Journal of Neural Transmission

, Volume 117, Issue 6, pp 781–791 | Cite as

Development of neural correlates of empathy from childhood to early adulthood: an fMRI study in boys and adult men

  • E. Greimel
  • M. Schulte-Rüther
  • G. R. Fink
  • M. Piefke
  • B. Herpertz-Dahlmann
  • K. Konrad
Biological Child and Adolescent Psychiatry-Original Article

Abstract

Although empathy is rooted early in life, the ability to understand and share the emotions of others continues to develop after childhood. Here, we aimed at exploring developmental changes in the neural mechanisms underlying empathy from childhood to early adulthood. Using functional magnetic resonance imaging, 47 healthy male subjects aged 8–27 years were investigated during an explicit empathy task. Emotional faces were presented and participants were either asked to infer the emotional state from the face (other-task) or to judge their own emotional response to the face (self-task). A perceptual decision on the width of faces was used as a control condition. Age-related activity increases were observed in the fusiform gyrus and inferior frontal gyrus, depending on whether subjects attributed emotions to self or other. During the self-task, activity in the right precuneus and right intraparietal sulcus decreased as a function of age. No age-related differences were observed in behavioral performance measures. Increased activity in the fusiform gyrus and in the frontal component of the human mirror neuron system with increasing age may be explained by greater experience and expertise accumulated during socio-emotional interactions. Greater recruitment of right parietal structures in younger as compared to older subjects might reflect developmental differences in the cognitive strategies to infer one’s own emotional response. This study is the first to show developmental changes in the neural mechanisms supporting empathy. Our findings may have important implications for the development of novel therapeutic interventions in clinical conditions characterized by empathy deficits, such as autism spectrum disorder.

Keywords

fMRI Development Empathy Mirror neuron system Fusiform gyrus 

Supplementary material

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Supplementary material 1 (PDF 149 kb)
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Supplementary material 2 (PDF 146 kb)
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Supplementary material 3 (PDF 144 kb)
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Supplementary material 4 (PDF 139 kb)

References

  1. Achenbach TM (1993) Empirically based taxonomy: how to use syndromes and profile types derived from the CBCL from 4 to 18, TRF, and WSR. University of Vermont, Department of Psychiatry, BurlingtonGoogle Scholar
  2. Adams GR (1983) Social competence during adolescence: social sensitivity, locus of control, empathy, and peer popularity. J Youth Adolesc 12:203–211CrossRefGoogle Scholar
  3. Adams GR, Schvaneveldt JD, Jenson GO (1979) Sex, age and perceived competency as correlates of empathic ability in adolescence. Adolescence 14:811–818Google Scholar
  4. Aylward EH, Park JE, Field KM, Parsons AC, Richards TL, Cramer SC, Meltzoff AN (2005) Brain activation during face perception: evidence of a developmental change. J Cogn Neurosci 17:308–319CrossRefPubMedGoogle Scholar
  5. Bastiaansen JACJ, Thioux M, Keysers C (2009) Evidence for mirror systems in emotions. Philos Trans R Soc Lond B Biol Sci 364:2391–2404CrossRefPubMedGoogle Scholar
  6. Blakemore S-J (2008) The social brain in adolescence. Nat Rev Neurosci 9:267–277CrossRefPubMedGoogle Scholar
  7. Blakemore S-J, den Ouden H, Choudhury S, Frith C (2007) Adolescent development of the neural circuitry for thinking about intentions. SCAN 2:130–139PubMedGoogle Scholar
  8. Buccino G, Binkofski F, Fink GR, Fadiga L, Fogassi L, Gallese V, Seitz RJ, Zilles K, Rizzolatti G, Freund HJ (2001) Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study. Eur J Neurosci 13:400–404PubMedGoogle Scholar
  9. Büchel C, Wise RJS, Mummery CJ, Poline J-B, Friston KJ (1996) Nonlinear regression in parametric activation studies. Neuroimage 4:60–66CrossRefPubMedGoogle Scholar
  10. Burnett S, Bird G, Moll J, Frith C, Blakemore S-J (2009) Development during adolescence of the neural processing of social emotion. J Cogn Neurosci 21:1736–1750CrossRefPubMedGoogle Scholar
  11. Calvo-Merino B, Glaser DE, Grèzes J, Passingham RE, Haggard P (2004) Action observation and acquired motor skills: an fMRI study with expert dancers. Cereb Cortex 15:1243–1249CrossRefPubMedGoogle Scholar
  12. Carr L, Iacoboni M, Dubeau M-C, Mazziotta JC, Lenzi GL (2003) Neural mechanisms of empathy in humans: a relay from neural systems for imitation to limbic areas. Proc Natl Acad Sci USA 100:5497–5502CrossRefPubMedGoogle Scholar
  13. Cavanna AE, Trimble MR (2006) The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129:564–583CrossRefPubMedGoogle Scholar
  14. Cross ES, Hamilton AF, Grafton ST (2006) Building a motor simulation de novo: observation of dance by dancers. Neuroimage 31:1257–1267CrossRefPubMedGoogle Scholar
  15. Dadds MR, Hunter K, Hawes DJ, Frost ADJ, Vassallo S, Bunn P, Merz S, El Masry J (2008) A measure of affective and cognitive empathy in children using parent ratings. Child Psychiatry Hum Dev 39:111–122CrossRefPubMedGoogle Scholar
  16. Dapretto M, Davies MS, Pfeifer JH, Scott AA, Sigman M, Bookheimer SY, Iacoboni M (2006) Understanding emotions in others: mirror neuron dysfunction in children with autism spectrum disorders. Nat Neurosci 9:28–30CrossRefPubMedGoogle Scholar
  17. Davis M (1980) A multidimensional approach to individual differences in empathy. JSAS 10:85Google Scholar
  18. Davis MD, Franzoi SL (1991) Stability and change in adolescent self-consciousness and empathy. J Res Pers 25:70–87CrossRefGoogle Scholar
  19. Decety J, Jackson PL (2004) The functional architecture of human empathy. Behav Cogn Neurosci Rev 3:71–100CrossRefPubMedGoogle Scholar
  20. Decety J, Moriguchi Y (2007) The empathic brain and its dysfunction in psychiatric populations: implications for intervention across different clinical conditions. Biopsychosoc Med 16:1–22Google Scholar
  21. Decety J, Michalska K, Akitsuki Y (2008) Who caused the pain? An fMRI investigation of empathy and intentionality in children. Neuropsychologia 46:2607–2614CrossRefPubMedGoogle Scholar
  22. Decety J, Michalska KJ, Akitsuki Y, Lahey BB (2009) Atypical empathic responses in adolescents with aggressive conduct disorder: A functional MRI investigation. Biol Psychiatry 80:203–211CrossRefGoogle Scholar
  23. Deeley Q, Daly EM, Azuma R, Surguladze S, Giampietro V, Brammer MJ, Hallahan B, Dunbar RIM, Phillips ML, Murphy DGM (2008) Changes in male brain responses to emotional faces from adolescence to middle age. Neuroimage 40:389–397CrossRefPubMedGoogle Scholar
  24. Derogatis LR (1993) Brief Symptom Inventory (BSI), administration, scoring, and procedures manual. National Computer Services, MinneapolisGoogle Scholar
  25. Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25:1325–1335CrossRefPubMedGoogle Scholar
  26. Ekman P, Friesen W, Hager J (2002) Facial action coding system. Research Nexus, Salt Lake City, UTGoogle Scholar
  27. Gauthier I, Tarr MJ, Anderson AW, Skudlarski P, Gore JC (1999) Activation of the middle fusiform “face are” increases with expertise in recognizing novel objects. Nat Neurosci 2:568–573CrossRefPubMedGoogle Scholar
  28. Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijdenbos A, Paus T, Evans AC, Rapoport JL (1999) Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci 2:861–863CrossRefPubMedGoogle Scholar
  29. Gitelman DR (2002) ILAB: a program for postexperimental eye movement analysis. Behav Res Meth Inst C 34:605–612Google Scholar
  30. Greimel E, Schulte-Rüther M, Kircher T, Kamp-Becker I, Remschmidt H, Fink GR, Herpertz-Dahlmann B, Konrad K (2010) Neural mechanisms of empathy in adolescents with autism spectrum disorder and their fathers. Neuroimage 49:1055–1065CrossRefPubMedGoogle Scholar
  31. Guyer AE, Monk CS, McClure-Tone EB, Nelson EE, Roberson-Nay R, Adler AD, Fromm SJ, Leibenluft E, Pine DS, Ernst M (2008) A developmental examination of amygdala response to facial expressions. J Cogn Neurosci 20:1565–1582CrossRefPubMedGoogle Scholar
  32. Hatfield E, Cacioppo JT, Rapson RL (1994) Emotional contagion. Cambridge University Press, New YorkGoogle Scholar
  33. Herba C, Phillips M (2004) Annotation: development of facial expression recognition from childhood to adolescence: behavioural and neurological perspectives. J Child Psychol Psychiatry 45:1185–1198CrossRefPubMedGoogle Scholar
  34. Iacoboni M, Dapretto M (2006) The mirror neuron system and the consequences of its dysfunction. Nat Rev Neurosci 7:942–951CrossRefPubMedGoogle Scholar
  35. Iacoboni M, Mazziotta JC (2007) Mirror neuron system: basic findings and clinical applications. Ann Neurol 62:213–218CrossRefPubMedGoogle Scholar
  36. Iacoboni M, Woods RP, Brass M, Bekkering H, Mazziotta JC, Rizzolatti G (1999) Cortical mechanisms of human imitation. Science 286:2526–2528CrossRefPubMedGoogle Scholar
  37. Jabbi M, Swart M, Keysers C (2007) Empathy for positive and negative emotions in the gustatory cortex. Neuroimage 34:1744–1753CrossRefPubMedGoogle Scholar
  38. Kaplan JT, Iacoboni M (2006) Getting a grip on other minds: mirror neurons, intention understanding, and cognitive empathy. Soc Neurosci 1:175–183CrossRefPubMedGoogle Scholar
  39. Kaufman J, Birmaher B, Brent D, Rao U, Flynn C, Moreci P, Williamson D, Ryan N (1997) 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 36:980–988CrossRefPubMedGoogle Scholar
  40. Kilner JM, Blakemore S-J (2007) How does the mirror neuron system change during development? Dev Psychol 10:524–526Google Scholar
  41. Kobayashi C, Glover GH, Temple E (2007) Children′s and adults′ neural bases of verbal and nonverbal “theory of mind”. Neuropsychologia 45:1522–1532CrossRefPubMedGoogle Scholar
  42. Kobayashi C, Glover GH, Temple E (2008) Switching language switches mind: linguistic effects on developmental neural bases of “Theory of Mind”. SCAN 3:62–70PubMedGoogle Scholar
  43. Leichnetz GR (2001) Connections of the medial posterior parietal cortex (area 7 m) in the monkey. Anat Rec 263:215–235CrossRefPubMedGoogle Scholar
  44. Leslie KR, Johnson-Frey SH, Grafton ST (2004) Functional imaging of face and hand imitation: towards a motor theory of empathy. Neuroimage 21:601–607CrossRefPubMedGoogle Scholar
  45. Light SN, Zahn-Waxler C, Frye C, Goldsmith HH, Davidson RJ (2009) Empathy is associated with dynamic change in prefrontal brain electrical activity during positive emotion in children. Child Dev 80:1210–1231CrossRefPubMedGoogle Scholar
  46. Litvack-Miller W, McDougal D, Romney DM (1997) The structure of empathy during middle childhood and its relationship to prosocial behaviour. Genet Soc Gen Psychol Monogr 123:303–325PubMedGoogle Scholar
  47. Lou HC, Luber B, Crupain M, Keenan JP, Nowak M, Kjaer TW, Sackeim HA, Lisanby SH (2004) Parietal cortex and the representation of the mental Self. Proc Natl Acad Sci USA 27:6832Google Scholar
  48. Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19:1233–1239CrossRefPubMedGoogle Scholar
  49. Mehrabian A (1997) Relations among personality scales of aggression, violence, and empathy: validational evidence bearing on the risk of eruptive violence scale. Aggress Behav 23:433–445CrossRefGoogle Scholar
  50. Monk CS, McClure EB, Nelson EE, Zarahn E, Bilder RM, Leibenluft E, Charney DS, Ernst M, Pine DS (2003) Adolescent immaturity in attention-related brain engagement to emotional facial expressions. Neuroimage 20:420–428CrossRefPubMedGoogle Scholar
  51. Moriguchi Y, Ohnishi T, Mori T, Matsuda H, Komaki G (2007) Changes of brain activity in the neural substrates for theory of mind during childhood and adolescence. Psychiatry Clin Neurosci 61:355–363CrossRefPubMedGoogle Scholar
  52. Oldfield RC (1971) Assessment and analysis of handedness—Edinburgh Inventory. Neuropsychologia 9:97–113CrossRefPubMedGoogle Scholar
  53. Pfeifer JH, Lieberman MD, Dapretto M (2007) “I know you are but what am I?”: neural bases of self- and social knowledge retrieval in children and adults. J Cogn Neurosci 19:1323–1337CrossRefPubMedGoogle Scholar
  54. Pfeifer JH, Iacoboni M, Mazziotta JC, Dapretto M (2008) Mirroring others′ emotions relates to empathy and interpersonal competence in children. Neuroimage 39:2076–2085CrossRefPubMedGoogle Scholar
  55. Platek SM, Loughead JW, Gur RC, Busch S, Ruparel K, Phend N, Panyavin IS, Langleben DD (2006) Neural substrates for functionally discriminating self-face from personally familiar faces. Hum Brain Mapp 27:91–98CrossRefPubMedGoogle Scholar
  56. Premack D, Woodruff G (1978) Does the chimpanzee have a theory of mind? Behav Brain Sci 1:515–526CrossRefGoogle Scholar
  57. Preston SD, de Waal FBM (2002) Empathy: its ultimate and proximate bases. Behav Brain Sci 25:1–72PubMedGoogle Scholar
  58. Sagi A, Hoffmann ML (1976) Empathic distress in the newborn. Dev Psychol 12:175–176CrossRefGoogle Scholar
  59. Schulte-Rüther M, Markowitsch HJ, Fink GR, Piefke M (2007) Mirror neuron and theory of mind mechanisms involved in face-to-face interactions: a functional magnetic resonance imaging approach to empathy. J Cogn Neurosci 19:1354–1372CrossRefPubMedGoogle Scholar
  60. Schulte-Rüther M, Markowitsch HJ, Shah NJ, Fink GR, Piefke M (2008) Gender differences in brain networks supporting empathy. Neuroimage 42:393–403CrossRefPubMedGoogle Scholar
  61. Schulte-Rüther M, Greimel E, Markowitsch HJ, Kamp-Becker I, Remschmidt H, Fink GR, Piefke M (in press) Dysfunctions of brain networks supporting empathy—an fMRI investigation in adults with autism spectrum disorder. Soc NeurosciGoogle Scholar
  62. Schultz RT (2005) Developmental deficits in social perception in autism: the role of the amygdala and fusiform face area. Int J Dev Neurosci 23:125–141CrossRefPubMedGoogle Scholar
  63. Shamay-Tsoory SG, Aharon-Peretz J, Perry D (2009) Two systems for empathy: a double dissociation between emotional and cognitive empathy in inferior frontal gyrus versus ventromedial prefrontal lesions. Brain 132:617–627CrossRefPubMedGoogle Scholar
  64. Strayer J (1993) Children’s concordant emotions and cognitions in response to observed emotions. Child Dev 64:188–201CrossRefPubMedGoogle Scholar
  65. Thomas KM, Drevets WC, Whalen PJ, Eccard CH, Dahl RE, Ryan ND, Casey BJ (2001) Amygdala response to facial expressions in children and adults. Biol Psychiatry 49:309–316CrossRefPubMedGoogle Scholar
  66. Uddin LQ, Kaplan JT, Molnar-Szakacs I, Zaidel E, Iacoboni M (2005) Self-face recognition activates a frontoparietal “mirror” network in the right hemisphere: an event-related fMRI study. Neuroimage 25:926–935CrossRefPubMedGoogle Scholar
  67. Wang AT, Lee SS, Sigman M, Dapretto M (2006) Developmental changes in the neural basis of interpreting communicative intent. SCAN 1:107–121PubMedGoogle Scholar
  68. Wechsler D (1991) Manual for the Wechsler Intelligence Scale for Children, 3rd edn. Psychological Corporation, San AntonioGoogle Scholar
  69. Wechsler D (1997) Manual for the Wechsler Adult Intelligence Scale-III. Psychological Corporation, San AntonioGoogle Scholar
  70. Wild B, Erb M, Bartels M (2001) Are emotions contagious? Evoked emotions while viewing emotionally expressive faces: quality, quantity, time course and gender differences. Psychiatry Res 102:109–124CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • E. Greimel
    • 1
    • 2
    • 3
  • M. Schulte-Rüther
    • 1
    • 3
  • G. R. Fink
    • 3
    • 4
  • M. Piefke
    • 5
  • B. Herpertz-Dahlmann
    • 2
  • K. Konrad
    • 1
  1. 1.Child Neuropsychology Section, Department of Child and Adolescent Psychiatry and PsychotherapyUniversity Hospital of the RWTH AachenAachenGermany
  2. 2.Department of Child and Adolescent Psychiatry and PsychotherapyUniversity Hospital of the RWTH AachenAachenGermany
  3. 3.Cognitive Neurology SectionInstitute of Neuroscience and Medicine (INM-3), Research Center JülichJülichGermany
  4. 4.Department of NeurologyUniversity Hospital CologneCologneGermany
  5. 5.Cognitive Neuroscience Section, Department of BiologyBielefeld UniversityBielefeldGermany

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