Abstract

Enhanced selective attention toward nonsocial objects and impaired attention to social stimuli constitute key clinical features of autism spectrum disorder (ASD). Yet, the mechanisms associated with atypical selective attention in ASD are poorly understood, which limits the development of more effective interventions. In typically developing individuals, selective attention to social and nonsocial stimuli is associated with the informational value of the stimuli, which is typically learned over the course of repeated interactions with the stimuli. To examine value learning (VL) of social and nonsocial stimuli and its association with selective attention in preschoolers with and without ASD. This case-control study compared children with ASD vs children with developmental delay (DD) and children with typical development (TD) recruited between March 3, 2017, and June 13, 2018, at a university-based research laboratory. Participants were preschoolers with ASD, DD, or TD. Procedure consisted of an eye-tracking gaze-contingent VL task involving social (faces) and nonsocial (fractals) stimuli and consisting of baseline, training, and choice test phases. Outcome measures were preferential attention to stimuli reinforced (high value) vs not reinforced (low value) during training. The hypotheses were stated before data collection. Included were 115 preschoolers with ASD (n = 48; mean [SD] age, 38.30 [15.55] months; 37 [77%] boys), DD (n = 31; mean [SD] age, 45.73 [19.49] months; 19 [61%] boys), or TD (n = 36; mean [SD] age, 36.53 [12.39] months; 22 [61%] boys). The groups did not differ in sex distribution; participants with ASD or TD had similar chronological age; and participants with ASD or DD had similar verbal IQ and nonverbal IQ. After training, the ASD group showed preference for the high-value nonsocial stimuli (mean proportion, 0.61 [95% CI, 0.56-0.65]; P < .001) but not for the high-value social stimuli (mean proportion, 0.51 [95% CI, 0.46-0.56]; P = .58). In contrast, the DD and TD groups demonstrated preference for the high-value social stimuli (DD mean proportion, 0.59 [95% CI, 0.54-0.64]; P = .001 and TD mean proportion, 0.57 [95% CI, 0.53-0.61]; P = .002) but not for the high-value nonsocial stimuli (DD mean proportion, 0.52 [95% CI, 0.44-0.59]; P = .64 and TD mean proportion, 0.50 [95% CI, 0.44-0.57]; P = .91). Controlling for age and nonverbal IQ, autism severity was positively correlated with enhanced learning in the nonsocial domain (r = 0.22; P = .03) and with poorer learning in the social domain (r = -0.26; P = .01). Increased attention to objects in preschoolers with ASD may be associated with enhanced VL in the nonsocial domain. When paired with poor VL in the social domain, enhanced value-driven attention to objects may play a formative role in the emergence of autism symptoms by altering attentional priorities and thus learning opportunities in affected children.

Highlights

  • The groups did not differ in sex distribution; participants with autism spectrum disorder (ASD) or typical development (TD) had similar chronological age; and participants with ASD or developmental delay (DD) had similar verbal IQ and nonverbal IQ

  • Increased attention to objects in preschoolers with ASD may be associated with enhanced value learning (VL) in the nonsocial domain

  • Using a novel VL task, this study found for the first time, to our knowledge, that enhanced valuedriven selective attention in the nonsocial domain is associated with ASD in young children compared with DD and TD

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Summary

Introduction

Impaired selective visual attention to social targets, such as the faces of interactive partners, constitutes a hallmark feature of autism spectrum disorder (ASD)[1] in young children, which has been documented in both laboratory and real-world contexts.[2,3,4,5,6,7,8] Given the wealth of information conveyed by faces and facial gestures, poor attentional attunement to this class of stimuli during prodromal[9,10,11,12,13] and early syndromal stages of the disorder[3,8,14,15] is associated with less favorable social, adaptive, and language outcomes.[16,17,18] Poor selective attention to social targets is typically accompanied by enhanced attention to certain classes of nonsocial stimuli (eg, geometric patterns or idiosyncratic objects), which may draw the child’s limited processing resources toward less socially relevant aspects of the environment.[2,14,19] Despite the importance of atypical selective attention in ASD, both as a core feature and a treatment target, its underlying mechanisms remain poorly understood.In the real world, the number of stimuli placing demand on the sensory system vastly exceeds the processing capacity of an individual. Visual selective attention serves to resolve this problem by prioritizing certain inputs over others for further processing.[20] A key mechanism driving selective attention in human and nonhuman primates is the appraisal of stimuli values.[21,22,23,24] The value of a visual stimulus, whether it be social or nonsocial, is defined by the usefulness or relevance of the information it provides to the individual.[23,25,26,27,28] This information helps individuals gauge the likelihood of favorable or unfavorable outcomes and guides their subsequent behavior. The association between value learning (VL) systems and visual attention have been demonstrated in primates on neuroanatomical and neurophysiological levels,[26,29] and there is extensive evidence that previously reinforced (high value [HV]) stimuli are detected faster and attended to longer than nonreinforced (low value [LV]) stimuli in typically developing children and adults.[30,31,32,33] The present study sought to investigate whether observed impairments in selective attention among young children with ASD are associated with atypical VL across social and nonsocial domains

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