Altered Neuronal Habituation to Hearing Others' Pain in Adults with Autistic Traits

Overview

Journal Sci Rep

Specialty Science

Date 2020 Sep 15

PMID 32929157

Citations 7

Authors

Jing Meng

Zuoshan Li

Lin Shen

Affiliations

Soon will be listed here.

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.

Citing Articles

Group empathy for pain is stronger than individual empathy for pain in the auditory modality.

Shao M, Qiu Y, Zhang Y, Qian H, Wei Z, Hong M Soc Cogn Affect Neurosci. 2024; 19(1).

PMID: 39417280 PMC: 11523625. DOI: 10.1093/scan/nsae074.

Intact painful sensation but enhanced non-painful sensation in individuals with autistic traits.

Qian H, Shao M, Wei Z, Zhang Y, Liu S, Chen L Front Psychiatry. 2024; 15:1432149.

PMID: 39045552 PMC: 11263351. DOI: 10.3389/fpsyt.2024.1432149.

The relationship between autistic traits and the stress of social isolation: Development of an explanatory model.

Shao M, Luo S, Qian H, Li X, Wei Z, Hong M Heliyon. 2024; 10(4):e26082.

PMID: 38404812 PMC: 10884416. DOI: 10.1016/j.heliyon.2024.e26082.

The Empathy for Pain Stimuli System (EPSS): Development and preliminary validation.

Meng J, Li Y, Luo L, Li L, Jiang J, Liu X Behav Res Methods. 2023; 56(2):784-803.

PMID: 36862304 PMC: 10830729. DOI: 10.3758/s13428-023-02087-4.

Empathy for pain in individuals with autistic traits during observation of static and dynamic stimuli.

Li Y, Wei Z, Shao M, Hong M, Yang D, Luo L Front Psychiatry. 2022; 13:1022087.

PMID: 36465286 PMC: 9709309. DOI: 10.3389/fpsyt.2022.1022087.

References

de Vignemont F, Singer T . The empathic brain: how, when and why?. Trends Cogn Sci. 2006; 10(10):435-41. DOI: 10.1016/j.tics.2006.08.008. View

Fitzgibbon B, Giummarra M, Georgiou-Karistianis N, Enticott P, Bradshaw J . Shared pain: from empathy to synaesthesia. Neurosci Biobehav Rev. 2009; 34(4):500-12. DOI: 10.1016/j.neubiorev.2009.10.007. View

Decety J, Jackson P . The functional architecture of human empathy. Behav Cogn Neurosci Rev. 2004; 3(2):71-100. DOI: 10.1177/1534582304267187. View

Danziger N, Prkachin K, Willer J . Is pain the price of empathy? The perception of others' pain in patients with congenital insensitivity to pain. Brain. 2006; 129(Pt 9):2494-507. DOI: 10.1093/brain/awl155. View

Gu X, Han S . Attention and reality constraints on the neural processes of empathy for pain. Neuroimage. 2007; 36(1):256-67. DOI: 10.1016/j.neuroimage.2007.02.025. View

Fan Y, Han S . Temporal dynamic of neural mechanisms involved in empathy for pain: an event-related brain potential study. Neuropsychologia. 2007; 46(1):160-73. DOI: 10.1016/j.neuropsychologia.2007.07.023. View

Meng J, Shen L, Li Z, Peng W . Top-down attention modulation on the perception of others' vocal pain: An event-related potential study. Neuropsychologia. 2019; 133:107177. DOI: 10.1016/j.neuropsychologia.2019.107177. View

Lazar S, Evans D, Myers S, Moreno-De Luca A, Moore G . Social cognition and neural substrates of face perception: implications for neurodevelopmental and neuropsychiatric disorders. Behav Brain Res. 2014; 263:1-8. DOI: 10.1016/j.bbr.2014.01.010. View

Baron-Cohen S, Wheelwright S, Skinner R, Martin J, Clubley E . The autism-spectrum quotient (AQ): evidence from Asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. J Autism Dev Disord. 2001; 31(1):5-17. DOI: 10.1023/a:1005653411471. View

10.

Gokcen E, Petrides K, Hudry K, Frederickson N, Smillie L . Sub-threshold autism traits: the role of trait emotional intelligence and cognitive flexibility. Br J Psychol. 2014; 105(2):187-99. PMC: 4209115. DOI: 10.1111/bjop.12033. View

11.

Baron-Cohen S, Wheelwright S . The empathy quotient: an investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences. J Autism Dev Disord. 2004; 34(2):163-75. DOI: 10.1023/b:jadd.0000022607.19833.00. View

12.

Poljac E, Poljac E, Wagemans J . Reduced accuracy and sensitivity in the perception of emotional facial expressions in individuals with high autism spectrum traits. Autism. 2012; 17(6):668-80. DOI: 10.1177/1362361312455703. View

13.

Meng J, Shen L, Li Z, Peng W . Top-down Effects on Empathy for Pain in Adults with Autistic Traits. Sci Rep. 2019; 9(1):8022. PMC: 6541648. DOI: 10.1038/s41598-019-44400-2. View

14.

Millin R, Kolodny T, Flevaris A, Kale A, Schallmo M, Gerdts J . Reduced auditory cortical adaptation in autism spectrum disorder. Elife. 2018; 7. PMC: 6203433. DOI: 10.7554/eLife.36493. View

15.

Lawson R, Aylward J, White S, Rees G . A striking reduction of simple loudness adaptation in autism. Sci Rep. 2015; 5:16157. PMC: 4633623. DOI: 10.1038/srep16157. View

16.

Puts N, Wodka E, Tommerdahl M, Mostofsky S, Edden R . Impaired tactile processing in children with autism spectrum disorder. J Neurophysiol. 2014; 111(9):1803-11. PMC: 4044368. DOI: 10.1152/jn.00890.2013. View

17.

Fiorentini C, Gray L, Rhodes G, Jeffery L, Pellicano E . Reduced face identity aftereffects in relatives of children with autism. Neuropsychologia. 2012; 50(12):2926-2932. DOI: 10.1016/j.neuropsychologia.2012.08.019. View

18.

Mosconi M, Luna B, Kay-Stacey M, Nowinski C, Rubin L, Scudder C . Saccade adaptation abnormalities implicate dysfunction of cerebellar-dependent learning mechanisms in Autism Spectrum Disorders (ASD). PLoS One. 2013; 8(5):e63709. PMC: 3660571. DOI: 10.1371/journal.pone.0063709. View

19.

Hudac C, DesChamps T, Arnett A, Cairney B, Ma R, Webb S . Early enhanced processing and delayed habituation to deviance sounds in autism spectrum disorder. Brain Cogn. 2018; 123:110-119. PMC: 5893357. DOI: 10.1016/j.bandc.2018.03.004. View

20.

Tam F, King J, Geisler D, Korb F, Sareng J, Ritschel F . Altered behavioral and amygdala habituation in high-functioning adults with autism spectrum disorder: an fMRI study. Sci Rep. 2017; 7(1):13611. PMC: 5648793. DOI: 10.1038/s41598-017-14097-2. View