Journal of the Korean Academy of Child and Adolescent Psychiatry

Korean Academy of Child and Adolescent Psychiatry (대한소아청소년정신의학회)
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The Relationship Between Brain Activation for Taking Others' Perspective and Interoceptive Abilities in Autism Spectrum Disorder: An fMRI Study

  • Huiyeong Jeon (Department of Psychiatry, Chungbuk National University Hospital) ;
  • Ahjeong Hur (Department of Psychology, Chungbuk National University) ;
  • Hoyeon Lee (Autism and Developmental Disorders Treatment Center, Chungbuk National University Hospital) ;
  • Yong-Wook Shin (Department of Psychiatry, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Sang-Ick Lee (Department of Psychiatry, Chungbuk National University Hospital) ;
  • Chul-Jin Shin (Department of Psychiatry, Chungbuk National University Hospital) ;
  • Siekyeong Kim (Department of Psychiatry, Chungbuk National University Hospital) ;
  • Gawon Ju (Department of Psychiatry, Chungbuk National University Hospital) ;
  • Jeonghwan Lee (Department of Psychiatry, Chungbuk National University Hospital) ;
  • Joon Hyung Jung (Department of Psychiatry, Chungbuk National University Hospital) ;
  • Seungwon Chung (Department of Psychiatry, Chungbuk National University Hospital) ;
  • Jung-Woo Son (Department of Psychiatry, Chungbuk National University Hospital)
  • Received : 2024.03.11
  • Accepted : 2024.05.07
  • Published : 2024.07.01
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Abstract

Objectives: In this functional magnetic resonance imaging study, we aimed to investigate the differences in brain activation between individuals with autism spectrum disorder (ASD) and typically developing (TD) individuals during perspective taking. We also examined the association between brain activation and empathic and interoceptive abilities. Methods: During scanning, participants from the ASD (n=17) and TD (n=22) groups were shown pain stimuli and asked to rate the level of the observed pain from both self- and other-perspectives. Empathic abilities, including perspective taking, were measured using an empathic questionnaire, and three dimensions of interoception were assessed: interoceptive accuracy, interoceptive sensibility, and interoceptive trait prediction errors. Results: During self-perspective taking, the ASD group exhibited greater activation in the left precuneus than the TD group. During other-perspective taking, relative hyperactivation extended to areas including the right precuneus, right superior frontal gyrus, left caudate nucleus, and left amygdala. Brain activation levels in the right superior frontal gyrus while taking other-perspective were negatively correlated with interoceptive accuracy, and those in the left caudate were negatively correlated with perspective taking ability in the ASD group. Conclusion: Individuals with ASD show atypical brain activation during perspective taking. Notably, their brain regions associated with stress reactions and escape responses are overactivated when taking other-perspective. This overactivity is related to poor interoceptive accuracy, suggesting that individuals with ASD may experience difficulties with the self-other distinction or atypical embodiment when considering another person's perspective.

Keywords

Acknowledgement

The authors would like to thank all the participants and their parents who participated in this study for their commitment. The authors are also grateful to the staff at Autism and Developmental Treatment Center in Chungbuk National University Hospital.

References

  1. American Psychiatric Association. Diagnostic and statistical manual of mental disorders. 5th ed. Arlington: American Psychiatric Association;2013. 
  2. Hwang JW, Lee JS. Korean clinical guideline for autism spectrum disorder - clinical features, course, epidemiology, and cause. J Korean Acad Child Adolesc Psychiatry 2024;35:8-14.  https://doi.org/10.5765/jkacap.230040
  3. Blakemore SJ, Choudhury S. Development of the adolescent brain: implications for executive function and social cognition. J Child Psychol Psychiatry 2006;47:296-312.  https://doi.org/10.1111/j.1469-7610.2006.01611.x
  4. Healey ML, Grossman M. Cognitive and affective perspective-taking: evidence for shared and dissociable anatomical substrates. Front Neurol 2018;9:491. 
  5. Israelashvili J, Sauter D, Fischer A. Two facets of affective empathy: concern and distress have opposite relationships to emotion recognition. Cogn Emot 2020;34:1112-1122.  https://doi.org/10.1080/02699931.2020.1724893
  6. Song Y, Nie T, Shi W, Zhao X, Yang Y. Empathy impairment in individuals with autism spectrum conditions from a multidimensional perspective: a meta-analysis. Front Psychol 2019;10:1902. 
  7. Jackson PL, Brunet E, Meltzoff AN, Decety J. Empathy examined through the neural mechanisms involved in imagining how I feel versus how you feel pain. Neuropsychologia 2006;44:752-761.  https://doi.org/10.1016/j.neuropsychologia.2005.07.015
  8. Decety J, Chen C, Harenski C, Kiehl KA. An fMRI study of affective perspective taking in individuals with psychopathy: imagining another in pain does not evoke empathy. Front Hum Neurosci 2013;7:489. 
  9. Craig AD. Interoception: the sense of the physiological condition of the body. Curr Opin Neurobiol 2003;13:500-505.  https://doi.org/10.1016/S0959-4388(03)00090-4
  10. Damasio A, Carvalho GB. The nature of feelings: evolutionary and neurobiological origins. Nat Rev Neurosci 2013;14:143-152.  https://doi.org/10.1038/nrn3403
  11. Ondobaka S, Kilner J, Friston K. The role of interoceptive inference in theory of mind. Brain Cogn 2017;112:64-68.  https://doi.org/10.1016/j.bandc.2015.08.002
  12. Shah P, Catmur C, Bird G. From heart to mind: Linking interoception, emotion, and theory of mind. Cortex 2017;93:220-223.  https://doi.org/10.1016/j.cortex.2017.02.010
  13. von Mohr M, Finotti G, Villani V, Tsakiris M. Taking the pulse of social cognition: cardiac afferent activity and interoceptive accuracy modulate emotional egocentricity bias. Cortex 2021;145:327-340.  https://doi.org/10.1016/j.cortex.2021.10.004
  14. Quattrocki E, Friston K. Autism, oxytocin and interoception. Neurosci Biobehav Rev 2014;47:410-430.  https://doi.org/10.1016/j.neubiorev.2014.09.012
  15. Garfinkel SN, Seth AK, Barrett AB, Suzuki K, Critchley HD. Knowing your own heart: distinguishing interoceptive accuracy from interoceptive awareness. Biol Psychol 2015;104:65-74.  https://doi.org/10.1016/j.biopsycho.2014.11.004
  16. Lord C, Rutter M, DiLavore PC, Risi S, Gotham K, Bishop S. Autism diagnostic observation schedule, second edition (ADOS-2) manual (part I): modules 1-4. Torrance: Western Psychological Services;2012. 
  17. Yoo SW, Kim YS, Noh JS, Oh KS, Kim CH, Namkoong K, et al. [Validity of Korean version of the mini-international neuropsychiatric interview]. Anxiety Mood 2006;2:50-55. Korean 
  18. Sheehan DV, Sheehan KH, Shytle RD, Janavs J, Bannon Y, Rogers JE, et al. Reliability and validity of the mini international neuropsychiatric interview for children and adolescents (MINI-KID). J Clin Psychiatry 2010;71:313-326.  https://doi.org/10.4088/JCP.09m05305whi
  19. Hwang K, Oh SW. [Validity of the K-WISC-IV short forms]. Kor J Clin Psychol 2017;36:381-390. Korean  https://doi.org/10.15842/kjcp.2017.36.3.008
  20. Choe AY, Hwang ST, Kim JH, Park KB, Chey J, Hong SH. [Validity of the K-WAIS-IV short forms]. Kor J Clin Psychol 2014;33:413-428. Korean  https://doi.org/10.15842/kjcp.2014.33.2.011
  21. Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971;9:97-113.  https://doi.org/10.1016/0028-3932(71)90067-4
  22. Davis MH. A multidimensional approach to individual differences in empathy. JCAS Cat Sel Doc Psychol 1980;75:989-1015. 
  23. Kang I, Kee S, Kim SE, Jeong B, Hwang JH, Song JE, et al. [Reliability and validity of the Korean-version of interpersonal reactivity index]. J Korean Neuropsychiatr Assoc 2009;48:352-358. Korean 
  24. Schandry R. Heart beat perception and emotional experience. Psychophysiology 1981;18:483-488.  https://doi.org/10.1111/j.1469-8986.1981.tb02486.x
  25. Cabrera A, Kolacz J, Pailhez G, Bulbena-Cabre A, Bulbena A, Porges SW. Assessing body awareness and autonomic reactivity: factor structure and psychometric properties of the body perception questionnaire-short form (BPQ-SF). Int J Methods Psychiatr Res 2018;27:e1596. 
  26. Garfinkel SN, Tiley C, O'Keeffe S, Harrison NA, Seth AK, Critchley HD. Discrepancies between dimensions of interoception in autism: implications for emotion and anxiety. Biol Psychol 2016;114:117-126.  https://doi.org/10.1016/j.biopsycho.2015.12.003
  27. Paulus FM, Muller-Pinzler L, Walper D, Marx S, Hamschmidt L, Rademacher L, et al. Image database to supplement "Paulus, F.M. et al. Pain empathy but not surprise in response to unexpected action explains arousal related pupil dilation." (VIPER database) [Internet]. Geneva: Zenodo;2017 [cited 2024 Mar 14]. Available from: https://doi.org/10.5281/zenodo.322426. 
  28. Rolls ET, Huang CC, Lin CP, Feng J, Joliot M. Automated anatomical labelling atlas 3. Neuroimage 2020;206:116189. 
  29. Brett M, Anton JL, Valabregue R, Poline JB. Region of interest analysis using an SPM toolbox (abstract 497). Proceedings of the 8th International Conference on Functional Mapping of the Human Brain; 2002 Jun 2-6; Sendai: Japan. Orlando: Academic Press;2002. 
  30. Chung S, Son JW, Lee S, Ghim HR, Lee SI, Shin CJ, et al. [Neural correlates of cognitive and emotional empathy in patients with autism spectrum disorder]. J Korean Acad Child Adolesc Psychiatry 2016;27:196-206. Korean  https://doi.org/10.5765/jkacap.2016.27.3.196
  31. Dziobek I, Rogers K, Fleck S, Bahnemann M, Heekeren HR, Wolf OT, et al. Dissociation of cognitive and emotional empathy in adults with Asperger syndrome using the multifaceted empathy test (MET). J Autism Dev Disord 2008;38:464-473.  https://doi.org/10.1007/s10803-007-0486-x
  32. Butera C, Kaplan J, Kilroy E, Harrison L, Jayashankar A, Loureiro F, et al. The relationship between alexithymia, interoception, and neural functional connectivity during facial expression processing in autism spectrum disorder. Neuropsychologia 2023;180:108469. 
  33. Schauder KB, Mash LE, Bryant LK, Cascio CJ. Interoceptive ability and body awareness in autism spectrum disorder. J Exp Child Psychol 2015;131:193-200.  https://doi.org/10.1016/j.jecp.2014.11.002
  34. Nicholson TM, Williams DM, Grainger C, Christensen JF, Calvo-Merino B, Gaigg SB. Interoceptive impairments do not lie at the heart of autism or alexithymia. J Abnorm Psychol 2018;127:612-622.  https://doi.org/10.1037/abn0000370
  35. Nicholson T, Williams D, Carpenter K, Kallitsounaki A. Interoception is impaired in children, but not adults, with autism spectrum disorder. J Autism Dev Disord 2019;49:3625-3637.  https://doi.org/10.1007/s10803-019-04079-w
  36. Shah P, Catmur C, Bird G. Emotional decision-making in autism spectrum disorder: the roles of interoception and alexithymia. Mol Autism 2016;7:43. 
  37. Williams ZJ, Suzman E, Bordman SL, Markfeld JE, Kaiser SM, Dunham KA, et al. Characterizing interoceptive differences in autism: a systematic review and meta-analysis of case-control studies. J Autism Dev Disord 2023;53:947-962.  https://doi.org/10.1007/s10803-022-05656-2
  38. Corradi-Dell'Acqua C, Hofstetter C, Vuilleumier P. Felt and seen pain evoke the same local patterns of cortical activity in insular and cingulate cortex. J Neurosci 2011;31:17996-18006.  https://doi.org/10.1523/JNEUROSCI.2686-11.2011
  39. Dadario NB, Sughrue ME. The functional role of the precuneus. Brain 2023;146:3598-3607.  https://doi.org/10.1093/brain/awad181
  40. Cheng W, Rolls ET, Gu H, Zhang J, Feng J. Autism: reduced connectivity between cortical areas involved in face expression, theory of mind, and the sense of self. Brain 2015;138(Pt 5):1382-1393.  https://doi.org/10.1093/brain/awv051
  41. Wise SP, Boussaoud D, Johnson PB, Caminiti R. Premotor and parietal cortex: corticocortical connectivity and combinatorial computations. Annu Rev Neurosci 1997;20:25-42.  https://doi.org/10.1146/annurev.neuro.20.1.25
  42. Meister I, Krings T, Foltys H, Boroojerdi B, Muller M, Topper R, et al. Effects of long-term practice and task complexity in musicians and nonmusicians performing simple and complex motor tasks: implications for cortical motor organization. Hum Brain Mapp 2005;25:345-352.  https://doi.org/10.1002/hbm.20112
  43. Palmer CE, Tsakiris M. Going at the heart of social cognition: is there a role for interoception in self-other distinction? Curr Opin Psychol 2018;24:21-26.  https://doi.org/10.1016/j.copsyc.2018.04.008
  44. Paulus MP, Stein MB. An insular view of anxiety. Biol Psychiatry 2006;60:383-387.  https://doi.org/10.1016/j.biopsych.2006.03.042
  45. Conner CM, White SW, Beck KB, Golt J, Smith IC, Mazefsky CA. Improving emotion regulation ability in autism: the emotional awareness and skills enhancement (EASE) program. Autism 2019;23:1273-1287.  https://doi.org/10.1177/1362361318810709
  46. Loftus T, Mathersul DC, Ooi M, Yau SH. The efficacy of mindfulness-based therapy for anxiety, social skills, and aggressive behaviors in children and young people with autism spectrum disorder: a systematic review. Front Psychiatry 2023;14:1079471. 
  47. Korner A, Topolinski S, Strack F. Routes to embodiment. Front Psychol 2015;6:940. 
  48. Dijkstra K, Post L. Mechanisms of embodiment. Front Psychol 2015;6:1525. 
  49. Erle TM. Level-2 visuo-spatial perspective-taking and interoception - More evidence for the embodiment of perspective-taking. PLoS One 2019;14:e0219005. 
  50. Baiano C, Job X, Santangelo G, Auvray M, Kirsch LP. Interactions between interoception and perspective-taking: current state of research and future directions. Neurosci Biobehav Rev 2021;130:252-262.  https://doi.org/10.1016/j.neubiorev.2021.08.007
  51. Stanley AT, Lippiello P, Sulzer D, Miniaci MC. Roles for the dorsal striatum in aversive behavior. Front Cell Neurosci 2021;15:634493. 
  52. Feinstein JS, Adolphs R, Damasio A, Tranel D. The human amygdala and the induction and experience of fear. Curr Biol 2011;21:34-38.  https://doi.org/10.1016/j.cub.2010.11.042
  53. Zhang X, Ge TT, Yin G, Cui R, Zhao G, Yang W. Stress-induced functional alterations in amygdala: implications for neuropsychiatric diseases. Front Neurosci 2018;12:367. 
  54. Roozendaal B, McEwen BS, Chattarji S. Stress, memory and the amygdala. Nat Rev Neurosci 2009;10:423-433.  https://doi.org/10.1038/nrn2651
  55. Herlin B, Navarro V, Dupont S. The temporal pole: from anatomy to function-a literature appraisal. J Chem Neuroanat 2021;113:101925.