During eye contact those with ASD have significantly reduced activity in the dorsal parietal cortex

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A hallmark of autism spectrum disorder, ASD, is the reluctance to make eye contact with others in natural conditions.

Although eye contact is a critically important part of everyday interactions, scientists have been limited in studying the neurological basis of live social interaction with eye-contact in ASD because of the inability to image the brains of two people simultaneously.

However, using an innovative technology that enables imaging of two individuals during live and natural conditions, Yale researchers have identified specific brain areas in the dorsal parietal region of the brain associated with the social symptomatology of autism.

The study, published Nov. 9 in the journal PLOS ONE, finds that these neural responses to live face and eye-contact may provide a biomarker for the diagnosis of ASD as well as provide a test of the efficacy of treatments for autism.

“Our brains are hungry for information about other people, and we need to understand how these social mechanisms operate in the context of a real and interactive world in both typically developed individuals as well as individuals with ASD,” said co-corresponding author Joy Hirsch, Elizabeth Mears and House Jameson Professor of Psychiatry, Comparative Medicine, and of Neuroscience at Yale.

The Yale team, led by Hirsch and James McPartland, Harris Professor at the Yale Child Study Center, analyzed brain activity during brief social interactions between pairs of adults — each including a typical participant and one with ASD — using functional near-infrared spectroscopy, a non-invasive optical neuroimaging method.

Both participants were fitted with caps with many sensors that emitted light into the brain and also recorded changes in light signals with information about brain activity during face gaze and eye-to-eye contact.

The investigators found that during eye contact, participants with ASD had significantly reduced activity in a brain region called the dorsal parietal cortex compared to those without ASD.

Further, the more severe the overall social symptoms of ASD as measured by ADOS (Autism Diagnostic Observation Schedule, 2nd Edition) scores, the less activity was observed in this brain region. Neural activity in these regions was synchronous between typical participants during real eye-to-eye contact but not during gaze at a video face.

This typical increase in neural coupling was not observed in ASD, and is consistent with the difficulties in social interactions.

“We now not only have a better understanding of the neurobiology of autism and social differences, but also of the underlying neural mechanisms that drive typical social connections,” Hirsch said.


The Role of Eye Gaze in the Development of ASD
A number of endophenotypes are potentially linked to the development of ASD, including differences in attentional disengagement, motor delays and sensory disturbances (Constantino et al., 2021; Johnson et al., 2015, 2021; Klin et al., 2020; Tiede & Walton, 2020; Varcin & Nelson, 2016). However, the most reliably replicated early predictor of ASD is differences in social attention, and in particular, attenuated eye gaze (Klin et al., 2020; Tiede & Walton, 2020).

Reduced eye gaze as a potential endophenotype to clinical ASD has received great interest over many decades (Itier & Batty, 2009; Klin et al., 2020; Phillips et al., 1992; Schultz, 2005; Tiede & Walton, 2020). Human babies have an innate preference for faces (Goren et al., 1975; Valenza et al., 1996) and the eye region in particular draws their attention (Batki et al., 2000). Relative to typically developing children, however, infants later diagnosed with ASD look less at faces and show reduced eye contact and gaze-following behaviour (Leekam et al., 1998; Merin et al., 2007; Riby et al., 2009). In fact, reduction in eye gaze over the first six months of life is correlated with the severity of later social difficulties (Jones & Klin, 2013). Eye gaze is likely to be critical for the development of social skills and higher order social-cognitive abilities, such as theory of mind and perspective taking (refer Stephenson et al., 2021 for a review). Eyes are an important source of social information. Indeed, eye contact improves the ability to infer mental states (Adams & Nelson, 2016). It is also critical for initiation of joint attention (Hamilton, 2016)—allowing people to share experiences. Importantly, eye contact signals a desire to interact with others (Mundy & Newell, 2007)—increasing opportunities for interaction, affiliation and social learning.

Consistent evidence supports the role of eye gaze in social development in both clinical and neurotypical populations throughout the lifespan. Gaze-following and use of eye contact to establish social interaction in infancy positively correlates with later acquisition of social cognition and social skills (Vaughan Van Hecke et al., 2007). Interestingly, a recent review has provided evidence that children with visual impairment experience language, communication and social difficulties during the second and third year of life and a disproportionate number of these children also exhibit stereotyped behaviours (Vervloed et al., 2020). It is possible that social difficulties in children with visual impairment are caused by reduced access to visual sources of social information. Eye contact also supports processing of social information and social skills during adulthood. For example, duration of eye contact in real life situations positively correlates with adult social skills and emotion recognition accuracy (Cherulnik et al., 1978; Hall et al., 2010), and eye gaze is also linked to better face identity memory (Davis et al., 2017). Meanwhile, studies of adults on the autism spectrum have found an association between reduced visual fixation on the eye region and greater social difficulties (Jones et al., 2008; Speer et al., 2007).

While the role of eye gaze in the development of ASD has received much attention, there are conflicting theories on the mechanisms responsible for differences in eye contact. A prominent explanation is that social stimuli, and especially the faces and eyes of others, are less salient for people on the autism spectrum (Baron-Cohen et al., 2000; Klin et al., 2002; Weeks & Hobson, 1987) because they are less rewarding (Chevallier et al., 2012; Grelotti et al., 2002) and/or less informative (Baron-Cohen et al., 1997; Grelotti et al., 2002). The amygdala theory of autism is a brain-based theory that claims people on the autism spectrum perceive faces and eyes as less salient relative to neurotypical people due to amygdala hypoactivation (Baron-Cohen et al., 2000). However, a more recent hypothesis challenges this theory. In 2013, Tanaka and Sung reviewed evidence of face processing difficulties in ASD and proposed the “eye avoidance hypothesis” of autism. According to this hypothesis, people on the autism spectrum experience high levels of unpleasant amygdala-mediated arousal in response to direct eye contact and use eye avoidance as a strategy to reduce this arousal (Tanaka & Sung, 2013). The remainder of this review provides an overview of these competing theories and seeks to arbitrate between them by reviewing studies that specifically measured the relationship between eye gaze and brain activity in ASD.

The Amygdala Theory of Autism
The amygdala is a subcortical brain region involved in rapid and non-conscious detection of stimuli with biological, social, and emotional salience (Zalla & Sperduti, 2013). Magnocellular retinal ganglion cells convey biologically important information to the amygdala via the superior colliculus and pulvinar nucleus of the thalamus (Méndez-Bértolo et al., 2016). This subcortical pathway is involved in detection of faces, especially direct eye contact (Johnson, 2005; Senju & Johnson, 2009; Skuse, 2003), and is implicated in infant face preferences (Johnson, 2005). The amygdala and related subcortical regions may be especially important for threat detection, including rapid detection of emotional expressions, especially fear (McFadyen et al., 2019; Méndez-Bértolo et al., 2016). The amygdala, in particular, drives arousal responses to emotionally salient and threatening stimuli (Rodriguez-Romaguera et al., 2020). Importantly, activity in the amygdala modulates cortical regions involved with the interpretation of social information (Hadjikhani et al., 2017a, 2017b; Senju & Johnson, 2009). Given its central role in processing social and emotional stimuli, the amygdala has been the focus of a great deal of research on the neurobiological underpinnings of ASD.

We do not provide an exhaustive review of evidence supporting the amygdala theory of autism in the current paper, as this has been done elsewhere (refer Sweeten et al., 2002). Briefly, advocates of the amygdala theory argue that people on the autism spectrum exhibit a similar profile of difficulties to people with amygdala lesions. Neurotypical participants have a tendency to focus on the eye region when asked to make judgements about faces; for example, judgements of emotion or gender (Peterson & Eckstein, 2011).

However, people with amygdala damage (Schyns et al., 2005) and people on the autism spectrum (Papagiannopoulou et al., 2014; Pelphrey et al., 2002; Spezio et al., 2007) spend less time looking at the eyes relative to controls. Moreover, people on the autism spectrum and people with amygdala damage have more difficulty in face tasks that rely on information from the eye region, such as recognising complex mental states (amygdala damage: Adolphs et al., 2002; Tranel et al., 1994; ASD: Baron-Cohen et al., 1997) and negative emotions (amygdala damage: Anderson et al., 2000; ASD: Ashwin et al., 2006), especially fear (amygdala damage: Adolphs et al., 2002; Broks et al., 1998; Calder, 1996; Schyns et al., 2005; Tranel et al., 1994; ASD: Howard et al., 2000; Uljarevic & Hamilton, 2013).

Differences in amygdala activation are also cited as evidence supporting the amygdala theory of autism. In neurotypical individuals, activity in the amygdala increases in response to eye contact (Skuse, 2003) and emotional expressions (Wright et al., 2002), particularly those that are negative (Morris et al., 1996). However, there is evidence of amygdala hypoactivation during face processing tasks in people on the autism spectrum (Baron-Cohen et al., 1999; Critchley et al., 2000). Indeed, a recent meta-analysis of whole brain fMRI studies concluded that the primary difference between participants on the autism spectrum and neurotypical controls during face processing tasks was reduced amygdala activation in the participants diagnosed with ASD (Costa et al., 2021).

reference link :https://link.springer.com/article/10.1007/s10803-022-05443-z


Original Research: The findings will appear in PLOS ONE

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