Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-21T15:47:22.024Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  26 October 2018

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  and
Jan K. Buitelaar
...Show all authors
Sophie E.A. Akkermans*
Affiliation:
Department of Cognitive Neuroscience, Radboud University Medical Center, Donders Institute for Brain, Cognition and Behaviour, Nijmegen, The Netherlands Radboud University, Donders Institute for Brain, Cognition and Behaviour, Centre for Cognitive Neuroimaging, Nijmegen, The Netherlands
Nicole Rheinheimer
Affiliation:
Department of Cognitive Neuroscience, Radboud University Medical Center, Donders Institute for Brain, Cognition and Behaviour, Nijmegen, The Netherlands Radboud University, Donders Institute for Brain, Cognition and Behaviour, Centre for Cognitive Neuroimaging, Nijmegen, The Netherlands
Muriel M.K. Bruchhage
Affiliation:
Department of Neuroimaging, King's College London, Institute of Psychiatry, Psychology, and Neuroscience, London, UK
Sarah Durston
Affiliation:
NICHE Lab, Department of Psychiatry, Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht, The Netherlands
Daniel Brandeis
Affiliation:
Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Mannheim, Germany
Tobias Banaschewski
Affiliation:
Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Mannheim, Germany
Regina Boecker-Schlier
Affiliation:
Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Mannheim, Germany
Isabella Wolf
Affiliation:
Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Mannheim, Germany
Steven C.R. Williams
Affiliation:
Department of Neuroimaging, King's College London, Institute of Psychiatry, Psychology, and Neuroscience, London, UK
Jan K. Buitelaar
Affiliation:
Department of Cognitive Neuroscience, Radboud University Medical Center, Donders Institute for Brain, Cognition and Behaviour, Nijmegen, The Netherlands Radboud University, Donders Institute for Brain, Cognition and Behaviour, Centre for Cognitive Neuroimaging, Nijmegen, The Netherlands Karakter Child and Adolescent Psychiatry University Centre, Nijmegen, The Netherlands
Daan van Rooij
Affiliation:
Department of Cognitive Neuroscience, Radboud University Medical Center, Donders Institute for Brain, Cognition and Behaviour, Nijmegen, The Netherlands Radboud University, Donders Institute for Brain, Cognition and Behaviour, Centre for Cognitive Neuroimaging, Nijmegen, The Netherlands
Marianne Oldehinkel
Affiliation:
Department of Cognitive Neuroscience, Radboud University Medical Center, Donders Institute for Brain, Cognition and Behaviour, Nijmegen, The Netherlands Radboud University, Donders Institute for Brain, Cognition and Behaviour, Centre for Cognitive Neuroimaging, Nijmegen, The Netherlands
*
Author for correspondence: Sophie E.A. Akkermans, E-mail: s.akkermans@donders.ru.nl
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Autism 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.

Methods

A 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.

Results

No 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.

Conclusions

We 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)compulsivityfrontostriatal circuitsfunctional connectivityfunctional magnetic resonance imaging (fMRI)nucleus accumbensobsessive–compulsive disorder (OCD)repetitive behaviourresting statestriatumtransdiagnostic
Type
Original Articles
Information
Psychological Medicine , Volume 49 , Issue 13 , October 2019 , pp. 2247 - 2255
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

van Rooij and Oldehinkel share last authorship.

†

Members of the TACTICS consortium are listed in the acknowledgements.

References

Abe, Y, Sakai, Y, Nishida, S, Nakamae, T, Yamada, K, Fukui, K and Narumoto, J (2015) Hyper-influence of the orbitofrontal cortex over the ventral striatum in obsessive-compulsive disorder. European Neuropsychopharmacology 25, 1898–1905.Google Scholar
Achenbach, TM and Rescorla, LA (2001) Manual for the ASEBA School-age Forms & Profiles. Burlington, VT: University of Vermont, Research Center for Children, Youth, & Families.Google Scholar
Alexander, GE, DeLong, MR and Strick, PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annual Review of Neuroscience 9, 357–381.Google Scholar
American Psychiatric Association (2000) Diagnostic and Statistical Manual of Mental Disorders, 4th Edn. (text rev.). Washington, DC: American Psychiatric Association.Google Scholar
Andersson, JLR, Jenkinson, M and Smith, S (2010) Non-linear registration, aka spatial normalisation. FMRIB technical report TR07JA2.Google Scholar
Bernstein, GA, Mueller, BA, Schreiner, MW, Campbell, SM, Regan, EK, Nelson, PM, Houri, AK, Lee, SS, Zagoloff, AD, Lim, KO, Yacoub, ES and Cullen, KR (2016) Abnormal striatal resting-state functional connectivity in adolescents with obsessive-compulsive disorder. Psychiatry Research: Neuroimaging 247, 49–56.Google Scholar
Carlisi, CO, Norman, L, Murphy, CM, Christakou, A, Chantiluke, K, Giampietro, V, Simmons, A, Brammer, M, Murphy, DG, MRC AIMS consortium, Mataix-Cols, D and Rubia, K (2017 a) Comparison of neural substrates of temporal discounting between youth with autism spectrum disorder and with obsessive-compulsive disorder. Psychological Medicine 47, 2513–2527.Google Scholar
Carlisi, CO, Norman, L, Murphy, CM, Christakou, A, Chantiluke, K, Giampietro, V, Simmons, A, Brammer, M, Murphy, DG, Mataix-Cols, D and Rubia, K, MRC AIMS consortium (2017 b) Shared and disorder-specific neurocomputational mechanisms of decision-making in autism spectrum disorder and obsessive-compulsive disorder. Cerebral Cortex 27, 5804–5816.Google Scholar
Chauvin, RJ, Mennes, M, Buitelaar, JK and Beckmann, CF (2017) Assessing age-dependent multi-task functional co-activation changes using measures of task-potency. Developmental Cognitive Neuroscience, in press, doi: 10.1016/j.dcn.2017.11.011.Google Scholar
de Wit, SJ, de Vries, FE, van der Werf, YD, Cath, DC, Heslenfeld, DJ, Veltman, EM, van Balkom, AJLM, Veltman, DJ and van den Heuvel, OA (2012) Presupplementary motor area hyperactivity during response inhibition: a candidate endophenotype of obsessive-compulsive disorder. The American Journal of Psychiatry 169, 1100–1108.Google Scholar
Del Casale, A, Rapinesi, C, Kotzalidis, GD, De Rossi, P, Curto, M, Janiri, D, Criscuolo, S, Alessi, MC, Ferri, VR, De Giorgi, R, Sani, G, Ferracuti, S, Girardi, P and Brugnoli, R (2016) Executive functions in obsessive–compulsive disorder: an activation likelihood estimate meta-analysis of fMRI studies. The World Journal of Biological Psychiatry 17, 378–393.Google Scholar
Delmonte, S, Gallagher, L, O'Hanlon, E, McGrath, J and Balsters, JH (2013) Functional and structural connectivity of frontostriatal circuitry in autism spectrum disorder. Frontiers in Human Neuroscience 7, 430.Google Scholar
Di Martino, A, Scheres, A, Margulies, DS, Kelly, AMC, Uddin, LQ, Shehzad, Z, Biswal, B, Walters, JR, Castellanos, FX and Milham, MP (2008) Functional connectivity of human striatum: a resting state fMRI study. Cerebral Cortex 18, 2735–2747.Google Scholar
Dichter, GS, Felder, JN, Green, SR, Rittenberg, AM, Sasson, NJ and Bodfish, JW (2012a) Reward circuitry function in autism spectrum disorders. Social Cognitive and Affective Neuroscience 7, 160–172.Google Scholar
Dichter, GS, Richey, JA, Rittenberg, AM, Sabatino, A and Bodfish, JW (2012b) Reward circuitry function in autism during face anticipation and outcomes. Journal of Autism and Developmental Disorders 42, 147–160.Google Scholar
Durston, S and Casey, BJ (2006) What have we learned about cognitive development from neuroimaging? Neuropsychologia 44, 2149–2157.Google Scholar
Figee, M, Vink, M, de Geus, F, Vulink, N, Veltman, DJ, Westenberg, H and Denys, D (2011) Dysfunctional reward circuitry in obsessive-compulsive disorder. Biological Psychiatry 69, 867–874.Google Scholar
Figee, M, Luigjes, J, Smolders, R, Valencia-Alfonso, C-E, van Wingen, G, de Kwaasteniet, B, Mantione, M, Ooms, P, de Koning, P, Vulink, N, Levar, N, Droge, L, van den Munckhof, P, Schuurman, PR, Nederveen, A, van den Brink, W, Mazaheri, A, Vink, M and Denys, D (2013) Deep brain stimulation restores frontostriatal network activity in obsessive-compulsive disorder. Nature Neuroscience 16, 386–387.Google Scholar
Fineberg, NA, Chamberlain, SR, Goudriaan, AE, Stein, DJ, Vanderschuren, LJMJ, Gillan, CM, Shekar, S, Gorwood, PAPM, Voon, V, Morein-Zamir, S, Denys, D, Sahakian, BJ, Moeller, FG, Robbins, TW and Potenza, MN (2014) New developments in human neurocognition: clinical, genetic and brain imaging correlates of impulsivity and compulsivity. CNS Spectrums 19, 69–89.Google Scholar
Greve, DN and Fischl, B (2009) Accurate and robust brain image alignment using boundary-based registration. NeuroImage 48, 63–72.Google Scholar
Guo, K, Youssef, GJ, Dawson, A, Parkes, L, Oostermeijer, S, López-Solà, C, Lorenzetti, V, Greenwood, C, Fontenelle, LF and Yücel, M (2017) A psychometric validation study of the Impulsive-Compulsive Behaviours Checklist: a transdiagnostic tool for addictive and compulsive behaviours. Addictive Behaviors 67, 26–33.Google Scholar
Haber, SN (2003) The primate basal ganglia: parallel and integrative networks. Journal of Chemical Neuroanatomy 26, 317–330.Google Scholar
Harrison, BJ, Soriano-Mas, C, Pujol, J, Ortiz, H, López-Solà, M, Hernández-Ribas, R, Deus, J, Alonso, P, Yücel, M, Pantelis, C, Menchon, JM and Cardoner, N (2009) Altered corticostriatal functional connectivity in obsessive-compulsive disorder. Archives of General Psychiatry 66, 1189–1200.Google Scholar
Harrison, BJ, Pujol, J, Cardoner, N, Deus, J, Alonso, P, López-Solà, M, Contreras-Rodríguez, O, Real, E, Segalàs, C, Blanco-Hinojo, L, Menchon, JM and Soriano-Mas, C (2013) Brain corticostriatal systems and the major clinical symptom dimensions of obsessive-compulsive disorder. Biological Psychiatry 73, 321–328.Google Scholar
Helmich, RC, Derikx, LC, Bakker, M, Scheeringa, R, Bloem, BR and Toni, I (2010) Spatial remapping of cortico-striatal connectivity in Parkinson's disease. Cerebral Cortex 20, 1175–1186.Google Scholar
Ho, DE, Imai, K, King, G and Stuart, EA (2011) Matchit: nonparametric preprocessing for parametric causal inference. Journal of Statistical Software 42, 1–28.Google Scholar
Hou, J, Song, L, Zhang, W, Wu, W, Wang, J, Zhou, D, Qu, W, Guo, J, Gu, S, He, M, Xie, B and Li, H (2013) Morphologic and functional connectivity alterations of corticostriatal and default mode network in treatment-naïve patients with obsessive-compulsive disorder. PLoS ONE 8, e83931.Google Scholar
Itahashi, T, Yamada, T, Watanabe, H, Nakamura, M, Ohta, H, Kanai, C, Iwanami, A, Kato, N and Hashimoto, R (2015) Alterations of local spontaneous brain activity and connectivity in adults with high-functioning autism spectrum disorder. Molecular Autism 6, 30.Google Scholar
Jack, CR, Bernstein, MA, Fox, NC, Thompson, P, Alexander, G, Harvey, D, Borowski, B, Britson, PJ, Whitwell, JL, Ward, C, Dale, AM, Felmlee, JP, Gunter, JL, Hill, DLG, Killiany, R, Schuff, N, Fox-Bosetti, S, Lin, C, Studholme, C, DeCarli, CS, Krueger, G, Ward, HA, Metzger, GJ, Scott, KT, Mallozzi, R, Blezek, D, Levy, J, Debbins, JP, Fleisher, AS, Albert, M, Green, R, Bartzokis, G, Glover, G and Mugler, J, Weiner MW for the ADNI study (2008) The Alzheimer's Disease Neuroimaging Initiative (ADNI): MRI methods. Journal of Magnetic Resonance Imaging 27, 685–691.Google Scholar
Jenkinson, M, Bannister, P, Brady, M and Smith, S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage 17, 825–841.Google Scholar
Jiujias, M, Kelley, E and Hall, L (2017) Restricted, repetitive behaviors in autism spectrum disorder and obsessive–compulsive disorder: a comparative review. Child Psychiatry & Human Development 48, 944–959.Google Scholar
Jung, WH, Kang, D-H, Kim, E, Shin, KS, Jang, JH and Kwon, JS (2013) Abnormal corticostriatal-limbic functional connectivity in obsessive-compulsive disorder during reward processing and resting-state. NeuroImage: Clinical 3, 27–38.Google Scholar
Kaufman, J, Birmaher, B, Brent, D, Rao, U, Flynn, C, Moreci, P, Williamson, D and Ryan, N (1997) Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): initial reliability and validity data. Journal of the American Academy of Child & Adolescent Psychiatry 36, 980–988.Google Scholar
Kohls, G, Schulte-Rüther, M, Nehrkorn, B, Müller, K, Fink, GR, Kamp-Becker, I, Herpertz-Dahlmann, B, Schultz, RT and Konrad, K (2013) Reward system dysfunction in autism spectrum disorders. Social Cognitive and Affective Neuroscience 8, 565–572.Google Scholar
Kundu, P, Inati, SJ, Evans, JW, Luh, W-M and Bandettini, PA (2012) Differentiating BOLD and non-BOLD signals in fMRI time series using multi-echo EPI. NeuroImage 60, 1759–1770.Google Scholar
Lai, M-C, Lombardo, MV and Baron-Cohen, S (2014) Autism. The Lancet 383, 896–910.Google Scholar
Lam, KSL and Aman, MG (2007) The Repetitive Behavior Scale-Revised: independent validation in individuals with autism spectrum disorders. Journal of Autism and Developmental Disorders 37, 855–866.Google Scholar
Langen, M, Durston, S, Kas, MJH, van Engeland, H and Staal, WG (2011) The neurobiology of repetitive behavior: …and men. Neuroscience and Biobehavioral Reviews 35, 356–365.Google Scholar
Lázaro, L, Caldú, X, Junqué, C, Bargalló, N, Andrés, S, Morer, A and Castro-Fornieles, J (2008) Cerebral activation in children and adolescents with obsessive-compulsive disorder before and after treatment: a functional MRI study. Journal of Psychiatric Research 42, 1051–1059.Google Scholar
Leisman, G, Moustafa, A and Shafir, T (2016) Thinking, walking, talking: integratory motor and cognitive brain function. Frontiers in Public Health 4, 94.Google Scholar
Leyfer, OT, Folstein, SE, Bacalman, S, Davis, NO, Dinh, E, Morgan, J, Tager-Flusberg, H and Lainhart, JE (2006) Comorbid psychiatric disorders in children with autism: interview development and rates of disorders. Journal of Autism and Developmental Disorders 36, 849–861.Google Scholar
Lord, C, Rutter, M and Le Couteur, A (1994) Autism Diagnostic Interview – Revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Journal of Autism and Developmental Disorders 24, 659–685.Google Scholar
Meier, SM, Petersen, L, Schendel, DE, Mattheisen, M, Mortensen, PB and Mors, O (2015) Obsessive-compulsive disorder and autism spectrum disorders: longitudinal and offspring risk. PLoS ONE 10, e0141703.Google Scholar
Müller, R-A, Cauich, C, Rubio, MA, Mizuno, A and Courchesne, E (2004) Abnormal activity patterns in premotor cortex during sequence learning in autistic patients. Biological Psychiatry 56, 323–332.Google Scholar
Naaijen, J, de Ruiter, S, Zwiers, MP, Glennon, JC, Durston, S, Lythgoe, DJ, Williams, SCR, Banaschewski, T, Brandeis, D, Franke, B and Buitelaar, JK (2016) COMPULS: design of a multicenter phenotypic, cognitive, genetic, and magnetic resonance imaging study in children with compulsive syndromes. BMC Psychiatry 16, 361.Google Scholar
Naaijen, J, Zwiers, MP, Amiri, H, Williams, SCR, Durston, S, Oranje, B, Brandeis, D, Boecker-Schlier, R, Ruf, M, Wolf, I, Banaschewski, T, Glennon, JC, Franke, B, Buitelaar, JK and Lythgoe, DJ (2017) Fronto-striatal glutamate in autism spectrum disorder and obsessive compulsive disorder. Neuropsychopharmacology 42, 2456–2465.Google Scholar
Paakki, J-J, Rahko, J, Long, X, Moilanen, I, Tervonen, O, Nikkinen, J, Starck, T, Remes, J, Hurtig, T, Haapsamo, H, Jussila, K, Kuusikko-Gauffin, S, Mattila, M-L, Zang, Y and Kiviniemi, V (2010) Alterations in regional homogeneity of resting-state brain activity in autism spectrum disorders. Brain Research 1321, 169–179.Google Scholar
Padmanabhan, A, Lynn, A, Foran, W, Luna, B and O'Hearn, K (2013) Age related changes in striatal resting state functional connectivity in autism. Frontiers in Human Neuroscience 7, 814.Google Scholar
Parkes, L, Fulcher, B, Yücel, M and Fornito, A (2018) An evaluation of the efficacy, reliability, and sensitivity of motion correction strategies for resting-state functional MRI. NeuroImage 171, 415–436.Google Scholar
Patenaude, B, Smith, SM, Kennedy, DN and Jenkinson, M (2011) A Bayesian model of shape and appearance for subcortical brain segmentation. NeuroImage 56, 907–922.Google Scholar
Patriquin, MA, DeRamus, T, Libero, LE, Laird, A and Kana, RK (2016) Neuroanatomical and neurofunctional markers of social cognition in autism spectrum disorder. Human Brain Mapping 37, 3957–3978.Google Scholar
Polyanska, L, Critchley, HD and Rae, CL (2017) Centrality of prefrontal and motor preparation cortices to Tourette syndrome revealed by meta-analysis of task-based neuroimaging studies. NeuroImage: Clinical 16, 257–267.Google Scholar
Pruim, RHR, Mennes, M, Buitelaar, JK and Beckmann, CF (2015 a) Evaluation of ICA-AROMA and alternative strategies for motion artifact removal in resting state fMRI. NeuroImage 112, 278–287.Google Scholar
Pruim, RHR, Mennes, M, van Rooij, D, Llera, A, Buitelaar, JK and Beckmann, CF (2015 b) ICA-AROMA: a robust ICA-based strategy for removing motion artifacts from fMRI data. NeuroImage 112, 267–277.Google Scholar
R Core Team (2014) R: Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Robbins, TW, Gillan, CM, Smith, DG, de Wit, S and Ersche, KD (2012) Neurocognitive endophenotypes of impulsivity and compulsivity: towards dimensional psychiatry. Trends in Cognitive Sciences 16, 81–91.Google Scholar
Ruscio, AM, Stein, DJ, Chiu, WT and Kessler, RC (2010) The epidemiology of obsessive-compulsive disorder in the National Comorbidity Survey Replication. Molecular Psychiatry 15, 53–63.Google Scholar
Russo, M, Naro, A, Mastroeni, C, Morgante, F, Terranova, C, Muscatello, MR, Zoccali, R, Calabrò, RS and Quartarone, A (2014) Obsessive-compulsive disorder: a ‘sensory-motor’ problem? International Journal of Psychophysiology 92, 74–78.Google Scholar
Sakai, Y, Narumoto, J, Nishida, S, Nakamae, T, Yamada, K, Nishimura, T and Fukui, K (2011) Corticostriatal functional connectivity in non-medicated patients with obsessive-compulsive disorder. European Psychiatry 26, 463–469.Google Scholar
Scahill, L, Riddle, MA, McSwiggin-Hardin, M, Ort, SI, King, RA, Goodman, WK, Cicchetti, D and Leckman, JF (1997) Children's Yale-Brown Obsessive Compulsive Scale: reliability and validity. Journal of the American Academy of Child & Adolescent Psychiatry 36, 844–852.Google Scholar
Shaffer, D, Fisher, P, Lucas, CP, Dulcan, MK and Schwab-Stone, ME (2000) NIMH Diagnostic Interview Schedule for Children Version IV (NIMH DISC-IV): description, differences from previous versions, and reliability of some common diagnoses. Journal of the American Academy of Child & Adolescent Psychiatry 39, 28–38.Google Scholar
Smith, SM and Nichols, TE (2009) Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. NeuroImage 44, 83–98.Google Scholar
Streiner, DL and Norman, GR (2011) Correction for multiple testing: is there a resolution? Chest 140, 16–18.Google Scholar
Taylor, S (2011) Early versus late onset obsessive-compulsive disorder: evidence for distinct subtypes. Clinical Psychology Review 31, 1083–1100.Google Scholar
Togao, O, Yoshiura, T, Nakao, T, Nabeyama, M, Sanematsu, H, Nakagawa, A, Noguchi, T, Hiwatashi, A, Yamashita, K, Nagao, E, Kanba, S and Honda, H (2010) Regional gray and white matter volume abnormalities in obsessive-compulsive disorder: a voxel-based morphometry study. Psychiatry Research: Neuroimaging 184, 29–37.Google Scholar
Vaghi, MM, Vértes, PE, Kitzbichler, MG, Apergis-Schoute, AM, van der Flier, FE, Fineberg, NA, Sule, A, Zaman, R, Voon, V, Kundu, P, Bullmore, ET and Robbins, TW (2017) Specific frontostriatal circuits for impaired cognitive flexibility and goal-directed planning in obsessive-compulsive disorder: evidence from resting-state functional connectivity. Biological Psychiatry 81, 708–717.Google Scholar
van den Heuvel, OA, van Wingen, G, Soriano-Mas, C, Alonso, P, Chamberlain, SR, Nakamae, T, Denys, D, Goudriaan, AE and Veltman, DJ (2016) Brain circuitry of compulsivity. European Neuropsychopharmacology 26, 810–827.Google Scholar
von Hofsten, C and Rosander, K (2012) Perception-action in children with ASD. Frontiers in Integrative Neuroscience 6, 115.Google Scholar
von Rhein, D, Oldehinkel, M, Beckmann, CF, Oosterlaan, J, Heslenfeld, D, Hartman, CA, Hoekstra, PJ, Franke, B, Cools, R, Buitelaar, JK and Mennes, M (2016) Aberrant local striatal functional connectivity in attention-deficit/hyperactivity disorder. Journal of Child Psychology and Psychiatry 57, 697–705.Google Scholar
van Steensel, FJA, Bögels, SM and Perrin, S (2011) Anxiety disorders in children and adolescents with autistic spectrum disorders: a meta-analysis. Clinical Child and Family Psychology Review 14, 302–317.Google Scholar
Wechsler, D (2002) WISC-III Handleiding. London: The Psychological Corporation.Google Scholar
Winkler, AM, Ridgway, GR, Webster, MA, Smith, SM and Nichols, TE (2014) Permutation inference for the general linear model. NeuroImage 92, 381–397.Google Scholar
Yalachkov, Y, Kaiser, J and Naumer, MJ (2010) Sensory and motor aspects of addiction. Behavioural Brain Research 207, 215–222.Google Scholar
Yang, YJD, Sukhodolsky, DG, Lei, J, Dayan, E, Pelphrey, KA and Ventola, P (2017) Distinct neural bases of disruptive behavior and autism symptom severity in boys with autism spectrum disorder. Journal of Neurodevelopmental Disorders 9, 1.Google Scholar
Zhou, D-D, Wang, W, Wang, G-M, Li, D-Q and Kuang, L (2017) An updated meta-analysis: short-term therapeutic effects of repeated transcranial magnetic stimulation in treating obsessive-compulsive disorder. Journal of Affective Disorders 215, 187–196.Google Scholar
Supplementary material: File

Akkermans et al. supplementary material

Akkermans et al. supplementary material 1

Download Akkermans et al. supplementary material(File)
File 256.4 KB