Influence of anxiety and alexithymia on brain activations associated with the perception of others’ pain in autism

ABSTRACT

The circumstances under which empathy is altered in ASD remain unclear, as previous studies did not systematically find differences in brain activation between ASD and controls in empathy-eliciting paradigms, and did not always monitor whether differences were primarily due to ASD “per se”, or to conditions overlapping with ASD, such as alexithymia and anxiety. Here, we collected fMRI data from 47 participants (22 ASD) viewing pictures depicting hands and feet of unknown others in painful, disgusting, or neutral situations. We computed brain activity for painful and disgusting stimuli (vs. neutral) in whole brain and in regions of interest among the brain areas typically activated during the perception of nociceptive stimuli. Group differences in brain activation disappeared when either alexithymia or anxiety – both elevated in the ASD group – were controlled for. Regression analyses indicated that the influence of symptoms was mainly shared between autistic symptomatology, alexithymia and anxiety or driven by unique contributions from alexithymia or anxiety. Our results suggest that affective empathy may be affected in ASD, but that this association is complex. The respective contribution of alexithymia and anxiety to decreased affective empathy of people with ASD may be due to the association of those psychiatric conditions with reduced motor resonance/Theory of Mind.

KEYWORDS:

• Empathy
• ASD
• alexithymia
• anxiety
• fMRI

Acknowledgments

We want to thank Ophélie Rogier for her help in data acquisition, Karine Métrailler and Carole Burget for their support in participant’s recruitment and administrative assistance, and Anthony Lissot and Torsten Ruest for their help in data analysis.

Disclosure statement

No potential conflict of interest was reported by the authors.

Supplemental Material

Supplemental data for this article can be accessed here.

Notes

¹ 11 were diagnosed with Asperger Syndrome (AS), 6 were diagnosed with Autism Spectrum Disorder (ASD), and 2 were diagnosed with Pervasive Developmental Disorder Not Otherwise Specified (PDD-NOS).

² In Benuzzi et al. (2008), after each experiment, the 14 participants were asked to rate how disgusting (D) and painful (P) the video clips were on two separate 0–10 point scales; in each trial, the volunteers were asked to rate the perceived unpleasantness (U) of the stimulus. The video clips rated as the most painful or the most disgusting were selected for the present fMRI study. The ratings obtained by Benuzzi et al. (2008) for the stimuli we selected for the present study were the following: painful (mean P:7.98, sd:1.55), disgusting (mean D:4.56, sd:2.01), neutral (mean P:0.12, sd:0.32/ mean D:0.04, sd:0.14).

³ The behavioral data were not collected in one participant with ASD (female) and 3 control participants (all males), due to the behavioral response not being recorded during the experiment. Among the remaining 35 subjects (17 controls) 4 male subjects (1 with ASD) recognized none of the stimuli, for at least one category. Those were therefore excluded from the behavioral analyses, which included 31 subjects (14 controls).

⁴ Note that we included 39 subjects in this analysis. However, when the analysis was conducted with the 31 subjects included in the behavioral analysis, we obtained similar results (see supplementary materials).

Additional information

Funding

This work was supported by the Swiss National Science Foundation (PP00P3-130191 to NH), the Centre d’Imagerie BioMédicale (CIBM) of the University of Lausanne (UNIL), as well as the Foundation Rossi Di Montalera and the LifeWatch foundation. The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; and preparation, review, or approval of the manuscript. The authors report no potential conflict of interest.