Underconnectivity of the superior temporal sulcus predicts emotion recognition deficits in autism.
Neurodevelopmental disconnections have been assumed to cause behavioral alterations in autism spectrum disorders (ASDs). Here, we combined measurements of intrinsic functional connectivity (iFC) from resting-state functional magnetic resonance imaging (fMRI) with task-based fMRI to explore whether altered activity and/or iFC of the right posterior superior temporal sulcus (pSTS) mediates deficits in emotion recognition in ASD. Fifteen adults with ASD and 15 matched-controls underwent resting-state and task-based fMRI, during which participants discriminated emotional states from point light displays (PLDs). Intrinsic FC of the right pSTS was further examined using 584 (278 ASD/306 controls) resting-state data of the Autism Brain Imaging Data Exchange (ABIDE). Participants with ASD were less accurate than controls in recognizing emotional states from PLDs. Analyses revealed pronounced ASD-related reductions both in task-based activity and resting-state iFC of the right pSTS with fronto-parietal areas typically encompassing the action observation network (AON). Notably, pSTS-hypo-activity was related to pSTS-hypo-connectivity, and both measures were predictive of emotion recognition performance with each measure explaining a unique part of the variance. Analyses with the large independent ABIDE dataset replicated reductions in pSTS-iFC to fronto-parietal regions. These findings provide novel evidence that pSTS hypo-activity and hypo-connectivity with the fronto-parietal AON are linked to the social deficits characteristic of ASD.
Movement Control and Neuroplasticity Research Group, Department of Biomedical Kinesiology, Group Biomedical Sciences, KU Leuven, 3000 Leuven, Belgium, NYU Child Study Center, New York University, 10016 New York, NY, USA, Research Group Psychiatry, Child and Adolescent Psychiatry Department, KU Leuven, 3000 Leuven, Belgium, and Neural Control of Movement Lab, Department Health Sciences and Technology, ETH, 8057 Zurich, Switzerland Movement Control and Neuroplasticity Research Group, Department of Biomedical Kinesiology, Group Biomedical Sciences, KU Leuven, 3000 Leuven, Belgium, NYU Child Study Center, New York University, 10016 New York, NY, USA, Research Group Psychiatry, Child and Adolescent Psychiatry Department, KU Leuven, 3000 Leuven, Belgium, and Neural Control of Movement Lab, Department Health Sciences and Technology, ETH, 8057 Zurich, Switzerland Kaat.Alaerts@faber.kuleuven.be.
Kaat
K
Alaerts
Movement Control and Neuroplasticity Research Group, Department of Biomedical Kinesiology, Group Biomedical Sciences, KU Leuven, 3000 Leuven, Belgium, NYU Child Study Center, New York University, 10016 New York, NY, USA, Research Group Psychiatry, Child and Adolescent Psychiatry Department, KU Leuven, 3000 Leuven, Belgium, and Neural Control of Movement Lab, Department Health Sciences and Technology, ETH, 8057 Zurich, Switzerland.
Daniel G
DG
Woolley
Movement Control and Neuroplasticity Research Group, Department of Biomedical Kinesiology, Group Biomedical Sciences, KU Leuven, 3000 Leuven, Belgium, NYU Child Study Center, New York University, 10016 New York, NY, USA, Research Group Psychiatry, Child and Adolescent Psychiatry Department, KU Leuven, 3000 Leuven, Belgium, and Neural Control of Movement Lab, Department Health Sciences and Technology, ETH, 8057 Zurich, Switzerland.
Jean
J
Steyaert
Movement Control and Neuroplasticity Research Group, Department of Biomedical Kinesiology, Group Biomedical Sciences, KU Leuven, 3000 Leuven, Belgium, NYU Child Study Center, New York University, 10016 New York, NY, USA, Research Group Psychiatry, Child and Adolescent Psychiatry Department, KU Leuven, 3000 Leuven, Belgium, and Neural Control of Movement Lab, Department Health Sciences and Technology, ETH, 8057 Zurich, Switzerland.
Adriana
A
Di Martino
Movement Control and Neuroplasticity Research Group, Department of Biomedical Kinesiology, Group Biomedical Sciences, KU Leuven, 3000 Leuven, Belgium, NYU Child Study Center, New York University, 10016 New York, NY, USA, Research Group Psychiatry, Child and Adolescent Psychiatry Department, KU Leuven, 3000 Leuven, Belgium, and Neural Control of Movement Lab, Department Health Sciences and Technology, ETH, 8057 Zurich, Switzerland.
Stephan P
SP
Swinnen
Movement Control and Neuroplasticity Research Group, Department of Biomedical Kinesiology, Group Biomedical Sciences, KU Leuven, 3000 Leuven, Belgium, NYU Child Study Center, New York University, 10016 New York, NY, USA, Research Group Psychiatry, Child and Adolescent Psychiatry Department, KU Leuven, 3000 Leuven, Belgium, and Neural Control of Movement Lab, Department Health Sciences and Technology, ETH, 8057 Zurich, Switzerland Movement Control and Neuroplasticity Research Group, Department of Biomedical Kinesiology, Group Biomedical Sciences, KU Leuven, 3000 Leuven, Belgium, NYU Child Study Center, New York University, 10016 New York, NY, USA, Research Group Psychiatry, Child and Adolescent Psychiatry Department, KU Leuven, 3000 Leuven, Belgium, and Neural Control of Movement Lab, Department Health Sciences and Technology, ETH, 8057 Zurich, Switzerland.
Nicole
N
Wenderoth
D000293:Adolescent; D000328:Adult; D000704:Analysis of Variance; D001321:Autistic Disorder / Q000150:complications*; D001931:Brain Mapping; D016022:Case-Control Studies; D005260:Female; D006801:Humans; D007091:Image Processing, Computer-Assisted; D008279:Magnetic Resonance Imaging; D008297:Male; D019964:Mood Disorders / Q000209:etiology* / Q000473:pathology*; D009483:Neuropsychological Tests; D010100:Oxygen / Q000097:blood; D011569:Psychiatric Status Rating Scales; D011930:Reaction Time; D021641:Recognition, Psychology / Q000502:physiology*; D012146:Rest / Q000502:physiology; D013702:Temporal Lobe / Q000098:blood supply / Q000473:pathology*; D055815:Young Adult
D010100:Oxygen
autism spectrum disorders; emotion recognition; functional connectivity; functional magnetic resonance imaging; superior temporal sulcus