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Dynamic Brain Topography of Somatosensory Evoked Potentials and Equivalent Dipoles in Response to Graded Painful Skin and Muscle Stimulation

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Abstract

The differential effects of painful stimulation of skin vs. muscle on the cerebral electrophysiology have been poorly described. This study examined the somatosensory evoked potentials (SEPs) and the associated dipole models of non-painful and graded painful electrical stimulation applied to the skin and muscle in 20 healthy subjects. With the psychophysical stimulus-response functions determined, the skin stimulation showed a steeper slope than muscle stimulation. For both types of stimulation, the SEPs indicated a similar temporo-spatial activation sequence: F4/N90-P4/P95, Fc2/N135, Cz/P250, Cz/P300, and Cz/N460. The SEP amplitudes increased significantly with the stimulus intensities in these components. The peak SEP latencies of skin stimulation were in general shorter than that of muscle stimulation. The SEP amplitudes to skin stimulation were significantly larger than those caused by muscle stimulation at every stimulus intensity level, except the early mid-latency component. In this case, muscle stimulation caused higher amplitudes over the contralateral parietal-frontal sites. For both types of stimulation, the topographic maps were quite similar. Equivalent dipole modeling revealed identical site parameters (<1.0 cm) between skin and muscle stimulation. However, the electrical skin stimulation did not correlate with the pain intensity. Pain intensity, in contrast, was uniquely associated with the Cz/P250 amplitudes for the muscle stimulation. It is concluded that non-nociceptive and nociceptive electrical stimuli applied to skin and muscle are processed in the common cerebral areas, but exhibit differential SEP effects.

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References

  • Allison, T., McCarthy, G., Wood, C.C. and Jones, S.J. Potentials evoked in human and monkey cerebral cortex by stimulation of the median nerve. A review of scalp and intracranial recordings. Brain, 1991, 114: 2465-2503.

    Google Scholar 

  • Arendt-Nielsen, L. Induction and assessment of experimental pain from human skin, muscle, and viscera. Proceedings of the 8th World Congress on Pain, Progress in Pain Research and Management, 1997, 8: 393-425.

    Google Scholar 

  • Arendt-Nielsen, L., Yamasaki, H., Nielsen, J., Naka, D. and Kakigi, R. Magnetoencephalographic responses to painful impact stimulation. Brain Res., 1999, 839: 203-208.

    Google Scholar 

  • Beydoun, A., Morrow, T.J., Shen, J.F. and Casey, K.L. Variability of laser-evoked potentials: attention, arousal and lateralized differences. Electroencephalogr. Clin. Neurophysiol., 1993, 88: 173-181.

    Google Scholar 

  • Boulu, P., De Broucker, T., Maitre, P., Meunier, S. and Willer, J.C. Somatosensory evoked potential and pain. I. Late cortical responses obtained at different levels of stimulation. Rev. Electroencephalogr. Neurophysiol. Clin., 1985, 15: 19-25.

    Google Scholar 

  • Brennum, J. and Jensen, T.S. Relationship between vertex potentials and magnitude of pre-pain and pain sensations evoked by electrical skin stimuli. Electroencephalogr. Clin. Neurophysiol., 1992, 82: 387-390.

    Google Scholar 

  • Bromm, B. and Lorenz, J. Neurophysiological evaluation of pain. Electroencephalogr. Clin. Neurophysiol., 1998, 107: 227-253.

    Google Scholar 

  • Bromm, B. and Scharein, E. Principal component analysis of pain-related cerebral potentials to mechanical and electrical stimulation in man. Electroencephalogr. Clin. Neurophysiol., 1982, 53: 94-103.

    Google Scholar 

  • Bromm, B. and Chen, A.C. Brain electrical source analysis of laser evoked potentials in response to painful trigeminal nerve stimulation. Electroencephalogr. Clin. Neurophysiol., 1995, 95: 14-26.

    Google Scholar 

  • Casey, K.L. Forebrain mechanisms of nociception and pain: analysis through imaging. Proc. Natl. Acad. Sci., USA, 1999, 96: 7668-7674.

    Google Scholar 

  • Chen, A.C.N. and Bromm, B. Pain-related generators of laser-evoked brain potentials: brain mapping and dipole modelling. Advances in pain research and therapy, 1995, 22: 245-266.

    Google Scholar 

  • Chen, A.C.N., Arendt-Nielsen, L. and Plaghki, L. Laser-Evoked potentials in human pain I. Use and possible misuse. Pain Forum, 1998a, 7: 174-184.

    Google Scholar 

  • Chen, A.C.N., Arendt-Nielsen, L., and Plaghki, L. Laser-evoked potentials in human pain: cerebral generators. Pain Forum, 1998b, 7: 201-230.

    Google Scholar 

  • Derbyshire, S.W.G. Meta-analysis of thirty-four independent samples studied using PET reveals a significantly attenuated central response to noxious stimulation in clinical patients. Current Review of Pain, 1999, 3: 265-280.

    Google Scholar 

  • Dowman, R. and Goshko, L. Evaluation of reference sites for scalp potentials evoked by painful and non-painful sural nerve stimulation. Electroencephal. Clin. Neurophysiol., 1992, 84: 477-485.

    Google Scholar 

  • Frot, M., Rambaud, L., Guenot, M. and Mauguiere, F. Intracortical recordings of early pain-related CO2-laser evoked potentials in the human second somatosensory (SII) area. Clin. Neurophysiol., 1999, 110: 133-145.

    Google Scholar 

  • Hari, R., Portin, K., Kettenmann, B., Jousmaki, V. and Kobal, G. Right-hemisphere preponderance of responses to painful CO2 stimulation of the human nasal mucosa. Pain, 1997, 72: 145-151.

    Google Scholar 

  • Hari, R. and Forss, N. Magnetoencephalography in the study of human somatosensory cortical processing. Philos. Trans. R. Soc. Lond. B. Biol. Sci., 1999, 354: 1145-1154.

    Google Scholar 

  • Ingvar, M. Pain and functional imaging. Philos. Trans. R. Soc. Lond. B. Biol. Sci., 1999, 354: 1347-1358.

    Google Scholar 

  • Kakigi, R., Watanabe, S., Yamasaki, H. and Maeda, K. Pain-related brain activities: magnetoencephalographic studies. Electroencephalogr. Clin. Neurophysiol. Suppl., 1999, 49: 245-249.

    Google Scholar 

  • Kanda, M., Nagamine, T., Ikeda, A., Ohara, S., Kunieda, T., Fujiwara, N., Yazawa, S., Sawamoto, N., Matsumoto, R., Taki, W. and Shibasaki, H. Primary somatosensory cortex is actively involved in pain processing in human. Brain Res., 2000, 853: 282-289.

    Google Scholar 

  • Kany, C. and Treede, R.D. Median and tibial nerve somatosensory evoked potentials: middle-latency components from the vicinity of the secondary somatosensory cortex in humans. Electroencephalogr. Clin. Neurophysiol., 1997, 104: 402-410.

    Google Scholar 

  • Kitamura, Y., Kakigi, R., Hoshiyama, M., Koyama, S., Shimojo, M. and Watanabe, S. Pain-related somatosensory evoked magnetic fields. Electroencephalogr. Clin. Neurophysiol. 1995, 95: 463-474.

    Google Scholar 

  • Lenz, F.A., Rios, M., Zirh, A., Chau, D., Krauss, G. and Lesser, R.P. Painful stimuli evoke potentials recorded over the human anterior cingulate gyrus. J. Neurophysiol., 1998, 79: 2231-2234.

    Google Scholar 

  • Lenz, F.A., Krauss, G., Treede, R.D., Lee, J.L., Boatman, D., Crone, N., Minahan, R., Port, J. and Rios, M. Different generators in human temporal-parasylvian cortex account for subdural laser-evoked potentials, auditory-evoked potentials, and event-related potentials. Neurosci. Lett., 2000, 279: 153-156.

    Google Scholar 

  • Mauguiere, F., Merlet, I., Forss, N., Vanni, S., Jousmaki, V., Adeleine, P. and Hari, R. Activation of a distributed somatosensory cortical network in the human brain. A dipole modelling study of magnetic fields evoked by median nerve stimulation. Part I: Location and activation timing of SEF sources. Electroencephalogr. Clin. Neurophysiol., 1997a, 104: 281-289.

    Google Scholar 

  • Mauguiere, F., Merlet, I., Forss, N., Vanni, S., Jousmaki, V., Adeleine, P. and Hari, R. Activation of a distributed somatosensory cortical network in the human brain: a dipole modelling study of magnetic fields evoked by median nerve stimulation. Part II: Effects of stimulus rate, attention and stimulus detection. Electroencephalogr. Clin. Neurophysiol., 1997b, 104: 290-295.

    Google Scholar 

  • Mauguiere, F., Frot, M., Peyron, R., Garcia-Larrea, L., Laurent, B. and Michel, D. The role of parietal opercular and insular cortex in pain sensation in humans: data from PET activation studies and intracortical recordings of CO2 laser evoked potentials (LEPs). Electroencephalogr. Clin. Neurophysiol. Suppl., 1999, 49: 255-260.

    Google Scholar 

  • Mense, S., Nociception from skeletal muscle in relation to clinical muscle pain. Pain, 1993, 54: 241-289.

    Google Scholar 

  • Mense, S. Group III and IV receptors in skeletal muscle: are they specific or polymodal? Prog. Brain. Res., 1996a, 113: 83-100.

    Google Scholar 

  • Mense, S. Nociceptors in skeletal muscle and their reaction to pathological tissue changes. In: C. Belmonte and F. Cervero (Eds.) Neurobiology of Nociceptors, New York: Oxford University Press, 1996: 184-201.

    Google Scholar 

  • Ploner, M., Schmitz, F., Freund, H.J. and Schnitzler, A. Parallel activation of primary and secondary somatosensory cortices in human pain processing. J. Neurophysiol., 1999, 81: 3100-3104.

    Google Scholar 

  • Ploner, M., Schmitz, F., Freund, H.J. and Schnitzler, A. Differential organization of touch and pain in human primary somatosensory cortex. J. Neurophysiol., 2000, 83: 1770-1776.

    Google Scholar 

  • Rossini, P.M., Gigli, G.L., Marciani, M.G., Zarola, F. and Caramia, M. Non-invasive evaluation of input-output characteristics of sensorimotor cerebral areas in healthy humans. Electroencephalogr. Clin. Neurophysiol., 1987, 68: 88-100.

    Google Scholar 

  • Svensson, P., Beydoun, A., Morrow, T.J. and Casey, K.L. Non-painful and painful stimulation of human skin and muscle: analysis of cerebral evoked potentials. Electroencephalogr. Clin. Neurophysiol., 1997a, 104: 343-350.

    Google Scholar 

  • Svensson, P., Beydoun, A., Morrow, T.J. and Casey, K.L. Human intramuscular and cutaneous pain: psychophysical comparisons. Exp. Brain Res., 1997b, 114: 390-392.

    Google Scholar 

  • Svensson, P., Minoshima, S., Beydoun, A., Morrow, T.J. and Casey, K.L. Cerebral processing of acute skin and muscle pain in humans. J. Neurophysiol., 1997c, 78: 450-460.

    Google Scholar 

  • Tarkka, I.M. and Treede, R.D. Equivalent electrical source analysis of pain-related somatosensory evoked potentials elicited by a CO2 laser. J. Clin. Neurophysiol., 1993, 10: 513-519.

    Google Scholar 

  • Valeriani, M., Rambaud, L. and Mauguiere, F. Scalp topography and dipole source modelling of potentials evoked by CO2 laser stimulation of the hand. Electroencephalogr. Clin. Neurophysiol., 1996, 100: 343-353.

    Google Scholar 

  • Watanabe, S., Kakigi, R., Koyama, S., Hoshiyama, M. and Kaneoke, Y. Pain processing traced by magneto-encephalography in the human brain. Brain Topogr. 1998, 10: 255-264.

    Google Scholar 

  • Witting, N., Svensson, P., Arendt-Nielsen, L. and Troels, S. Jensen. Differential effect of painful heterotopic stimulation on capsaicin-induced pain and allodynia. Brain Research, 1998, 801: 206-210.

    Google Scholar 

  • Witting, N., Svensson, P., Gottrup, H., Arendt-Nielsen, L. and Jensen, T.S. Intramuscular and intradermal injection of capsaicin: a comparison of local and referred pain. Pain, 2000, 84:407-412.

    Google Scholar 

  • Yamasaki, H., Kakigi, R., Watanabe, S. and Naka, D. Effects of distraction on pain perception: magneto-and electro-encephalographic studies. Brain. Res. Cogn. Brain Res., 1999, 8: 73-76.

    Google Scholar 

  • Yamasaki, H., Kakigi, R., Watanabe, S. and Hoshiyama, M. Effects of distraction on pain-related somatosensory evoked magnetic fields and potentials following painful electrical stimulation. Brain Res. Cogn. Brain Res., 2000, 9: 165-175.

    Google Scholar 

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Authors and Affiliations

  1. Human Brain Mapping and Cortical Imaging Laboratory, Center for Sensory-Motor Interaction, Aalborg University, Denmark

    Motoko Shimojo, Peter Svensson, Lars Arendt-Nielsen & Andrew C.N. Chen

  2. Department of Integrative Physiology, National Institute for Physiological Sciences, Japan

    Motoko Shimojo

  3. Department of Prosthetic Dentistry and Stomatognathic Physiology, University of Aarhus, Denmark

    Peter Svensson

Authors
  1. Motoko Shimojo
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  2. Peter Svensson
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  3. Lars Arendt-Nielsen
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  4. Andrew C.N. Chen
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Shimojo, M., Svensson, P., Arendt-Nielsen, L. et al. Dynamic Brain Topography of Somatosensory Evoked Potentials and Equivalent Dipoles in Response to Graded Painful Skin and Muscle Stimulation. Brain Topogr 13, 43–58 (2000). https://doi.org/10.1023/A:1007834319135

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