Brain Activation Related to Perspective-Taking in Adolescents : Differences from Adults

관점 획득과 관련된 청소년에서의 뇌 활성화 : 성인과의 차이

  • Park, Seong Kyoung (Onyourhan Psychiatric Clinic) ;
  • 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)
  • 박성경 (온유한정신건강의학과) ;
  • 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)
  • Received : 2019.04.29
  • Accepted : 2019.07.12
  • Published : 2019.10.31

Abstract

Objectives The purpose of this study was to investigate the differences between adolescents and adults, in the perspective-taking ability, as well as the brain activation patterns during the perspective-taking situation. Methods We recruited healthy adolescents aged 13 years to 15 years (n = 20) and adults aged 19 years to 29 years (n = 20). All the subjects were scanned while performing the perspective-taking task, in which an emotional situation was presented in the form of statements comprising first person, as well as third person perspectives. Differences in brain activation between groups were assessed by contrasting neural activity during the tasks. Results In the between-group analysis, while performing the third-person perspective-taking task, the adolescent group showed greater neural activities in the middle frontal gyrus and precentral gyrus as compared to the adult group. Positive correlation was observed between the activity in the frontal areas (Brodmann area 6/9) and the score of scales related to perspective-taking and social cognition in the adolescent group. Conclusions This study suggests that several frontal brain areas of adolescents needs to be overactivated in order to compensate for low perspective-taking ability when they ought to take another person's point of view.

Keywords

References

  1. Spear LP. The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 2000;24:417-463. https://doi.org/10.1016/S0149-7634(00)00014-2
  2. Ruby P, Decety J. What you believe versus what you think they believe: a neuroimaging study of conceptual perspective-taking. Eur J Neurosci 2003;17:2475-2480. https://doi.org/10.1046/j.1460-9568.2003.02673.x
  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. Ha YH, Edwards GP. The effect of parents attachment, socioeconomic status, and perspective-taking on early adolescents' prosocial behavior toward parents and siblings. Korean J Cult Soc Issues 2005;11:43-57.
  5. Han SC. Risk Behavior during the Adolescence: peer relation and role transitions within family. Korean J Youth Stud 1998;5:45-62.
  6. Mounoud P. Perspective taking and belief attribution: from Piaget's theory to children's theory of mind. Swiss J Psychol 1996;55:93-103.
  7. Ruby P, Decety J. Effect of subjective perspective taking during simulation of action: a PET investigation of agency. Nat Neurosci 2001;4:546-550. https://doi.org/10.1038/87510
  8. Ruby P, Decety J. How would you feel versus how do you think she would feel? A neuroimaging study of perspective-taking with social emotions. J Cogn Neurosci 2004;16:988-999. https://doi.org/10.1162/0898929041502661
  9. Oh IK, Son JW, Lee SB, Ghim HR. The difference of neural activity in viewing between one's own emotional situation and other's: a neuroimaging study about perspective-taking. Korean J Biol Psychiatry2009;16:159-169.
  10. Lamm C, Nusbaum HC, Meltzoff AN, Decety J. What are you feeling? Using functional magnetic resonance imaging to assess the modulation of sensory and affective responses during empathy for pain. PLoS One 2007;2:e1292. https://doi.org/10.1371/journal.pone.0001292
  11. Schnell K, Bluschke S, Konradt B, Walter H. Functional relations of empathy and mentalizing: an fMRI study on the neural basis of cognitive empathy. Neuroimage 2011;54:1743-1754. https://doi.org/10.1016/j.neuroimage.2010.08.024
  12. Choudhury S, Blakemore SJ, Charman T. Social cognitive development during adolescence. Soc Cogn Affect Neurosci 2006;1:165-174. https://doi.org/10.1093/scan/nsl024
  13. Dosch M, Loenneker T, Bucher K, Martin E, Klaver P. Learning to appreciate others: neural development of cognitive perspective taking. Neuroimage 2010;50:837-846. https://doi.org/10.1016/j.neuroimage.2009.12.013
  14. Zhu Y, Zhang L, Fan J, Han S. Neural basis of cultural influence on self-representation. Neuroimage 2007;34:1310-1316. https://doi.org/10.1016/j.neuroimage.2006.08.047
  15. 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.
  16. Lennon R, Eisenberg N. Gender and age differences in empathy and sympathy. In: Eisenberg N, Strayer J, editors. Empathy and Its Development (Cambridge Studies in Social and Emotional Development). New York, NY: Cambridge University Press;1987. p.195-217.
  17. 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
  18. Kim JH, Lee SJ. Reliability and validity of the Korean version of the empathy quotient scale. Psychiatry Investig 2010;7:24-30. https://doi.org/10.4306/pi.2010.7.1.24
  19. 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
  20. Kang I, Kee SW, Kim SE, Jeong BS, 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.
  21. Hawk ST, Keijsers L, Branje SJ, Graaff JV, Wied Md, Meeus W. Examining the Interpersonal Reactivity Index (IRI) among early and late adolescents and their mothers. J Pers Assess 2013;95:96-106. https://doi.org/10.1080/00223891.2012.696080
  22. Hynes CA, Baird AA, Grafton ST. Differential role of the orbital frontal lobe in emotional versus cognitive perspective-taking. Neuropsychologia 2006;44:374-383. https://doi.org/10.1016/j.neuropsychologia.2005.06.011
  23. Frith C, Frith U. Theory of mind. Curr Biol 2005;15:R644-R646. https://doi.org/10.1016/j.cub.2005.08.041
  24. Brunet E, Sarfati Y, Hardy-Bayle MC, Decety J. A PET investigation of the attribution of intentions with a nonverbal task. Neuroimage 2000;11:157-166. https://doi.org/10.1006/nimg.1999.0525
  25. Kim JI. Cognitive and emotional empathy in adolescent ADHD: an fMRI study [dissertation]. Cheongju: Chungbuk National University; 2015.
  26. McRae K, Gross JJ, Weber J, Robertson ER, Sokol-Hessner P, Ray RD, et al. The development of emotion regulation: an fMRI study of cognitive reappraisal in children, adolescents and young adults. Soc Cogn Affect Neurosci 2012;7:11-22. https://doi.org/10.1093/scan/nsr093
  27. Lane RD, Chua PM, Dolan RJ. Common effects of emotional valence, arousal and attention on neural activation during visual processing of pictures. Neuropsychologia 1999;37:989-997. https://doi.org/10.1016/S0028-3932(99)00017-2
  28. Goel V, Grafman J, Sadato N, Hallett M. Modeling other minds. Neuroreport 1995;6:1741-1746. https://doi.org/10.1097/00001756-199509000-00009
  29. Elkind D. Egocentrism in adolescence. Child Dev 1967;38:1025-1034. https://doi.org/10.1111/j.1467-8624.1967.tb04378.x
  30. Zysset S, Huber O, Ferstl E, von Cramon DY. The anterior frontomedian cortex and evaluative judgment: an fMRI study. Neuroimage 2002;15:983-991. https://doi.org/10.1006/nimg.2001.1008
  31. Blakemore SJ. The social brain in adolescence. Nat Rev Neurosci 2008;9:267-277. https://doi.org/10.1038/nrn2353
  32. Fransson P, Marrelec G. The precuneus/posterior cingulate cortex plays a pivotal role in the default mode network: evidence from a partial correlation network analysis. Neuroimage 2008;42:1178-1184. https://doi.org/10.1016/j.neuroimage.2008.05.059
  33. Kim H, Daselaar SM, Cabeza R. Overlapping brain activity between episodic memory encoding and retrieval: roles of the task-positive and task-negative networks. Neuroimage 2010;49:1045-1054. https://doi.org/10.1016/j.neuroimage.2009.07.058
  34. Cabeza R, St Jacques P. Functional neuroimaging of autobiographical memory. Trends Cogn Sci 2007;11:219-227. https://doi.org/10.1016/j.tics.2007.02.005
  35. Seger CA, Cincotta CM. The roles of the caudate nucleus in human classification learning. J Neurosci 2005;25:2941-2951. https://doi.org/10.1523/JNEUROSCI.3401-04.2005
  36. Seger CA. The visual corticostriatal loop through the tail of the caudate: circuitry and function. Front Syst Neurosci 2013;7:104. https://doi.org/10.3389/fnsys.2013.00104
  37. Wicker B, Perrett DI, Baron-Cohen S, Decety J. Being the target of another's emotion: a PET study. Neuropsychologia 2003;41:139-146. https://doi.org/10.1016/S0028-3932(02)00144-6
  38. Pekkola J, Ojanen V, Autti T, Jaaskelainen IP, Mottonen R, Tarkiainen A, et al. Primary auditory cortex activation by visual speech: an fMRI study at 3 T. Neuroreport 2005;16:125-128. https://doi.org/10.1097/00001756-200502080-00010
  39. Freton M, Lemogne C, Bergouignan L, Delaveau P, Lehericy S, et al. The eye of the self: precuneus volume and visual perspective during autobiographical memory retrieval. Brain Struct Funct 2014;219:959-968. https://doi.org/10.1007/s00429-013-0546-2
  40. Lamm C, Batson CD, Decety J. The neural substrate of human empathy: effects of perspective-taking and cognitive appraisal. J Cogn Neurosci 2007;19:42-58. https://doi.org/10.1162/jocn.2007.19.1.42
  41. Deppe M, Schwindt W, Kugel H, Plassmann H, Kenning P. Nonlinear responses within the medial prefrontal cortex reveal when specific implicit information influences economic decision making. J Neuroimaging 2005;15:171-182. https://doi.org/10.1111/j.1552-6569.2005.tb00303.x
  42. Freton M, Lemogne C, Bergouignan L, Delaveau P, Lehericy S, Fossati P. The eye of the self: precuneus volume and visual perspective during autobiographical memory retrieval. Brain Struct Funct 2014;219:959-968. https://doi.org/10.1007/s00429-013-0546-2
  43. Williams JH, Waiter GD, Perra O, Perrett DI, Whiten A. An fMRI study of joint attention experience. Neuroimage 2005;25:133-140. https://doi.org/10.1016/j.neuroimage.2004.10.047
  44. Bermpohl F, Pascual-Leone A, Amedi A, Merabet LB, Fregni F, Gaab N, et al. Attentional modulation of emotional stimulus processing: an fMRI study using emotional expectancy. Hum Brain Mapp 2006;27:662-677. https://doi.org/10.1002/hbm.20209
  45. Moriguchi Y, Ohnishi T, Mori T, Matsuda H, Komaki G. Changes of brain activity in the neural substrates for theory of mind during childhood and adolescence. Psychiatry Clin Neurosci 2007;61:355-363. https://doi.org/10.1111/j.1440-1819.2007.01687.x
  46. Yurgelun-Todd DA, Killgore WD. Fear-related activity in the prefrontal cortex increases with age during adolescence: a preliminary fMRI study. Neurosci Lett 2006;406:194-199. https://doi.org/10.1016/j.neulet.2006.07.046
  47. Nichelli P, Grafman J, Pietrini P, Alway D, Carton JC, Miletich R. Brain activity in chess playing. Nature 1994;369:191. https://doi.org/10.1038/369191a0
  48. Kim SI. Brain-based learning science: what can the brain science tell us about education? Korean J Cogn Sci 2006;17:375-398.
  49. Blakemore SJ. Imaging brain development: the adolescent brain. Neuroimage 2012;61:397-406. https://doi.org/10.1016/j.neuroimage.2011.11.080