Aging is associated with changes in the neural circuits underlying empathy

Neurobiology of Aging

Volumn 35, Issue 4, 2014, Pages 827-836

  Chen, Yao Chu ^a   Chen, Cheng Chiang ^a,b   Decety, Jean ^c   Cheng, Yawei ^a  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b CATHAY GENERAL HOSPITAL   (Taiwan)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

Agency; Aging; Dynamic causal modeling; Effective connectivity; Empathy; Functional MRI; Gray matter volume

Indexed keywords

ADULT; AGE; AGED; AGING; ANTERIOR CINGULATE; ANTERIOR INSULA; ARTICLE; BRAIN SIZE; CAUSAL MODELING; CHINESE; COGNITION; CONNECTOME; CONTROLLED STUDY; EMPATHY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAY MATTER; HEMODYNAMICS; HUMAN; HUMAN EXPERIMENT; MALE; MIDDLE AGED; NERVE POTENTIAL; NEUROIMAGING; NORMAL HUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; SUPERIOR TEMPORAL SULCUS; VERY ELDERLY; VISUAL STIMULATION; YOUNG ADULT;

AGENCY; AGING; DYNAMIC CAUSAL MODELING; EFFECTIVE CONNECTIVITY; EMPATHY; FUNCTIONAL MRI; GRAY MATTER VOLUME;

ADULT; AGED; AGED, 80 AND OVER; AGING; EMPATHY; FEMALE; GYRUS CINGULI; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NERVE NET; PAIN; PHOTIC STIMULATION; WOUNDS AND INJURIES; YOUNG ADULT;

EID: 84891372880     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2013.10.080     Document Type: Article

References (85)

1. Akitsuki Y., Decety J. Social context and perceived agency affects empathy for pain: an event-related fMRI investigation. Neuroimage 2009, 47:722-734.
2. Anderson N.D., Iidaka T., Cabeza R., Kapur S., McIntosh A.R., Craik F.I. The effects of divided attention on encoding- and retrieval-related brain activity: a PET study of younger and older adults. J.Cogn. Neurosci. 2000, 12:775-792.
3. Bailey P.E., Henry J.D. Growing less empathic with age: disinhibition of the self-perspective. J.Gerontol. B Psychol. Sci. Soc. Sci. 2008, 63:P219-P226.
4. Bailey P.E., Henry J.D., Von Hippel W. Empathy and social functioning in late adulthood. Aging Ment. Health 2008, 12:499-503.
5. Bandstra N.F., Chambers C.T., McGrath P.J., Moore C. The behavioural expression of empathy to others' pain versus others' sadness in young children. Pain 2011, 152:1074-1082.
6. Batson C.D. These things called empathy: eight related but distinct phenomena. The Social Neuroscience of Empathy 2009, 3-15. MIT press, Cambridge. J. Decety, W. Ickes (Eds.).
7. Bieri D., Reeve R.A., Champion G.D., Addicoat L., Ziegler J.B. The Faces Pain Scale for the self-assessment of the severity of pain experienced by children: development, initial validation, and preliminary investigation for ratio scale properties. Pain 1990, 41:139-150.
8. Botvinick M., Jha A.P., Bylsma L.M., Fabian S.A., Solomon P.E., Prkachin K.M. Viewing facial expressions of pain engages cortical areas involved in the direct experience of pain. Neuroimage 2005, 25:312-319.
9. Brunet E., Sarfati Y., Hardy-Bayle M.C., Decety J. APET investigation of the attribution of intentions with a nonverbal task. Neuroimage 2000, 11:157-166.
10. Cabeza R. Hemispheric asymmetry reduction in older adults: the HAROLD model. Psychol. Aging 2002, 17:85-100.
11. Carstensen L.L., Turan B., Scheibe S., Ram N., Ersner-Hershfield H., Samanez-Larkin G.R., Brooks K.P., Nesselroade J.R. Emotional experience improves with age: evidence based on over 10 years of experience sampling. Psychol. Aging 2011, 26:21-33.
12. Castelli I., Baglio F., Blasi V., Alberoni M., Falini A., Liverta-Sempio O., Nemni R., Marchetti A. Effects of aging on mindreading ability through the eyes: an fMRI study. Neuropsychologia 2010, 48:2586-2594.
13. Charles S.T., Piazza J.R. Memories of social interactions: age differences in emotional intensity. Psychol. Aging 2007, 22:300-309.
14. Chen C., Yang C.Y., Cheng Y. Sensorimotor resonance is an outcome but not a platform to anticipating harm to others. Soc. Neurosci. 2012, 7:578-590.
15. Cheng Y., Chen C., Lin C.P., Chou K.H., Decety J. Love hurts: an fRMI study. Neuroimage 2010, 51:923-929.
16. Cheng Y., Lin C.P., Liu H.L., Hsu Y.Y., Lim K.E., Hung D., Decety J. Expertise modulates the perception of pain in others. Curr. Biol. 2007, 17:1708-1713.
17. Choudhury S., Charman T., Blakemore S.J. Mentalizing and Development during Adolescence 2009, Guilford, New York.
18. Decety J. The neurodevelopment of empathy in humans. Dev. Neurosci. 2010, 32:257-267.
19. Decety J., Echols S., Correll J. The blame game: the effect of responsibility and social stigma on empathy for pain. J.Cogn. Neurosci. 2010, 22:985-997.
20. Decety J., Grèzes J. The power of simulation: Imagining one's own and other's behavior. Brain Research 2006, 1079:4-14.
21. Decety J., Michalska K.J. Neurodevelopmental changes in the circuits underlying empathy and sympathy from childhood to adulthood. Dev. Sci. 2010, 13:886-899.
22. Decety J., Michalska K.J., Akitsuki Y. Who caused the pain? an fMRI investigation of empathy and intentionality in children. Neuropsychologia 2008, 46:2607-2614.
23. Decety J., Michalska K.J., Akitsuki Y., Lahey B.B. Atypical empathic responses in adolescents with aggressive conduct disorder: a functional MRI investigation. Biol. Psychol. 2009, 80:203-211.
24. Decety J., Michalska K.J., Kinzler K.D. The contribution of emotion and cognition to moral sensitivity: a neurodevelopmental study. Cereb. Cortex 2012, 22:209-220.
25. Decety J., Porges E.C. Imagining being the agent of actions that carry different moral consequences: an fMRI study. Neuropsychologia 2011, 49:2994-3001.
26. Decety J., Sommerville J.A. Shared representations between self and others: a social cognitive neuroscience view. Trends Cogn. Sci. 2003, 7:527-533.
27. Decety J., Svetlova M. Putting together phylogenetic and ontogenetic perspectives on empathy. Dev. Cogn. Neurosci. 2012, 2:1-24.
28. Diehl M., Coyle N., Labouvie-Vief G. Age and sex differences in strategies of coping and defense across the life span. Psychol. Aging 1996, 11:127-139.
29. Eisenberg N., Eggum N.D. Empathic responding: sympathy and personal distress. The Social Neuroscience of Empathy 2009, 71-83. MIT press, Cambridge. J. Decety, W. Ickes (Eds.).
30. Eysenck S.B., Pearson P.R., Easting G., Allsopp J. Age norms for impulsiveness, venturesomeness and empathy in adults. Pers. Indiv. Differ 1985, 6:613-619.
31. Gleichgerrcht E., Torralva T., Roca M., Pose M., Manes F. The role of social cognition in moral judgment in frontotemporal dementia. Soc. Neurosci. 2011, 6:113-122.
32. Good C.D., Johnsrude I.S., Ashburner J., Henson R.N., Friston K.J., Frackowiak R.S. Avoxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 2001, 14:21-36.
33. Grady C. The cognitive neuroscience of ageing. Nat. Rev. Neurosci. 2012, 13:491-505.
34. Grady C.L., Springer M.V., Hongwanishkul D., McIntosh A.R., Winocur G. Age-related changes in brain activity across the adult lifespan. J.Cogn. Neurosci. 2006, 18:227-241.
35. Gray K., Wegner D.M. The sting of intentional pain. Psychol. Sci. 2008, 19:1260-1262.
36. Gross J.J., Carstensen L.L., Pasupathi M., Tsai J., Skorpen C.G., Hsu A.Y. Emotion and aging: experience, expression, and control. Psychol. Aging 1997, 12:590-599.
37. Grühn D., Rebucal K., Diehl M., Lumley M., Labouvie-Vief G. Empathy across the adult lifespan: longitudinal and experience-sampling findings. Emotion 2008, 8:753-765.
38. Gu X., Liu X., Guise K.G., Naidich T.P., Hof P.R., Fan J. Functional dissociation of the frontoinsular and anterior cingulate cortices in empathy for pain. J.Neurosci. 2010, 30:3739-3744.
39. Gunning-Dixon F.M., Gur R.C., Perkins A.C., Schroeder L., Turner T., Turetsky B.I., Chan R.M., Loughead J.W., Alsop D.C., Maldjian J., Gur R.E. Age-related differences in brain activation during emotional face processing. Neurobiol. Aging 2003, 24:285-295.
40. Gutchess A.H., Kensinger E.A., Schacter D.L. Aging self-referencing, and medial prefrontal cortex. Soc. Neurosci. 2007, 2:117-133.
41. Haug H., Eggers R. Morphometry of the human cortex cerebri and corpus striatum during aging. Neurobiol. Aging 1991, 12:336-338. discussion 52-55.
42. Hazlett E.A., Buchsbaum M.S., Mohs R.C., Spiegel-Cohen J., Wei T.C., Azueta R., Haznedar M.M., Singer M.B., Shihabuddin L., Luu-Hsia C., Harvey P.D. Age-related shift in brain region activity during successful memory performance. Neurobiol. Aging 1998, 19:437-445.
43. Helson R., Jones C., Kwan V.S. Personality change over 40 years of adulthood: hierarchical linear modeling analyses of two longitudinal samples. J.Pers. Soc. Psychol. 2002, 83:752-766.
44. Iidaka T., Sadato N., Yamada H., Murata T., Omori M., Yonekura Y. An fMRI study of the functional neuroanatomy of picture encoding in younger and older adults. Brain Res. Cogn. Brain Res. 2001, 11:1-11.
45. Jackson P.L., Brunet E., Meltzoff A.N., Decety J. Empathy examined through the neural mechanisms involved in imagining how I feel versus how you feel pain. Neuropsychologia 2006, 44:752-761.
46. Jackson P.L., Meltzoff A.N., Decety J. How do we perceive the pain of others? A window into the neural processes involved in empathy. Neuroimage 2005, 24:771-779.
47. Johannsen P., Jakobsen J., Bruhn P., Hansen S.B., Gee A., Stodkilde-Jorgensen H., Gjedde A. Cortical sites of sustained and divided attention in normal elderly humans. Neuroimage 1997, 6:145-155.
48. Kausler D.H. Experimental Psychology, Cognition, and Human Aging 1991, Springer, New York, USA. second ed.
49. Keightley M.L., Winocur G., Burianova H., Hongwanishkul D., Grady C.L. Age effects on social cognition: faces tell a different story. Psychol. Aging 2006, 21:558-572.
50. LaBar K.S., Mesulam M., Gitelman D.R., Weintraub S. Emotional curiosity: modulation of visuospatial attention by arousal is preserved in aging and early-stage Alzheimer's disease. Neuropsychologia 2000, 38:1734-1740.
51. Lamm C., Batson C.D., Decety J. The neural substrate of human empathy: effects of perspective-taking and cognitive appraisal. J.Cogn. Neurosci. 2007, 19:42-58.
52. 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.
53. Levine L.J., Bluck S. Experienced and remembered emotional intensity in older adults. Psychol. Aging 1997, 12:514-523.
54. Lin K.N., Wang P.N., Liu C.Y., Chen W.T., Lee Y.C., Liu H.C. Cutoff scores of the cognitive abilities screening instrument, Chinese version in screening of dementia. Dement. Geriatr. Cogn. Disord. 2002, 14:176-182.
55. Lough S., Kipps C.M., Treise C., Watson P., Blair J.R., Hodges J.R. Social reasoning, emotion and empathy in frontotemporal dementia. Neuropsychologia 2006, 44:950-958.
56. Madden D.J., Gottlob L.R., Denny L.L., Turkington T.G., Provenzale J.M., Hawk T.C., Coleman R.E. Aging and recognition memory: changes in regional cerebral blood flow associated with components of reaction time distributions. J.Cogn. Neurosci. 1999, 11:511-520.
57. Marcus D.S., Wang T.H., Parker J., Csernansky J.G., Morris J.C., Buckner R.L. Open Access Series of Imaging Studies (OASIS): cross-sectional MRI data in young, middle aged, nondemented, and demented older adults. J.Cogn. Neurosci. 2007, 19:1498-1507.
58. Mather M., Canli T., English T., Whitfield S., Wais P., Ochsner K., Gabrieli J.D., Carstensen L.L. Amygdala responses to emotionally valenced stimuli in older and younger adults. Psychol. Sci. 2004, 15:259-263.
59. Mather M., Carstensen L.L. Aging and attentional biases for emotional faces. Psychol. Sci. 2003, 14:409-415.
60. Mather M., Knight M.R. Angry faces get noticed quickly: threat detection is not impaired among older adults. J.Gerontol. B-Psychol. Sci. Soc. Sci. 2006, 61:54-57.
61. Menon V., Uddin L.Q. Saliency, switching, attention and control: a network model of insula function. Brain Struct. Funct. 2010, 214:655-667.
62. Penny W.D., Stephan K.E., Daunizeau J., Rosa M.J., Friston K.J., Schofield T.M., Leff A.P. Comparing families of dynamic causal models. PLoS Comput. Biol. 2010, 6:e1000709.
63. Phillips L.H., MacLean R.D., Allen R. Age and the understanding of emotions: neuropsychological and sociocognitive perspectives. J.Gerontol. Ser. B- Psychol. Sci. Soc. Sci. 2002, 57:526-530.
64. Resnick S.M., Pham D.L., Kraut M.A., Zonderman A.B., Davatzikos C. Longitudinal magnetic resonance imaging studies of older adults: a shrinking brain. J.Neurosci. 2003, 23:3295-3301.
65. Reuter-Lorenz P.A., Jonides J., Smith E.E., Hartley A., Miller A., Marshuetz C., Koeppe R.A. Age differences in the frontal lateralization of verbal and spatial working memory revealed by PET. J.Cogn. Neurosci. 2000, 12:174-187.
66. Reuter-Lorenz P.A., Lustig C. Brain aging: reorganizing discoveries about the aging mind. Curr. Opin. Neurobiol. 2005, 15:245-251.
67. Richter D., Kunzmann U. Age differences in three facets of empathy: performance-based evidence. Psychol. Aging 2011, 26:60-70.
68. Riecker A., Grodd W., Klose U., Schulz J.B., Gröschel K., Erb M., Ackermann H., Kastrup A. Relation between regional functional MRI activation and vascular reactivity to carbon dioxide during normal aging. J.Cereb. Blood Flow Metab. 2003, 23:565-573.
69. Roth-Hanania R., Davidov M., Zahn-Waxler C. Empathy development from 8 to 16 months: early signs of concern for others. Infant Behav. Dev. 2011, 34:447-458.
70. Ruffman T., Henry J.D., Livingstone V., Phillips L.H. Ameta-analytic review of emotion recognition and aging: implications for neuropsychological models of aging. Neurosci. Biobehav. Rev. 2008, 32:863-881.
71. Rypma B., D'Esposito M. Isolating the neural mechanisms of age-related changes in human working memory. Nat. Neurosci. 2000, 3:509-515.
72. Salat D.H., Buckner R.L., Snyder A.Z., Greve D.N., Desikan R.S., Busa E., Morris J.C., Dale A.M., Fischl B. Thinning of the cerebral cortex in aging. Cereb. Cortex 2004, 14:721-730.
73. Schieman S., van Gundy K. The personal and social links between age and self-reported empathy. Soc. Psychol. Quart. 2000, 63:152-174.
74. Schulze E.T., Geary E.K., Susmaras T.M., Paliga J.T., Maki P.M., Little D.M. Anatomical correlates of age-related working memory declines. J.Aging Res. 2011, 2011:606871.
75. Shackman A.J., Salomons T.V., Slagter H.A., Fox A.S., Winter J.J., Davidson R.J. The integration of negative affect, pain and cognitive control in the cingulate cortex. Nat. Rev. Neurosci. 2011, 12:154-167.
76. Shamay-Tsoory S. Empathic processing: its cognitive and affective dimensions and neuroanatomical basis 2009, MIT press, Cambridge.
77. Singer T., Seymour B., O'Doherty J., Kaube H., Dolan R.J., Frith C.D. Empathy for pain involves the affective but not sensory components of pain. Science 2004, 303:1157-1162.
78. Smith E.E., Geva A., Jonides J., Miller A., Reuter-Lorenz P., Koeppe R.A. The neural basis of task-switching in working memory: effects of performance and aging. Proc. Natl. Acad. Sci. U.S.A 2001, 98:2095-2100.
79. St Jacques P., Dolcos F., Cabeza R. Effects of aging on functional connectivity of the amygdala during negative evaluation: a network analysis of fMRI data. Neurobiol. Aging 2010, 31:315-327.
80. Tisserand D.J., Pruessner J.C., Sanz Arigita E.J., van Boxtel M.P., Evans A.C., Jolles J., Uylings H.B. Regional frontal cortical volumes decrease differentially in aging: an MRI study to compare volumetric approaches and voxel-based morphometry. Neuroimage 2002, 17:657-669.
81. Vaish A., Warneken F. Social-Cognitive Contribution To Young Children's Empathic and Pro-Social Behavior 2012, MIT press, Cambridge.
82. Vollm B.A., Taylor A.N., Richardson P., Corcoran R., Stirling J., McKie S., Deakin J.F., Elliott R. Neuronal correlates of theory of mind and empathy: a functional magnetic resonance imaging study in a nonverbal task. Neuroimage 2006, 29:90-98.
83. Walhovd K.B., Fjell A.M., Reinvang I., Lundervold A., Dale A.M., Eilertsen D.E., Quinn B.T., Salat D., Makris N., Fischl B. Effects of age on volumes of cortex, white matter and subcortical structures. Neurobiol. Aging 2005, 26:1261-1270. discussion 75-78.
84. West R.L. An application of prefrontal cortex function theory to cognitive aging. Psychol. Bull. 1996, 120:272-292.
85. Zahn-Waxler C., Radke-Yarrow M., Wagner E., Chapman M. Development of concern for others. Dev. Psychol. 1992, 28:126-136.