Vicarious responses to pain in anterior cingulate cortex: Is empathy a multisensory issue?

  • India Morrison
  • Donna Lloyd
  • Giuseppe Di Pellegrino
  • Neil Roberts
Article

Abstract

Results obtained with functional magnetic resonance imaging show that both feeling a moderately painful pinprick stimulus to the fingertips and witnessing another person’s hand undergo similar stimulation are associated with common activity in a pain-related area in the right dorsal anterior cingulate cortex (ACC). Common activity in response to noxious tactile and visual stimulation was restricted to the right inferior Brodmann’s area 24b. These results suggest a shared neural substrate for felt and seen pain for aversive ecological events happening to strangers and in the absence of overt symbolic cues. In contrast to ACC 24b, the primary somatosensory cortex showed significant activations in response to both noxious and innocuous tactile, but not visual, stimuli. The different response patterns in the two areas are consistent with the ACC’s role in coding the motivational-affective dimension of pain, which is associated with the preparation of behavioral responses to aversive events.

References

  1. Bancaud, J., & Talairach, J. (1992). Clinical semiology of frontal lobe seizures. Advances in Neurology, 57, 3–58.PubMedGoogle Scholar
  2. Blankenburg, F., Ruben, J., Meyer, R., Schwiemann, J., & Villringer, A. (2003). Evidence for a rostral-to-caudal somatotopic organization in human primary somatosensory cortex with mirrorreversal in areas 3b and 1. Cerebral Cortex, 13, 987–993.PubMedCrossRefGoogle Scholar
  3. Bradshaw, J. L., & Mattingley, J. B. (2001). Allodynia: A sensory analogue of motor mirror neurons in a hyperaesthetic patient reporting instantaneous discomfort to another’s perceived sudden minor injury? Journal of Neurology, Neurosurgery, & Psychiatry, 70, 135–136.CrossRefGoogle Scholar
  4. Burton, H., MacLeod, A. M., Videen, T. O., & Raichle, M. E. (1997). Multiple foci in parietal and frontal cortex activated by rubbing embossed grating patterns across fingerpads: A positron emission tomography study in humans. Cerebral Cortex, 7, 3–17.PubMedCrossRefGoogle Scholar
  5. Bush, G., Luu, P., & Posner, M. I. (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends in Cognitive Sciences, 4, 215–222.PubMedCrossRefGoogle Scholar
  6. Bush, G., Vogt, B. A., Holmes, J., Dale, A. M., Greve, D., Jenike, M. A., & Rosen, B. R. (2002). Dorsal anterior cingulate cortex: A role in reward-based decision making. Proceedings of the National Academy of Sciences, 99, 523–528.CrossRefGoogle Scholar
  7. Calvert, G. A., Campbell, R., & Brammer, M. J. (2000). Evidence from functional magnetic resonance imaging of crossmodal binding in the human heteromodal cortex. Current Biology, 10, 649–657.PubMedCrossRefGoogle Scholar
  8. Calvert, G. A., Hansen, P. C., Iversen, S. D., & Brammer, M. J. (2001). Detection of audio-visual integration sites in humans by application of electrophysiological criteria to the BOLD effect. Neuro-Image, 14, 427–438.PubMedGoogle Scholar
  9. Carr, L., Iacoboni, M., Dubeau, M. C., Mazziotta, J. C., & Lenzi, G. L. (2003). Neural mechanisms of empathy in humans: A relay from neural systems for imitation to limbic areas. Proceedings of the National Academy of Sciences, 100, 5497–5502.CrossRefGoogle Scholar
  10. Craig, A. D. (2003). Interoception: The sense of the physiological condition of the body. Current Opinion in Neurobiology, 13, 500–505.PubMedCrossRefGoogle Scholar
  11. Davis, K. D., Hutchison, W. D., Lozano, A. M., & Dostrovsky, J. O. (1994). Altered pain and temperature perception following cingulotomy and capsulotomy in a patient with schizoaffective disorder. Pain, 59, 189–199.PubMedCrossRefGoogle Scholar
  12. Davis, K. D., Taylor, S. J., Crawley, A. P., Wood, M. L., & Mikulis, D. J. (1997). Functional MRI of pain- and attention-related activations in the human cingulate cortex. Journal of Neurophysiology, 77, 3370–3380.PubMedGoogle Scholar
  13. Decety, J., & Chaminade, T. (2003). Neural correlates of feeling sympathy. Neuropsychologia, 41, 127–138.PubMedCrossRefGoogle Scholar
  14. Devinsky, O., Morrell, M. J., & Vogt, B. A. (1995). Contributions of anterior cingulate cortex to behavior. Brain, 118, 279–306.PubMedCrossRefGoogle Scholar
  15. di Pellegrino, G., Fadiga, L., Fogassi, L., Gallese, V., & Rizzolatti, G. (1992). Understanding motor events: A neurophysiological study. Experimental Brain Research, 91, 176–180.CrossRefGoogle Scholar
  16. Downar, J., Crawley, A. P., Mikulis, D. J., & Davis, K. D. (2002). A cortical network sensitive to stimulus salience in a neutral behavioral context across multiple sensory modalities. Journal of Neurophysiology, 87, 615–620.PubMedGoogle Scholar
  17. Eisenberger, N. I., Lieberman, M. D., & Williams, K. D. (2003). Does rejection hurt? An f MRI study of social exclusion. Science, 302, 290–292.PubMedCrossRefGoogle Scholar
  18. Forman, S. D., Cohen, J. D., Fitzgerald, M., Eddy, W. F., Mintun, M. A., & Noll, D. C. (1995). Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): Use of a cluster-size threshold. Magnetic Resonance in Medicine, 33, 636–647.PubMedCrossRefGoogle Scholar
  19. Francis, S. T., Kelly, E. F., Bowtell, R., Dunseath, W. J., Folger, S. E., & McGlone, F. (2000). f MRI of the responses to vibratory stimulation of digit tips. NeuroImage, 11, 188–202.PubMedCrossRefGoogle Scholar
  20. Friston, K. J., Worsley, K. J., Frackowiak, R. S. J., Mazziotta, J., & Evans, A. C. (1994). Assessing the significance of focal activations using their spatial extent. Human Brain Mapping, 1, 214–220.CrossRefGoogle Scholar
  21. Gallese, V. (2001). The shared manifold hypothesis: From mirror neurons to empathy. Journal of Consciousness Studies, 8, 33–50.Google Scholar
  22. Gallese, V. (2003). The manifold nature of interpersonal relations: The quest for a common mechanism. Philosophical Transactions of the Royal Society of London: Series B, 358, 517–528.CrossRefGoogle Scholar
  23. Gelnar, P. A., Krauss, B. R., Szeverenyi, N. M., & Apkarian, A. V. (1998). Fingertip representation in the human somatosensory cortex: An fMRI study. NeuroImage, 7, 261–283.PubMedCrossRefGoogle Scholar
  24. Hadland, K. A., Rushworth, M. F. S., Gaffan, D., & Passingham, R. E. (2003a). The anterior cingulate and reward-guided selection of actions. Journal of Neurophysiology, 89, 1161–1164.PubMedCrossRefGoogle Scholar
  25. Hadland, K. A., Rushworth, M. F. S., Gaffan, D., & Passingham, R. E. (2003b). The effect of cingulate lesions on social behavior and emotion. Neuropsychologia, 41, 919–931.PubMedCrossRefGoogle Scholar
  26. Hari, R., Forss, N., Avikainen, S., Kirveskari, E., Salenius, S., & Rizzolatti, G. (1998). Activation of human primary motor cortex during action observation: A neuromagnetic study. Proceedings of the National Academy of Sciences, 95, 15061–15065.CrossRefGoogle Scholar
  27. Hikosaka, K. (1997). Responsiveness of neurons in the posterior inferotemporal cortex to visual patterns in the macaque monkey. Behavioural Brain Research, 89, 275–283.PubMedCrossRefGoogle Scholar
  28. Hofbauer, R. K., Rainville, P., Duncan, G. H., & Bushnell, M. C. (2001). Cortical representation of the sensory dimension of pain. Journal of Neurophysiology, 86, 402–411.PubMedGoogle Scholar
  29. Hsieh, J.-C., Stone-Elander, S., & Ingvar, M. (1999). Anticipatory coping of pain expressed in the human anterior cingulate cortex: A positron emission tomography study. Neuroscience Letters, 262, 61–64.PubMedCrossRefGoogle Scholar
  30. Hutchison, W. D., Davis, K. D., Lozano, A. M., Tasker, R. R., & Dostrovsky, J. O. (1999). Pain-related neurons in the human cingulate cortex. Nature Neuroscience, 2, 403–405.PubMedCrossRefGoogle Scholar
  31. Iacoboni, M., Woods, R. P., Brass, M., Bekkering, H., Mazziotta, J. C., & Rizzolatti, G. (1999). Cortical mechanisms of human imitation. Science, 286, 2526–2528.PubMedCrossRefGoogle Scholar
  32. Jackson, P. L., Meltzoff, A. N., & Decety, J. (2004, April). Perceiving others in painful situations activates the affective pain neural network. Paper presented at the annual meeting of the Cognitive Neuroscience Society, San Francisco.Google Scholar
  33. Jenkinson, M., Bannister, P., Brady, M., & Smith, S. (2002). Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage, 17, 825–841.PubMedCrossRefGoogle Scholar
  34. Kaas, J. H., & Collins, C. E. (2001). The organization of sensory cortex. Current Opinion in Neurobiology, 11, 498–504.PubMedCrossRefGoogle Scholar
  35. Keightley, M. L., Winocur, G., Graham, S. J., Mayberg, H. S., Hevenor, S. J., & Grady, C. L. (2003). An fMRI study investigating cognitive modulation of brain regions associated with emotional processing of visual stimuli. Neuropsychologia, 41, 585–596.PubMedCrossRefGoogle Scholar
  36. Kenshalo, D. R., Iwata, K., Sholas, M., & Thomas, D. A. (2000). Response properties and organization of nociceptive neurons in area 1 monkey primary somatosensory cortex. Journal of Neurophysiology, 84, 719–729.PubMedGoogle Scholar
  37. Koyama, T., Kato, K., Tanaka, Y. Z., & Mikami, A. (2001). Anterior cingulate activity during pain-avoidance and reward tasks in monkeys. Neuroscience Research, 39, 421–430.PubMedCrossRefGoogle Scholar
  38. Koyama, T., Tanaka, Y. Z., & Mikami, A. (1998). Nociceptive neurons in the macaque anterior cingulate activate during anticipation of pain. NeuroReport, 9, 2663–2667.PubMedCrossRefGoogle Scholar
  39. Matelli, M., Luppino, G., & Rizzolatti, G. (1991). Architecture of superior and mesial area 6 and the adjacent cingulate cortex in the macaque monkey. Journal of Comparative Neurology, 311, 445–462.PubMedCrossRefGoogle Scholar
  40. McGlone, F., Kelly, E. F., Trulsson, M., Francis, S. T., Westling, G., & Bowtell, R. (2002). Functional neuroimaging studies of human somatosensory cortex. Behavioural Brain Research, 135, 147–158.PubMedCrossRefGoogle Scholar
  41. Melzack, R. (1999). From the gate to the neuromatrix. Pain, 6(Suppl.), S121-S126.PubMedCrossRefGoogle Scholar
  42. Milham, M. P., Banich, M. T., Claus, E. D., & Cohen, N. J. (2003). Practice-related effects demonstrate complementary roles of anterior cingulate and prefrontal cortices in attentional control. NeuroImage, 18, 483–493.PubMedCrossRefGoogle Scholar
  43. Paus, T., Petrides, M., Evans, A. C., & Meyer, E. (1993). Role of the human anterior cingulate cortex in the control of oculomotor, manual, and speech responses: A positron emission tomography study. Journal of Neurophysiology, 70, 453–469.PubMedGoogle Scholar
  44. Peyron, R., Garcia-Larrea, L., Gregoire, M. C., Convers, P., Richard, A., Lavenne, F., Barral, F. G., Mauguiere, F., Michel, D., & Laurent, B. (2000). Parietal and cingulate processes in central pain. A combined positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) study of an unusual case. Pain, 84, 77–87.PubMedCrossRefGoogle Scholar
  45. Peyron, R., Laurent, B., & Garcia-Larrea, L. (2000). Functional imaging of brain responses to pain: A review and meta-analysis (2000). Clinical Neurophysiology, 30, 263–288.PubMedCrossRefGoogle Scholar
  46. Phillips, M. L., Young, A.W., Senior, C., Brammer, M., Andrews, C., Calder, A. J., Bullmore, E. T., Perrett, D. I., Rowland, D., Williams, S. C. R., Gray, J. A., & David, A. S. (1997). A specific neural substrate for perceiving facial expressions of disgust. Nature, 389, 495–498.PubMedCrossRefGoogle Scholar
  47. Ploner, M., Freund, H. J., & Schnitzler, A. (1999). Pain affect without pain sensation in a patient with a postcentral lesion. Pain, 81, 211–214.PubMedCrossRefGoogle Scholar
  48. Porro, C. A., Cettolo, V., Francescato, M. P., & Baraldi, P. (2003). Functional activity mapping of the mesial hemispheric wall during anticipation of pain. NeuroImage, 19, 1738–1747.PubMedCrossRefGoogle Scholar
  49. Powell, T. P. S., & Mountcastle, V. B. (1959). The cytoarchitecture of the postcentral gyrus of the monkey Macaca mulatta. Bulletin of Johns Hopkins Hospital, 105, 108–131.Google Scholar
  50. Preston, S. D., & de Waal, F. B. M. (2002). Empathy: Its ultimate and proximate bases. Behavioral & Brain Science, 25, 1–20.Google Scholar
  51. Rainville, P. (2002). Brain mechanisms of pain affect and pain modulation. Current Opinion in Neurobiology, 12, 195–204.PubMedCrossRefGoogle Scholar
  52. Rainville, P., Carrier, B., Hofbauer, R. K., Bushnell, M. C., & Duncan, G. H. (1999). Dissociation of sensory and affective dimensions of pain using hypnotic modulation. Pain, 82, 159–171.PubMedCrossRefGoogle Scholar
  53. Rainville, P., Duncan, G. H., Price, D. D., Carrier, B., & Bushnell, M. C. (1997). Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science, 277, 968–971.PubMedCrossRefGoogle Scholar
  54. Ringler, R., Greiner, M., Kohlloeffel, L., Handwerker, H. O., Forster, C. (2003). BOLD effects in different areas of the cerebral cortex during painful mechanical stimulation. Pain, 105, 445–453.PubMedCrossRefGoogle Scholar
  55. Rizzolatti, G., Fadiga, L., Fogassi, L., & Gallese, V. (1999). Resonance behaviors and mirror neurons. Archives Italiennes de Biologie, 137, 85–100.PubMedGoogle Scholar
  56. Rizzolatti, G., Fadiga, L., Gallese, V., & Fogassi, L. (1996). Premotor cortex and the recognition of motor actions. Cognitive Brain Research, 3, 131–141.PubMedCrossRefGoogle Scholar
  57. Rizzolatti, G., & Luppino, G. (2001). The cortical motor system. Neuron, 31, 889–901.PubMedCrossRefGoogle Scholar
  58. Rushworth, M. F. S., Hadland, K. A., & Passingham, R. E. (2003). The effect of cingulate cortex lesions on task switching and working memory. Journal of Cognitive Neuroscience, 15, 338–353.PubMedCrossRefGoogle Scholar
  59. Schnitzler, A., & Ploner, M. (2000). Neurophysiology and functional neuroanatomy of pain perception. Journal of Clinical Neurophysiology, 17, 592–603.PubMedCrossRefGoogle Scholar
  60. Schnitzler, A., Seitz, R. J., & Freund, H.-J. (2000). The somatosensory system. In A. W. Toga & J. C. Mazziotta (Eds.), Brain mapping: The systems (pp. 291–329). San Diego: Academic Press.CrossRefGoogle Scholar
  61. Sewards, T. V., & Sewards, M. A. (2002). The medial pain system: Neural representations of the motivational aspect of pain. Brain Research Bulletin, 59, 163–180.PubMedCrossRefGoogle Scholar
  62. Singer, T., Seymour, B., O’Doherty, J., Kaube, H., Dolan, R. J., & Frith, C. D. (2004). Empathy for pain involves the affective but not sensory components of pain. Science, 303, 1157–1162.PubMedCrossRefGoogle Scholar
  63. Smith, S. M. (2002). Fast robust automated brain extraction. Human Brain Mapping, 17, 143–155.PubMedCrossRefGoogle Scholar
  64. 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. Journal of Neurophysiology, 86, 1499–1503.PubMedGoogle Scholar
  65. Vogt, B. A., Nimchinsky, E. A., Vogt, L. J., & Hof, P. R. (1995). Human cingulate cortex: Surface features, flat maps, and cytoarchitecture. Journal of Comparative Neurology, 359, 490–506.PubMedCrossRefGoogle Scholar
  66. Vogt, B. A., & Pandya, D. N. (1987). Cingulate cortex of the rhesus monkey: II. Cortical afferents. Journal of Comparative Neurology, 262, 271–289.PubMedCrossRefGoogle Scholar
  67. Vogt, B. A., & Sikes, R.W. (2000). The medial pain system, cingulate cortex, and parallel processing of nociceptive information. Progress in Brain Research, 122, 223–235.PubMedCrossRefGoogle Scholar
  68. Walton, M. E., Bannerman, D. M., Alterescu, K., & Rushworth, M. F. (2003). Functional specialization within medial frontal cortex of the anterior cingulate for evaluating effort-related decisions. Journal of Neuroscience, 23, 6475–6479.PubMedGoogle Scholar
  69. Wicker, B., Keysers, C., Plailly, J., Royet, J. P., 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.PubMedCrossRefGoogle Scholar
  70. Wispé, L. (1991). The psychology of sympathy. New York: Plenum.Google Scholar
  71. Woolrich, M. W., Ripley, B. D., Brady, M., & Smith, S. M. (2001). Temporal autocorrelation in univariate linear modeling of fMRI data. NeuroImage, 14, 1370–1386.PubMedCrossRefGoogle Scholar
  72. Worsley, K. J., Evans, A. C., Marrett, S., & Neelin, P. (1992). A three-dimensional statistical analysis for CBF activation studies in human brain. Journal of Cerebral Blood Flow Metabolism, 12, 900–918.PubMedGoogle Scholar
  73. Yamasaki, H., LaBar, K. S., & McCarthy, G. (2002). Dissociable prefrontal brain systems for attention and emotion. Proceedings of the National Academy of Sciences, 99, 11447–11451.CrossRefGoogle Scholar

Copyright information

© Psychonomic Society, Inc. 2004

Authors and Affiliations

  • India Morrison
    • 3
  • Donna Lloyd
    • 1
  • Giuseppe Di Pellegrino
    • 2
  • Neil Roberts
    • 1
  1. 1.University of LiverpoolLiverpoolEngland
  2. 2.University of UrbinoUrbinoItaly
  3. 3.Centre for Cognitive Neuroscience, School of PsychologyUniversity of Wales, BangorGwyneddU.K.

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