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Table of Contents
Vol. 32, No. 4, 2010
Issue release date: December 2010
Section title: Mini Review
Free Access
Dev Neurosci 2010;32:257–267
(DOI:10.1159/000317771)

The Neurodevelopment of Empathy in Humans

Decety J.
Center for Cognitive and Social Neuroscience, Departments of Psychology and Psychiatry, University of Chicago, Chicago, Ill., USA
email Corresponding Author

Abstract

Empathy, which implies a shared interpersonal experience, is implicated in many aspects of social cognition, notably prosocial behavior, morality and the regulation of aggression. The purpose of this paper is to critically examine the current knowledge in developmental and affective neuroscience with an emphasis on the perception of pain in others. It will be argued that human empathy involves several components: affective arousal, emotion understanding and emotion regulation, each with different developmental trajectories. These components are implemented by a complex network of distributed, often recursively connected, interacting neural regions including the superior temporal sulcus, insula, medial and orbitofrontal cortices, amygdala and anterior cingulate cortex, as well as autonomic and neuroendocrine processes implicated in social behaviors and emotional states. Decomposing the construct of empathy into subcomponents that operate in conjunction in the healthy brain and examining their developmental trajectory provides added value to our current approaches to understanding human development. It can also benefit our understanding of both typical and atypical development.

© 2010 S. Karger AG, Basel


  

Key Words

  • Affective neuroscience
  • Amygdala
  • Empathy
  • Theory of mind
  • Neurodevelopment
  • Orbitofrontal cortex
  • Ventromedial prefrontal cortex

References

  1. Akitsuki Y, Decety J (2009): Social context and perceived agency modulate brain activity in the neural circuits underpinning empathy for pain: an event-related fMRI study. Neuroimage 47:722–734.
  2. Barrett LF, Mesquita B, Ochsner KN, Gross JJ (2007): The experience of emotion. Annu Rev Psychol 58:373–403.
  3. Bell MA, Wolfe CD (2007): The cognitive neuroscience of early socioemotional development; in Brownell CA, Kopp CB (eds): Socioemotional Development in Toddler Years. New York, Guilford, pp 345–369.
  4. Brunet E, Sarfati Y, Hardy-Bayle MC, Decety J (2000): A PET investigation of attribution of intentions to others with a non-verbal task. Neuroimage 11:157–166.
  5. Bunge SA, Dudukovic NM, Thomasson ME, Vaidya CJ, Gabrieli JDE (2002): Immature frontal lobe contributions to cognitive control in children: evidence from fMRI. Neuron 33:301–311.
  6. Calkins SD, Fox NA (2002): Self-regulatory processes in early personality development: a multilevel approach to the study of childhood social withdrawal and aggression. Dev Psychopathol 14:477–498.
  7. Carlson SM, Mandell DJ, Williams L (2004): Executive function and theory of mind: stability and prediction from ages 2 to 3. Dev Psychol 40:1105–1122.
  8. Carroll JJ, Steward MS (1984): The role of cognitive development in children’s understandings of their own feelings. Dev Psychol 55:1486–1492.
  9. Carter SS, Harris J, Porges SW (2009): Neural and evolutionary perspectives on empathy; in Decety J, Ickes W (eds): The Social Neuroscience of Empathy. Cambridge, MIT Press, pp 169–182.
  10. Casey BJ, Tottenham N, Liston C, Durston S (2005): Imaging the developing brain: what have we learned about cognitive development? Trends Cogn Sci 9:104–110.
  11. Craig AD (2003): Interoception: the sense of the physiological condition of the body. Curr Opin Neurobiol 13:500–505.
  12. Craig AD (2004): Human feelings: why are some more aware than others? Trends Cogn Sci 8:239–241.
  13. Decety J (2005): Perspective taking as the royal avenue to empathy; in Malle BF, Hodges SD (eds): Other Minds. How Humans Bridge the Divide between Self and Others. New York, Guilford, pp 135–149.
  14. Decety J (2010): To what extent is the experience of empathy mediated by shared neural circuits. Emot Rev 2:204–207.

    External Resources

  15. Decety J, Jackson PL (2004): The functional architecture of human empathy. Behav Cogn Neurosci Rev 3:71–100.
  16. Decety J, Meyer M (2008): From emotion resonance to empathic understanding: a social developmental neuroscience account. Dev Psychopathol 20:1053–1080.
  17. Decety J, Michalska KJ (2010): Neurodevelopmental changes in the circuits underlying empathy and sympathy from childhood to adulthood. Dev Sci, E-pub ahead of print.
  18. Decety J, Michalska KJ, Akitsuki Y (2008): Who caused the pain? A functional MRI investigation of empathy and intentionality in children. Neuropsychologia 46:2607–2614.
  19. de Haan M, Gunnar, MR (2009): The brain in a social environment: why study development? In de Haan M, Gunnar MR (eds): Handbook of Developmental Social Neuroscience. New York, Guilford, pp 3–10.
  20. de Wied M, van Boxtel A, Zaalberg R, Goudena PP, Matthys M (2006): Facial EMG responses to dynamic emotional facial expressions in boys with disruptive behavior disorders. J Psychiatr Res 40:112–121.
  21. Diamond A (2002): Normal development of prefrontal cortex from birth to young adulthood: cognitive functions, anatomy, and biochemistry; in Stuss DT, Knight RT (eds): Principles of Frontal Lobe Function. New York, Oxford University Press, pp 446–503.
  22. Dondi M, Simion F, Caltran G (1999): Can newborns discriminate between their own cry and the cry of another newborn infant? Dev Psychol 35:418–426.
  23. Duncan S, Barrett LF (2007): Affect is a form of cognition: a neurobiological analysis. Cogn Emot 21:1184–1211.
  24. Eisenberg N, Eggum ND (2009): Empathic responding: sympathy and personal distress; in Decety J, Ickes W (eds): The Social Neuroscience of Empathy. Cambridge, MIT Press, pp 71–83.
  25. Eisenberg N, Shea CL, Carlo G, Knight GP (1991): Empathy-related responding and cognition: a chicken and the egg dilemma; in Kurtines WM (ed): Handbook of Moral Behavior and Development. Hillsdale, Erlbaum, vol 2: Research, pp 63–88.
  26. Fox NA (1994): The Development of Emotion Regulation. Biological and Behavioral Considerations. Monogr Soc Res Child Dev 59.
  27. Gross AL, Ballif B (1991): Children’s understanding of emotion from facial expressions and situations: a review. Dev Rev 11:368–398.

    External Resources

  28. Haidt J, Graham J (2007): When morality opposes justice: conservatives have moral intuitions that liberals may not recognize. Soc Justice Res 20:98–116.

    External Resources

  29. Harris PL (1994): The child’s understanding of emotion: developmental change and the family environment. J Child Psychol Psychiatry 35:3–28.
  30. Harris PL, Olthof T, Meerum-Terwogt M (1981): Children’s knowledge of emotion. J Child Psychol Psychiatry 22:247–261.
  31. Haviland JM, Lewica M (1987): The induced affect response: ten-week-old infants’ responses to three emotion expressions. Dev Psychol 23:97–104.

    External Resources

  32. Hodges SD, Klein KJK (2001): Regulating the costs of empathy: the price of being human. J Socio Econ 30:437–452.

    External Resources

  33. Hughes C, Dunn J (1998): Understanding mind and emotion: longitudinal associations with mental state talk between young friends. Dev Psychol 34:1026–1037.
  34. Hurliman E, Nagode JC, Pardo JV (2005): Double dissociation of exteroceptive and interoceptive feedback systems in the orbital and ventromedial prefrontal cortex of humans. J Neurosci 25:4641–4648.
  35. Izard CE (1982): Measuring Emotions in Infants and Young Children. New York, Cambridge Press.
  36. Jackson PL, Rainville P, Decety J (2006): To what extent do we share the pain of others? Insight from the neural bases of pain empathy. Pain 125:5–9.
  37. Killgore WDS, Yurgelun-Todd DA (2007): Unconscious processing of facial affect in children and adolescents. Soc Neurosci 2:28–47.
  38. Knafo A, Zahn-Waxler C, van Hulle C, Robinson JL, Rhee SH (2008): The developmental origins of a disposition toward empathy: genetic and environmental contributions. Emotion 8:737–752.
  39. Lamm C, Batson CD, Decety J (2007): The neural substrate of human empathy: effects of perspective-taking and cognitive appraisal. J Cogn Neurosci 19:42–58.
  40. Leppanen JM, Nelson CA (2009): Tuning the developing brain to social signals of emotions. Nat Rev Neurosci 10:37–47.
  41. Lewis M (2000): Self-conscious emotions: embarrassment, pride, shame, and guilt; in Lewis M, Haviland JM (eds): Handbook of Emotions. New York, Guilford, pp 623–636.
  42. Lewis MD, Lamm C, Segalowitz SJ, Stieben J, Zelazo PD (2006): Neurophysiological correlates of emotion regulation in children and adolescents. J Cogn Neurosci 18:430–443.
  43. Ludemann PM, Nelson CA (1988): Categorical representation of facial expressions by 7-month-old infants. Dev Psychol 24:492–501.
  44. MacLean P (1987): The midline frontal limbic cortex and the evolution of crying and laughter; in Perecman E (ed): The Frontal Lobes Revisited. New York, IRBN, pp 121–140.
  45. More BS (1990): The origins and development of empathy. Motiv Emot 14:75–79.

    External Resources

  46. Moriguchi Y, Ohnishi T, Mori T, Matsuda H, Komaki G (2007): Changes of brain activity in the neural substrates for theory of mind in childhood and adolescence. Psychiatry Clin Neurosci 61:355–363.
  47. Nielsen L (2002): The simulation of emotion experience: on the emotional foundations of theory of mind. Phenomenol Cogn Sci 1:255–286.

    External Resources

  48. Nyström P (2008): The infant mirror neuron system studied with high density EEG. Soc Neurosci 3:334–347.
  49. Ochsner KN, Bunge SA, Gross JJ, Gabrieli JDE (2002): Rethinking feelings: an fMRI study of cognitive regulation of emotion. J Cogn Neurosci 14:1215–1229.
  50. Pfeifer JH, Iacoboni M, Maziotta JC, Dapretto M (2008): Mirroring other’s emotions relates to empathy and interpersonal competence in children. Neuroimage 39:2076–2098.
  51. Philips ML, Ladouceur CD, Drevets WC (2008): A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Mol Psychiatry 13:833–857.

    External Resources

  52. Rothbart MK, Ahadi SA, Hershey KL (1994): Temperament and social behavior in childhood. Merrill Palmer Q 40:21–39.
  53. Sabbagh MA, Bowman LC, Evraire LE, Ito JMB (2009): Neurodevelopmental correlates of theory of mind in preschool children. Child Dev 80:1147–1162.
  54. Saxe RR, Whitfield-Gabrieli S, Pelphrey KA, Scholz J (2009): Brain regions for perceiving and reasoning about other people in school-aged children. Child Dev 80:1197–1209.
  55. Strum VE, Rosen HJ, Allison S, Miller BL, Levenson RW (2006): Self-conscious emotion deficits in frontotemporal lobar degeneration. Brain 129:2508–2516.
  56. Swick D, Ashley V, Turken AU (2008): Left inferior frontal gyrus is critical for response inhibition. BMC Neurosci 9:102e.
  57. Tamm L, Menon V, Reiss AL (2002): Maturation of brain function associated with response inhibition. J Am Acad Child Adolesc Psychiatry 41:1231–1238.
  58. Tonks J, Williams H, Frampton I, Yates P, Slater A (2007): Assessing emotion recognition in 9- to 15-year-olds: preliminary analysis of abilities in reading emotion from faces, voices and eyes. Brain Inj 21:623–629.
  59. Vaish A, Carpenter M, Tomasello M (2009): Sympathy through affective perspective-taking, and its relation to prosocial behavior in toddlers. Dev Psychol 45:534–543.
  60. Warneken F, Tomasello M (2009): The roots of human altruism. Br J Psychol 100:455–471.
  61. Yurgelun-Todd D (2007): Emotional and cognitive changes during adolescence. Curr Opin Neurobiol 17:251–257.
  62. Zaki J, Weber J, Bolger N, Ochsner K (2009): The neural bases of empathic accuracy. Proc Natl Acad Sci USA 106:11382–11387.
  63. Zelazo PD, Craik FI, Booth L (2004): Executive function across the life span. Acta Psychol (Amst) 115:167–183.

  

Author Contacts

Jean Decety
Center for Cognitive and Social Neuroscience
Departments of Psychology and Psychiatry, University of Chicago
5848 South University Avenue, Chicago, IL 60637 (USA)
E-Mail decety@uchicago.edu

  

Article Information

Received: March 22, 2010
Accepted after revision: June 14, 2010
Published online: August 31, 2010
Number of Print Pages : 11
Number of Figures : 3, Number of Tables : 1, Number of References : 63

  

Publication Details

Developmental Neuroscience

Vol. 32, No. 4, Year 2010 (Cover Date: December 2010)

Journal Editor: Levison S.W. (Newark, N.J.)
ISSN: 0378-5866 (Print), eISSN: 1421-9859 (Online)

For additional information: http://www.karger.com/DNE


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References

  1. Akitsuki Y, Decety J (2009): Social context and perceived agency modulate brain activity in the neural circuits underpinning empathy for pain: an event-related fMRI study. Neuroimage 47:722–734.
  2. Barrett LF, Mesquita B, Ochsner KN, Gross JJ (2007): The experience of emotion. Annu Rev Psychol 58:373–403.
  3. Bell MA, Wolfe CD (2007): The cognitive neuroscience of early socioemotional development; in Brownell CA, Kopp CB (eds): Socioemotional Development in Toddler Years. New York, Guilford, pp 345–369.
  4. Brunet E, Sarfati Y, Hardy-Bayle MC, Decety J (2000): A PET investigation of attribution of intentions to others with a non-verbal task. Neuroimage 11:157–166.
  5. Bunge SA, Dudukovic NM, Thomasson ME, Vaidya CJ, Gabrieli JDE (2002): Immature frontal lobe contributions to cognitive control in children: evidence from fMRI. Neuron 33:301–311.
  6. Calkins SD, Fox NA (2002): Self-regulatory processes in early personality development: a multilevel approach to the study of childhood social withdrawal and aggression. Dev Psychopathol 14:477–498.
  7. Carlson SM, Mandell DJ, Williams L (2004): Executive function and theory of mind: stability and prediction from ages 2 to 3. Dev Psychol 40:1105–1122.
  8. Carroll JJ, Steward MS (1984): The role of cognitive development in children’s understandings of their own feelings. Dev Psychol 55:1486–1492.
  9. Carter SS, Harris J, Porges SW (2009): Neural and evolutionary perspectives on empathy; in Decety J, Ickes W (eds): The Social Neuroscience of Empathy. Cambridge, MIT Press, pp 169–182.
  10. Casey BJ, Tottenham N, Liston C, Durston S (2005): Imaging the developing brain: what have we learned about cognitive development? Trends Cogn Sci 9:104–110.
  11. Craig AD (2003): Interoception: the sense of the physiological condition of the body. Curr Opin Neurobiol 13:500–505.
  12. Craig AD (2004): Human feelings: why are some more aware than others? Trends Cogn Sci 8:239–241.
  13. Decety J (2005): Perspective taking as the royal avenue to empathy; in Malle BF, Hodges SD (eds): Other Minds. How Humans Bridge the Divide between Self and Others. New York, Guilford, pp 135–149.
  14. Decety J (2010): To what extent is the experience of empathy mediated by shared neural circuits. Emot Rev 2:204–207.

    External Resources

  15. Decety J, Jackson PL (2004): The functional architecture of human empathy. Behav Cogn Neurosci Rev 3:71–100.
  16. Decety J, Meyer M (2008): From emotion resonance to empathic understanding: a social developmental neuroscience account. Dev Psychopathol 20:1053–1080.
  17. Decety J, Michalska KJ (2010): Neurodevelopmental changes in the circuits underlying empathy and sympathy from childhood to adulthood. Dev Sci, E-pub ahead of print.
  18. Decety J, Michalska KJ, Akitsuki Y (2008): Who caused the pain? A functional MRI investigation of empathy and intentionality in children. Neuropsychologia 46:2607–2614.
  19. de Haan M, Gunnar, MR (2009): The brain in a social environment: why study development? In de Haan M, Gunnar MR (eds): Handbook of Developmental Social Neuroscience. New York, Guilford, pp 3–10.
  20. de Wied M, van Boxtel A, Zaalberg R, Goudena PP, Matthys M (2006): Facial EMG responses to dynamic emotional facial expressions in boys with disruptive behavior disorders. J Psychiatr Res 40:112–121.
  21. Diamond A (2002): Normal development of prefrontal cortex from birth to young adulthood: cognitive functions, anatomy, and biochemistry; in Stuss DT, Knight RT (eds): Principles of Frontal Lobe Function. New York, Oxford University Press, pp 446–503.
  22. Dondi M, Simion F, Caltran G (1999): Can newborns discriminate between their own cry and the cry of another newborn infant? Dev Psychol 35:418–426.
  23. Duncan S, Barrett LF (2007): Affect is a form of cognition: a neurobiological analysis. Cogn Emot 21:1184–1211.
  24. Eisenberg N, Eggum ND (2009): Empathic responding: sympathy and personal distress; in Decety J, Ickes W (eds): The Social Neuroscience of Empathy. Cambridge, MIT Press, pp 71–83.
  25. Eisenberg N, Shea CL, Carlo G, Knight GP (1991): Empathy-related responding and cognition: a chicken and the egg dilemma; in Kurtines WM (ed): Handbook of Moral Behavior and Development. Hillsdale, Erlbaum, vol 2: Research, pp 63–88.
  26. Fox NA (1994): The Development of Emotion Regulation. Biological and Behavioral Considerations. Monogr Soc Res Child Dev 59.
  27. Gross AL, Ballif B (1991): Children’s understanding of emotion from facial expressions and situations: a review. Dev Rev 11:368–398.

    External Resources

  28. Haidt J, Graham J (2007): When morality opposes justice: conservatives have moral intuitions that liberals may not recognize. Soc Justice Res 20:98–116.

    External Resources

  29. Harris PL (1994): The child’s understanding of emotion: developmental change and the family environment. J Child Psychol Psychiatry 35:3–28.
  30. Harris PL, Olthof T, Meerum-Terwogt M (1981): Children’s knowledge of emotion. J Child Psychol Psychiatry 22:247–261.
  31. Haviland JM, Lewica M (1987): The induced affect response: ten-week-old infants’ responses to three emotion expressions. Dev Psychol 23:97–104.

    External Resources

  32. Hodges SD, Klein KJK (2001): Regulating the costs of empathy: the price of being human. J Socio Econ 30:437–452.

    External Resources

  33. Hughes C, Dunn J (1998): Understanding mind and emotion: longitudinal associations with mental state talk between young friends. Dev Psychol 34:1026–1037.
  34. Hurliman E, Nagode JC, Pardo JV (2005): Double dissociation of exteroceptive and interoceptive feedback systems in the orbital and ventromedial prefrontal cortex of humans. J Neurosci 25:4641–4648.
  35. Izard CE (1982): Measuring Emotions in Infants and Young Children. New York, Cambridge Press.
  36. Jackson PL, Rainville P, Decety J (2006): To what extent do we share the pain of others? Insight from the neural bases of pain empathy. Pain 125:5–9.
  37. Killgore WDS, Yurgelun-Todd DA (2007): Unconscious processing of facial affect in children and adolescents. Soc Neurosci 2:28–47.
  38. Knafo A, Zahn-Waxler C, van Hulle C, Robinson JL, Rhee SH (2008): The developmental origins of a disposition toward empathy: genetic and environmental contributions. Emotion 8:737–752.
  39. Lamm C, Batson CD, Decety J (2007): The neural substrate of human empathy: effects of perspective-taking and cognitive appraisal. J Cogn Neurosci 19:42–58.
  40. Leppanen JM, Nelson CA (2009): Tuning the developing brain to social signals of emotions. Nat Rev Neurosci 10:37–47.
  41. Lewis M (2000): Self-conscious emotions: embarrassment, pride, shame, and guilt; in Lewis M, Haviland JM (eds): Handbook of Emotions. New York, Guilford, pp 623–636.
  42. Lewis MD, Lamm C, Segalowitz SJ, Stieben J, Zelazo PD (2006): Neurophysiological correlates of emotion regulation in children and adolescents. J Cogn Neurosci 18:430–443.
  43. Ludemann PM, Nelson CA (1988): Categorical representation of facial expressions by 7-month-old infants. Dev Psychol 24:492–501.
  44. MacLean P (1987): The midline frontal limbic cortex and the evolution of crying and laughter; in Perecman E (ed): The Frontal Lobes Revisited. New York, IRBN, pp 121–140.
  45. More BS (1990): The origins and development of empathy. Motiv Emot 14:75–79.

    External Resources

  46. Moriguchi Y, Ohnishi T, Mori T, Matsuda H, Komaki G (2007): Changes of brain activity in the neural substrates for theory of mind in childhood and adolescence. Psychiatry Clin Neurosci 61:355–363.
  47. Nielsen L (2002): The simulation of emotion experience: on the emotional foundations of theory of mind. Phenomenol Cogn Sci 1:255–286.

    External Resources

  48. Nyström P (2008): The infant mirror neuron system studied with high density EEG. Soc Neurosci 3:334–347.
  49. Ochsner KN, Bunge SA, Gross JJ, Gabrieli JDE (2002): Rethinking feelings: an fMRI study of cognitive regulation of emotion. J Cogn Neurosci 14:1215–1229.
  50. Pfeifer JH, Iacoboni M, Maziotta JC, Dapretto M (2008): Mirroring other’s emotions relates to empathy and interpersonal competence in children. Neuroimage 39:2076–2098.
  51. Philips ML, Ladouceur CD, Drevets WC (2008): A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Mol Psychiatry 13:833–857.

    External Resources

  52. Rothbart MK, Ahadi SA, Hershey KL (1994): Temperament and social behavior in childhood. Merrill Palmer Q 40:21–39.
  53. Sabbagh MA, Bowman LC, Evraire LE, Ito JMB (2009): Neurodevelopmental correlates of theory of mind in preschool children. Child Dev 80:1147–1162.
  54. Saxe RR, Whitfield-Gabrieli S, Pelphrey KA, Scholz J (2009): Brain regions for perceiving and reasoning about other people in school-aged children. Child Dev 80:1197–1209.
  55. Strum VE, Rosen HJ, Allison S, Miller BL, Levenson RW (2006): Self-conscious emotion deficits in frontotemporal lobar degeneration. Brain 129:2508–2516.
  56. Swick D, Ashley V, Turken AU (2008): Left inferior frontal gyrus is critical for response inhibition. BMC Neurosci 9:102e.
  57. Tamm L, Menon V, Reiss AL (2002): Maturation of brain function associated with response inhibition. J Am Acad Child Adolesc Psychiatry 41:1231–1238.
  58. Tonks J, Williams H, Frampton I, Yates P, Slater A (2007): Assessing emotion recognition in 9- to 15-year-olds: preliminary analysis of abilities in reading emotion from faces, voices and eyes. Brain Inj 21:623–629.
  59. Vaish A, Carpenter M, Tomasello M (2009): Sympathy through affective perspective-taking, and its relation to prosocial behavior in toddlers. Dev Psychol 45:534–543.
  60. Warneken F, Tomasello M (2009): The roots of human altruism. Br J Psychol 100:455–471.
  61. Yurgelun-Todd D (2007): Emotional and cognitive changes during adolescence. Curr Opin Neurobiol 17:251–257.
  62. Zaki J, Weber J, Bolger N, Ochsner K (2009): The neural bases of empathic accuracy. Proc Natl Acad Sci USA 106:11382–11387.
  63. Zelazo PD, Craik FI, Booth L (2004): Executive function across the life span. Acta Psychol (Amst) 115:167–183.