Prantik; Lombardo, Michael V.; Spooren, Will; Loth, Eva; Murphy, Declan G.M.; Beckmann, Christian F.; Buitelaar, Jan K.

In: Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, Vol. 4, No. 3, 03.2019, p. 260-270.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Altered Connectivity Between Cerebellum, Visual, and Sensory-Motor Networks in Autism Spectrum Disorder

T2 - Results from the EU-AIMS Longitudinal European Autism Project

AU - Oldehinkel, Marianne

AU - Mennes, Maarten

AU - Marquand, Andre

AU - Charman, Tony

AU - Tillmann, Julian

AU - Ecker, Christine

AU - Dell'Acqua, Flavio

AU - Brandeis, Daniel

AU - Banaschewski, Tobias

AU - Baumeister, Sarah

AU - Moessnang, Carolin

AU - Baron-Cohen, Simon

AU - Holt, Rosemary

AU - Bölte, Sven

AU - Durston, Sarah

AU - Kundu, Prantik

AU - Lombardo, Michael V.

AU - Spooren, Will

AU - Loth, Eva

AU - Murphy, Declan G.M.

AU - Beckmann, Christian F.

AU - Buitelaar, Jan K.

PY - 2019/3

Y1 - 2019/3

N2 - Background: Resting-state functional magnetic resonance imaging–based studies on functional connectivity in autism spectrum disorder (ASD) have generated inconsistent results. Interpretation of findings is further hampered by small samples and a focus on a limited number of networks, with networks underlying sensory processing being largely underexamined. We aimed to comprehensively characterize ASD-related alterations within and between 20 well-characterized resting-state networks using baseline data from the EU-AIMS (European Autism Interventions—A Multicentre Study for Developing New Medications) Longitudinal European Autism Project. Methods: Resting-state functional magnetic resonance imaging data was available for 265 individuals with ASD (7.5–30.3 years; 73.2% male) and 218 typically developing individuals (6.9–29.8 years; 64.2% male), all with IQ > 70. We compared functional connectivity within 20 networks—obtained using independent component analysis—between the ASD and typically developing groups, and related functional connectivity within these networks to continuous (overall) autism trait severity scores derived from the Social Responsiveness Scale Second Edition across all participants. Furthermore, we investigated case-control differences and autism trait–related alterations in between-network connectivity. Results: Higher autism traits were associated with increased connectivity within salience, medial motor, and orbitofrontal networks. However, we did not replicate previously reported case-control differences within these networks. The between-network analysis did reveal case-control differences showing on average 1) decreased connectivity of the visual association network with somatosensory, medial, and lateral motor networks, and 2) increased connectivity of the cerebellum with these sensory and motor networks in ASD compared with typically developing subjects. Conclusions: We demonstrate ASD-related alterations in within- and between-network connectivity. The between-network alterations broadly affect connectivity between cerebellum, visual, and sensory-motor networks, potentially underlying impairments in multisensory and visual-motor integration frequently observed in ASD.

AB - Background: Resting-state functional magnetic resonance imaging–based studies on functional connectivity in autism spectrum disorder (ASD) have generated inconsistent results. Interpretation of findings is further hampered by small samples and a focus on a limited number of networks, with networks underlying sensory processing being largely underexamined. We aimed to comprehensively characterize ASD-related alterations within and between 20 well-characterized resting-state networks using baseline data from the EU-AIMS (European Autism Interventions—A Multicentre Study for Developing New Medications) Longitudinal European Autism Project. Methods: Resting-state functional magnetic resonance imaging data was available for 265 individuals with ASD (7.5–30.3 years; 73.2% male) and 218 typically developing individuals (6.9–29.8 years; 64.2% male), all with IQ > 70. We compared functional connectivity within 20 networks—obtained using independent component analysis—between the ASD and typically developing groups, and related functional connectivity within these networks to continuous (overall) autism trait severity scores derived from the Social Responsiveness Scale Second Edition across all participants. Furthermore, we investigated case-control differences and autism trait–related alterations in between-network connectivity. Results: Higher autism traits were associated with increased connectivity within salience, medial motor, and orbitofrontal networks. However, we did not replicate previously reported case-control differences within these networks. The between-network analysis did reveal case-control differences showing on average 1) decreased connectivity of the visual association network with somatosensory, medial, and lateral motor networks, and 2) increased connectivity of the cerebellum with these sensory and motor networks in ASD compared with typically developing subjects. Conclusions: We demonstrate ASD-related alterations in within- and between-network connectivity. The between-network alterations broadly affect connectivity between cerebellum, visual, and sensory-motor networks, potentially underlying impairments in multisensory and visual-motor integration frequently observed in ASD.

KW - Autism

KW - Cerebellum

KW - Functional connectivity

KW - Resting-state fMRI

KW - Sensory networks

KW - Visual-motor integration

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