Atypical neural networks for social orienting in autism spectrum disorders

Abstract

Autism spectrum disorders (ASD) are characterized by significant social impairments, including deficits in orienting attention following social cues. Behavioral studies investigating social orienting in ASD, however, have yielded mixed results, as the use of naturalistic paradigms typically reveals clear deficits whereas computerized laboratory experiments often report normative behavior. The present study is the first to examine the neural mechanisms underlying social orienting in ASD in order to provide new insight into the social attention impairments that characterize this disorder. Using fMRI, we examined the neural correlates of social orienting in children and adolescents with ASD and in a matched sample of typically developing (TD) controls while they performed a spatial cueing paradigm with social (eye gaze) and nonsocial (arrow) cues. Cues were either directional (indicating left or right) or neutral (indicating no direction), and directional cues were uninformative of the upcoming target location in order to engage automatic processes by minimizing expectations. Behavioral results demonstrated intact orienting effects for social and nonsocial cues, with no differences between groups. The imaging results, however, revealed clear group differences in brain activity. When attention was directed by social cues compared to nonsocial cues, the TD group showed increased activity in frontoparietal attention networks, visual processing regions, and the striatum, whereas the ASD group only showed increased activity in the superior parietal lobule. Significant group × cue type interactions confirmed greater responsivity in task-relevant networks for social cues than nonsocial cues in TD as compared to ASD, despite similar behavioral performance. These results indicate that, in the autistic brain, social cues are not assigned the same privileged status as they are in the typically developing brain. These findings provide the first empirical evidence that the neural circuitry involved in social orienting is disrupted in ASD and highlight that normative behavioral performance in a laboratory setting may reflect compensatory mechanisms rather than intact social attention.

Impairments to visual disengagement in autism spectrum disorder: A review of experimental studies from infancy to adulthood

“…The authors found that both groups performed similarly on both cue types, with more errors for invalid cueing than valid cueing. Finally, Green et al (2011) also report similar performance between adolescence with ASD and their TD peers. When presented with eye gaze directional cues and arrow cues, both groups performed similarly.…”

“…Quick disengagement from faces has also been reported in children with Fragile X Syndrome, a disorder with symptomology closely associated with ASD (Williams et al, 2013). When presented with social cues to direct their spatial attention in orienting task, or social stimuli in Gap-Overlap tasks, individuals with ASD have been reported to respond more (Stauder et al, 2011;Senju et al, 2004;Stauder et al, 2011;Sacrey et al, 2013) or similarly to their TD peers (Fischer et al, 2013;Vlamings et al, 2005;Pruett et al, 2011;Kuhn et al, 2010;Green et al, 2011). As noted previously, differences in stimuli and methodologies likely account for the incongruent results across studies.…”

“…Further examination of the methodologies of these ten studies reveals similarities that may have contributed to the discordant results. First, several of the studies report ISI durations of longer than 1000 ms between the presentation of the central and peripheral stimulus (Chawarska et al, 2010;Fischer et al, 2013;Kikuchi et al, 2011;Kawakubo et al, 2004;Mosconi et al, 2009;Pruett et al, 2011; data not available for Green et al, 2011). Examination of the effects of variable ISI durations indicates that ASD are slower to disengage at short ISIs (under 500 ms) but are no different from TD at longer ISIs (800 ms or longer; Harris et al, 1999;Casey et al, 1993;Townsend et al, 1996aTownsend et al, ,b, 1999Wainwright-Sharp and Bryson, 1993; also replicated in recent meta-analysis by Landry and Parker, 2013).…”

Differentiating High-Functioning Autism and Social Phobia

“…In ASD, research shows that social orienting is associated with a much less widespread pattern of brain activations, as measured by fMRI, than in typically developing individuals, in spite of a lack of difference in behavioral performance compared to controls (Greene et al 2011). Such findings suggest a privileged status for social cues in the typically developing, but not ASD brain.…”

Teaching children with autism to attend to socially relevant stimuli

“…In addition to research focused on identifying attention deficits in children with autism, a multitude of experimental studies aim to distinguish attention deficits by classifying them within complex information processing (Goldstein et al, 2001) or deficiencies of executive function (Rinehart et al, 2001) and others approach the topic from a neurocognitive perspective wherein deficits in shifting attention are thought to be caused by dysfunctions in underlying neurological mechanisms and cerebral pathology (Courchesne et al, 1994;Greene et al, 2011). While the priority of previous research has been on identifying shifting attention impairments in children with autism and classifying the orientation of such deficits, it is imperative that current research also emphasize finding methods for effective treatment of such deficits.…”