"Feeling" others' painful actions: The sensorimotor integration of pain and action information

Human Brain Mapping

Volumn 34, Issue 8, 2013, Pages 1982-1998

  Morrison, India ^a   Tipper, Steve P ^b   Fenton Adams, Wendy L ^b   Bach, Patric ^c  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b BANGOR UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF PLYMOUTH   (United Kingdom)

Author keywords

Action perception; Empathy; FMRI; Pain observation; Somatosensory; Tactile discrimination

Indexed keywords

ADULT; ARTICLE; BEHAVIOR; EXPERIMENTAL DESIGN; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MALE; PAIN; PRIMARY SOMATOSENSORY CORTEX; PRIORITY JOURNAL; SENSORIMOTOR CORTEX; SENSORIMOTOR INTEGRATION; SIGNAL DETECTION; SOMATOSENSORY CORTEX; SOMATOSENSORY SYSTEM; TACTILE STIMULATION;

ACTION PERCEPTION; EMPATHY; FMRI; PAIN OBSERVATION; SOMATOSENSORY; TACTILE DISCRIMINATION;

ADULT; BRAIN MAPPING; EMOTIONS; EMPATHY; FEMALE; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; PAIN; PHOTIC STIMULATION; SOMATOSENSORY CORTEX; YOUNG ADULT;

EID: 84880135069     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.22040     Document Type: Article

References (81)

1. Avenanti A, Bueti D, Galati G, Aglioti SM ( 2005): Transcranial magnetic stimulation highlights the sensorimotor side of empathy for pain. Nat Neurosci 8: 955-960.
2. Avenanti A, Bolognini N, Maravita A, Aglioti SM ( 2007): Somatic and motor components of action simulation. Curr Biol 7: 2129-2135.
3. Avikainen S, Forss N, Hari R ( 2002): Modulated activation of the human SI and SII cortices during observation of hand actions. Neuroimage 15: 640-646.
4. Bach P, Knoblich G, Gunter TC, Friederici AD, Prinz W ( 2005): Action comprehension: Deriving spatial and functional relations. J Exp Psychol Hum Percept Perform 31: 465-479.
5. Bach P, Peelen MV, Tipper SP ( 2010): On the role of object information in action observation: An fMRI study. Cereb Cortex 20: 2798-2809.
6. Bach P, Bayliss AP, Tipper SP ( 2011): The predictive mirror: Interactions of mirror and affordance processes during action observation. Psychon Bull Rev 18: 171-176.
7. Benuzzi F, Lui F, Duzzi D, Nichelli PF, Porro CA ( 2008): Does it look painful or disgusting? Ask your parietal and cingulate cortex. J Neurosci 28: 923-931.
8. Betti V, Zappasodi F, Rossini PM, Aglioti SM, Tecchio F ( 2009): Synchronous with your feelings: Sensorimotor {gamma} band and empathy for pain. J Neurosci 29: 12384-12392.
9. Binkofski F, Buccino G, Posse S, Seitz RJ, Rizzolatti G, Freund H ( 1999): A fronto-parietal circuit for object manipulation in man: Evidence from an fMRI-study. Eur J Neurosci 11: 3276-3286.
10. Blakemore SJ, Bristow D, Bird G, Frith C, Ward J ( 2005): Somatosensory activations during the observation of touch and a case of vision-touch synaesthesia. Brain 128: 1571-1583.
11. Bonini L, Serventi FU, Simone L, Rozzi S, Ferrari PF, Fogassi L ( 2011): Grasping neurons of monkey parietal and premotor cortices encode action goals at distinct levels of abstraction during complex action sequences. J Neurosci 31: 5876-5886.
12. Bodegård A, Geyer S, Grefkes C, Zilles K, Roland PE ( 2001): Hierarchical processing of tactile shape in the human brain. Neuron 31: 317-328.
13. Bufalari I, Aprile T, Avenanti A, Di Russo F, Aglioti SM ( 2007): Empathy for pain and touch in the human somatosensory cortex. Cereb Cortex 17: 2553-2561.
14. Carlsson K, Petrovic P, Skare S, Petersson KM, Ingvar M ( 2000): Tickling expectations: Neural processing in anticipation of a sensory stimulus. J Cogn Neurosci 12: 691-703.
15. Caspers S, Geyer S, Schleicher A, Mohlberg H, Amunts K, Zilles K ( 2006): The human inferior parietal cortex: Cytoarchitectonic parcellation and interindividual variability. Neuroimage 33: 430-448.
16. Caspers S, Eickhoff SB, Geyer S, Scheperjans F, Mohlberg H, Zilles K, Amunts K ( 2008): The human inferior parietal lobule in stereotaxic space. Brain Struct Funct 212: 481-495.
17. Caspers S, Zilles K, Laird AR, Eickhoff SB ( 2010): ALE meta-analysis of action observation and imitation in the human brain. Neuroimage 50: 1148-1167.
18. Cheng Y, Lin C-P, Liu H-L, Hsu Y-Y, Lim K-E, Hung D, Decety J ( 2007): Expertise modulates the perception of pain in others. Curr Biol 9: 1708-1713.
19. Cheng Y, Yang CY, Lin CP, Lee PL, Decety J ( 2008): The perception of pain in others suppresses somatosensory oscillations: A magnetoencephalography study. Neuroimage 40: 1833-1840.
20. Cunnington R, Windischberger C, Robinson S, Moser E ( 2006): The selection of intended actions and the observation of others' actions: A time-resolved fMRI study. Neuroimage 29: 1294-1302.
21. de Lange FP, Spronk M, Willems RM, Toni I, Bekkering H ( 2008): Complementary systems for understanding action intentions. Curr Biol 18: 454-457.
22. Dijkerman HC, de Haan EH ( 2007): Somatosensory processes subserving perception and action. Behav Brain Sci 30: 189-201.
23. Dinstein I, Hasson U, Rubin N, Heeger DJ ( 2007): Brain areas selective for both observed and executed movements. J Neurophysiol 98: 1415-1427.
24. di Pellegrino G, Fadiga L, Fogassi L, Gallese V, Rizzolatti G ( 1992): Understanding motor events: A neurophysiological study. Exp Brain Res 91: 176-809.
25. Dong WK, Chudler EH, Sugiyama K, Roberts VJ, Hayashi T ( 1994): Somatosensory, multisensory, and task-related neurons in cortical area 7b (PF) of unanesthetized monkeys. J Neurophysiol 72: 542-564.
26. Downing PE, Jiang Y, Shuman M, Kanwisher N ( 2001): A cortical area selective for visual processing of the human body. Science 293: 2470-2473.
27. Ebisch SJ, Perrucci MG, Ferretti A, Del Gratta C, Romani GL, Gallese V ( 2008): The sense of touch: Embodied simulation in a visuotactile mirroring mechanism for observed animate or inanimate touch. J Cogn Neurosci 20: 1611-1623.
28. Eickhoff SB, Amunts K, Mohlberg H, Zilles K ( 2006a) Human parietal operculum I. Cytoarchetectonic mapping of subdivisions. Cereb Cortex 16: 254-267.
29. Eickhoff SB, Lotze M, Wietek B, Amunts K, Enck P, Zilles K ( 2006b): Human parietal operculum II: Stereotaxic maps and correlation with functional imaging results. Cereb Cortex 16: 268-279.
30. Eickhoff SB, Grefkes C, Zilles K, Fink GR ( 2007): The somatotopic organization of cytoarchitectonic areas on the human parietal operculum. Cereb Cortex 17: 1800-1811.
31. Fogassi L, Ferrari PF, Gesierich B, Rozzi S, Chersi F, Rizzolatti G ( 2005): Parietal lobe: From action organization to intention understanding. Science 308: 662-667.
32. Fox PT, Lancaster JL ( 2002): Mapping context and content: The Brain Map model. Nat Rev Neurosci 3: 319-321.
33. Friston KJ, Zarahn E, Josephs O, Henson RN, Dale AM ( 1999): Stochastic designs in event-related fMRI. Neuroimage 10: 607-619.
34. Gazzola V, Keysers C ( 2009): The observation and execution of actions share motor and somatosensory voxels in all tested subjects: Single-subject analyses of unsmoothed fMRI data. Cereb Cortex 19: 1239-1255.
35. Gazzola V, Rizzolatti G, Wicker B, Keysers C ( 2007): The anthropomorphic brain: The mirror neuron system responds to human and robotic actions. Neuroimage 35: 1674-1684.
36. Gu X, Han S ( 2007): Attention and reality constraints on the neural processes of empathy for pain. Neuroimage 36: 256-267.
37. Hasson U, Nir U, Levy I, Fuhrmann G, Malach R ( 2004): Intersubject synchronization of cortical activation during natural vision. Science 303: 1634-1640.
38. Hinkley LB, Krubitzer LA, Nagarajan SS, Disbrow EA ( 2007): Sensorimotor integration in S2, PV, and parietal rostroventral areas of the human sylvian fissure. J Neurophysiol 97: 1288-1297.
39. Hutchison WD, Davis KD, Lozano AM, Tasker RR, Dostrovsky JO ( 1999): Pain-related neurons in the human cingulate cortex. Nat Neurosci 2: 403-405.
40. Jackson PL, Meltzoff AN, Decety J ( 2005): How do we perceive the pain of others? Neuroimage 24: 771-779.
41. Jackson PL, Brunet E, Meltzoff AN, Decety J ( 2006): Empathy examined through the neural mechanisms involved in imagining how I feel versus how you would feel pain: An event-related fMRI study. Neuropsychologia 44: 752-761.
42. Kellenbach M, Brett M, Patterson K ( 2003): Actions speak louder than functions. The importance of manipulability and action in tool representation. J Cognit Neurosci 15: 30-46.
43. Keysers C, Gazzola V ( 2009): Expanding the mirror: Vicarious activity for actions, emotions, and sensations. Curr Opin Neurobiol 19: 666-671.
44. Keysers C, Wicker B, Gazzola V, Anton JL, Fogassi L, Gallese V ( 2004): A touching sight: SII/PV activation during the observation and experience of touch. Neuron 42: 335-346.
45. Keysers C, Kaas JH, Gazzola V ( 2010): Somatosensation in social perception. Nat Rev Neurosci 11: 417-428.
46. Laird AR, Eickhoff SB, Kurth F, Fox PM, Uecker AM, Turner JA, Robinson JL, Lancaster JL, Fox PT ( 2009): ALE meta-analysis workflows via the BrainMap database: Progress towards a probabilistic functional brain atlas. Front Neuroinform 3: 23.
47. Lamm C, Fischer MH, Decety J ( 2007a) Predicting the actions of others taps into one's own somatosensory representations-a functional MRI study. Neuropsychologia 45: 2480-2491.
48. Lamm C, Nusbaum HC, Meltzoff AN, Decety J ( 2007b): What are you feeling? Using functional magnetic resonance imaging to assess the modulation of sensory and affective responses during empathy for pain. PLoS ONE 2: e1292.
49. Lamm C, Meltzoff AN, Decety J ( 2009): How do we empathize with someone who is not like us? A functional magnetic resonance imaging study. J Cogn Neurosci 22: 362-376.
50. Lamm C, Decety J, Singer T ( 2011): Meta-analytic evidence for common and distinct neural networks associated with directly experienced pain and empathy for pain. Neuroimage 54: 2492-2502.
51. Lancaster JL, Tordesillas-Gutierrez D, Martinez M, Salinas F, Evans A, Zilles K, Mazziotta JC, Fox PT ( 2007): Bias between MNI and Talairach coordinates analyzed using the ICBM-152 brain template. Hum Brain Mapp 28: 1194-1205.
52. Lindemann O, Nuku P, Rueschemeyer SA, Bekkering H ( 2011): Grasping the other's attention: The role of animacy in action cueing of joint attention. Vision Res 51: 940-944.
53. Lloyd D, Morrison I, Roberts N ( 2006): Role for human posterior parietal cortex in visual processing of aversive objects in peripersonal space. J Neurophysiol 95: 205-214.
54. Mazzola L, Isnard J, Mauguière F ( 2006): Somatosensory and pain responses to stimulation of the second somatosensory area (SII) in humans. A comparison with SI and insular responses. Cereb Cortex 16: 960-968.
55. Meyer K, Kaplan JT, Essex R, Damasio H, Damasio A ( 2011): Seeing touch is correlated with content-specific activity in primary somatosensory cortex. Cereb Cortex 21: 2113-2121.
56. Miquée A, Xerri C, Rainville C, Anton JL, Nazarian B, Roth M, Zennou-Azogui Y ( 2008): Neuronal substrates of haptic shape encoding and matching: A functional magnetic resonance imaging study. Neuroscience 152: 29-39.
57. Moriguchi Y, Decety J, Ohnishi T, Maeda M, Mori T, Nemoto K, Matsuda H, Komaki G ( 2007): Empathy and judging other's pain: An fMRI study of alexithymia. Cereb Cortex 17: 2223-2234.
58. Morrison I, Downing PE ( 2007): Organization of felt and seen pain responses in anterior cingulate cortex. Neuroimage 37: 642-651.
59. Morrison I, Lloyd DM, Roberts N ( 2004): Vicarious pain in anterior cingulate cortex: Is empathy a multisensory issue? Cogn Affect Behav Neurosci 4: 270-278.
60. Morrison I, Peelen MV, Downing PE ( 2007): The sight of others' pain modulates motor processing in human cingulate cortex. Cereb Cortex 17: 2214-2222.
61. Morrison I, Björnsdotter M, Olausson H ( 2011a) Vicarious responses to social touch in posterior insular cortex are tuned to pleasant caressing speeds. J Neurosci 31: 9554-9562.
62. Morrison I, Löken LS, Minde J, Wessberg J, Perini I, Nennesmo I, Olausson H ( 2011b) Reduced C-afferent fibre density affects perceived pleasantness and empathy for touch. Brain 134: 1116-1126.
63. Naito E, Ehrsson HH ( 2006): Somatic sensation of hand-object interactive movement is associated with activity in the left inferior parietal cortex. J Neurosci 26: 3783-3790.
64. Noppeney U ( 2008): The neural systems of tool and action semantics: A perspective from functional imaging. J Physiol-Paris 102: 40-49.
65. Ogino Y, Nemoto H, Inui K, Saito S, Kakigi R, Goto F ( 2007):. Inner experience of pain: Imagination of pain while viewing images showing painful events forms subjective pain representation in human brain. Cereb Cortex 17: 1139-1146.
66. Oouchida Y, Okada T, Nakashima T, Matsumura M, Sadato N, Naito E ( 2004): Your hand movements in my somatosensory cortex: A visuo-kinesthetic function in human area 2. Neuroreport 15: 2019-2023.
67. Osborn J, Derbyshire SW ( 2010): Pain sensation evoked by observing injury in others. Pain 148: 268-274.
68. Porro CA, Lui F, Facchin P, Maieron M, Baraldi P ( 2004): Percept-related activity in the human somatosensory system: Functional magnetic resonance imaging studies. Magn Reson Imaging 22: 1539-1548.
69. Reed CL, Shoham S, Halgren E ( 2004): Neural substrates of tactile object recognition: An fMRI study. Hum Brain Mapp 21: 236-246.
70. Rizzolatti G, Sinigaglia C ( 2010): The functional role of the parieto-frontal mirror circuit: Interpretations and misinterpretations. Nat Rev Neurosci 11: 264-274.
71. Rossi S, Tecchio F, Pasqualetti P, Ulivelli M, Pizzella V, Romani GL, Passero S, Battistini N, Rossini PM ( 2002): Somatosensory processing during movement observation in humans. Clin Neurophysiol 113: 16-24.
72. Rostomily RC, Berger MS, Ojemann GA, Lettich E ( 1991): Postoperative deficits following removal of tumors in the dominant hemisphere supplementary motor area. J Neurosurg 75: 62-68.
73. Rozzi S, Calzavara R, Belmalih A, Borra E, Gregoriou GG, Matelli M, Luppino G ( 2006): Cortical connections of the inferior parietal cortical convexity of the macaque monkey. Cereb Cortex 16: 1389-1417.
74. Rozzi S, Ferrari PF, Bonini L, Rizzolatti G, Fogassi L ( 2008): Functional organization of inferior parietal lobule convexity in the macaque monkey: Electrophysiological characterization of motor, sensory and mirror responses and their correlation with cytoarchitectonic areas. Eur J Neurosci 28: 1569-1588.
75. Saarela MV, Hlushchuk Y, Williams AC, Schurmann M, Kalso E, Hari R ( 2007): The compassionate brain: Humans detect intensity of pain from another's face. Cereb Cortex 17: 230-237.
76. Schaefer M, Xu B, Flor H, Cohen LG ( 2009): Effects of different viewing perspectives on somatosensory activations during observation of touch. Hum Brain Mapp 30: 2722-2730.
77. Shima K, Tanji J ( 1998): Role for cingulate motor area cells in voluntarymovement selection based on reward. Science 282: 1335-1338.
78. Singer T, Seymour B, O'Doherty J, Kaube H, Dolan RJ, Frith CD ( 2004): Empathy for pain involves the affective but not sensory components of pain. Science 20: 1157-1162.
79. Stoeckel MC, Weder B, Binkofski F, Buccino G, Shah NJ, Seitza RJ ( 2003): A fronto-parietal circuit for tactile object discrimination: An event-related fMRI study. Neuroimage 19: 1103-1114.
80. Talairach J, Tournoux P (1988): Co-planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System - an Approach to Cerebral Imaging. Thieme Medical Publishers: New York.
81. Taylor JC, Wiggett AJ, Downing PE ( 2007): Functional MRI analysis of body and body part representations in the extrastriate and fusiform body areas. J Neurophysiol 98: 1626-1633.