DOI QR코드

DOI QR Code

Disrupted Association Between Empathy and Brain Structure in Attention-Deficit/Hyperactivity Disorder

  • Lee, Jeonghwan (Department of Psychiatry, Chungbuk National University Hospital) ;
  • Son, Jung-Woo (Department of Psychiatry, Chungbuk National University Hospital) ;
  • Kim, Siekyeong (Department of Psychiatry, Chungbuk National University Hospital) ;
  • Kim, Ji-eun (Ma-Eum Pyong-On Psychiatric Clinic) ;
  • Chung, Seungwon (Department of Psychiatry, Chungbuk National University Hospital) ;
  • Ghim, Hei-Rhee (Department of Psychology, Chungbuk National University) ;
  • Lee, Sang-Ick (Department of Psychiatry, Chungbuk National University Hospital) ;
  • Shin, Chul-Jin (Department of Psychiatry, Chungbuk National University Hospital) ;
  • Ju, Gawon (Department of Psychiatry, Chungbuk National University Hospital)
  • 투고 : 2021.03.26
  • 심사 : 2021.05.07
  • 발행 : 2021.10.01

초록

Objectives: To investigate the relationship between brain structure and empathy in early adolescents with attention-deficit/hyperactivity disorder (ADHD). Methods: Nineteen early adolescents with ADHD and 20 healthy controls underwent 3T MRI. All the participants were assessed for different aspects of empathy using measures including the Interpersonal Reactivity Index and Empathy Quotient. Cortical thickness and subcortical structural volume based on T1-weighted scans were analyzed using FreeSurfer. Results: Cognitive empathy (t=-2.52, p=0.016) and perspective taking (t=-2.10, p=0.043) were impaired in the ADHD group compared with the control group. The cluster encompassing the left posterior insular, supramarginal, and transverse temporal cortices [cluster-wise p-value (CWP)=0.001], which are associated with emotional empathy, was significantly smaller in the ADHD group, and the volume of the left nucleus accumbens was greater than that of the control group (F=10.12, p=0.003, effect size=0.22). In the control group, the left superior temporal (CWP=0.002) and lingual cortical (CWP=0.035) thicknesses were positively associated with cognitive empathy, while the right amygdala volume was positively associated with empathic concern (Coef=14.26, t=3.92, p=0.001). However, there was no significant correlation between empathy and brain structure in the ADHD group. Conclusion: The ADHD group had a smaller volume of the cortical area associated with emotional empathy than the control group, and there was no brain region showing significant correlation with empathy, unlike in the control group.

키워드

과제정보

The preliminary findings of this study were presented as an E-poster at the 33rd European College of Neuropsychopharmacology Congress.

참고문헌

  1. Stenseng F, Belsky J, Skalicka V, Wichstrom L. Peer rejection and attention deficit hyperactivity disorder symptoms: reciprocal relations through ages 4, 6, and 8. Child Dev 2016;87:365-373. https://doi.org/10.1111/cdev.12471
  2. Nijmeijer JS, Minderaa RB, Buitelaar JK, Mulligan A, Hartman CA, Hoekstra PJ. Attention-deficit/hyperactivity disorder and social dysfunctioning. Clin Psychol Rev 2008;28:692-708. https://doi.org/10.1016/j.cpr.2007.10.003
  3. Cadesky EB, Mota VL, Schachar RJ. Beyond words: how do children with ADHD and/or conduct problems process nonverbal information about affect? J Am Acad Child Adolesc Psychiatry 2000;39:1160-1167. https://doi.org/10.1097/00004583-200009000-00016
  4. Deschamps PK, Schutter DJ, Kenemans JL, Matthys W. Empathy and prosocial behavior in response to sadness and distress in 6- to 7-year olds diagnosed with disruptive behavior disorder and attention-deficit hyperactivity disorder. Eur Child Adolesc Psychiatry 2015;24:105-113. https://doi.org/10.1007/s00787-014-0535-x
  5. de Waal FB. Putting the altruism back into altruism: the evolution of empathy. Annu Rev Psychol 2008;59:279-300. https://doi.org/10.1146/annurev.psych.59.103006.093625
  6. 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
  7. Shamay-Tsoory SG. The neural bases for empathy. Neuroscientist 2011;17:18-24. https://doi.org/10.1177/1073858410379268
  8. Decety J, Michalska KJ. Neurodevelopmental changes in the circuits underlying empathy and sympathy from childhood to adulthood. Dev Sci 2010;13:886-899. https://doi.org/10.1111/j.1467-7687.2009.00940.x
  9. Miller SR, Miller CJ, Bloom JS, Hynd GW, Craggs JG. Right hemisphere brain morphology, attention-deficit hyperactivity disorder (ADHD) subtype, and social comprehension. J Child Neurol 2006;21:139-144. https://doi.org/10.1177/08830738060210021901
  10. Kwak KJ, Oh SW, Kim CT. Korean-Wechsler Intelligence Scale for Children. 4th ed. Seoul: Inpsyt;2011. p.11-13.
  11. 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
  12. Pappas D. ADHD Rating Scale-IV: checklists, norms, and clinical interpretation. J Psychoeduc Assess 2006;24:172-178. https://doi.org/10.1177/0734282905285792
  13. Davis MH. Measuring individual differences in empathy: evidence for a multidimensional approach. J Pers Soc Psychol 1983;44:113-126. https://doi.org/10.1037//0022-3514.44.1.113
  14. Pfeifer JH, Iacoboni M, Mazziotta JC, Dapretto M. Mirroring others' emotions relates to empathy and interpersonal competence in children. Neuroimage 2008;39:2076-2085. https://doi.org/10.1016/j.neuroimage.2007.10.032
  15. Ghim HR, Son JW, Eom JS, Jung MS, Park M, Park YO. Children's facial mimicry to dynamic emotional facial expressions and their emotional empathy. Korean J Cogn Biol Psychol 2012;24:433-452. https://doi.org/10.22172/cogbio.2012.24.4.007
  16. Fischl B, Dale AM. Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci U S A 2000;97:11050-11055. https://doi.org/10.1073/pnas.200033797
  17. Groen Y, den Heijer AE, Fuermaier ABM, Althaus M, Tucha O. Reduced emotional empathy in adults with subclinical ADHD: evidence from the empathy and systemizing quotient. Atten Defic Hyperact Disord 2018;10:141-150. https://doi.org/10.1007/s12402-017-0236-7
  18. Marton I, Wiener J, Rogers M, Moore C, Tannock R. Empathy and social perspective taking in children with attention-deficit/hyperactivity disorder. J Abnorm Child Psychol 2009;37:107-118. https://doi.org/10.1007/s10802-008-9262-4
  19. Nilsen ES, Mewhort Buist TA, Gillis R, Fugelsang J. Communicative perspective-taking performance of adults with ADHD symptoms. J Atten Disord 2013;17:589-597. https://doi.org/10.1177/1087054711428947
  20. Lockwood PL. The anatomy of empathy: vicarious experience and disorders of social cognition. Behav Brain Res 2016;311:255-266. https://doi.org/10.1016/j.bbr.2016.05.048
  21. Goerlich-Dobre KS, Lamm C, Pripfl J, Habel U, Votinov M. The left amygdala: a shared substrate of alexithymia and empathy. Neuroimage 2015;122:20-32. https://doi.org/10.1016/j.neuroimage.2015.08.014
  22. Kral TRA, Solis E, Mumford JA, Schuyler BS, Flook L, Rifken K, et al. Neural correlates of empathic accuracy in adolescence. Soc Cogn Affect Neurosci 2017;12:1701-1710. https://doi.org/10.1093/scan/nsx099
  23. Li Y, Zhang T, Li W, Zhang J, Jin Z, Li L. Linking brain structure and activation in anterior insula cortex to explain the trait empathy for pain. Hum Brain Mapp 2020;41:1030-1042. https://doi.org/10.1002/hbm.24858
  24. 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
  25. Mackes NK, Golm D, O'Daly OG, Sarkar S, Sonuga-Barke EJS, Fairchild G, et al. Tracking emotions in the brain-revisiting the empathic accuracy task. Neuroimage 2018;178:677-686. https://doi.org/10.1016/j.neuroimage.2018.05.080
  26. Uribe C, Puig-Davi A, Abos A, Baggio HC, Junque C, Segura B. Neuroanatomical and functional correlates of cognitive and affective empathy in young healthy adults. Front Behav Neurosci 2019;13:85. https://doi.org/10.3389/fnbeh.2019.00085
  27. Hoogman M, Muetzel R, Guimaraes JP, Shumskaya E, Mennes M, Zwiers MP, et al. Brain imaging of the cortex in ADHD: a coordinated analysis of large-scale clinical and population-based samples. Am J Psychiatry 2019;176:531-542. https://doi.org/10.1176/appi.ajp.2019.18091033
  28. Nakao T, Radua J, Rubia K, Mataix-Cols D. Gray matter volume abnormalities in ADHD: voxel-based meta-analysis exploring the effects of age and stimulant medication. Am J Psychiatry 2011; 168:1154-1163. https://doi.org/10.1176/appi.ajp.2011.11020281
  29. Volkow ND, Wang GJ, Tomasi D, Kollins SH, Wigal TL, Newcorn JH, et al. Methylphenidate-elicited dopamine increases in ventral striatum are associated with long-term symptom improvement in adults with attention deficit hyperactivity disorder. J Neurosci 2012;32:841-849. https://doi.org/10.1523/JNEUROSCI.4461-11.2012
  30. Villemonteix T, De Brito SA, Kavec M, Baleriaux D, Metens T, Slama H, et al. Grey matter volumes in treatment naive vs. chronically treated children with attention deficit/hyperactivity disorder: a combined approach. Eur Neuropsychopharmacol 2015;25:1118-1127. https://doi.org/10.1016/j.euroneuro.2015.04.015
  31. Oakes HV, DeVee CE, Farmer B, Allen SA, Hall AN, Ensley T, et al. Neurogenesis within the hippocampus after chronic methylphenidate exposure. J Neural Transm (Vienna) 2019;126:201-209. https://doi.org/10.1007/s00702-018-1949-2
  32. Plessen KJ, Bansal R, Zhu H, Whiteman R, Amat J, Quackenbush GA, et al. Hippocampus and amygdala morphology in attentiondeficit/hyperactivity disorder. Arch Gen Psychiatry 2006;63:795-807. https://doi.org/10.1001/archpsyc.63.7.795