Attentional Capture In ASD: A Combined fMRI-EEG Study

Background: Previous descriptions of attentional modulation in autism spectrum disorder (ASD) are paradoxical; individuals with ASD are described as over-focused, yet susceptible to distraction. The coordination of goal-directed and stimulus-driven attentional processes is vital for the selection of behaviorally-relevant information. Contingent attentional capture, as when a task-irrelevant stimulus sharing a task-relevant feature captures attention, is one such example of this top-down/bottom-up interaction.

Objectives: To evaluate the neural basis of top-down and bottom-up attentional modulation during contingent attentional capture in children and adolescents with ASD.

Methods: Participants were nine children and adolescents with ASD and 16 age- and IQ-matched typically developing (TD) children and adolescents. The study consisted of separate functional magnetic resonance imaging (fMRI) and electroencephalography (EEG) / eye-tracking sessions of a rapid serial visual presentation experiment. Stimuli included three streams of numbers (0–9). Each trial lasted 480ms and consisted of four iterations of simultaneously varying numbers (120ms per iteration). The central stream was composed of numbers of various colors. Digits presented in the peripheral streams were gray in most trials; colored peripheral distractors appeared infrequently in either the left or right peripheral streams and were either the same color as the target (red) or a non-target color that did not appear in the center stream (green). Participants were required to respond via button press to the identity of targets (red numbers) appearing only in the central stream (left button ≤ 4; right button ≥ 5).  On target present trials, a red number occurred in the center stream on the third iteration with or without the appearance of target- and non-target-colored peripheral distractors.  For target absent trials, no red number appeared in the center stream with the appearance of either target- or non-target-colored peripheral distractors. Participants completed four 6-minute runs for the fMRI session and sixteen 3-minute blocks for the EEG/eye-tracking session.

Results: No group difference in error rates to target present trials was found; both groups had increased error rates to target present trials with target-colored as compared to non-target-colored distractors.  To isolate attentional capture from target- and response-related activation, only target absent trials were examined for fMRI data. There were no group differences in activation to non-target-colored distractors.  For target-colored distractor trials, individuals with ASD exhibited greater activation of dorsal frontal-parietal regions; TD individuals exhibited greater activation of anterior cingulate cortex (ACC).  Correlational analyses revealed that reduced activation of ACC was related to greater social impairment in ASD. Analysis of EEG and eye-tracking data is ongoing.

Conclusions: In both groups, to-be-ignored distractors were more likely to capture attention when sharing a task-relevant feature. Activation to target-colored distractors was increased in the ASD group within the network responsible for endogenous control of visual attention, whereas it was atypically reduced in ACC, a region associated with task-control. Correlation of this latter finding with social impairment may suggest a crucial role of ACC dysfunction in ASD, consistent with some previous findings.