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; Rosemary Holt; Simon Baron-cohen; Sven Bölte; Sarah Durston; Prantik Kundu; Michael V. Lombardo; Will Spooren; Eva Loth; Declan G.M. Murphy; Christian F. Beckmann; Jan K. Buitelaar; EU-AIMS LEAP group; Jumana Ahmad; Sara Ambrosino; Bonnie Auyeung; Tobias Banaschewski; Simon Baron-cohen; Sarah Baumeister; Christian F. Beckmann; Sven Bölte; Thomas Bourgeron; Carsten Bours; Michael Brammer; Daniel Brandeis; Claudia Brogna; Tony Charman; Daisy Crawley; Christine Ecker; Jessica Faulkner; Hannah Hayward; Eva Loth; David J. Lythgoe; Andre Marquand; Declan G.m. Murphy; Bethany Oakley; Barbara Ruggeri; Antonia San José Cáceres; Emily Simonoff; Julian Tillmann; Steve C.R. Williams

doi: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

Marianne Oldehinkel, Maarten Mennes, Andre Marquand, Tony Charman, Julian Tillmann, Christine Ecker, Flavio Dell’acqua, Daniel Brandeis, Tobias Banaschewski, Sarah Baumeister, Carolin Moessnang, Rosemary Holt, Simon Baron-cohen, Sven Bölte, Sarah Durston, Prantik Kundu, Michael V. Lombardo, Will Spooren, Eva Loth, Declan G.M. MurphyChristian F. Beckmann, Jan K. Buitelaar, EU-AIMS LEAP group, Jumana Ahmad, Sara Ambrosino, Bonnie Auyeung, Tobias Banaschewski, Simon Baron-cohen, Sarah Baumeister, Christian F. Beckmann, Sven Bölte, Thomas Bourgeron, Carsten Bours, Michael Brammer, Daniel Brandeis, Claudia Brogna, Tony Charman, Daisy Crawley, Christine Ecker, Jessica Faulkner, Hannah Hayward, Eva Loth, David J. Lythgoe, Andre Marquand, Declan G.m. Murphy, Bethany Oakley, Barbara Ruggeri, Antonia San José Cáceres, Emily Simonoff, Julian Tillmann, Steve C.R. Williams

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

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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.

Original language	English
Pages (from-to)	260-270
Number of pages	11
Journal	Biological Psychiatry: Cognitive Neuroscience and Neuroimaging
Volume	4
Issue number	3
Early online date	5 Dec 2018
DOIs	https://doi.org/10.1016/j.bpsc.2018.11.010
Publication status	Published - Mar 2019

Keywords

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

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10.1016/j.bpsc.2018.11.010

Altered Connectivity Between Cerebellum_OLDEHINKEL_Publishedonline5December2018_GREEN AAM (CC BY-NC-ND)Accepted author manuscript, 4.31 MBLicence: CC BY-NC-ND

Cite this

Oldehinkel, M., Mennes, M., Marquand, A., Charman, T., Tillmann, J., Ecker, C., Dell’acqua, F., Brandeis, D., Banaschewski, T., Baumeister, S., Moessnang, C., Holt, R., Baron-cohen, S., Bölte, S., Durston, S., Kundu, P., Lombardo, M. V., Spooren, W., Loth, E., ... Williams, S. C. R. (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, 4(3), 260-270. https://doi.org/10.1016/j.bpsc.2018.11.010

@article{75bbe99bcacf4f278eadf3417545aac7,

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

abstract = "BackgroundResting-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.MethodsResting-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.ResultsHigher 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.ConclusionsWe 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{\textquoteright}acqua and Daniel Brandeis and Tobias Banaschewski and Sarah Baumeister and Carolin Moessnang and Rosemary Holt and Simon Baron-cohen 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.} and {EU-AIMS LEAP group} and Jumana Ahmad and Sara Ambrosino and Bonnie Auyeung and Tobias Banaschewski and Simon Baron-cohen and Sarah Baumeister and Beckmann, {Christian F.} and Sven B{\"o}lte and Thomas Bourgeron and Carsten Bours and Michael Brammer and Daniel Brandeis and Claudia Brogna and Tony Charman and Daisy Crawley and Christine Ecker and Jessica Faulkner and Hannah Hayward and Eva Loth and Lythgoe, {David J.} and Andre Marquand and Murphy, {Declan G.m.} and Bethany Oakley and Barbara Ruggeri and {San Jos{\'e} C{\'a}ceres}, Antonia and Emily Simonoff and Julian Tillmann and Williams, {Steve C.R.}",

year = "2019",

month = mar,

doi = "10.1016/j.bpsc.2018.11.010",

language = "English",

volume = "4",

pages = "260--270",

journal = "Biological Psychiatry: Cognitive Neuroscience and Neuroimaging",

issn = "2451-9022",

publisher = "Elsevier Inc.",

number = "3",

}

Oldehinkel, M, Mennes, M, Marquand, A , Charman, T , Tillmann, J , Ecker, C, Dell’acqua, F, Brandeis, D, Banaschewski, T, Baumeister, S, Moessnang, C, Holt, R, Baron-cohen, S, Bölte, S, Durston, S, Kundu, P, Lombardo, MV, Spooren, W, Loth, E , Murphy, DGM, Beckmann, CF, Buitelaar, JK, EU-AIMS LEAP group, Ahmad, J, Ambrosino, S, Auyeung, B, Banaschewski, T, Baron-cohen, S, Baumeister, S, Beckmann, CF, Bölte, S, Bourgeron, T, Bours, C, Brammer, M, Brandeis, D, Brogna, C, Charman, T , Crawley, D , Ecker, C , Faulkner, J , Hayward, H , Loth, E , Lythgoe, DJ , Marquand, A , Murphy, DGM , Oakley, B , Ruggeri, B , San José Cáceres, A , Simonoff, E , Tillmann, J & Williams, SCR 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 et al.
In: Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, Vol. 4, No. 3, 03.2019, p. 260-270.

Research output: Contribution to journal › Article › peer-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 - Holt, Rosemary

AU - Baron-cohen, Simon

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.

AU - EU-AIMS LEAP group

AU - Ahmad, Jumana

AU - Ambrosino, Sara

AU - Auyeung, Bonnie

AU - Banaschewski, Tobias

AU - Baron-cohen, Simon

AU - Baumeister, Sarah

AU - Beckmann, Christian F.

AU - Bölte, Sven

AU - Bourgeron, Thomas

AU - Bours, Carsten

AU - Brammer, Michael

AU - Brandeis, Daniel

AU - Brogna, Claudia

AU - Charman, Tony

AU - Crawley, Daisy

AU - Ecker, Christine

AU - Faulkner, Jessica

AU - Hayward, Hannah

AU - Loth, Eva

AU - Lythgoe, David J.

AU - Marquand, Andre

AU - Murphy, Declan G.m.

AU - Oakley, Bethany

AU - Ruggeri, Barbara

AU - San José Cáceres, Antonia

AU - Simonoff, Emily

AU - Tillmann, Julian

AU - Williams, Steve C.R.

PY - 2019/3

Y1 - 2019/3

N2 - BackgroundResting-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.MethodsResting-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.ResultsHigher 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.ConclusionsWe 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 - BackgroundResting-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.MethodsResting-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.ResultsHigher 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.ConclusionsWe 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

U2 - 10.1016/j.bpsc.2018.11.010

DO - 10.1016/j.bpsc.2018.11.010

M3 - Article

SN - 2451-9022

VL - 4

SP - 260

EP - 270

JO - Biological Psychiatry: Cognitive Neuroscience and Neuroimaging

JF - Biological Psychiatry: Cognitive Neuroscience and Neuroimaging

IS - 3

ER -

Oldehinkel M, Mennes M, Marquand A , Charman T , Tillmann J , Ecker C et al. 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. 2019 Mar;4(3):260-270. Epub 2018 Dec 5. doi: 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

Abstract

Keywords

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