Inability to empathize: Brain lesions that disrupt sharing and understanding another's emotions

Brain

Volumn 137, Issue 4, 2014, Pages 981-997

  Hillis, Argye E ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS HOSPITAL   (United States)

Author keywords

emotion; empathy; focal lesion studies; stroke

Indexed keywords

ALZHEIMER DISEASE; AMYGDALOID NUCLEUS; ANTERIOR CINGULATE; ANTERIOR INSULA; ANTISOCIAL BEHAVIOR; BRAIN ARTERY ANEURYSM RUPTURE; BRAIN DAMAGE; CEREBELLUM; CEREBROVASCULAR ACCIDENT; COMPREHENSION; COMPUTER ASSISTED TOMOGRAPHY; CORTICOBASAL DEGENERATION; DOUBLE DISSOCIATION; EMPATHY; ENCEPHALITIS; EXECUTIVE FUNCTION; FACIAL EXPRESSION; FRONTOTEMPORAL DEMENTIA; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GESTURE; GRAY MATTER; HUMAN; HUNTINGTON CHOREA; INFERIOR FRONTAL GYRUS; ORBITAL CORTEX; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROGRESSIVE SUPRANUCLEAR PALSY; REVIEW; SCHIZOPHRENIA; SOCIAL PSYCHOLOGY; SUPERIOR TEMPORAL SULCUS; TEMPORAL CORTEX; THALAMUS; TRAUMATIC BRAIN INJURY; VOXEL BASED MORPHOMETRY; WORKING MEMORY; BRAIN; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY;

BRAIN; EMPATHY; HUMANS; STROKE;

EID: 84897909998     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awt317     Document Type: Review

References (109)

1. Adolphs R. Cognitive neuroscience of human social behaviour. Nat Rev Neurosci 2003; 4: 165-78.
2. Amodio DM, Frith CD. Meeting of minds: the medial frontalcortex and social cognition. Nat Rev Neurosci 2006; 7: 268-77.
3. Baird A, Dewar BK, Critchley H, Dolan R, Shallice T, Cipolotti L. Social and emotional functions in three patients with medial frontal lobe damage including the anterior cingulate cortex. Cogn Neuropsychiatry 2006; 11: 369-88.
4. Baron-Cohen S, Jolliffe T, Mortimore C, Robertson M. Another advanced test of theory of mind: Evidence from very high functioning adults with autism or asperger syndrome. J Child Psychol Psychiatry 1997; 38: 813-22.
5. Bartsch K. The role of experience in children's developing folk epistem-ology: review and analysis from the theory-theory perspective. New Ideas Psychol 2002; 20: 145-61.
6. Bernhardt BC, Singer T. The neural basis of empathy. Ann Rev Neurosci 2012; 35: 1-23.
7. Bird CM, Castelli F, Malik O, Frith U, Husain M. The impact of extensive medial frontal lobe damage on 'theory of mind' and cognition. Brain 2004; 127: 914-28.
8. Bodini B, Iacoboni M, Lenzi GL. Acute stroke effects on emotions: an interpretation through the mirror system. Curr Opin Neurol 2004; 17: 55-60.
9. Bramham J, Morris RG, Hornak J, Bullock P, Polkey CE. Social and emotional functioning following bilateral and unilateral neurosurgical pre-frontal cortex lesions. J Neuropsychol 2009; 3: 125-43.
10. Brown S, Gao X, Tisdelle L, Eickhoff SB, Liotti M. Naturalizing aesthetics: brain areas for aesthetic appraisal across sensory modalities. Neuroimage 2011; 58: 250-8.
11. Brunnlieb C, Münte TF, Tempelmann C, Heldmann M. Vasopressin modulates neural responses related to emotional stimuli in the right amygdala. Brain Res 2013; 1499: 29-42.
12. Bzdok D, Schilbach L, Vogeley K, Schneider K, Laird AR, Langner R, Eickhoff SB. Parsing the neural correlates of moral cognition: ALE meta-analysis on morality, theory of mind, and empathy. Brain Struct Funct 2012; 217: 783-96.
13. Carr L, Iacoboni M, Dubeau M, Mazziotta JC, Lenzi GL. Neural mechanisms of empathy in humans: a relay from neural systems for imitation to limbic areas. Proc Natl Acad Sci USA 2003; 100: 5497-502.
14. Chakrabarti B, Bullmore E, Baron-Cohen S. Empathizing with basic emotions: common and discrete neural substrates. Soc Neurosci 2006; 1: 364-84.
15. Cheng Y, Chen C, Lin CP, Chou KH, Decety J. Love hurts: an fMRI study. Neuroimage 2010; 51: 923-9.
16. Couto B, Sedeño L, Sposato LA, Sigman M, Riccio PM, Salles A, et al. Insular networks for emotional processing and social cognition: comparison of two case reports with either cortical or subcortical involvement. Cortex 2013; 49: 1420-34.
17. Cox CL, Uddin LQ, Di Martino A, Castellanos FX, Milham MP, Kelly C. The balance between feeling and knowing: affective and cognitive empathy are reflected in the brain's intrinsic functional dynamics. Soc Cogn Affect Neurosci 2012; 7: 727-37.
18. Critchley HD. Psychophysiology of neural, cognitive and affective integration: fMRI and autonomic indicants. Int J Psychophysiol 2009; 73: 88-94.
19. Dapretto M, Davies MS, Pfeifer JH, Scott AA, Sigman M, Bookheimer SY, et al. Understanding emotions in others: mirror neuron dysfunction in children with autism spectrum disorders. Nat Neurosci 2006; 9: 28-30.
20. Dara C, Gottesman RF, Hillis AE. Right hemisphere dysfunction is more accurately detected by prosody impairment than by hemispatial neglect. International Stroke Conference. 2013a. Abstract.
21. Dara C, Kirsch-Darrow L, Ochfeld E, Slenz J, Agranovich A, Vasconcellos-Faria A, et al. Impaired emotion processing from vocal and facial cues in frontotemporal dementia compared to right hemisphere stroke. Neurocase 2013b; 19: 521-9.
22. Davis MH. Measuring individual differences in empathy: evidence for a multidimensional approach. J Pers Soc Psychol 1983; 44: 113-26.
23. Decety J. Dissecting the neural mechanisms mediating empathy. Emotion Rev 2011; 3: 92-108.
24. Decety J, Jackson PL. The functional architecture of human empathy. Behav Cogn Neurosci Rev 2004; 3: 71-100.
25. de Vignemont F, Singer T. The empathic brain: how, when and why? Trends Cogn Sci 2006; 10: 435-41.
26. Driscoll DM, Dal Monte O, Solomon J, Krueger F. Empathic deficits in combat veterans with traumatic brain injury: a voxel-based lesion-symptom mapping study. Cogn Behav Neurol 2012; 25: 160-6.
27. Dziobek I, Rogers K, Fleck S, Bahnemann M, Heekeren HR, Wolf OT, et al. Dissociation of cognitive and emotional empathy in adults with Asperger syndrome using the Multifaceted Empathy Test (MET). J Autism Dev Discord 2008; 38: 464-73.
28. Eslinger PJ. Neurological and neuropsychological bases of empathy. Eur Neurol 1998; 39: 193-9.
29. Eslinger PJ, Biddle KR, Grattan LM. Cognitive and social development in children with prefrontal cortex lesions. In: Krasnegor NA, Lyon GR, Goldman-Rakic PS, editors. Development of prefrontal cortex: evolution, neurobiology, and behavior. Baltimore: Brookes; 1997. p. 295-335.
30. Eslinger PJ, Moore P, Anderson C, Grossman M. Social cognition, executive functioning, and neuroimaging correlates of empathic deficits in frontotemporal dementia. J Neuropsychiatry Clin Neurosci 2011; 23: 74-82.
31. Eslinger PJ, Satish U, Grattan LM. Alterations in cognitively-and affectively-based empathy after cerebral damage. J Int Neuropsychol Soc 1996; 2: 15.
32. Fellows LK, Heberlein AS, Morales DA, Shivde G, Waller S, Wu DH. Method matters: an empirical study of impact in cognitive neurosci-ence. J Cogn Neurosci 2005; 17: 850-8.
33. Finger EC. New potential therapeutic approaches in frontotemporal dementia: oxytocin, vasopressin, and social cognition. J Mol Neurosci 2011; 45: 696-701.
34. Fischer-Shofty M, Brüne M, Ebert A, Shefet D, Levkovitz Y, Shamay-Tsoory SG. Improving social perception in schizophrenia: the role of oxytocin. Schizophr Res 2013; 146: 357-62.
35. Fisher T, Shamay-Tsoory S, Eran A, Aharon-Peretz J. Characterization of recovery and neuropsychological consequences of orbitofrontal lesion: a case study. Neurocase 2011; 17: 285-93.
36. Frith U, Frith CD. Development and neurophysiology of mentalizing. Philos Trans R Soc Lond Ser B 2003; 358: 459-73.
37. Gazzola V, Aziz-Zadeh L, Keysers C. Empathy and the somatotopic auditory mirror system in humans. Curr Biol 2006; 16: 1824-9.
38. Gorno-Tempini ML, Pradelli S, Serafini M, Pagnoni G, Baraldi P, Porro C, et al. Explicit and incidental facial expression processing: an fMRI study. Neuroimage 2001; 14: 465-73.
39. Grattan LM, Bloomer RH, Archambault FX, Eslinger PJ. Cognitive flexibility and empathy after frontal lobe lesion. Neuropsychiatry Neuropsychol Behav Neurol 1994; 7: 251-9.
40. Grattan LM, Eslinger PJ. Higher cognition and social behavior: changes in cognitive flexibility and empathy after cerebral lesions. Neuropsychology 1989; 3: 175-85.
41. Grattan LM, Eslinger PJ. Influence of cerebral lesion site upon the onset and progression of interpersonal deficits following brain injury. J Clin Exp Neuropsychol 1990; 12: 33.
42. Grattan LM, Eslinger PJ. Characteristics of favorable recovery from frontal lobe damage. Neurology 1991; 41 (suppl 1): 266.
43. Grattan LM, Eslinger PJ. Long-term psychological consequences of childhood frontal lobe lesion in patient DT. Brain Cogn 1992; 20: 185-95.
44. Gregory CA, Orrell M, Sahakian B, Hodges J.R. Can frontotemporal dementia and Alzheimer's disease be differentiated using a brief battery of tests? Int J Geriatr Psychiatry 1997; 12: 375-83.
45. Gu X, Gao Z, Wang X, Liu X, Knight RT, Hof PR, et al. Anterior insular cortex is necessary for empathetic pain perception. Brain 2012; 135: 2726-35.
46. Herbet G, Lafargue G, Bonnetblanc F, Moritz-Gasser S, Duffau H. Is the right frontal cortex really crucial in the mentalizing network? A longitudinal study in patients with a slow-growing lesion. Cortex 2013. in press.
47. Hétu S, Taschereau-Dumouchel V, Jackson PL. Stimulating the brain to study social interactions and empathy. Brain Stimulation: Basic, trans-lational, and clinical research in neuromodulation 2012; 5: 95-102.
48. Hooker CI, Bruce L, Lincoln SH, Fisher M, Vinogradov S. Theory of mind skills are related to gray matter volume in the ventromedial prefrontal cortex in schizophrenia. Biol Psychiatry 2011; 70: 1169-78.
49. Hooker CI, Verosky SC, Germine LT, Knight RT, D'Esposito M. Mentalizing about emotion and its relationship to empathy. Soc Cogn Affect Neurosci 2008; 3: 204-17.
50. Hurlemann R, Patin A, Onur OA, Cohen MX, Baumgartner T, Metzler S, et al. Oxytocin enhances amygdala-dependent, socially reinforced learning and emotional empathy in humans. J Neurosci 2010; 30: 4999-5007.
51. Jabbi M, Swart M, Keysers C. Empathy for positive and negative emotions in the gustatory cortex. Neuroimage 2007; 34: 1744-53.
52. Jenkins WM, Merzenich MM. Reorganization of neocortical representations after brain injury: a neurophysiological model of the bases of recovery from stroke. Prog Brain Res 1987; 71: 249-66.
53. Johnson SC. The recognition of mentalistic agents in infancy. Trends Cogn Sci 2000; 4: 22-8.
54. Jesso S, Morlog D, Ross S, Pell MD, Pasternak SH, Mitchell DG, et al. The effects of oxytocin on social cognition and behaviour in fronto-temporal dementia. Brain 2011; 134 (Pt 9): 2493-501.
55. Kemp J, Berthel MC, Dufour A, Després O, Henry A, Namer IJ, et al. Caudate nucleus and social cognition: Neuropsychological and SPECT evidence from a patient with focal caudate lesion. Cortex 2013; 49: 559-71.
56. Keysers C, Gazzola V. Towards a unifying neural theory of social cognition. Prog Brain Res 2006; 156: 379-401.
57. Kim EJ, Sidhu M, Gaus SE, Huang EJ, Hof PR, Miller BL, et al. Selective frontoinsular von Economo neuron and fork cell loss in early behavioral variant frontotemporal dementia. Cereb Cortex 2012; 22: 251-9.
58. Kringelbach ML, Rolls ET. The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsych-ology. Prog Neurobiol 2004; 72: 341-72.
59. 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: 2492-502.
60. Lee HS, Brennan PF, Daly BJ. Relationship of empathy to appraisal, depression, life satisfaction, and physical health in informal caregivers of older adults. Res Nurs Health 2001; 24: 44-56.
61. Lee J, Zaki J, Harvey PO, Ochsner K, Green MF. Schizophrenia patients are impaired in empathic accuracy. Psychol Med 2011; 41: 2297-304.
62. Leigh R, Oishi K, Hsu J, Lindquist M, Gottesman RF, Jarso S, et al. Acute lesions that impair affective empathy. Brain 2013; 136: 2539-49.
63. Leopold A, Krueger F, Dal Monte O, Pardini M, Pulaski SJ, et al. Damage to the left ventromedial prefrontal cortex impacts affective theory of mind. Soc Cogn Affect Neurosci 2012; 7: 871-80.
64. McDonald S, Flanagan S. Social perception deficits after traumatic brain injury: interaction between emotion recognition, mentalizing ability, and social communication. Neuropsychology 2004; 18: 572-9.
65. Meltzoff AN, Decety J. What imitation tells us about social cognition: a rapprochement between developmental psychology and cognitive neuroscience. Philos Trans R Soc Lond Ser B 2003; 358: 491-500.
66. Mesulam MM, Mufson EJ. Insula of the old world monkey. I. Architectonics in the insulo-orbito-temporal component of the para-limbic brain. J Comp Neurol 1982; 212: 1-22.
67. Meyer ML, Masten CL, Ma Y, Wang C, Shi Z, Eisenberger NI, et al. Empathy for the social suffering of friends and strangers recruits distinct patterns of brain activation. Soc Cogn Affect Neurosci 2013; 8: 446-54.
68. Narvid J, Gorno-Tempini ML, Slavotinek A, Dearmond SJ, Cha YH, Miller BL, et al. Of brain and bone: the unusual case of Dr. A. Neurocase 2009; 15: 190-205.
69. Neumann D, Zupan B, Babbage DR, Radnovich AJ, Tomita M, Hammond F, et al. Affect recognition, empathy, and dysosmia after traumatic brain injury. Arch Phys Med Rehabil 2012; 93: 1414-20.
70. O'Keeffe FM, Murray B, Coen RF, Dockree PM, Bellgrove MA, Garavan H, et al. Loss of insight in frontotemporal dementia, cortico-basal degeneration and progressive supranuclear palsy. Brain 2007; 130 (Pt 3): 753-64.
71. Pell MD. Judging emotion and attitudes from prosody following brain damage. Prog Brain Res 2006; 156: 303-17.
72. Perry RJ, Rosen HR, Kramer JH, Beer JS, Levenson RL, Miller BL. Hemispheric dominance for emotions, empathy and social behaviour: evidence from right and left handers with frontotemporal dementia. Neurocase 2001; 7: 145-60.
73. Rankin KP, Gorno-Tempini ML, Allison SC, Stanley CM, Glenn S, Weiner MW, et al. Structural anatomy of empathy in neurodegenera-tive disease. Brain 2006; 129: 2945-56.
74. Rankin KP, Kramer J, Miller BL. Patterns of cognitive and emotional empathy in frontotemporal lobar degeneration. Cog Behav Neurol 2005; 18: 28-36.
75. Rascovsky K, Hodges JR, Knopman D, Mendez MF, Kramer JH, Xie S, et al. Sensitivity of revised diagnostic criteria for the behavioral variant of frontotemporal dementia. Brain 2011; 134: 2456-77.
76. Robertson LC, Knight RT, Rafal R, Shimamura AP. Cognitive neuropsych-ology is more than single-case studies. J Exp Psychol Learn Mem Cogn 1993; 19: 710-17.
77. Roldan Gerschcovich E, Cerquetti D, Tenca E, Leiguarda R. The impact of bilateral cerebellar damage on theory of mind, empathy and decision making. Neurocase 2011; 17: 270-5.
78. Rosen HJ, Allison SC, Schauer GF, Gorno-Tempini ML, Weiner MW, Miller BL. Neuroanatomical correlates of behavioural disorders in dementia. Brain 2005; 128: 2612-25.
79. Ross ED, Monnot M. Neurology of affective prosody and its functional-anatomic organization in right hemisphere. Brain Lang 2008; 104: 51-74.
80. Samson D, Apperly IA, Chiavarino C, Humphreys GW. Left temporopar-ietal junction is necessary for representing someone else's belief. Nat Neurosci 2004; 7: 499-500.
81. Samson D, Apperly IA, Humphreys GW. Error analyses reveal contrasting deficits in 'theory of mind': neuropsychological evidence from a 3-option false belief task. Neuropsychologia 2007; 45: 2561-9.
82. Samson D, Apperly IA, Kathirgamanathan U, Humphreys GW. Seeing it my way: a case of a selective deficit in inhibiting self-perspective. Brain 2005; 128: 1102-11.
83. Saxe R, Kanwisher N. People thinking about thinking people: The role of the temporo-parietal junction in 'Theory of Mind'. Neuroimage 2003; 19: 1835-42.
84. Schmahmann JD, Weilburg J, Sherman C. The neuropsychiatry of the cerebellum-insights from the clinic. Cerebellum 2007; 6: 254-267.
85. 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: 1743-54.
86. Schoenfeld MA, Noesselt T, Poggel D, Tempelmann C, Hopf JM, Woldorff MG, et al. Analysis of pathways mediating preserved vision after striate cortex lesions. Ann Neurol 2002; 52: 814-24.
87. Sebastian CL, Fontaine NM, Bird G, Blakemore SJ, Brito SA, McCrory EJ, et al. Neural processing associated with cognitive and affective theory of mind in adolescents and adults. Soc Cogn Affect Neurosci 2012; 7: 53-63.
88. Seeley WW. Selective functional, regional, and neuronal vulnerability in frontotemporal dementia. Curr Opin Neurol 2008; 21: 701-7.
89. Seeley WW, Carlin DA, Allman JM, Macedo MN, Bush C, Miller BL, et al. Early frontotemporal dementia targets neurons unique to apes and humans. Ann Neurol 2006; 60: 660-7.
90. Shamay-Tsoory SG. The neural bases for empathy. Neuroscientist 2011; 17: 18-24.
91. Shamay-Tsoory SG, Aharon-Peretz J. Dissociable prefrontal networks for cognitive and affective theory of mind: a lesion study. Neuropsychologia 2007; 45: 3054-67.
92. Shamay-Tsoory SG, Aharon-Peretz J, Levkovitz Y. The neuroanatomical basis of affective mentalizing in schizophrenia: comparison of patients with schizophrenia and patients with localized prefrontal lesions. Schizophr Res 2007; 90: 274-83.
93. Shamay-Tsoory SG, Aharon-Peretz J, Perry D. Two systems for em-pathy:a double dissociation between emotional and cognitive empathy in inferior frontal gyrus versus ventromedial prefrontal lesions. Brain 2009; 132: 617-27.
94. Shamay-Tsoory SG, Lester H, Chisin R, Israel O, Bar-Shalom R, Peretz A, et al. The neural correlates of understanding the other's distress: a positron emission tomography investigation of accurate empathy. Neuroimage 2005a; 27: 468-72.
95. Shamay-Tsoory SG, Tomer R, Berger BD, Aharon-Peretz J. Characterization of empathy deficits following prefrontal brain damage: the role of the right ventromedial prefrontal cortex. J Cogn Neurosci 2003; 15: 324-37.
96. Shamay-Tsoory SG, Tomer R, Berger BD, Goldsher D, Aharon-Peretz J. Impaired 'affective theory of mind' is associated with right ventro-medial prefrontal damage. Cogn Behav Neurol 2005b; 18: 55-67.
97. Shamay-Tsoory SG, Tomer R, Goldsher D, Berger BD, Aharon-Peretz J. Impairment in cognitive and affective empathy in patients with brain lesions: anatomical and cognitive correlates. J Clin Exp Neuropsychol 2004; 26: 1113-27.
98. Singer T, Seymour B, O'Doherty J, Kaube H, Dolan RJ, Firth CD. Empathy for pain involves the affective but not sensory components of pain. Science 2004; 303: 1157-62.
99. Snowden JS, Gibbons ZC, Blackshaw A, Doubleday E, Thompson J, Craufurd D, et al. Social cognition in frontotemporal dementia and Huntington's disease. Neuropsychologia 2003; 41: 688-701.
100. Spikman JM, Timmerman ME, Milders MV, Veenstra WS, van der Naalt J. Social cognition impairments in relation to general cognitive deficits, injury severity, and prefrontal lesions in traumatic brain injury patients. J Neurotrauma 2012; 29: 101-11.
101. Squire LR, Wixted JT, Clark RE. Recognition memory and the medial temporal lobe: a new perspective. Nat Rev Neurosci 2007; 8: 872-83.
102. Stone VE, Baron-Cohen S, Calder A, Keane J, Young A. Acquired theory of mind impairments in individuals with bilateral amygdala lesions. Neuropsychologia 2003; 41: 209-20.
103. Stuss DT, Anderson V. The frontal lobes and theory of mind: developmental concepts from adult focal lesion research. Brain Cogn 2004; 55: 69-83.
104. Trinkler I, Cleret de Langavant L, Bachoud-Lévi AC. Joint recognition-expression impairment of facial emotions in Huntington's disease despite intact understanding of feelings. Cortex 2013; 49: 549-58.
105. Turkeltaub PE, Eden GF, Jones KM, Zeffiro TA. Meta-analysis of the functional neuroanatomy of single-word reading: method and validation. Neuroimage 2002; 16: 765-80.
106. Viskontas IV, Possin KL, Miller BL. Symptoms of frontotemporal dementia provide insights into orbitofrontal cortex function and social behavior. Ann N Y Acad Sci 2007; 1121: 528-45.
107. Xerri C, Merzenich MM, Peterson BE, Jenkins W. Plasticity of primary somatosensory cortex paralleling sensorimotor skill recovery from stroke in adult monkeys. J Neurophysiol 1998; 79: 2119-48.
108. Zahn R, Moll J, Iyengar V, Huey ED, Tierney M, Krueger F, et al. Social conceptual impairments in frontotemporal lobar degeneration with right anterior temporal hypometabolism. Brain 2009; 132: 604-16.
109. Zahn R, Moll J, Krueger F, Huey ED, Garrido G, Grafman J. Social concepts are represented in the superior anterior temporal cortex. Proc Natl Acad Sci USA 2007; 104: 6430-5.