Frontostriatal functional connectivity correlates with repetitive behaviour across autism spectrum disorder and obsessive-compulsive disorder

Sophie E.A. Akkermans, Nicole Rheinheimer, Muriel M.K. Bruchhage, Sarah Durston, Daniel Brandeis, Tobias Banaschewski, Regina Boecker-Schlier, Isabella Wolf, Steven C.R. Williams, Jan K. Buitelaar, Daan Van Rooij, Marianne Oldehinkel

Research output: Contribution to journalArticleResearchpeer-review

2 Citations (Scopus)

Abstract

BackgroundAutism spectrum disorder (ASD) and obsessive-compulsive disorder (OCD) are neurodevelopmental disorders with considerable overlap in terms of their defining symptoms of compulsivity/repetitive behaviour. Little is known about the extent to which ASD and OCD have common versus distinct neural correlates of compulsivity. Previous research points to potentially common dysfunction in frontostriatal connectivity, but direct comparisons in one study are lacking. Here, we assessed frontostriatal resting-state functional connectivity in youth with ASD or OCD, and healthy controls. In addition, we applied a cross-disorder approach to examine whether repetitive behaviour across ASD and OCD has common neural substrates.MethodsA sample of 78 children and adolescents aged 8-16 years was used (ASD n = 24; OCD n = 25; healthy controls n = 29), originating from the multicentre study COMPULS. We tested whether diagnostic group, repetitive behaviour (measured with the Repetitive Behavior Scale-Revised) or their interaction was associated with resting-state functional connectivity of striatal seed regions.ResultsNo diagnosis-specific differences were detected. The cross-disorder analysis, on the other hand, showed that increased functional connectivity between the left nucleus accumbens (NAcc) and a cluster in the right premotor cortex/middle frontal gyrus was related to more severe symptoms of repetitive behaviour.ConclusionsWe demonstrate the fruitfulness of applying a cross-disorder approach to investigate the neural underpinnings of compulsivity/repetitive behaviour, by revealing a shared alteration in functional connectivity in ASD and OCD. We argue that this alteration might reflect aberrant reward or motivational processing of the NAcc with excessive connectivity to the premotor cortex implementing learned action patterns.

Original languageEnglish
Pages (from-to)2247-2255
Number of pages9
JournalPsychological Medicine
Volume49
Issue number13
DOIs
Publication statusPublished - Oct 2019
Externally publishedYes

Keywords

  • Autism spectrum disorder (ASD)
  • compulsivity
  • frontostriatal circuits
  • functional connectivity
  • functional magnetic resonance imaging (fMRI)
  • nucleus accumbens
  • obsessive-compulsive disorder (OCD)
  • repetitive behaviour
  • resting state
  • striatum
  • transdiagnostic

Cite this

Akkermans, Sophie E.A. ; Rheinheimer, Nicole ; Bruchhage, Muriel M.K. ; Durston, Sarah ; Brandeis, Daniel ; Banaschewski, Tobias ; Boecker-Schlier, Regina ; Wolf, Isabella ; Williams, Steven C.R. ; Buitelaar, Jan K. ; Van Rooij, Daan ; Oldehinkel, Marianne. / Frontostriatal functional connectivity correlates with repetitive behaviour across autism spectrum disorder and obsessive-compulsive disorder. In: Psychological Medicine. 2019 ; Vol. 49, No. 13. pp. 2247-2255.
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title = "Frontostriatal functional connectivity correlates with repetitive behaviour across autism spectrum disorder and obsessive-compulsive disorder",
abstract = "BackgroundAutism spectrum disorder (ASD) and obsessive-compulsive disorder (OCD) are neurodevelopmental disorders with considerable overlap in terms of their defining symptoms of compulsivity/repetitive behaviour. Little is known about the extent to which ASD and OCD have common versus distinct neural correlates of compulsivity. Previous research points to potentially common dysfunction in frontostriatal connectivity, but direct comparisons in one study are lacking. Here, we assessed frontostriatal resting-state functional connectivity in youth with ASD or OCD, and healthy controls. In addition, we applied a cross-disorder approach to examine whether repetitive behaviour across ASD and OCD has common neural substrates.MethodsA sample of 78 children and adolescents aged 8-16 years was used (ASD n = 24; OCD n = 25; healthy controls n = 29), originating from the multicentre study COMPULS. We tested whether diagnostic group, repetitive behaviour (measured with the Repetitive Behavior Scale-Revised) or their interaction was associated with resting-state functional connectivity of striatal seed regions.ResultsNo diagnosis-specific differences were detected. The cross-disorder analysis, on the other hand, showed that increased functional connectivity between the left nucleus accumbens (NAcc) and a cluster in the right premotor cortex/middle frontal gyrus was related to more severe symptoms of repetitive behaviour.ConclusionsWe demonstrate the fruitfulness of applying a cross-disorder approach to investigate the neural underpinnings of compulsivity/repetitive behaviour, by revealing a shared alteration in functional connectivity in ASD and OCD. We argue that this alteration might reflect aberrant reward or motivational processing of the NAcc with excessive connectivity to the premotor cortex implementing learned action patterns.",
keywords = "Autism spectrum disorder (ASD), compulsivity, frontostriatal circuits, functional connectivity, functional magnetic resonance imaging (fMRI), nucleus accumbens, obsessive-compulsive disorder (OCD), repetitive behaviour, resting state, striatum, transdiagnostic",
author = "Akkermans, {Sophie E.A.} and Nicole Rheinheimer and Bruchhage, {Muriel M.K.} and Sarah Durston and Daniel Brandeis and Tobias Banaschewski and Regina Boecker-Schlier and Isabella Wolf and Williams, {Steven C.R.} and Buitelaar, {Jan K.} and {Van Rooij}, Daan and Marianne Oldehinkel",
year = "2019",
month = "10",
doi = "10.1017/S0033291718003136",
language = "English",
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pages = "2247--2255",
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Akkermans, SEA, Rheinheimer, N, Bruchhage, MMK, Durston, S, Brandeis, D, Banaschewski, T, Boecker-Schlier, R, Wolf, I, Williams, SCR, Buitelaar, JK, Van Rooij, D & Oldehinkel, M 2019, 'Frontostriatal functional connectivity correlates with repetitive behaviour across autism spectrum disorder and obsessive-compulsive disorder', Psychological Medicine, vol. 49, no. 13, pp. 2247-2255. https://doi.org/10.1017/S0033291718003136

Frontostriatal functional connectivity correlates with repetitive behaviour across autism spectrum disorder and obsessive-compulsive disorder. / Akkermans, Sophie E.A.; Rheinheimer, Nicole; Bruchhage, Muriel M.K.; Durston, Sarah; Brandeis, Daniel; Banaschewski, Tobias; Boecker-Schlier, Regina; Wolf, Isabella; Williams, Steven C.R.; Buitelaar, Jan K.; Van Rooij, Daan; Oldehinkel, Marianne.

In: Psychological Medicine, Vol. 49, No. 13, 10.2019, p. 2247-2255.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Frontostriatal functional connectivity correlates with repetitive behaviour across autism spectrum disorder and obsessive-compulsive disorder

AU - Akkermans, Sophie E.A.

AU - Rheinheimer, Nicole

AU - Bruchhage, Muriel M.K.

AU - Durston, Sarah

AU - Brandeis, Daniel

AU - Banaschewski, Tobias

AU - Boecker-Schlier, Regina

AU - Wolf, Isabella

AU - Williams, Steven C.R.

AU - Buitelaar, Jan K.

AU - Van Rooij, Daan

AU - Oldehinkel, Marianne

PY - 2019/10

Y1 - 2019/10

N2 - BackgroundAutism spectrum disorder (ASD) and obsessive-compulsive disorder (OCD) are neurodevelopmental disorders with considerable overlap in terms of their defining symptoms of compulsivity/repetitive behaviour. Little is known about the extent to which ASD and OCD have common versus distinct neural correlates of compulsivity. Previous research points to potentially common dysfunction in frontostriatal connectivity, but direct comparisons in one study are lacking. Here, we assessed frontostriatal resting-state functional connectivity in youth with ASD or OCD, and healthy controls. In addition, we applied a cross-disorder approach to examine whether repetitive behaviour across ASD and OCD has common neural substrates.MethodsA sample of 78 children and adolescents aged 8-16 years was used (ASD n = 24; OCD n = 25; healthy controls n = 29), originating from the multicentre study COMPULS. We tested whether diagnostic group, repetitive behaviour (measured with the Repetitive Behavior Scale-Revised) or their interaction was associated with resting-state functional connectivity of striatal seed regions.ResultsNo diagnosis-specific differences were detected. The cross-disorder analysis, on the other hand, showed that increased functional connectivity between the left nucleus accumbens (NAcc) and a cluster in the right premotor cortex/middle frontal gyrus was related to more severe symptoms of repetitive behaviour.ConclusionsWe demonstrate the fruitfulness of applying a cross-disorder approach to investigate the neural underpinnings of compulsivity/repetitive behaviour, by revealing a shared alteration in functional connectivity in ASD and OCD. We argue that this alteration might reflect aberrant reward or motivational processing of the NAcc with excessive connectivity to the premotor cortex implementing learned action patterns.

AB - BackgroundAutism spectrum disorder (ASD) and obsessive-compulsive disorder (OCD) are neurodevelopmental disorders with considerable overlap in terms of their defining symptoms of compulsivity/repetitive behaviour. Little is known about the extent to which ASD and OCD have common versus distinct neural correlates of compulsivity. Previous research points to potentially common dysfunction in frontostriatal connectivity, but direct comparisons in one study are lacking. Here, we assessed frontostriatal resting-state functional connectivity in youth with ASD or OCD, and healthy controls. In addition, we applied a cross-disorder approach to examine whether repetitive behaviour across ASD and OCD has common neural substrates.MethodsA sample of 78 children and adolescents aged 8-16 years was used (ASD n = 24; OCD n = 25; healthy controls n = 29), originating from the multicentre study COMPULS. We tested whether diagnostic group, repetitive behaviour (measured with the Repetitive Behavior Scale-Revised) or their interaction was associated with resting-state functional connectivity of striatal seed regions.ResultsNo diagnosis-specific differences were detected. The cross-disorder analysis, on the other hand, showed that increased functional connectivity between the left nucleus accumbens (NAcc) and a cluster in the right premotor cortex/middle frontal gyrus was related to more severe symptoms of repetitive behaviour.ConclusionsWe demonstrate the fruitfulness of applying a cross-disorder approach to investigate the neural underpinnings of compulsivity/repetitive behaviour, by revealing a shared alteration in functional connectivity in ASD and OCD. We argue that this alteration might reflect aberrant reward or motivational processing of the NAcc with excessive connectivity to the premotor cortex implementing learned action patterns.

KW - Autism spectrum disorder (ASD)

KW - compulsivity

KW - frontostriatal circuits

KW - functional connectivity

KW - functional magnetic resonance imaging (fMRI)

KW - nucleus accumbens

KW - obsessive-compulsive disorder (OCD)

KW - repetitive behaviour

KW - resting state

KW - striatum

KW - transdiagnostic

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U2 - 10.1017/S0033291718003136

DO - 10.1017/S0033291718003136

M3 - Article

VL - 49

SP - 2247

EP - 2255

JO - Psychological Medicine

JF - Psychological Medicine

SN - 0033-2917

IS - 13

ER -