Cardiac Vagal Tone Predicts Eye Gaze Fixation in the Broad Autism Phenotype

Background:   Diminished gaze fixation is a primary feature of autism spectrum disorder (ASD) that is associated with abnormal neural activation patterns (Dalton et al., 2005; Senju et al., 2005). Diminished gaze fixation has also been documented as part of the broad autism phenotype (BAP), both in infant siblings of children with ASD (Dalton et al., 2005), as well as among parents of children with ASD (Adolphs et al., 2008). The expression of the BAP among unaffected relatives is believed to reflect genetic liability for ASD, and studies aimed at defining mechanisms underlying these features may hold important clues into causal pathways in ASD. Autonomic nervous system dysfunction is present among some individuals with ASD and is thought to underlie aberrant social behavior (Klusek et al., 2015). The present study examined cardiac vagal tone, an index of the parasympathetic “rest and restore” response, as a potential mechanism for diminished gaze fixation in the broad autism phenotype.

Objectives:   To investigate the relationship between cardiac vagal tone and gaze fixation patterns in response to direct and averted eye gaze among mothers of children with ASD and control mothers of children with typical development.

Methods:   Eye movements of 16 mothers of children with ASD (mean age=48.39 years) and 21 control mothers of children with typical development (mean age=43.15) were recorded while watching an animated female face displaying either direct or averted gaze for 6.3 seconds (stimuli from Weiser et al., 2009). Trials began with participants fixating within the eye region and the percent of time dwelling within the eye region was quantified. Prior to completing the eyetracking paradigm, baseline cardiac activity was measured during a 3 minute baseline where participants viewed a calming ocean scene. CardioEdit/Batch software (Brain-Body Center, University of Illinois) was used to extract mean estimates for respiratory sinus arrhythmia, an index of vagal tone. Higher vagal tone reflects increased parasympathetic control and thus improved autonomic flexibility. 

Results:   Repeated measures ANOVA tested the effect of vagal tone, group, their interaction, and condition (averted vs. direct gaze) on the percent of time spent dwelling within the eye region of the face. A significant group-by-vagal tone interaction was detected, where higher vagal tone was associated with a greater percent of time dwelling within the eye region among the mothers of children with ASD, whereas these variables were unrelated in the control mothers (F [1,33] = 4.70, p = .038). The effect of condition was not significant (p = .449).

Conclusions:   Poorer autonomic nervous system flexibility among mothers of children with ASD, indexed by dampened parasympathetic vagal tone, was associated with decreased gaze fixation. This finding highlights autonomic nervous system dysfunction as a potential mechanism that may underlie atypical gaze fixation patterns seen in ASD and its broader phenotypes.