Altered brain activity during emotional empathy in somatoform disorder

Human Brain Mapping

Volumn 33, Issue 11, 2012, Pages 2666-2685

  De Greck, Moritz ^a   Scheidt, Lisa ^b   Bölter, Annette F ^b   Frommer, Jörg ^b   Ulrich, Cornelia ^c   Stockum, Eva ^b   Enzi, Björn ^d   Tempelmann, Claus ^b   Hoffmann, Thilo ^c   Han, Shihui ^a   Northoff, Georg ^e  

^a PEKING UNIVERSITY   (China)

^b OTTO VON GUERICKE UNIVERSITY   (Germany)

^c Fachklinikum Uchtspringe ^*  (Germany)

^d RUHR UNIVERSITY BOCHUM   (Germany)

^e ROYAL OTTAWA HOSPITAL   (Canada)

Author keywords

Emotion; Empathy; fMRI; Somatoform disorder

Indexed keywords

ADULT; ALEXITHYMIA; AMYGDALOID NUCLEUS; ANGER; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CEREBELLUM; CLINICAL ARTICLE; CLUSTER ANALYSIS; CONTROLLED STUDY; DEPRESSION; EMOTION; EMOTIONAL DISORDER; EMOTIONAL STRESS; EMPATHY; FACIAL EXPRESSION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MALE; MEMORY; NUCLEAR MAGNETIC RESONANCE SCANNER; PARAHIPPOCAMPAL GYRUS; POSTCENTRAL GYRUS; POSTERIOR INSULA; PRIORITY JOURNAL; QUESTIONNAIRE; SOMATIZATION; SOMATOFORM DISORDER; SUPERIOR TEMPORAL GYRUS;

ADULT; BRAIN; BRAIN MAPPING; EMOTIONS; EMPATHY; FEMALE; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; SOMATOFORM DISORDERS;

EID: 84867646590     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.21392     Document Type: Article

References (88)

1. Adolphs R, Damasio H, Tranel D, Cooper G, Damasio AR (2000): A role for somatosensory cortices in the visual recognition of emotion as revealed by three-dimensional lesion mapping. J Neurosci 20: 2683-2690.
2. Bach M, Bach D (1996): Alexithymia in somatoform disorder and somatic disease: A comparative study. Psychother Psychosom 65: 150-152.
3. Bagby RM, Taylor GJ, Parker JD (1994): The Twenty-item Toronto Alexithymia Scale-II. Convergent, discriminant, and concurrent validity. J Psychosom Res 38: 33-40.
4. Bailey PE, Henry JD (2007): Alexithymia, somatization and negative affect in a community sample. Psychiatry Res 150: 13-20.
5. Banissy MJ, Sauter DA, Ward J, Warren JE, Walsh V, Scott SK (2010): Suppressing sensorimotor activity modulates the discrimination of auditory emotions but not speaker identity. J Neurosci 30: 13552-13557.
6. Bankier B, Aigner M, Bach M (2001): Alexithymia in DSM-IV disorder: Comparative evaluation of somatoform disorder, panic disorder, obsessive-compulsive disorder, and depression. Psychosomatics 42: 235-240.
7. Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J (1961): An inventory for measuring depression. Arch Gen Psychiatry 4: 561-571.
8. Bermpohl F, Pascual-Leone A, Amedi A, Merabet LB, Fregni F, Gaab N, Alsop D, Schlaug G, Northoff G (2006): Dissociable networks for the expectancy and perception of emotional stimuli in the human brain. Neuroimage 30: 588-600.
9. Blair RJ (2003): Facial expressions, their communicatory functions and neuro-cognitive substrates. Philos Trans R Soc Lond B Biol Sci 358: 561-572.
10. Blair RJ, Morris JS, Frith CD, Perrett DI, Dolan RJ (1999): Dissociable neural responses to facial expressions of sadness and anger. Brain 122(Pt 5): 883-893.
11. Bowers D, Blonder LX, Heilman KM (1999): Florida Affect Battery: Center for Neuropsychological Studies, Cognitive Neuroscience Laboratory. Florida: University of Florida.
12. Bowlby J (1973): Attachment and Loss: Vol. 2. Separation: Anger and Anxiety. The Travistock Institute of Human Relations, London.
13. Breitenstein C, Daum I, Ackermann H, Lütgehetmann R, Müller E (1996): Erfassung der Emotionswahrnehmung bei zentralnervösen Läsionen und Erkrankungen: Psychometrische Gütekriterien der "Tübinger Affekt Batterie". Neurol Rehabil 2: 9.
14. Breiter HC, Etcoff NL, Whalen PJ, Kennedy WA, Rauch SL, Buckner RL, Strauss MM, Hyman SE, Rosen BR (1996): Response and habituation of the human amygdala during visual processing of facial expression. Neuron 17: 875-887.
15. Bressi C, Taylor G, Parker J, Bressi S, Brambilla V, Aguglia E, Allegranti I, Bongiorno A, Giberti F, Bucca M, Todarello O, Callegari C, Vender S, Gala C, Invernizzi G. (1996): Cross validation of the factor structure of the 20-item Toronto Alexithymia Scale: An Italian multicenter study. J Psychosom Res 41: 551-559.
16. Burba B, Oswald R, Grigaliunien V, Neverauskiene S, Jankuviene O, Chue P (2006): A controlled study of alexithymia in adolescent patients with persistent somatoform pain disorder. Can J Psychiatry 51: 468-471.
17. Carr L, Iacoboni M, Dubeau MC, 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 U S A 100: 5497-5502.
18. Cox RW (1996): AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29: 162-173.
19. Csukly G, Czobor P, Szily E, Takacs B, Simon L (2009): Facial expression recognition in depressed subjects: the impact of intensity level and arousal dimension. J Nerv Ment Dis 197: 98-103.
20. Damasio AR, Grabowski TJ, Bechara A, Damasio H, Ponto LL, Parvizi J, Hichwa RD (2000): Subcortical and cortical brain activity during the feeling of self-generated emotions. Nat Neurosci 3: 1049-1056.
21. Davis MH (1983): Measuring individual differences in empathy: Evidence for a multidimensional approach. J Personality Soc Psychol 44: 14.
22. de Greck M, Gang W, Yang X, Wang X, Northoff G, Han S: Neural substrates underlying intentional empathy. Soc Cogn Affect Neurosci (in press).
23. de Greck M, Scheidt L, Bolter AF, Frommer J, Ulrich C, Stockum E, Enzi B, Tempelmann C, Hoffmann T, Northoff G (2011): Multimodal psychodynamic psychotherapy induces normalization of reward related activity in somatoform disorder. World J Biol Psychiatry 12: 296-308.
24. Decety J, Jackson PL (2004): The functional architecture of human empathy. Behav Cogn Neurosci Rev 3: 71-100.
25. Decety J, Moriguchi Y (2007): The empathic brain and its dysfunction in psychiatric populations: implications for intervention across different clinical conditions. Biopsychosoc Med 1: 22.
26. Derntl B, Habel U, Windischberger C, Robinson S, Kryspin-Exner I, Gur RC, Moser E (2009): General and specific responsiveness of the amygdala during explicit emotion recognition in females and males. BMC Neurosci 10: 91.
27. Derogatis LR (1977): SCL-90-R, administration, scoring and procedures manual-I for the R(evised) version. Baltimore, MD: Johns Hopkins University School of Medicine.
28. Duddu V, Isaac MK, Chaturvedi SK (2003): Alexithymia in somatoform and depressive disorders. J Psychosom Res 54: 435-438.
29. Fan Y, Duncan NW, de Greck M, Northoff G (2011): Is there a core neural network in empathy? An fMRI based quantitative meta-analysis. Neurosci Biobehav Rev 35: 903-911.
30. Franke GH (2002): Die Symptom-Checkliste von Derogatis-Deutsche version-Manual. Göttingen, Germany: Beltz.
31. Friston KJ, Holmes AP, Worsley KJ, Poline JP, Frith CD, Frackowiak RS (1995): Statistical parametric maps in functional imaging: A general linear approach. Hum Brain Mapp 2: 12.
32. Fusar-Poli P, Placentino A, Carletti F, Landi P, Allen P, Surguladze S, Benedetti F, Abbamonte M, Gasparotti R, Barale F, Perez J, McGuire P, Politi P (2009): Functional atlas of emotional faces processing: A voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. J Psychiatry Neurosci 34: 418-432.
33. Gallese V, Keysers C, Rizzolatti G (2004): A unifying view of the basis of social cognition. Trends Cogn Sci 8: 396-403.
34. Gerlach C, Aaside CT, Humphreys GW, Gade A, Paulson OB, Law I (2002): Brain activity related to integrative processes in visual object recognition: bottom-up integration and the modulatory influence of stored knowledge. Neuropsychologia 40: 1254-1267.
35. Grabe HJ, Spitzer C, Freyberger HJ (2004): Alexithymia and personality in relation to dimensions of psychopathology. Am J Psychiatry 161: 1299-1301.
36. Gur RC, Schroeder L, Turner T, McGrath C, Chan RM, Turetsky BI, Alsop D, Maldjian J, Gur RE (2002): Brain activation during facial emotion processing. Neuroimage 16(3 Pt 1): 651-662.
37. Guttman H, Laporte L (2002): Alexithymia, empathy, and psychological symptoms in a family context. Compr Psychiatry 43: 448-455.
38. Hanel G, Henningsen P, Herzog W, Sauer N, Schaefert R, Szecsenyi J, Lowe B (2009): Depression, anxiety, and somatoform disorders: vague or distinct categories in primary care? Results from a large cross-sectional study. J Psychosom Res 67: 189-197.
39. Henry JD, Bailey PE, Rendell PG (2008): Empathy, social functioning and schizotypy. Psychiatry Res 160: 15-22.
40. Hiller W, Cebulla M, Korn HJ, Leibbrand R, Roers B, Nilges P (2010): Causal symptom attributions in somatoform disorder and chronic pain. J Psychosom Res 68: 9-19.
41. Hoekert M, Bais L, Kahn RS, Aleman A (2008): Time course of the involvement of the right anterior superior temporal gyrus and the right fronto-parietal operculum in emotional prosody perception. PLoS One 3: e2244.
42. Hooker CI, Verosky SC, Germine LT, Knight RT, D'Esposito M (2008): Mentalizing about emotion and its relationship to empathy. Soc Cogn Affect Neurosci 3: 204-217.
43. Hooker CI, Verosky SC, Germine LT, Knight RT, D'Esposito M (2010): Neural activity during social signal perception correlates with self-reported empathy. Brain Res 1308: 100-113.
44. Immordino-Yang MH, McColl A, Damasio H, Damasio A (2009): Neural correlates of admiration and compassion. Proc Natl Acad Sci U S A 106: 8021-8026.
45. Jabbi M, Swart M, Keysers C (2007): Empathy for positive and negative emotions in the gustatory cortex. Neuroimage 34: 1744-1753.
46. Josephs O, Turner R, Friston K (1997): Event-related f MRI. Hum Brain Mapp 5: 243-248.
47. Keysers C, Gazzola V (2006): Towards a unifying neural theory of social cognition. Prog Brain Res 156: 379-401.
48. Kirmayer LJ, Robbins JM, Paris J (1994): Somatoform disorders: personality and the social matrix of somatic distress. J Abnorm Psychol 103: 125-136.
49. Kooiman CG, Bolk JH, Brand R, Trijsburg RW, Rooijmans HG (2000): Is alexithymia a risk factor for unexplained physical symptoms in general medical outpatients? Psychosom Med 62: 768-778.
50. Kramer UM, Mohammadi B, Donamayor N, Samii A, Munte TF (2010): Emotional and cognitive aspects of empathy and their relation to social cognition--an fMRI-study. Brain Res 1311: 110-120.
51. Kroenke K (2006): Physical symptom disorder: A simpler diagnostic category for somatization-spectrum conditions. J Psychosom Res 60: 335-339.
52. 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.
53. Lee BT, Paik JW, Kang RH, Chung SY, Kwon HI, Khang HS, Lyoo IK, Chae JH, Kwon JH, Kim JW, Lee MS, Ham BJ (2009): The neural substrates of affective face recognition in patients with Hwa-Byung and healthy individuals in Korea. World J Biol Psychiatry 10: 552-559.
54. Lin KM (1983): Hwa-Byung: A Korean culture-bound syndrome? Am J Psychiatry 140: 105-107.
55. Loughead JW, Luborsky L, Weingarten CP, Krause ED, German RE, Kirk D, Gur RC (2010): Brain activation during autobiographical relationship episode narratives: A core conflictual relationship theme approach. Psychother Res 20: 321-336.
56. Matsumuto D, Ekman P (1988): Japanese and Caucasian Facial Expressions of Emotion (JACFEE) and Neutral Faces JACNeuF. San Francisco: University of California.
57. Mattila AK, Kronholm E, Jula A, Salminen JK, Koivisto AM, Mielonen RL, Joukamaa M (2008): Alexithymia and somatization in general population. Psychosom Med 70: 716-722.
58. Maunder R, Hunter J (2004): An integrated approach to the formulation and psychotherapy of medically unexplained symptoms: Meaning-and attachment-based intervention. Am J Psychother 58: 17-33.
59. Mayou R, Kirmayer LJ, Simon G, Kroenke K, Sharpe M (2005): Somatoform disorders: Time for a new approach in DSM-V. Am J Psychiatry 162: 847-855.
60. Min SK (2008): Clinical correlates of hwa-byung and a proposal for a new anger disorder. Psychiatry Investig 5: 125-141.
61. Min SK, Suh SY (2010): The anger syndrome hwa-byung and its comorbidity. J Affect Disord 124: 211-214.
62. Min SK, Suh SY, Song KJ (2009): Symptoms to use for diagnostic criteria of hwa-byung, an anger syndrome. Psychiatry Investig 6: 7-12.
63. Morris JS, Frith CD, Perrett DI, Rowland D, Young AW, Calder AJ, Dolan RJ (1996): A differential neural response in the human amygdala to fearful and happy facial expressions. Nature 383: 812-815.
64. Nichols T, Hayasaka S (2003): Controlling the familywise error rate in functional neuroimaging: A comparative review. Stat Methods Med Res 12: 419-446.
65. Nomi JS, Scherfeld D, Friederichs S, Schafer R, Franz M, Wittsack HJ, Azari NP, Missimer J, Seitz RJ (2008): On the neural networks of empathy: A principal component analysis of an fMRI study. Behav Brain Funct 4: 41.
66. Nummenmaa L, Hirvonen J, Parkkola R, Hietanen JK (2008): Is emotional contagion special? An fMRI study on neural systems for affective and cognitive empathy. Neuroimage 43: 9.
67. Ochsner KN, Knierim K, Ludlow DH, Hanelin J, Ramachandran T, Glover G, Mackey SC (2004): Reflecting upon feelings: An fMRI study of neural systems supporting the attribution of emotion to self and other. J Cogn Neurosci 16: 1746-1772.
68. Pedrosa Gil F, Scheidt CE, Hoeger D, Nickel M (2008): Relationship between attachment style, parental bonding and alexithymia in adults with somatoform disorders. Int J Psychiatry Med 38: 437-451.
69. Pedrosa Gil F, Ridout N, Kessler H, Neuffer M, Schoechlin C, Traue HC, Nickel M (2009): Facial emotion recognition and alexithymia in adults with somatoform disorders. Depress Anxiety 26: E26-33.
70. Phillips ML, Young AW, Senior C, Brammer M, Andrew C, Calder AJ, Bullmore ET, Perrett DI, Rowland D, Williams SC, Gray JA, David AS (1997): A specific neural substrate for perceiving facial expressions of disgust. Nature 389: 495-498.
71. Preston SD, de Waal FB (2002): Empathy: Its ultimate and proximate bases. Behav Brain Sci 25: 1-20; discussion 20-71.
72. Rudrauf D, Lachaux JP, Damasio A, Baillet S, Hugueville L, Martinerie J, Damasio H, Renault B (2009): Enter feelings: Somatosensory responses following early stages of visual induction of emotion. Int J Psychophysiol 72: 13-23.
73. Schutter DJ, van Honk J (2005): The cerebellum on the rise in human emotion. Cerebellum 4: 290-294.
74. Shamay-Tsoory SG (2011): The Neural Bases for Empathy. Neuroscientist 17: 18-24.
75. Smith AP, Henson RN, Dolan RJ, Rugg MD (2004): fMRI correlates of the episodic retrieval of emotional contexts. Neuroimage 22: 868-878.
76. Sprengelmeyer R, Rausch M, Eysel UT, Przuntek H (1998): Neural structures associated with recognition of facial expressions of basic emotions. Proc Biol Sci 265: 1927-1931.
77. Stein DJ, Muller J (2008): Cognitive-affective neuroscience of somatization disorder and functional somatic syndromes: Reconceptualizing the triad of depression-anxiety-somatic symptoms. CNS Spectr 13: 379-384.
78. Sterpenich V, D'Argembeau A, Desseilles M, Balteau E, Albouy G, Vandewalle G, Degueldre C, Luxen A, Collette F, Maquet P (2006): The locus ceruleus is involved in the successful retrieval of emotional memories in humans. J Neurosci 26: 7416-7423.
79. Svoboda E, McKinnon MC, Levine B (2006): The functional neuroanatomy of autobiographical memory: A meta-analysis. Neuropsychologia 44: 2189-2208.
80. Talairach J, Tournoux P (1988): Co-planar stereotaxic atlas of the human brain. New York: Thieme.
81. Voigt K, Nagel A, Meyer B, Langs G, Braukhaus C, Lowe B (2010): Towards positive diagnostic criteria: A systematic review of somatoform disorder diagnoses and suggestions for future classification. J Psychosom Res 68: 403-414.
82. Waller E, Scheidt CE (2004): Somatoform disorders as disorders of affect regulation: A study comparing the TAS-20 with non-self-report measures of alexithymia. J Psychosom Res 57: 239-247.
83. Waller E, Scheidt CE (2006): Somatoform disorders as disorders of affect regulation: A development perspective. Int Rev Psychiatry 18: 13-24.
84. Wicker B, Keysers C, Plailly J, Royet JP, Gallese V, Rizzolatti G (2003): Both of us disgusted in My insula: The common neural basis of seeing and feeling disgust. Neuron 40: 655-664.
85. Williams C, Wood RL (2010): Alexithymia and emotional empathy following traumatic brain injury. J Clin Exp Neuropsychol 32: 259-267.
86. Wittchen HU, Zaudig M, Fydrich T (1997): SKID. Strukturiertes Klinisches Interview für DSM-IV. Göttingen, Germany: Hogrefe, Verlag für Psychologie.
87. Wood RL, Williams C, Kalyani T (2009): The impact of alexithymia on somatization after traumatic brain injury. Brain Inj 23: 649-654.
88. Yamada M, Decety J (2009): Unconscious affective processing and empathy: An investigation of subliminal priming on the detection of painful facial expressions. Pain 143: 71-75.