The relationship between alexithymia, interoception, and neural functional connectivity during facial expression processing in autism spectrum disorder

Christiana Butera; Jonas Kaplan; Emily Kilroy; Laura Harrison; Aditya Jayashankar; Fernanda Loureiro; Lisa Aziz-Zadeh

doi:10.1016/j.neuropsychologia.2023.108469

The relationship between alexithymia, interoception, and neural functional connectivity during facial expression processing in autism spectrum disorder

Neuropsychologia. 2023 Feb 10:180:108469. doi: 10.1016/j.neuropsychologia.2023.108469. Epub 2023 Jan 4.

Authors

Christiana Butera¹, Jonas Kaplan², Emily Kilroy¹, Laura Harrison¹, Aditya Jayashankar¹, Fernanda Loureiro², Lisa Aziz-Zadeh³

Affiliations

¹ Brain & Creativity Institute, University of Southern California, Los Angeles, CA, 90089, USA; Division of Occupational Science, University of Southern California, Los Angeles, CA, 90089, USA.
² Brain & Creativity Institute, University of Southern California, Los Angeles, CA, 90089, USA.
³ Brain & Creativity Institute, University of Southern California, Los Angeles, CA, 90089, USA; Division of Occupational Science, University of Southern California, Los Angeles, CA, 90089, USA. Electronic address: lazizzad@usc.edu.

PMID: 36610493
PMCID: PMC9898240
DOI: 10.1016/j.neuropsychologia.2023.108469

Abstract

Neural processing differences of emotional facial expressions, while common in autism spectrum disorder (ASD), may be related to co-occurring alexithymia and interoceptive processing differences rather than autism per se. Here, we investigate relationships between alexithymia, interoceptive awareness of emotions, and functional connectivity during observation of facial expressions in youth (aged 8-17) with ASD (n = 28) compared to typically developing peers (TD; n = 37). Behaviorally, we found no significant differences between ASD and TD groups in interoceptive awareness of emotions, though alexithymia severity was significantly higher in the ASD group. In the ASD group, increased alexithymia was significantly correlated with lower interoceptive sensation felt during emotion. Using psycho-physiological interaction (PPI) analysis, the ASD group showed higher functional connectivity between the left ventral anterior insula and the left lateral prefrontal cortex than the TD group when viewing facial expressions. Further, alexithymia was associated with reduced left anterior insula-right precuneus connectivity and reduced right dorsal anterior insula-left ventral anterior insula connectivity when viewing facial expressions. In the ASD group, the degree of interoceptive sensation felt during emotion was positively correlated with left ventral anterior insula-right IFG connectivity when viewing facial expressions. However, across all participants, neither alexithymia nor interoceptive awareness of emotions predicted connectivity between emotion-related brain regions when viewing emotional facial expressions. To summarize, we found that in ASD compared to TD: 1) there is stronger connectivity between the insula and lateral prefrontal cortex; and 2) differences in interhemispheric and within left hemisphere connectivity between the insula and other emotion-related brain regions are related to individual differences in interoceptive processing and alexithymia. These results highlight complex relationships between alexithymia, interoception, and brain processing in ASD.

Keywords: Alexithymia; Autism spectrum disorder; Empathy; Facial expressions; Functional connectivity; Interoception.

Publication types

Research Support, Non-U.S. Gov't
Research Support, N.I.H., Extramural

MeSH terms

Adolescent
Affective Symptoms / diagnostic imaging
Affective Symptoms / etiology
Autism Spectrum Disorder*
Emotions / physiology
Facial Expression
Humans
Interoception* / physiology
Magnetic Resonance Imaging / methods

Grants and funding

R01 HD079432/HD/NICHD NIH HHS/United States