Study Objectives Converging evidence from neuroimaging, sleep, and genetic studies suggests that dysregulation of thalamocortical interactions mediated by the thalamic reticular nucleus (TRN) contribute to autism spectrum disorder (ASD). Sleep spindles assay TRN function, and their coordination with cortical slow oscillations (SOs) indexes thalamocortical communication. These oscillations mediate memory consolidation during sleep. In the present study, we comprehensively characterized spindles and their coordination with SOs in relation to memory and age in children with ASD. Methods Nineteen children and adolescents with ASD, without intellectual disability, and 18 typically developing (TD) peers, aged 9-17, completed a home polysomnography study with testing on a spatial memory task before and after sleep. Spindles, SOs, and their coordination were characterized during stages 2 (N2) and 3 (N3) non-rapid eye movement sleep. Results ASD participants showed disrupted SO-spindle coordination during N2 sleep. Spindles peaked later in SO upstates and their timing was less consistent. They also showed a spindle density (#/min) deficit during N3 sleep. Both groups showed significant sleep-dependent memory consolidation, but its relations with spindle density differed. While TD participants showed the expected positive correlations, ASD participants showed the opposite. Conclusions The disrupted SO-spindle coordination and spindle deficit provide further evidence of abnormal thalamocortical interactions and TRN dysfunction in ASD. The inverse relations of spindle density with memory suggest a different function for spindles in ASD than TD. We propose that abnormal sleep oscillations reflect genetically mediated disruptions of TRN-dependent thalamocortical circuit development that contribute to the manifestations of ASD and are potentially treatable.
Eye-tracking studies on social attention have consistently shown that humans prefer to attend to other human beings. Much less is known about whether a similar preference is also evident in covert attentional processes. To enable a direct comparison, this study examined covert and overt attentional guidance within two different experimental setups using complex naturalistic scenes instead of isolated single features. In the first experiment, a modified version of the dot-probe paradigm served as a measure of covert reflexive attention toward briefly presented scenes containing a social feature in one half of the visual field compared to nonsocial elements in the other while controlling for low-level visual saliency. Participants showed a stable congruency effect with faster reaction times and fewer errors for probes presented on the social side of the scene. In a second experiment, we tracked eye movements for the same set of stimuli while manipulating the presentation time to allow for differentiating reflexive and more sustained aspects of overt attention. Supportive of the first results, analyses revealed a robust preference for social features concerning initial saccade direction as well as fixation allocation. Collectively, these experiments imply preferential processing of social features over visually salient aspects for automatic allocation of covert as well as overt attention.
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