Sensorimotor Abnormalities in Biological Mothers and Fathers of Individuals with ASD

Background:   Eye movement studies provide a precisely quantifiable and translational method for examining sensorimotor impairments in autism spectrum disorder (ASD). Individuals with ASD show reduced accuracy and increased accuracy variability of saccadic eye movements. We have demonstrated that unaffected first-degree relatives of individuals with ASD also show reduced saccade accuracy and increased saccade variability suggesting that eye movement abnormalities may be familial. Here, we used a family trio design to determine the extent to which eye movement abnormalities are familial, and to examine whether they are differentially expressed in mothers versus fathers.

Objectives:   To assess the familiality of eye movement abnormalities in individuals with ASD and their unaffected parents. 

Methods:   Thirty-five family trios (proband with ASD, biological mother, biological father) and 70 age-, IQ- and gender-matched healthy controls (42 proband controls, 28 parent controls) completed eye movement testing. Participants with ASD were between ages 6-20 years, 89% male, and had a Performance IQ >70. Parents of probands were <55 years old and completed the Broad Autism Phenotype-Questionnaire (BAP-Q). Participants completed 60 trials of a visually-guided saccade task during which they made saccades to peripheral targets that appeared with equal probability at 12 or 24 deg to the left or right of center. Saccade accuracy, accuracy variability, peak velocity, and peak acceleration were measured for each trial.

Results:   During the visually-guided saccade task, individuals with ASD demonstrated reduced saccade accuracy and increased accuracy variability compared to age-matched controls. Mothers of individuals with ASD also demonstrated reduced saccade accuracy compared to adult female controls. Fathers of individuals with ASD did not show any differences in the accuracy or variability of their saccades relative to male controls. Deficits in saccade accuracy, peak velocity, and peak acceleration were found to be highly familial, co-varying more strongly in mother-child versus father-child dyads. However, their saccade accuracy and accuracy variability were associated with BAP-Q rated social aloofness, pragmatic language deficits, and behavioral rigidity for fathers of individuals with ASD. This was not observed for mothers, and no other cognitive or demographic characteristics related to their oculomotor deficits.    

Conclusions:  

Our findings provide further support that sensorimotor impairments in ASD are familial, with novel evidence suggesting primarily maternal influences. Fathers did not show sensorimotor deficits compared to controls, but their ability to make accurate saccades was related to broader autism phenotypic characteristics suggesting that sensorimotor processes among unaffected fathers may be one component of a broader constellation of sub-clinical features that confer risk onto their offspring. In contrast, mothers in our sample appear to have relatively isolated sensorimotor deficits that may be directly related to the deficits observed in their offspring, yet have factors protecting them from exhibiting broader phenotypic characteristics. Future studies should be aimed at better understanding maternal versus paternal contributions to risk susceptibility in ASD, identifying potential protective factors in mothers, and determining how maternal and paternal influences affect sensorimotor functioning in female probands.