Abstract
While empathic responses of individuals with autism-spectrum disorder have been reported to be modulated by top-down attention, it remains unclear whether empathy for pain in typically developing individuals with autistic traits also involves such top-down modulation mechanisms. This study employed the autism-spectrum quotient (AQ) to quantify autistic traits in a group of 1,231 healthy adults. Two subset groups (High-AQ and Low-AQ groups) were randomly selected from the highest and lowest 10% AQ scores respectively. We explored whether participants in both groups would differ in their response to others’ pain when their attention was directed toward (A-P tasks) or away (A-N tasks) from pain cues in auditory and visual experimental modalities. Compared to Low-AQ individuals, High-AQ individuals exhibited more suppressed N1 and P2 amplitudes in response to painful vocal cues in auditory A-N tasks. This suggests suppressed attentional and emotional processes of empathy for pain when High-AQ individuals have their attention directed away from others’ pain cues. No significant difference was found between both groups in the auditory A-P task, nor in the visual A-P and A-N tasks. These results suggest that top-down attention modulation of cortical empathic responses to others’ vocal pain is influenced by autistic traits.
Highlights
As a social species, typically developing (TD) human individuals have the ability to empathize with others, i.e., comprehend others’ emotions and feelings as if these were their own[1,2]
The attention allocation of participants is typically manipulated via two different task instructions: (1) a pain judgement task, where participants are instructed to judge the pain experienced by models depicted in pictures, which usually requires participants to direct their attention to the pain cues; (2) a number-counting task, where participants are instructed to count the number of hands depicted in pictures, which directs participants’ attention away from the models’ feelings
Post hoc analyses of variance (ANOVA) indicated that the High-autism-spectrum quotient (AQ) group was slower than the low AQ scores (Low-AQ) group in the auditory modality [reaction times (RTs): F(1,28) = 6.489, p = 0.017, η2 = 0.188; inverse efficiency scores (IESs): F(1,28) = 5.604, p = 0.025, η2 = 0.167]
Summary
Typically developing (TD) human individuals have the ability to empathize with others, i.e., comprehend others’ emotions and feelings as if these were their own[1,2]. In contrast to the number-counting task, the pain judgement task results in increased activation of the pain matrix (e.g., insula, paracingulate, and the left middle frontal gyrus)[4] and a positive shift at late event-related potential (ERP) components (P3 and LPC), indexing the cognitive evaluation of others’ pain[3] in response to the presented pictures These results indicate that the process of evaluation and judgement of others’ pain is influenced by the attention allocation to the depicted pain cues. Amplitudes of early ERP components to empathy for pain (N1 and P2) over the frontal-central area were correlated with subjective reports of the degree of perceived pain in others and of the participants’ personal discomfort These results indicate that the early automatic response indexes emotional sharing and the late response indexes the cognitive evaluation of others’ pain[3]. Since the processes of empathy for pain may not be identical to the recognition of facial expressions, it remains an open question whether empathy for pain in individuals with both ASD and autistic traits would be modulated by top-down attention
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