Empathy for pain and touch in the human somatosensory cortex

Cerebral Cortex

Volumn 17, Issue 11, 2007, Pages 2553-2561

  Bufalari, Ilaria ^a,b   Aprile, Taryn ^a,b   Avenanti, Alessio ^a,b   Di Russo, Francesco ^b,c   Aglioti, Salvatore Maria ^a,b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^c UNIVERSITY OF ROME FORO ITALICO   (Italy)

Author keywords

Mirror systems; Primary somatosensory cortex; Simulation theory; Social cognition; Somatosensory evoked potentials

Indexed keywords

ADULT; ARTICLE; AVERSION; CORRELATION ANALYSIS; EMPATHY; EVOKED SOMATOSENSORY RESPONSE; FEMALE; HUMAN; HUMAN EXPERIMENT; MALE; NEUROMODULATION; NOCICEPTION; NOCICEPTIVE STIMULATION; NORMAL HUMAN; PAIN; PRIORITY JOURNAL; SENSORY STIMULATION; SOMATOSENSORY CORTEX; TOUCH; VIDEORECORDING;

ADULT; EMOTIONS; EMPATHY; EVOKED POTENTIALS, SOMATOSENSORY; FEMALE; HUMANS; MALE; PAIN; SOCIAL BEHAVIOR; SOMATOSENSORY CORTEX; TOUCH; VISUAL PERCEPTION;

EID: 34848822013     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhl161     Document Type: Article

References (66)

1. Adolphs R, Damasio H, Tranel D, Cooper G, Damasio AR. 2000. A role for somatosensory cortices in the visual recognition of emotions as revealed by three-dimensional lesion mapping. J Neurosci. 20:2683-2690.
2. Allison T, McCarthy G, Wood CC. 1992. The relationship between human long-latency somatosensory evoked potentials recorded from the cortical surface and from the scalp. Electroencephalogr Clin Neurophysiol. 84:301-314.
3. Allison T, McCarthy G, Wood CC, Jones SJ. 1991. Potentials evoked in human and monkey cerebral cortex by stimulation of the median nerve: a review of scalp and intracranial recordings. Brain. 114:2465-2503.
4. Avenanti A, Aglioti SM. 2006. The sensorimotor side of empathy for pain. In: Mancia M, editor. Psychoanalysis and neuroscience. Milan (Italy): Springer-Verlag. p. 235-256.
5. 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.
6. Avenanti A, Paluello IM, Bufalari I, Aglioti SM. 2006. Stimulus-driven modulation of motor evoked potentials during observation of others' pain. Neuroimage. 32:316-324.
7. 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.
8. Barba C, Frot M, Valeriani M, Tonali P, Mauguiere F. 2002. Distinct fronto-central N60 and supra-sylvian N70 middle-latency components of the median nerve SEPs as assessed by scalp topographic analysis, dipolar source modeling and depth recordings. Clin Neurophysiol. 113:981-992.
9. Baron R, Baron Y, Disbrow E, Roberts TP. 2000. Activation of the somatosensory cortex during Abeta-fiber mediated hyperalgesia. A MSI study. Brain Res. 871:75-82.
10. Bingel U, Lorenz J, Glauche V, Knab R, Glascher J, Weiller C, Buchel C. 2004. Somatotopic organization of human somatosensory cortices for pain: a single trial fMRI study. Neuroimage. 23:224-232.
11. 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.
12. Botvinick M, Jha AP, Bylsma LM, Fabian SA, Solomon PE, Prkachin KM. 2005. Viewing facial expressions of pain engages cortical areas involved in the direct experience of pain. Neuroimage. 25:312-319.
13. Buchner H, Waberski TD, Fuchs M, Wischmann HA, Beckmann R, Rienacker A. 1995. Origin of P16 median nerve SEP component identified by dipole source analysis - subthalamic or within the thalamo-cortical radiation? Exp Brain Res. 104:511-518.
14. Burke D, Gandevia SC. 1988. Interfering cutaneous stimulation and muscle afferent contribution to cortical potentials. Electroencephalogr Clin Neurophysiol. 70:118-125.
15. Bushnell MC, Duncan GH, Hofbauer RK, Ha B, Chen JI, Carrier B. 1999. Pain perception: is there a role for primary somatosensory cortex? Proc Natl Acad Sci USA. 96:7705-7709.
16. 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 USA. 100:5497-5502.
17. Davis H. 1996. Empathy: a social psychological approach. Madison (WI): Westview Press.
18. Decety J, Grezes J. 2006. The power of simulation: imagining one's own and other's behavior. Brain Res. 1079:4-14.
19. Decety J, Jackson PL. 2004. The functional architecture of human empathy. Behav Cogn Neurosci Rev. 3:71-100.
20. Desmedt JE, Nguyen TH, Bourguet M. 1987. Bit-mapped color imaging of human evoked potentials with reference to the N20, P22, P27 and N30 somatosensory responses. Electroencephalogr Clin Neurophysiol. 68:1-19.
21. Desmedt JE, Tomberg C. 1989. Mapping early somatosensory evoked potentials in selective attention: critical evaluation of control conditions used for titrating by difference the cognitive P30, P40, P100 and N140. Electroencephalogr Clin Neurophysiol. 74:321-346.
22. 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.
23. Forster B, Eimer M. 2005. Vision and gaze direction modulates tactile processing in somatosensory cortex: evidence from event-related brain potentials. Exp Brain Res. 165:8-18.
24. Frot M, Mauguière F. 1999. Timing and spatial distribution of somatosensory responses recorded in the upper bank of the sylvian fissure (SII area) in humans. Cereb Cortex. 9:854-863.
25. Gallese V. 2003. The manifold nature of interpersonal relations: the quest for a common mechanism. Philos Trans R Soc Lond B Biol Sci. 358:517-528.
26. Gallese V, Fadiga L, Fogassi L, Rizzolatti G. 1996. Action recognition in the premotor cortex. Brain. 119:593-609.
27. Gandevia SC, Burke P, McKeon B. 1983. Convergence in the somatosensory pathway between cutaneous afferents from index and middle finger in man. Exp Brain Res. 50:415-425.
28. Garcia-Larrea L, Bastuji H, Mauguiere F. 1991. Mapping study of somatosensory evoked potentials during selective spatial attention. Electroencephalogr Clin Neurophysiol. 80:201-214.
29. Garcia-Larrea L, Bastuji H, Mauguière F. 1992. Unmasking of cortical SEP components by change in stimulus rate: a topographic study. Electroencephalogr Clin Neurophysiol. 84:71-83.
30. Humphrey DR. 1968a. Re-analysis of the antidromic cortical response. I. Potentials evoked by stimulation of the isolated pyramidal tract. Electroencephalogr Clin Neurophysiol. 24:116-129.
31. Humphrey DR. 1968b. Re-analysis of the antidromic cortical response. II. On the contribution of cell discharge and PSPs to evoked potentials. Electroencephalogr Clin Neurophysiol. 24:421-442.
32. Huttunen J, Homberg V. 1991. Influence of stimulus repetition rate on cortical somatosensory potentials evoked by median nerve stimulation: implications for generation mechanisms. J Neurol Sci. 105:37-43.
33. Inui K, Wang X, Qiu Y, Nguyen YT, Ojima S, Tamura Y, Nakata H, Wasaka T, Tran TD, Kakigi R. 2003. Pain processing within the primary somatosensory cortex in humans. Eur J Neurosci. 18:2859-2866.
34. Jackson PL, Brunet E, Meltzoff AN, Decety J. 2006. Empathy examined through the neural mechanisms involved in imagining how I feel versus how you feel pain. Neuropsychologia. 44:752-761.
35. Jackson PL, Meltzoff AN, Decety J. 2005. How do we perceive the pain of others? A window into the neural processes involved in empathy. Neuroimage. 24:771-779.
36. Jones SJ, Power C. 1984. Scalp topography of human SEPs: the effect of interfering tactile stimuli applied to the hand. Electroencephalogr Clin Neurophysiol. 58:25-36.
37. Kanda M, Nagamine T, Ikeda A, Ohara S, Kunieda T, Fujiwara N, Yazawa S, Sawamoto N, Matsumoto R, Taki W, Shibasaki H. 2000. Primary somatosensory cortex is actively involved in pain processing in human. Brain Res. 853:282-289.
38. Kenshalo DR Jr, Isensee O. 1983. Responses of primate S1 cortical neurons to noxious stimuli. J Neurophysiol. 50:1479-1496.
39. 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.
40. Li CL. 1961. Cortical intracellular synaptic potentials. J Cell Comp Physiol. 58:153-167.
41. Maihofner C, Schmelz M, Forster C, Neundorfer B, Handwerker HO. 2004. Neural activation during experimental allodynia: a functional magnetic resonance imaging study. Eur J Neurosci. 19:3211-3218.
42. McCarthy G, Wood CC. 1985. Scalp distributions of event-related potentials: an ambiguity associated with analysis of variance models. Electroencephalogr Clin Neurophysiol. 62:203-208.
43. Melzack R. 1999. From the gate to the neuromatrix. Pain. 6(Suppl): 121-126.
44. Minio-Paluello I, Avenanti A, Aglioti SM. Forthcoming 2006. Left hemisphere dominance in reading the sensory qualities of others' pain? Soc Neurosci.1:320-333.
45. Morrison I, Lloyd D, di Pellegrino G, Roberts N. 2004. Vicarious responses to pain in anterior cingulate cortex: is empathy a multisensory issue? Cogn Affect Behav Neurosci. 4:270-278.
46. Ogino Y, Nemoto H, Inui K, Saito S, Kakigi R, Goto F. July 19, 2006. Inner experience of pain: imagination of pain while viewing images showing painful events forms subjective pain representation in human brain. Cereb Cortex. 10.1093/cercor/bhl023.
47. Oldfield RC. 1971. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 9:97-113.
48. Penfield W, Boldrey E. 1937. Somatic motor and sensory representation of man as studied by electrical stimulation. Brain. 60:389-443.
49. Peyron R, Laurent B, Garcia-Larrea L. 2000. Functional imaging of brain responses to pain. A review and meta-analysis. Clin Neurophysiol. 30:263-288.
50. Peyron R, Schneider F, Faillenot I, Convers P, Barral FG, Garcia-Larrea L, Laurent B. 2004. An fMRI study of cortical representation of mechanical allodynia in patients with neuropathic pain. Neurology. 63:1838-1846.
51. Ploner M, Schmitz F, Freund HJ, Schnitzler A. 2000. Differential organization of touch and pain in human primary somatosensory cortex. J Neurophysiol. 83:1770-1776.
52. Porro CA, Cettolo V, Francescato MP, Baraldi P. 1998. Temporal and intensity coding of pain in human cortex. J Neurophysiol. 80:3312-3320.
53. Pourtois G, Sander D, Andres M, Grandjean D, Reveret L, Olivier E, Vuilleumier P. 2004. Dissociable roles of the human somatosensory and superior temporal cortices for processing social face signals. Eur J Neurosci. 20:3507-3515.
54. Preston SD, de Waal FBM. 2002. Empathy: its ultimate and proximate bases. Behav Brain Sci. 25:1-71.
55. Rizzolatti G, Fogassi L, Gallese V. 2001. Neurophysiologic mechanisms underlying the understanding and imitation of action. Nat Rev Neurosci. 2:661-670.
56. 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.
57. 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.
58. Schaefer M, Flor H, Heinze HJ, Rotte M. 2006. Dynamic modulation of the primary somatosensory cortex during seeing and feeling a touched hand. Neuroimage. 29:587-592.
59. 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. 303:1157-1162.
60. Singer T, Seymour B, O'Doherty JP, Stephan KE, Dolan RJ, Frith CD. 2006. Empathic neural responses are modulated by the perceived fairness of others. Nature. 439:466-469.
61. Timmermann L, Ploner M, Haucke K, Schmitz F, Baltissen R, Schnitzler A. 2001. Differential coding of pain intensity in the human primary and secondary somatosensory cortex. J Neurophysiol. 86:1499-1503.
62. Valeriani M, Barba C, Le Pera D, Restuccia D, Colicchio G, Tonali P, Gagliardo O, Treede RD. 2004. Different neuronal contribution to N20 somatosensory evoked potential and to CO2 laser evoked potentials: an intracerebral recording study. Clin Neurophysiol. 115:211-216.
63. Valeriani M, Le Pera D, Tonali P. 2001. Characterizing somatosensory evoked potential sources with dipole models: advantages and limitations. Muscle Nerve. 24:325-339.
64. Valeriani M, Restuccia D, Di Lazzaro V, Le Pera D, Barba C, Tonali P, Mauguiere F. 1998. Dipolar source of the early scalp somatosensory evoked potentials to upper limb stimulation. Effect of increasing stimulus rates. Exp Brain Res. 120:306-315.
65. Waberski TD, Buchner H, Perkuhn M, Gobbele R, Wagner M, Kucker W, Silny J. 1999. N30 and the effect of explorative finger movements: a model of the contribution of the motor cortex to early somatosensory potentials. Clin Neurophysiol. 110:1589-1600.
66. 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.