Sex Differences in Social Attention and Motivation in Autism: An Eye Tracking Study

Background: The sex ratio in autism spectrum disorder (ASD) has remained constant and weighted toward males. As a result, considerably less is known about females, with the majority of published research including largely, or in some cases exclusively, males. However, subtle but important differences exist between the male and female phenotype of ASD, including greater social motivation in ASD females (Sedgewick et al., 2016) and fewer and more typical circumscribed interests (CI; Sutherland et al., 2017). Eye-tracking has quantified abnormalities in visual attention to social stimuli and CI in ASD, but these studies have relied primarily on male samples.

Objectives: The aim of this study is to use eye-tracking to understand sex differences in attention to social and CI stimuli.

Methods: 57 children (ages 6 to 10) provided sufficient eye-tracking data for inclusion (>20% fixation time on screen): 35 children with a diagnosis of ASD (15 female) and 23 typically developing (TD) children (13 female). Subjects completed a validated eye-tracking paradigm (Sasson & Touchstone, 2014; Unruh et al., 2016), with twenty slides of paired social and non-social (object) images presented. Half of the object images represent frequently occurring CI in ASD, known as high autism interest (HAI) objects (e.g., trains; South et al., 2005, Turner-Brown et al., 2011), and the other half represent objects not associated with CI in ASD (e.g., plants).

Results: There was a strong effect of sex on initial orientation to faces (F=5.81, p=.02) with females faster to prioritize social stimuli, particularly when paired with HAI stimuli (F=5.91, p=.01; Figure 1a). ASD females attended to social stimuli faster than all other groups and ASD males were the slowest (Figure 1a). There was a Sex*Diagnosis interaction for the number of fixations to social stimuli (F=5.77, p=.02), with ASD males fixating to social stimuli fewer times than TD males (p=.006) and a marginal effect when compared to ASD females (p=.06; Figure 1b). This was particularly apparent for faces paired with HAI images, with ASD males attending fewer times compared to all other groups (p=.04). There was marginal Sex*Diagnosis interaction for overall fixation time to social stimuli (F=3.60, p=.06), with ASD males fixating less than ASD females (p=.03; Figure 1c).

Conclusions: Our data for ASD males replicates that of previous studies consisting largely, or exclusively, of males (Sasson & Touchstone, 2014; Unruh et al., 2016). However, our findings for ASD females differed; ASD females demonstrated an opposite pattern of attention to social stimuli, with attention patterns more comparable to TD females. This could reflect a protective effect in ASD females. Our data differ both from a recent ERP study that found attenuated responses to social stimuli in ASD females (Coffman et al., 2015), suggesting there may be a disconnected profile in ASD females, with heightened visual attention in females not leading to greater processing and encoding of social stimuli. Further work includes examining the neural correlates of social attention as well as examining the pupil responses of ASD females to social stimuli and more complex, ecologically valid eye tracking paradigms.