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Transcranial magnetic stimulation highlights the sensorimotor side of empathy for pain

Abstract

Pain is intimately linked with action systems that are involved in observational learning and imitation. Motor responses to one's own pain allow freezing or escape reactions and ultimately survival. Here we show that similar motor responses occur as a result of observation of painful events in others. We used transcranial magnetic stimulation to record changes in corticospinal motor representations of hand muscles of individuals observing needles penetrating hands or feet of a human model or noncorporeal objects. We found a reduction in amplitude of motor-evoked potentials that was specific to the muscle that subjects observed being pricked. This inhibition correlated with the observer's subjective rating of the sensory qualities of the pain attributed to the model and with sensory, but not emotional, state or trait empathy measures. The empathic inference about the sensory qualities of others' pain and their automatic embodiment in the observer's motor system may be crucial for the social learning of reactions to pain.

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Figure 1: MEP amplitude with respect to the baseline during observation of 'Needle in FDI', 'Q-tip on FDI' and 'Non-corporeal' conditions of experiment 1.
Figure 2: MEPs amplitude with respect to the baseline during observation of 'Needle in foot' and 'Q-tip on foot' conditions of experiment 2.
Figure 3: MEP amplitude recorded from the FDI (black bars) and the ADM (white bars) muscles during the observation conditions of experiment 3.
Figure 4: Amplitude changes of MEPs recorded from the FDI muscle and subjective ratings (z-scores) of the pain ascribed to the model during the 'Needle in FDI' condition in experiment 1.
Figure 5: Amplitude changes of MEPs recorded from the ADM muscle and subjective ratings (z-scores) of the pain attributed to the model during the 'Needle in ADM' condition in experiment 3.
Figure 6: Amplitude changes of MEPs recorded from the FDI muscle during 'Needle in FDI' observation and state (a,b,c,d) and trait (e,f) empathy measures (z-scores) in experiment 5.

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References

  1. Preston, S.D. & de Waal, F.B.M. Empathy: its ultimate and proximate bases. Behav. Brain Sci. 25, 1–71 (2002).

    PubMed  Google Scholar 

  2. Decety, J. & Jackson, P.L. The functional architecture of human empathy. Behav. Cogn. Neurosci. Rev. 3, 71–100 (2004).

    Article  PubMed  Google Scholar 

  3. Gallese, V. The manifold nature of interpersonal relations: the quest for a common mechanism. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 517–528 (2003).

    Article  PubMed  PubMed Central  Google Scholar 

  4. Gallese, V., Fadiga, L., Fogassi, L. & Rizzolatti, G. Action recognition in the premotor cortex. Brain 119, 593–609 (1996).

    Article  PubMed  Google Scholar 

  5. Rizzolatti, G., Fogassi, L. & Gallese, V. Neurophysiological mechanisms underlying the understanding and imitation of action. Nat. Rev. Neurosci. 2, 661–670 (2001).

    Article  CAS  PubMed  Google Scholar 

  6. Fadiga, L., Fogassi, L., Pavesi, G. & Rizzolatti, G. Motor facilitation during action observation: a magnetic stimulation study. J. Neurophysiol. 73, 2608–2611 (1995).

    Article  CAS  PubMed  Google Scholar 

  7. Iacoboni, M. et al. Cortical mechanisms of human imitation. Science 286, 2526–2528 (1999).

    Article  CAS  PubMed  Google Scholar 

  8. Buccino, G. et al. Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study. Eur. J. Neurosci. 13, 400–404 (2001).

    CAS  PubMed  Google Scholar 

  9. Leslie, K.R., Johnson-Frey, S.H. & Grafton, S.T. Functional imaging of face and hand imitation: towards a motor theory of empathy. Neuroimage 21, 601–607 (2004).

    Article  PubMed  Google Scholar 

  10. Keysers, C. et al. A touching sight: SII/PV activation during the observation and experience of touch. Neuron 42, 335–346 (2004).

    Article  CAS  PubMed  Google Scholar 

  11. Carr, L. et al. Neural mechanisms of empathy in humans: a relay from neural systems for imitation to limbic areas. Proc. Natl. Acad. Sci. USA 100, 5497–5502 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Wicker, B. et al. Both of us disgusted in My insula: the common neural basis of seeing and feeling disgust. Neuron 40, 655–664 (2003).

    Article  CAS  PubMed  Google Scholar 

  13. Flor, H. Phantom-limb pain: characteristics, causes, and treatment. Lancet Neurol. 1, 182–189 (2002).

    Article  PubMed  Google Scholar 

  14. Eisenberger, N.I., Lieberman, M.D. & Williams, K.D. Does rejection hurt? An fMRI study of social exclusion. Science 302, 290–292 (2003).

    Article  CAS  PubMed  Google Scholar 

  15. Rainville, P. Brain mechanisms of pain affect and pain modulation. Curr. Opin. Neurobiol. 12, 195–204 (2002).

    Article  CAS  PubMed  Google Scholar 

  16. Ingvar, M. Pain and functional imaging. Philos. Trans. R. Soc. Lond. B Biol. Sci. 354, 1347–1358 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Wittgenstein, L. Philosophical Investigations (Blackwell, Oxford, 1963).

    Google Scholar 

  18. Williams, A.C. Facial expression of pain: an evolutionary account. Behav. Brain Sci. 25, 439–488 (2002).

    PubMed  Google Scholar 

  19. Hutchison, W.D. et al. Pain-related neurons in the human cingulate cortex. Nat. Neurosci. 2, 403–405 (1999).

    Article  CAS  PubMed  Google Scholar 

  20. Bradshaw, J.L. & Mattingley, J.B. Allodynia: a sensory analogue of motor mirror neurons in a hyperaesthetic patient reporting instantaneous discomfort to another's perceived sudden minor injury? J. Neurol. Neurosurg. Psychiatry 70, 135–136 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Singer, T. et al. Empathy for pain involves the affective but not sensory components of pain. Science 303, 1157–1162 (2004).

    Article  CAS  PubMed  Google Scholar 

  22. Jackson, P.L., Meltzoff, A.N. & Decety, J. How do we perceive the pain of others? A window into the neural processes involved in empathy. Neuroimage 24, 771–779 (2005).

    Article  PubMed  Google Scholar 

  23. Morrison, I., Lloyd, D., di Pellegrino, G. & Roberts, N. Vicarious responses to pain in anterior cingulate cortex: is empathy a multisensory issue? Cogn. Affect. Behav. Neurosci. 4, 270–278 (2004).

    Article  PubMed  Google Scholar 

  24. Wager, T.D. et al. Placebo-induced changes in FMRI in the anticipation and experience of pain. Science 303, 1162–1167 (2004).

    Article  CAS  PubMed  Google Scholar 

  25. Farina, S., Tinazzi, M., Le Pera, D. & Valeriani, M. Pain-related modulation of the human motor cortex. Neurol. Res. 25, 130–142 (2003).

    Article  PubMed  Google Scholar 

  26. Juottonen, K. et al. Altered central sensorimotor processing in patients with complex regional pain syndrome. Pain 98, 315–323 (2002).

    Article  PubMed  Google Scholar 

  27. Saitoh, Y., Shibata, M., Sanada, Y. & Mashimo, T. Motor cortex stimulation for phantom limb pain. Lancet 353, 212 (1999).

    Article  CAS  PubMed  Google Scholar 

  28. Farina, S. et al. Transient inhibition of the human motor cortex by capsaicin-induced pain. A study with transcranial magnetic stimulation. Neurosci. Lett. 314, 97–101 (2001).

    Article  CAS  PubMed  Google Scholar 

  29. Svensson, P., Miles, T.S., McKay, D. & Ridding, M.C. Suppression of motor evoked potentials in a hand muscle following prolonged painful stimulation. Eur. J. Pain 7, 55–62 (2003).

    Article  PubMed  Google Scholar 

  30. Urban, P.P. et al. Different short-term modulation of cortical motor output to distal and proximal upper-limb muscles during painful sensory nerve stimulation. Muscle Nerve 29, 663–669 (2004).

    Article  CAS  PubMed  Google Scholar 

  31. Maiani, G. & Sanavio, E. Semantics of pain in Italy: the Italian version of the McGill Pain Questionnaire. Pain 22, 399–405 (1985).

    Article  CAS  PubMed  Google Scholar 

  32. Melzack, R. The McGill Pain Questionnaire: major properties and scoring methods. Pain 1, 277–299 (1975).

    Article  CAS  PubMed  Google Scholar 

  33. Bonino, S., Lo Coco, A. & Tani, F. Empatia. I Processi di Condivisione delle Emozioni (Giunti, Florence, Italy, 1998).

    Google Scholar 

  34. Davis, M.H. Empathy: A Social Psychological Approach (Westview Press, Madison, Wisconsin, 1996).

    Google Scholar 

  35. Adolphs, R. Neural systems for recognizing emotion. Curr. Opin. Neurobiol. 12, 169–177 (2002).

    Article  CAS  PubMed  Google Scholar 

  36. Porro, C.A., Cettolo, V., Francescato, M.P. & Baraldi, P. Functional activity mapping of the mesial hemispheric wall during anticipation of pain. Neuroimage 19, 1738–1747 (2003).

    Article  PubMed  Google Scholar 

  37. Ploghaus, A., Becerra, L., Borras, C. & Borsook, D. Neural circuitry underlying pain modulation: expectation, hypnosis, placebo. Trends Cogn. Sci. 7, 197–200 (2003).

    Article  PubMed  Google Scholar 

  38. Meltzoff, A.N. & Decety, J. What imitation tells us about social cognition: a rapprochement between developmental psychology and cognitive neuroscience. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 491–500 (2003).

    Article  PubMed  PubMed Central  Google Scholar 

  39. Leibenluft, E., Gobbini, M.I., Harrison, T & Haxby, J.V. Mothers' neural activation in response to pictures of their children and other children. Biol. Psychiatry 56, 225–232 (2004).

    Article  PubMed  Google Scholar 

  40. Oldfield, R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97–113 (1971).

    Article  CAS  PubMed  Google Scholar 

  41. Wasserman, E.M. Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5–7, 1996. Electroenceph. Clin. Neurophysiol. 108, 1–16 (1998).

    Article  Google Scholar 

  42. Brasil-Neto, J.P. et al. Optimal focal transcranial magnetic activation of the human motor cortex: effects of coil orientation, shape of the induced current pulse, and stimulus intensity. J. Clin. Neurophysiol. 9, 132–136 (1992).

    Article  CAS  PubMed  Google Scholar 

  43. Mills, K.R., Boniface, S.J. & Schubert, M. Magnetic brain stimulation with a double coil: the importance of coil orientation. Electroencephalogr. Clin. Neurophysiol. 85, 17–21 (1992).

    Article  CAS  PubMed  Google Scholar 

  44. Rossini, P.M. et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr. Clin. Neurophysiol. 91, 79–92 (1994).

    Article  CAS  PubMed  Google Scholar 

  45. Eisen, A. Electromyography in disorders of muscle tone. Can. J. Neurol. Sci. 14, 501–505 (1987).

    Article  CAS  PubMed  Google Scholar 

  46. Kimura, J. Electrodiagnosis in Diseases of Nerve and Muscle (F.A. Davis Company, Philadelphia, 1993).

    Google Scholar 

  47. Maeda, F., Kleiner-Fisman, G. & Pascual-Leone, A. Motor facilitation while observing hand actions: specificity of the effect and role of observer's orientation. J. Neurophysiol. 87, 1329–1335 (2002).

    Article  PubMed  Google Scholar 

  48. Gangitano, M., Mottaghy, F.M. & Pascual-Leone, A. Modulation of premotor mirror neuron activity during observation of unpredictable grasping movements. Eur. J. Neurosci. 20, 2193–2202 (2004).

    Article  PubMed  Google Scholar 

  49. Järveläinen, J., Schürmann, M. & Hari, R. Activation of the human primary motor cortex during observation of tool use. Neuroimage 23, 187–192 (2004).

    Article  PubMed  Google Scholar 

  50. Chen, R. et al. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48, 1398–1403 (1997).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by grants from the Ministero Istruzione Università e Ricerca and Finanziamento Italiano Ricerca di Base, Italy, both awarded to S.M.A.

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Correspondence to Salvatore M Aglioti.

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Supplementary information

Supplementary Fig. 1

Examples of raw MEP amplitudes for each observation condition in a representative subject of experiment 1. (JPG 34 kb)

Supplementary Fig. 2

Sensory and affective qualities of the pain supposedly felt by the model during observation of the different types of video clips in experiments 1, 2 and 3. (JPG 68 kb)

Supplementary Fig. 3

Self-oriented emotional reactions during observation of the different movies of experiment 1 measured by means of VAS. (JPG 81 kb)

Supplementary Fig. 4

MEP amplitude recorded from the FDI (black bars) and the ADM (white bars) muscles during the observation of 'Needle in FDI' condition of experiment 5 (expressed with respect to the correspondening static condition). (JPG 29 kb)

Supplementary Table 1

Mean amplitude (± s.e.m.) of F and M waves recorded from the FDI muscle in experiment 4. (JPG 32 kb)

Supplementary Table 2

Simple correlations between MEP amplitude changes recorded from FDI and ADM muscles and subjective ratings of 'Needle in FDI' video clips of experiment 1 and 5, and 'Needle in ADM' video clips of experiment 3. (PDF 44 kb)

Supplementary Video 1

Representative video clips showing the dynamic conditions of experiment 1: (i) a needle entering a right hand ('Needle in FDI'), (ii) a Q-Tip touching the right hand in regions overlapping those pricked by the needle ('Q-Tip on FDI') and (iii) a needle entering a tomato ('Non-Corporeal'). (MOV 2299 kb)

Supplementary Note (PDF 73 kb)

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Avenanti, A., Bueti, D., Galati, G. et al. Transcranial magnetic stimulation highlights the sensorimotor side of empathy for pain. Nat Neurosci 8, 955–960 (2005). https://doi.org/10.1038/nn1481

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