Reduced beta connectivity during emotional face processing in adolescents with autism.
BACKGROUND
Autism spectrum disorder (ASD) is a neurodevelopmental disorder characterized by impairments in social cognition. The biological basis of deficits in social cognition in ASD, and their difficulty in processing emotional face information in particular, remains unclear. Atypical communication within and between brain regions has been reported in ASD. Interregional phase-locking is a neurophysiological mechanism mediating communication among brain areas and is understood to support cognitive functions. In the present study we investigated interregional magnetoencephalographic phase synchronization during the perception of emotional faces in adolescents with ASD.


METHODS
A total of 22 adolescents with ASD (18 males, mean age =14.2 ± 1.15 years, 22 right-handed) with mild to no cognitive delay and 17 healthy controls (14 males, mean age =14.4 ± 0.33 years, 16 right-handed) performed an implicit emotional processing task requiring perception of happy, angry and neutral faces while we recorded neuromagnetic signals. The faces were presented rapidly (80 ms duration) to the left or right of a central fixation cross and participants responded to a scrambled pattern that was presented concurrently on the opposite side of the fixation point. Task-dependent interregional phase-locking was calculated among source-resolved brain regions.


RESULTS
Task-dependent increases in interregional beta synchronization were observed. Beta-band interregional phase-locking in adolescents with ASD was reduced, relative to controls, during the perception of angry faces in a distributed network involving the right fusiform gyrus and insula. No significant group differences were found for happy or neutral faces, or other analyzed frequency ranges. Significant reductions in task-dependent beta connectivity strength, clustering and eigenvector centrality (all P <0.001) in the right insula were found in adolescents with ASD, relative to controls.


CONCLUSIONS
Reduced beta synchronization may reflect inadequate recruitment of task-relevant networks during emotional face processing in ASD. The right insula, specifically, was a hub of reduced functional connectivity and may play a prominent role in the inability to effectively extract emotional information from faces. These findings suggest that functional disconnection in brain networks mediating emotional processes may contribute to deficits in social cognition in this population.
Department of Diagnostic Imaging, Hospital for Sick Children, 555 University Avenue, Toronto, Ontario M5G 1X8 Canada ; Department of Psychology, University of Toronto, 100 St. George Street, 4th Floor, Sidney Smith Hall, Toronto, Ontario M5S 3G3 Canada ; Neuroscience & Mental Health, Hospital for Sick Children Research Institute, 555 University Avenue, Toronto, Ontario M5G 1X8 Canada.
Rachel C
RC
Leung
Department of Diagnostic Imaging, Hospital for Sick Children, 555 University Avenue, Toronto, Ontario M5G 1X8 Canada ; Neuroscience & Mental Health, Hospital for Sick Children Research Institute, 555 University Avenue, Toronto, Ontario M5G 1X8 Canada ; Institute of Medical Science, University of Toronto, Faculty of Medicine, Medical Sciences Building, 1 King's College Circle, Toronto, Ontario M5S 1A8 Canada.
Annette X
AX
Ye
Department of Diagnostic Imaging, Hospital for Sick Children, 555 University Avenue, Toronto, Ontario M5G 1X8 Canada.
Simeon M
SM
Wong
Department of Diagnostic Imaging, Hospital for Sick Children, 555 University Avenue, Toronto, Ontario M5G 1X8 Canada ; Department of Psychology, University of Toronto, 100 St. George Street, 4th Floor, Sidney Smith Hall, Toronto, Ontario M5S 3G3 Canada ; Neuroscience & Mental Health, Hospital for Sick Children Research Institute, 555 University Avenue, Toronto, Ontario M5G 1X8 Canada ; Institute of Medical Science, University of Toronto, Faculty of Medicine, Medical Sciences Building, 1 King's College Circle, Toronto, Ontario M5S 1A8 Canada ; Department of Medical Imaging, Faculty of Medicine, University of Toronto, 263 McCaul Street - 4th Floor, Toronto, Ontario M5T 1 W7 Canada.
Margot J
MJ
Taylor
Department of Diagnostic Imaging, Hospital for Sick Children, 555 University Avenue, Toronto, Ontario M5G 1X8 Canada ; Department of Psychology, University of Toronto, 100 St. George Street, 4th Floor, Sidney Smith Hall, Toronto, Ontario M5S 3G3 Canada ; Neuroscience & Mental Health, Hospital for Sick Children Research Institute, 555 University Avenue, Toronto, Ontario M5G 1X8 Canada ; Institute of Medical Science, University of Toronto, Faculty of Medicine, Medical Sciences Building, 1 King's College Circle, Toronto, Ontario M5S 1A8 Canada ; Department of Medical Imaging, Faculty of Medicine, University of Toronto, 263 McCaul Street - 4th Floor, Toronto, Ontario M5T 1 W7 Canada.
Sam M
SM
Doesburg
Affect processing; Autism spectrum disorders; Beta-band; Cognitive development; Face processing; Functional connectivity; Graph theory; Magnetoencephalography; Neural oscillation; Neural synchrony; Social cognition