. 2021 May 14;4(1):574.

doi: 10.1038/s42003-021-02015-2.

Imbalanced social-communicative and restricted repetitive behavior subtypes of autism spectrum disorder exhibit different neural circuitry

Natasha Bertelsen^{1

2}, Isotta Landi¹, Richard A I Bethlehem³, Jakob Seidlitz^{4

5}, Elena Maria Busuoli^{1

2}, Veronica Mandelli^{1

2}, Eleonora Satta¹, Stavros Trakoshis^{1

6}, Bonnie Auyeung^{7

8}, Prantik Kundu⁹, Eva Loth^{10

11}, Guillaume Dumas¹², Sarah Baumeister¹³, Christian F Beckmann¹⁴, Sven Bölte^{15

16

17}, Thomas Bourgeron¹², Tony Charman¹⁸, Sarah Durston¹⁹, Christine Ecker²⁰, Rosemary J Holt⁸, Mark H Johnson²¹, Emily J H Jones²², Luke Mason²², Andreas Meyer-Lindenberg²³, Carolin Moessnang²³, Marianne Oldehinkel^{14

24}, Antonio M Persico^{25

26}, Julian Tillmann^{18

27}, Steve C R Williams²⁸, Will Spooren²⁹, Declan G M Murphy^{10

11}, Jan K Buitelaar¹⁴; EU-AIMS LEAP group; Simon Baron-Cohen⁸, Meng-Chuan Lai^{8

30

31

32

33}, Michael V Lombardo^{34

35}

Collaborators, Affiliations

Collaborators

EU-AIMS LEAP group:
Jumana Ahmad, Sara Ambrosino, Tobias Banaschewski, Carsten Bours, Michael Brammer, Daniel Brandeis, Claudia Brogna, Yvette de Bruijn, Bhismadev Chakrabarti, Chris Chatham, Ineke Cornelissen, Daisy Crawley, Flavio Dell'Acqua, Jessica Faulkner, Vincent Frouin, Pilar Garcés, David Goyard, Lindsay Ham, Hannah Hayward, Joerg Hipp, Rosemary J Holt, Xavier Liogier D'ardhuy, David J Lythgoe, René Mandl, Andre Marquand, Maarten Mennes, Nico Mueller, Bethany Oakley, Laurence O'Dwyer, Bob Oranje, Gahan Pandina, Antonio M Persico, Barbara Ruggeri, Amber N V Ruigrok, Jessica Sabet, Roberto Sacco, Antonia San José Cáceres, Emily Simonoff, Roberto Toro, Heike Tost, Jack Waldman, Steve C R Williams, Caroline Wooldridge, Marcel P Zwiers

Affiliations

¹ Laboratory for Autism and Neurodevelopmental Disorders, Center for Neuroscience and Cognitive Systems @UniTn, Istituto Italiano di Tecnologia, Rovereto, TN, Italy.
² Center for Mind/Brain Sciences, University of Trento, Rovereto, TN, Italy.
³ Department of Psychiatry, University of Cambridge, Cambridge, UK.
⁴ Department of Child and Adolescent Psychiatry and Behavioral Science, Children's Hospital of Philadelphia, Philadelphia, PA, USA.
⁵ Department of Psychiatry, University of Pennsylvania, Philadelphia, PA, USA.
⁶ Department of Psychology, University of Cyprus, Nicosia, Cyprus.
⁷ Department of Psychology, School of Philosophy, Psychology, and Language Sciences, University of Edinburgh, Edinburgh, UK.
⁸ Autism Research Centre, Department of Psychiatry, University of Cambridge, Cambridge, UK.
⁹ Brain Mapping Unit, Department of Psychiatry, University of Cambridge, Cambridge, UK.
¹⁰ Sackler Institute for Translational Neurodevelopment, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
¹¹ Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
¹² Human Genetics and Cognitive Functions, Institut Pasteur, UMR3571 CNRS, Université de Paris, Paris, France.
¹³ Child and Adolescent Psychiatry, Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Mannheim, Germany.
¹⁴ Department of Cognitive Neuroscience, Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Centre, Nijmegen, The Netherlands.
¹⁵ Department of Women's and Children's Health; Center of Neurodevelopmental Disorders (KIND), Centre for Psychiatry Research, Karolinska Institutet & Stockholm Health Care Services, Region Stockholm, Stockholm, Sweden.
¹⁶ Child and Adolescent Psychiatry, Stockholm Health Care Services, Stockholm, Sweden.
¹⁷ Curtin Autism Research Group, School of Occupational Therapy, Social Work and Speech Pathology, Curtin University, Perth, Australia.
¹⁸ Department of Psychology, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
¹⁹ Department of Psychiatry, Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht, The Netherlands.
²⁰ Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, University Hospital Frankfurt am Main, Goethe University, Frankfurt, Germany.
²¹ Department of Psychology, University of Cambridge, Cambridge, UK.
²² Centre for Brain and Cognitive Development, Birkbeck, University of London, Henry Wellcome Building, London, UK.
²³ Department of Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Mannheim, Germany.
²⁴ Turner Institute for Brain and Mental Health, School of Psychological Sciences, Monash University, Victoria, Australia.
²⁵ Child and Adolescent Neuropsychiatry Unit, Gaetano Martino University Hospital, University of Messina, Messina, Italy.
²⁶ University Campus Bio-Medico, Rome, Italy.
²⁷ Department of Applied Psychology: Health, Development, Enhancement, and Intervention, University of Vienna, Vienna, Austria.
²⁸ Department of Neuroimaging, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
²⁹ Roche Pharma Research and Early Development, Neuroscience, Ophthalmology and Rare Diseases, Roche Innovation Center Basel, Basel, Switzerland.
³⁰ The Margaret and Wallace McCain Centre for Child, Youth & Family Mental Health, Azrieli Adult Neurodevelopmental Centre, and Campbell Family Mental Health Research Institute, Centre for Addiction and Mental Health, Toronto, Canada.
³¹ Department of Psychiatry and Autism Research Unit, The Hospital for Sick Children, Toronto, Canada.
³² Department of Psychiatry, Faculty of Medicine, University of Toronto, Toronto, Canada.
³³ Department of Psychiatry, National Taiwan University Hospital and College of Medicine, Taipei, Taiwan.
³⁴ Laboratory for Autism and Neurodevelopmental Disorders, Center for Neuroscience and Cognitive Systems @UniTn, Istituto Italiano di Tecnologia, Rovereto, TN, Italy. michael.lombardo@iit.it.
³⁵ Autism Research Centre, Department of Psychiatry, University of Cambridge, Cambridge, UK. michael.lombardo@iit.it.

PMID: 33990680
PMCID: PMC8121854
DOI: 10.1038/s42003-021-02015-2

Imbalanced social-communicative and restricted repetitive behavior subtypes of autism spectrum disorder exhibit different neural circuitry

Natasha Bertelsen et al. Commun Biol. 2021.

. 2021 May 14;4(1):574.

doi: 10.1038/s42003-021-02015-2.

Authors

Collaborators

EU-AIMS LEAP group:
Jumana Ahmad, Sara Ambrosino, Tobias Banaschewski, Carsten Bours, Michael Brammer, Daniel Brandeis, Claudia Brogna, Yvette de Bruijn, Bhismadev Chakrabarti, Chris Chatham, Ineke Cornelissen, Daisy Crawley, Flavio Dell'Acqua, Jessica Faulkner, Vincent Frouin, Pilar Garcés, David Goyard, Lindsay Ham, Hannah Hayward, Joerg Hipp, Rosemary J Holt, Xavier Liogier D'ardhuy, David J Lythgoe, René Mandl, Andre Marquand, Maarten Mennes, Nico Mueller, Bethany Oakley, Laurence O'Dwyer, Bob Oranje, Gahan Pandina, Antonio M Persico, Barbara Ruggeri, Amber N V Ruigrok, Jessica Sabet, Roberto Sacco, Antonia San José Cáceres, Emily Simonoff, Roberto Toro, Heike Tost, Jack Waldman, Steve C R Williams, Caroline Wooldridge, Marcel P Zwiers

Affiliations

¹ Laboratory for Autism and Neurodevelopmental Disorders, Center for Neuroscience and Cognitive Systems @UniTn, Istituto Italiano di Tecnologia, Rovereto, TN, Italy.
² Center for Mind/Brain Sciences, University of Trento, Rovereto, TN, Italy.
³ Department of Psychiatry, University of Cambridge, Cambridge, UK.
⁴ Department of Child and Adolescent Psychiatry and Behavioral Science, Children's Hospital of Philadelphia, Philadelphia, PA, USA.
⁵ Department of Psychiatry, University of Pennsylvania, Philadelphia, PA, USA.
⁶ Department of Psychology, University of Cyprus, Nicosia, Cyprus.
⁷ Department of Psychology, School of Philosophy, Psychology, and Language Sciences, University of Edinburgh, Edinburgh, UK.
⁸ Autism Research Centre, Department of Psychiatry, University of Cambridge, Cambridge, UK.
⁹ Brain Mapping Unit, Department of Psychiatry, University of Cambridge, Cambridge, UK.
¹⁰ Sackler Institute for Translational Neurodevelopment, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
¹¹ Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
¹² Human Genetics and Cognitive Functions, Institut Pasteur, UMR3571 CNRS, Université de Paris, Paris, France.
¹³ Child and Adolescent Psychiatry, Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Mannheim, Germany.
¹⁴ Department of Cognitive Neuroscience, Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Centre, Nijmegen, The Netherlands.
¹⁵ Department of Women's and Children's Health; Center of Neurodevelopmental Disorders (KIND), Centre for Psychiatry Research, Karolinska Institutet & Stockholm Health Care Services, Region Stockholm, Stockholm, Sweden.
¹⁶ Child and Adolescent Psychiatry, Stockholm Health Care Services, Stockholm, Sweden.
¹⁷ Curtin Autism Research Group, School of Occupational Therapy, Social Work and Speech Pathology, Curtin University, Perth, Australia.
¹⁸ Department of Psychology, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
¹⁹ Department of Psychiatry, Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht, The Netherlands.
²⁰ Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, University Hospital Frankfurt am Main, Goethe University, Frankfurt, Germany.
²¹ Department of Psychology, University of Cambridge, Cambridge, UK.
²² Centre for Brain and Cognitive Development, Birkbeck, University of London, Henry Wellcome Building, London, UK.
²³ Department of Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Mannheim, Germany.
²⁴ Turner Institute for Brain and Mental Health, School of Psychological Sciences, Monash University, Victoria, Australia.
²⁵ Child and Adolescent Neuropsychiatry Unit, Gaetano Martino University Hospital, University of Messina, Messina, Italy.
²⁶ University Campus Bio-Medico, Rome, Italy.
²⁷ Department of Applied Psychology: Health, Development, Enhancement, and Intervention, University of Vienna, Vienna, Austria.
²⁸ Department of Neuroimaging, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
²⁹ Roche Pharma Research and Early Development, Neuroscience, Ophthalmology and Rare Diseases, Roche Innovation Center Basel, Basel, Switzerland.
³⁰ The Margaret and Wallace McCain Centre for Child, Youth & Family Mental Health, Azrieli Adult Neurodevelopmental Centre, and Campbell Family Mental Health Research Institute, Centre for Addiction and Mental Health, Toronto, Canada.
³¹ Department of Psychiatry and Autism Research Unit, The Hospital for Sick Children, Toronto, Canada.
³² Department of Psychiatry, Faculty of Medicine, University of Toronto, Toronto, Canada.
³³ Department of Psychiatry, National Taiwan University Hospital and College of Medicine, Taipei, Taiwan.
³⁴ Laboratory for Autism and Neurodevelopmental Disorders, Center for Neuroscience and Cognitive Systems @UniTn, Istituto Italiano di Tecnologia, Rovereto, TN, Italy. michael.lombardo@iit.it.
³⁵ Autism Research Centre, Department of Psychiatry, University of Cambridge, Cambridge, UK. michael.lombardo@iit.it.

PMID: 33990680
PMCID: PMC8121854
DOI: 10.1038/s42003-021-02015-2

Abstract

Social-communication (SC) and restricted repetitive behaviors (RRB) are autism diagnostic symptom domains. SC and RRB severity can markedly differ within and between individuals and may be underpinned by different neural circuitry and genetic mechanisms. Modeling SC-RRB balance could help identify how neural circuitry and genetic mechanisms map onto such phenotypic heterogeneity. Here, we developed a phenotypic stratification model that makes highly accurate (97-99%) out-of-sample SC = RRB, SC > RRB, and RRB > SC subtype predictions. Applying this model to resting state fMRI data from the EU-AIMS LEAP dataset (n = 509), we find that while the phenotypic subtypes share many commonalities in terms of intrinsic functional connectivity, they also show replicable differences within some networks compared to a typically-developing group (TD). Specifically, the somatomotor network is hypoconnected with perisylvian circuitry in SC > RRB and visual association circuitry in SC = RRB. The SC = RRB subtype show hyperconnectivity between medial motor and anterior salience circuitry. Genes that are highly expressed within these networks show a differential enrichment pattern with known autism-associated genes, indicating that such circuits are affected by differing autism-associated genomic mechanisms. These results suggest that SC-RRB imbalance subtypes share many commonalities, but also express subtle differences in functional neural circuitry and the genomic underpinnings behind such circuitry.

PubMed Disclaimer

Conflict of interest statement

JKB has been a consultant to, advisory board member of, and a speaker for Janssen Cilag BV, Eli Lilly, Shire, Lundbeck, Roche, and Servier. He is not an employee of any of these companies and not a stock shareholder of any of these companies. He has no other financial or material support, including expert testimony, patents, or royalties. CFB is director and shareholder in SBGneuro Ltd. SB discloses that he has in the last 5 years acted as an author, consultant, or lecturer for Shire/Takeda, Medice, Roche, Eli Lilly, and Prima Psychiatry. He receives royalties for textbooks and diagnostic tools from Huber/Hogrefe, Kohlhammer, and UTB. TC has received consultancy from Roche and Servier and received book royalties from Guildford Press and Sage. DGMM has been a consultant to, and advisory board member, for Roche and Servier. He is not an employee of any of these companies, and not a stock shareholder of any of these companies. AML has received consultant fees from Boehringer Ingelheim, Elsevier, Brainsway, Lundbeck Int. Neuroscience Foundation, Lundbeck A/S, The Wolfson Foundation, Bloomfield Holding Ltd, Shanghai Research Center for Brain Science, Thieme Verlag, Sage Therapeutics, v Behring Röntgen Stiftung, Fondation FondaMental, Janssen-Cilag GmbH, MedinCell, Brain Mind Institute, Agence Nationale de la Recherche, CISSN (Catania Internat. Summer School of Neuroscience), Daimler und Benz Stiftung and American Association for the Advancement of Science. Additionally, he has received speaker fees from Italian Society of Biological Psychiatry, Merz-Stiftung, Forum Werkstatt Karlsruhe, Lundbeck SAS France, BAG Psychiatrie Oberbayern, Klinik für Psychiatrie und Psychotherapie Ingolstadt, med Update GmbH, Society of Biological Psychiatry and Siemens Healthineers. He is not an employee of any of these companies, and not a stock shareholder of any of these companies. JT is a consultant to Roche. All other authors declare no competing interests.

Figures

**Fig. 1. Approach towards testing common pathway versus multiple pathways explanations behind SC-RRB balance in autism.**
In this figure we depict two alternatives for how SC-RRB balance subtypes (phenome level; SC = RRB, green; RRB > SC, pink; SC > RRB, blue) could be explained at the level of macroscale functional connectome phenotypes measured with rsfMRI (connectome level) and autism-associated functional genomic mechanisms (e.g., transcriptome and genome levels). Columns in this figure depict the common pathway (middle) and multiple pathways (right) models. The common pathway model predicts that when each subtype is compared to a typically-developing (TD) comparison group, they converge and share a common difference from TD in affected macroscale rsfMRI functional connectome phenotype. Underpinning this shared connectome phenotype are a myriad of differing functional genomic mechanisms. At the level of the transcriptome, we identify genes linked to macroscale functional networks by identifying genes whose spatial expression pattern across the brain is similar to the spatial topology of the macroscale functional network. This procedure generates a list of genes relevant for such macroscale networks and these lists are then tested for enrichment in autism-association functional genomic mechanisms. The gene list at the genome level represents an example of possible autism-associated genes that may (bold) or may not (non-bold) be linked to macroscale functional networks. In contrast to the common pathway model, the multiple pathways model would highlight that differential connectome phenotypes when compared to TD are unique to each subtype, and that each of these subtype-specific connectome phenotypes is underpinned by a differing set of autism-associated functional genomic mechanisms.

**Fig. 2. Supervised subtyping of autism by SC-RRB balance.**
Panel (a) shows the subtypes derived from a z-normalized difference score of SC-RRB, with a z-score threshold for cutting the subtypes at z = 1. Red shows the RRB > SC subtype, green shows the SC = RRB subtype, and blue shows the SC > RRB subtype. Panel (b) shows a confusion matrix with actual subtype labels for the NDAR Replication dataset along with the columns and the subtyping model’s predicted labels (trained on the NDAR Discovery dataset) along the rows. The colors within the cells indicate the percentage of individuals relative to the actual labels with predicted labels in each cell. Over a range of z-thresholds from 0.5 to 1, the accuracy ranged from 97–99% accuracy. Panel (c) shows SC-RRB subtypes from the EU-AIMS LEAP datasets derived using norms estimated from NDAR.

**Fig. 3. Replicable subtype differences in functional connectivity.**
This figure shows chord diagrams of replicable functional connectivity differences between SC = RRB vs TD (left) or SC > RRB vs TD (right) when subtypes are defined at a z-threshold of 1. However, edges shown in these diagrams are consensus edges that appear in every analysis of connectivity differences irrespective of the z-threshold used to define the subtypes. Red edges indicate hyperconnectivity in the autism subtype relative to TD, while blue edges indicate hypoconnectivity in the autism subtype relative to TD. The intensity of edge color indicates standardized effect size (Cohen’s d) shown on the color bar on the right. The cortical surface renderings of each component are unthresholded z-stat maps. Areas with higher z-stats (dark red) are of primary importance for the IC map. The top row shows effects in the EU-AIMS LEAP Discovery set, while the bottom row shows effects in the EU-AIMS LEAP Replication set.

**Fig. 4. Overlap between genes expressed in functional connectivity networks and genes linked to autism.**
In panel (a) we depict the analysis approach of identifying genes that are highly expressed in similar spatial patterns to the rsfMRI spatial IC maps (i.e., gene expression decoding). Once IC gene lists have been identified, we test these lists for enrichment with known lists of autism-associated functional genomic mechanisms (top left). In panel (b) we show enrichment odds ratios (numbers in each cell) along with the −log10 p value (coloring of the cells) for enrichment tests of specific networks (columns) against known lists of autism-associated genomic mechanisms (rows). Cells outlined with thick black rectangles survive FDR q < 0.05. The column labeled SC > RRB shows the enrichment results when the gene list under consideration comprises genes unique to IC17, but not any of the other ICs. The column labeled SC = RRB shows the enrichment results when the gene list under consideration consists of genes unique to IC03, IC07, and IC13, but not IC12 or IC17. ASD dnPTV, Autism de novo protein-truncating variants; ASD SFARI, SFARI Gene autism-associated genes; ASD DE Downreg, autism differentially expressed downregulated genes; ASD DE Upreg, autism differentially expressed upregulated genes; ASD CTX Downreg CoExpMods, autism downregulated cortical co-expression modules; ASD CTX Upreg CoExpMods, autism upregulated cortical co-expression modules; ASD Excitatory, autism differentially expressed genes in excitatory neurons; ASD Inhibitory, autism differentially expressed genes in inhibitory neurons; ASD Microglia, autism differentially expressed genes in microglia; ASD Oligodendrocyte, autism differentially expressed genes in oligodendrocytes; ASD Astrocyte, autism differentially expressed genes in astrocytes; ASD Endothelial, autism differentially expressed genes in endothelial cells; SCZ DE, schizophrenia differentially expressed genes; BD DE, bipolar disorder differentially expressed genes.

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Imbalanced social-communicative and restricted repetitive behavior subtypes of autism spectrum disorder exhibit different neural circuitry

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Imbalanced social-communicative and restricted repetitive behavior subtypes of autism spectrum disorder exhibit different neural circuitry

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