DOI QR코드

DOI QR Code

Neural Correlates of Cognitive and Emotional Empathy in Patients with Autism Spectrum Disorder

자폐스펙트럼장애 환자에서의 인지적 공감 및 정서적 공감의 신경 상관물

  • Chung, Seungwon (Department of Psychiatry, Chungbuk National University Hospital) ;
  • Son, Jung-Woo (Department of Neuropsychiatry, College of Medicine, Chungbuk National University) ;
  • Lee, Seungbok (Department of Psychology, Chungbuk National University) ;
  • Ghim, Hei-Rhee (Department of Psychology, Chungbuk National University) ;
  • Lee, Sang-Ick (Department of Neuropsychiatry, College of Medicine, Chungbuk National University) ;
  • Shin, Chul-Jin (Department of Neuropsychiatry, College of Medicine, Chungbuk National University) ;
  • Kim, Siekyeong (Department of Neuropsychiatry, College of Medicine, Chungbuk National University) ;
  • Ju, Gawon (Department of Psychiatry, Chungbuk National University Hospital) ;
  • Choi, Sang Cheol (Didim Psychiatric Clinic) ;
  • Kim, Yang Yeol (SeoulTop Child Adolescent Psychiatric Clinic) ;
  • Koo, Young Jin (MindDoctor's Clinic for Junior)
  • 정승원 (충북대학교병원 정신건강의학과) ;
  • 손정우 (충북대학교 의과대학 정신건강의학교실) ;
  • 이승복 (충북대학교 심리학과) ;
  • 김혜리 (충북대학교 심리학과) ;
  • 이상익 (충북대학교 의과대학 정신건강의학교실) ;
  • 신철진 (충북대학교 의과대학 정신건강의학교실) ;
  • 김시경 (충북대학교 의과대학 정신건강의학교실) ;
  • 주가원 (충북대학교병원 정신건강의학과) ;
  • 최상철 (디딤정신건강의학과의원) ;
  • 김양렬 (서울탑정신건강의학과의원) ;
  • 구영진 (마인드닥터 주니어 정신건강의학과의원)
  • Received : 2016.07.29
  • Accepted : 2016.09.02
  • Published : 2016.09.30

Abstract

Objectives: Individuals with autism spectrum disorder (ASD) are considered to have problems with empathy. It has recently been suggested that there are two systems for empathy; cognitive and emotional. We aimed to investigate the neural response to cognitive and emotional empathy and elucidate the neurobiological aspects of empathy in patients with ASD. Methods: We recruited patients with ASD (N=17, ASD group) and healthy controls (HC) (N=22, HC group) for an functional magnetic resonance imaging study. All of the subjects were scanned while performing cognitive and emotional empathy tasks. The differences in brain activation between the groups were assessed by contrasting their neural activity during the tasks. Results: During both tasks, the ASD group showed greater neural activities in the bilateral occipital area compared to the HC group. The ASD group showed more activation in the bilateral precunei only during the emotional empathy task. No brain regions were more activated in the HC group than in the ASD group during the cognitive empathy task. While performing the emotional empathy task, the HC group exhibited greater neural activities in the left middle frontal gyrus and right anterior cingulate gyrus than the ASD group. Conclusion: This study showed that the brain regions associated with cognitive and emotional empathy in ASD patients differed from those in healthy individuals. The results of this study suggest that individuals with ASD might have defects both in cognitive empathy and in emotional empathy.

Keywords

References

  1. Decety J, Jackson PL. The functional architecture of human empathy. Behav Cogn Neurosci Rev 2004;3:71-100. https://doi.org/10.1177/1534582304267187
  2. Shamay-Tsoory SG. The neural bases for empathy. Neuroscientist 2011;17:18-24. https://doi.org/10.1177/1073858410379268
  3. Smith A. The empathy imbalance hypothesis of autism: a theoretical approach to cognitive and emotional empathy in autistic development. Psychol Rec 2009;59:489-510. https://doi.org/10.1007/BF03395675
  4. Decety J, Yang CY, Cheng Y. Physicians down-regulate their pain empathy response: an event-related brain potential study. Neuroimage 2010;50:1676-1682. https://doi.org/10.1016/j.neuroimage.2010.01.025
  5. Jabbi M, Swart M, Keysers C. Empathy for positive and negative emotions in the gustatory cortex. Neuroimage 2007;34:1744-1753. https://doi.org/10.1016/j.neuroimage.2006.10.032
  6. Van Overwalle F, Baetens K. Understanding others' actions and goals by mirror and mentalizing systems: a meta-analysis. Neuroimage 2009;48:564-584. https://doi.org/10.1016/j.neuroimage.2009.06.009
  7. Shamay-Tsoory SG, Aharon-Peretz J, Perry D. Two systems for empathy: a double dissociation between emotional and cognitive empathy in inferior frontal gyrus versus ventromedial prefrontal lesions. Brain 2009;132(Pt 3):617-627. https://doi.org/10.1093/brain/awn279
  8. Rogers K, Dziobek I, Hassenstab J, Wolf OT, Convit A. Who cares? Revisiting empathy in Asperger syndrome. J Autism Dev Disord 2007;37:709-715. https://doi.org/10.1007/s10803-006-0197-8
  9. 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
  10. Mazza M, Pino MC, Mariano M, Tempesta D, Ferrara M, De Berardis D, et al. Affective and cognitive empathy in adolescents with autism spectrum disorder. Front Hum Neurosci 2014;8:791.
  11. Kaufman J, Birmaher B, Brent D, Rao U, Flynn C, Moreci P, et al. Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime version (K-SADS-PL): initial reliability and validity data. J Am Acad Child Adolesc Psychiatry 1997;36:980-988. https://doi.org/10.1097/00004583-199707000-00021
  12. Kim YS, Cheon KA, Kim BN, Chang SA, Yoo HJ, Kim JW, et al. The reliability and validity of Kiddie-Schedule for Affective Disorders and Schizophrenia-Present and Lifetime version-Korean version (K-SADS-PL-K). Yonsei Med J 2004;45:81-89. https://doi.org/10.3349/ymj.2004.45.1.81
  13. 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;31:5-17. https://doi.org/10.1023/A:1005653411471
  14. Park EH, Ghim HR, Cho KJ, Koo JS. Individual differences in empathizing and systemizing. Korean J Woman Psychol 2009;14: 269-286. https://doi.org/10.18205/kpa.2009.14.2.004
  15. 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: 163-175. https://doi.org/10.1023/B:JADD.0000022607.19833.00
  16. Baron-Cohen S. Autism: the empathizing-systemizing (E-S) theory. Ann N Y Acad Sci 2009;1156:68-80. https://doi.org/10.1111/j.1749-6632.2009.04467.x
  17. Wheelwright S, Baron-Cohen S, Goldenfeld N, Delaney J, Fine D, Smith R, et al. Predicting Autism Spectrum Quotient (AQ) from the Systemizing Quotient-Revised (SQ-R) and Empathy Quotient (EQ). Brain Res 2006;1079:47-56. https://doi.org/10.1016/j.brainres.2006.01.012
  18. Davis MH. A multi-dimensional approach to individual differences in empathy. JCAS Cat Sel Doc Psychol 1980;75:989-1015.
  19. 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.
  20. Myles BS, Bock SJ, Simpson RL. Asperger Syndrome Diagnostic Scale. Austin: Pro-ED;2001.
  21. Kim JH, Shin MS. A study of reliability & validity for the Korean version of Asperger syndrome diagnostic scale. J Korean Acad Child Adolesc Psychiatry 2005;16:98-105.
  22. Constantino JN, Gruber CP. Social Responsiveness Scale (SRS). Los Angeles: Western Psychological Services;2005.
  23. Dziobek I, Preissler S, Grozdanovic Z, Heuser I, Heekeren HR, Roepke S. Neuronal correlates of altered empathy and social cognition in borderline personality disorder. Neuroimage 2011;57:539-548. https://doi.org/10.1016/j.neuroimage.2011.05.005
  24. Kim JE. Cognitive and emotional empathy in adolescent ADHD: an fMRI study [dissertation]. Cheongju: Chungbuk National Univ.; 2015.
  25. Golan O, Baron-Cohen S, Hill JJ, Rutherford MD. The 'Reading the Mind in the Voice' test-revised: a study of complex emotion recognition in adults with and without autism spectrum conditions. J Autism Dev Disord 2007;37:1096-1106. https://doi.org/10.1007/s10803-006-0252-5
  26. Lockwood PL, Bird G, Bridge M, Viding E. Dissecting empathy: high levels of psychopathic and autistic traits are characterized by difficulties in different social information processing domains. Front Hum Neurosci 2013;7:760.
  27. Passarotti AM, Sweeney JA, Pavuluri MN. Neural correlates of incidental and directed facial emotion processing in adolescents and adults. Soc Cogn Affect Neurosci 2009;4:387-398. https://doi.org/10.1093/scan/nsp029
  28. Straube T, Kolassa IT, Glauer M, Mentzel HJ, Miltner WH. Effect of task conditions on brain responses to threatening faces in social phobics: an event-related functional magnetic resonance imaging study. Biol Psychiatry 2004;56:921-930. https://doi.org/10.1016/j.biopsych.2004.09.024
  29. Straube T, Mentzel HJ, Miltner WH. Common and distinct brain activation to threat and safety signals in social phobia. Neuropsychobiology 2005;52:163-168. https://doi.org/10.1159/000087987
  30. Simonoff E, Pickles A, Charman T, Chandler S, Loucas T, Baird G. Psychiatric disorders in children with autism spectrum disorders: prevalence, comorbidity, and associated factors in a population-derived sample. J Am Acad Child Adolesc Psychiatry 2008;47:921-929. https://doi.org/10.1097/CHI.0b013e318179964f
  31. Pitcher D, Walsh V, Duchaine B. The role of the occipital face area in the cortical face perception network. Exp Brain Res 2011;209: 481-493. https://doi.org/10.1007/s00221-011-2579-1
  32. Uddin LQ, Iacoboni M, Lange C, Keenan JP. The self and social cognition: the role of cortical midline structures and mirror neurons. Trends Cogn Sci 2007;11:153-157. https://doi.org/10.1016/j.tics.2007.01.001
  33. de Vignemont F, Singer T. The empathic brain: how, when and why? Trends Cogn Sci 2006;10:435-441. https://doi.org/10.1016/j.tics.2006.08.008
  34. Lamm C, Decety J, Singer T. Meta-analytic evidence for common and distinct neural networks associated with directly experienced pain and empathy for pain. Neuroimage 2011;54:2492-2502. https://doi.org/10.1016/j.neuroimage.2010.10.014
  35. Baron-Cohen S. The extreme male brain theory of autism. Trends Cogn Sci 2002;6:248-254. https://doi.org/10.1016/S1364-6613(02)01904-6
  36. Constantino JN, Todd RD. Autistic traits in the general population: a twin study. Arch Gen Psychiatry 2003;60:524-530. https://doi.org/10.1001/archpsyc.60.5.524
  37. Lord C, Rutter M, Goode S, Heemsbergen J, Jordan H, Mawhood L, et al. Autism diagnostic observation schedule: a standardized observation of communicative and social behavior. J Autism Dev Disord 1989;19:185-212. https://doi.org/10.1007/BF02211841
  38. Le Couteur A, Lord C, Rutter M. The Autism Diagnostic Interview-Revised (ADI-R). Los Angeles: Western Psychological Services; 2003.
  39. Matson JL, Shoemaker M. Intellectual disability and its relationship to autism spectrum disorders. Res Dev Disabil 2009;30:1107-1114. https://doi.org/10.1016/j.ridd.2009.06.003

Cited by

  1. Empathy Impairment in Individuals With Autism Spectrum Conditions From a Multidimensional Perspective: A Meta-Analysis vol.10, pp.None, 2019, https://doi.org/10.3389/fpsyg.2019.01902
  2. Visual Perception in Autism Spectrum Disorder: A Review of Neuroimaging Studies vol.31, pp.3, 2016, https://doi.org/10.5765/jkacap.200018