Altered neuronal habituation to hearing others’ pain in adults with autistic traits

Abstract

This study tested the hypothesis that autistic traits influence the neuronal habituation that underlies the processing of others’ pain. Based on their autism-spectrum quotient (AQ), two groups of participants were classified according to their autistic traits: High-AQ and Low-AQ groups. Their event-related potentials in response to trains of three identical audio recordings, exhibiting either painful or neutral feelings of others, were compared during three experimental tasks. (1) In a Pain Judgment Task, participants were instructed to focus on pain-related cues in the presented audio recordings. (2) In a Gender Judgment Task, participants were instructed to focus on non-pain-related cues in the presented audio recordings. (3) In a Passive Listening Task, participants were instructed to passively listen. In the High-AQ group, an altered empathic pattern of habituation, indexed by frontal-central P2 responses of the second repeated painful audio recordings, was found during the Passive Listening Task. Nevertheless, both High-AQ and Low-AQ groups exhibited similar patterns of habituation to hearing others’ voices, both neutral and painful, in the Pain Judgment and Gender Judgment Tasks. These results suggest altered empathic neuronal habituation in the passive processing of others’ vocal pain by individuals with autistic traits.

Altered processing of social emotions in individuals with autistic traits

“…After confirming scalp topographies in both single-participant and group-level ERP waveforms, and based on previous studies [34,38], the dominant ERP components involved in Experiment 2 were identified, including early ERP components (N1 and P2) and LNC. N1 and P2 were identified as the most negative and positive deflections, respectively, at 100 -300 ms after the audio recording's onset with maximum distribution at the frontal-central electrodes.…”

“…As suggested by the social motivational theory of ASD [6], we hypothesized that individuals with autistic traits would display a similar alteration of their processing of social-emotional stimuli. In addition, as individuals with autistic traits exhibit worse recognition of negative emotional stimuli [28,38], the present study hypothesized that altered perception of social-emotional stimuli in such individuals would mainly be exhibited in regard to social-negative emotions.…”

“…Then, two subsets of participants, those exhibiting the top 10% and bottom 10% of AQ scores [38,40] from the total of 2,592 undergraduate students were randomly selected and divided into High-AQ (n=30) and Low-AQ (n=30) groups. The detailed demographic characteristics of the participants in the High-AQ and Low AQ groups are listed in Table 1.…”

Processing of expressions by individuals with autistic traits: Empathy deficit or sensory hyper-reactivity?

“…The results showed that when these stimuli were presented only once, no difference was found in the response between ASD individuals and a control group; however, when the stimuli were presented repetitively, the activation in the auditory cortex region of ASD individuals was stronger than that of control individuals [ 23 ]. Our recent study [ 24 ] used event-related potentials (ERPs) to measure the empathic neural responses that were induced by the repetition of three identical audio recordings (human voices, S1_S2_S3) in both high-AQ and low-AQ groups. P2 amplitudes of the second repetition were significantly higher for high-AQ groups rather than for low-AQ groups.…”

“…Reduced habituation (i.e., a change in response over time) was also found in the amygdala of ASD individuals [ 25 ]. Habituation is pervasive in sensory systems; it refers to changes in neural and behavioral responses that accompany prolonged exposure to an adapting stimulus with repeated features [ 24 , 32 ]. This may reflect that ASD individuals have a stronger neural response with increasing appearance of emotional faces.…”