Autism spectrum disorder, but not amygdala lesions, impairs social attention in visual search

Abstract

People with autism spectrum disorders (ASD) have pervasive impairments in social interactions, a diagnostic component that may have its roots in atypical social motivation and attention. One of the brain structures implicated in the social abnormalities seen in ASD is the amygdala. To further characterize the impairment of people with ASD in social attention, and to explore the possible role of the amygdala, we employed a series of visual search tasks with both social (faces and people with different postures, emotions, ages, and genders) and non-social stimuli (e.g., electronics, food, and utensils). We first conducted trial-wise analyses of fixation properties and elucidated visual search mechanisms. We found that an attentional mechanism of initial orientation could explain the detection advantage of non-social targets. We then zoomed into fixation-wise analyses. We defined target-relevant effects as the difference in the percentage of fixations that fell on target-congruent vs. target-incongruent items in the array. In Experiment 1, we tested 8 high-functioning adults with ASD, 3 adults with focal bilateral amygdala lesions, and 19 controls. Controls rapidly oriented to target-congruent items and showed a strong and sustained preference for fixating them. Strikingly, people with ASD oriented significantly less and more slowly to target-congruent items, an attentional deficit especially with social targets. By contrast, patients with amygdala lesions performed indistinguishably from controls. In Experiment 2, we recruited a different sample of 13 people with ASD and 8 healthy controls, and tested them on the same search arrays but with all array items equalized for low-level saliency. The results replicated those of Experiment 1. In Experiment 3, we recruited 13 people with ASD, 8 healthy controls, 3 amygdala lesion patients and another group of 11 controls and tested them on a simpler array. Here our group effect for ASD strongly diminished and all four subject groups showed similar target-relevant effects. These findings argue for an attentional deficit in ASD that is disproportionate for social stimuli, cannot be explained by low-level visual properties of the stimuli, and is more severe with high-load top-down task demands. Furthermore, this deficit appears to be independent of the amygdala, and not evident from general social bias independent of the target-directed search.

Keywords: Amygdala; Autism; Saliency; Social; Visual search.

Fig. 1

Task and sample stimuli. (A) Task structure. A target is presented for 1 s followed by the search array. Subjects have a maximum of 14 s to respond by pressing the space bar to indicate that the target is present, or the letter ‘N’ to indicate that the target is absent. Following target detection, subjects provide a mouse click on target. A feedback message of ‘Correct’, ‘Incorrect’ or ‘Time Out’ is displayed for 1 s before an ITI of 1–2 s. (B) Sample visual search arrays with fixations. Left: standard array used in Experiment 2. Right: simple array used in Experiment 3. Each circle represents a fixation. Green circle: start fixation. Magenta circle: end fixation. Yellow line: eye movement (saccade). Red box: target. Items in the search arrays are cropped and modified from Sasson et al. (2008). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 2

Behavioral performance for (A, B) Experiment 1, (C, D) Experiment 2, and (E, F) Experiment 3. (A, C, and E) Percentage of correct response. (B, D, and F) Reaction time (RT). Error bars denote one SEM of the mean. All trials analyzed in this figure are target-present trials.

Fig. 3

Quantification of fixation properties. All trials analyzed in this figure are target-present trials. (A–C) Distribution of the total number of fixations for social and non-social targets. (D–F) Average number of fixations for each condition. (G–I) Average fixation duration on array item. (J–L) The serial order of fixation that first landed on target. (M–O) Percentage of trials with missing detection of target despite direct fixation on the target. (P–R) Latency from first fixation onto target to detection of target. (S–U) Average number of fixations on social and non-social items. (A, D, G, J, M, P, and S) Experiment 1. (B, E, H, K, N, Q, and T) Experiment 2. (C, F, I, L, O, R, and U) Experiment 3. Error bars denote one SEM across subjects.

Fig. 3

Quantification of fixation properties. All trials analyzed in this figure are target-present trials. (A–C) Distribution of the total number of fixations for social and non-social targets. (D–F) Average number of fixations for each condition. (G–I) Average fixation duration on array item. (J–L) The serial order of fixation that first landed on target. (M–O) Percentage of trials with missing detection of target despite direct fixation on the target. (P–R) Latency from first fixation onto target to detection of target. (S–U) Average number of fixations on social and non-social items. (A, D, G, J, M, P, and S) Experiment 1. (B, E, H, K, N, Q, and T) Experiment 2. (C, F, I, L, O, R, and U) Experiment 3. Error bars denote one SEM across subjects.

Fig. 4

General social preference. (A) Experiment 1. (B) Experiment 2. (C) Experiment 3. We calculated social preference as the average number of fixations (irrespective of task condition) across all trials that fell onto social stimuli, minus the average number of fixations that fell onto non-social stimuli, expressed as a percentage.

Fig. 5

Social and non-social target effects. In Experiment 1, all subjects looked at target-congruent items in a fast and sustained manner. (A, B) Amygdala patients. (C, D) People with ASD. (E, F) General controls. (G, H) NUS controls. Red: social items. Blue: non-social items. Upper row (A, C, E, and G): when searching for social targets. Lower row (B, D, F, and H): when searching for non-social targets. Asterisk indicates significant difference between target-congruent items and target-incongruent items (two-tailed paired t-test: p<0.05). Shaded area denotes ±SEM over the group of subjects. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 6

Target-relevant effects. (A, B) Experiment 1. (C, D) Experiment 2. (E, F) Experiment 3. People with ASD have reduced attention towards social items when searching for social targets (A, C), an impairment that is less severe when searching for non-social targets (B, D) and with simpler search arrays (E, F).