Increased Gamma Oscillatory Activity within the Salience Network: Relationship to Social and Attention Functioning in ASD

Background: Autism spectrum disorders (ASD) are characterized by deficits in social and attention functioning. Research to date has failed to clarify the pathogenesis, and there is an urgent need to identify biomarkers to aid earlier diagnosis given its escalating prevalence. Deficits in the salience network (SN) have been shown to distinguish between children with autism and neurotypical children; however, links to clinical symptoms have not been established. The insula is a key node of the SN, responsible for “selecting” stimuli for additional processing. Disruptions in connectivity are believed to lead to aberrant salience processing, which may contribute to core symptoms of ASD (i.e. lack of attention to social stimuli).

Objectives: This study investigated relationships between neural synchrony within the SN and social/attention functioning.

Methods: Twelve children with ASD (Age: M = 9.2; SD = 1.0) and 13 neurotypical (NT) controls (Age: M = 9.3; SD = 1.3) underwent magnetoencephalography at rest. Synchronization of activity was quantified by calculating coherence (0 to 1) between the insula and other cortical regions of the SN. Group differences were computed using t-tests for each region pair. Kendall Tau correlations were computed to examine relationships between coherence and social/attention functioning, as measured by NEPSY-II Auditory Attention (AA)/Response Set (RS) and Social Responsiveness Scale-2 (SRS-2), respectively.

Results: Within gamma, higher coherence was noted in NT between L Insula (LI) to: R Angular Gyrus (p = .02), R Middle Occipital Gyrus (p=.05), and R Superior Occipital Gyrus (p = .04). In ASD, significant positive relationships were noted between SRS-2 Cognitive subscale and coherence from LI to: L Cingulate (p=.003), L Inferior Frontal Gyrus (IFG) (p=.04), L Superior Frontal Gyrus (SFG) (p=.03), R Cingulate (p=.007), R Insula (RI) (p=.04), and R SFG (p=.03). Significant relationships between SRS-2 Restricted and Repetitive Behavior (RRB) subscale and coherence from RI to L Cingulate (p=.05) and LI to: L Cingulate (p=.003), L SFG (p=.03), R Cingulate (p=.02), RI (p=.05), and R SFG (p=.03), were noted.  Within NT, significant negative relationships between NEPSY RS and coherence from LI to L IFG (p=.04) and LI to L MFG (p=.05) was noted. SRS-2 Communication and Motivation were positively related between coherence and LI to L Cingulate (both p=.04).

Conclusions: In NT, higher gamma band synchrony is noted in cross-hemispheric connections between LI and R parieto-occipital regions. In ASD, greater deficits in social cognition/RRB are related to higher gamma band synchrony, specifically within the left hemisphere and between insula and cingulate/frontal gyri. A similar relationship is reflected in heightened coherence between bilateral insula, cingulate and SFG. Better complex attention is related to lower gamma coherence between left insular and frontal regions in NT, while no relationship was found in ASD, suggesting alternate “selection” pathways. Overall, findings suggest enhanced frontal gamma oscillatory activity between the insula, a vital component of the SN, and other frontal regions may contribute to core symptoms of ASD.