Hostname: page-component-546b4f848f-bvkm5 Total loading time: 0 Render date: 2023-06-04T05:33:15.359Z Has data issue: false Feature Flags: { "useRatesEcommerce": true } hasContentIssue false

Oscillatory Characteristics of Nociceptive Responses in the SII Cortex

Published online by Cambridge University Press:  02 December 2014

Fu-Jung Hsiao
Institute of Physiology, National Yang-Ming University Institute of Brain Science, National Yang-Ming University Department of Medical Research and Education, Taipei Veterans General Hospital, Taipei, Taiwan
Wei-Ta Chen
Institute of Brain Science, National Yang-Ming University Institute of Neuroscience, National Yang-Ming University Neurological Institute, Taipei Veterans General Hospital, Taipei, Taiwan
Kwong-Kum Liao
Department of Neurology, National Yang-Ming University Neurological Institute, Taipei Veterans General Hospital, Taipei, Taiwan
Zin-An Wu
Department of Neurology, National Yang-Ming University Neurological Institute, Taipei Veterans General Hospital, Taipei, Taiwan
Low-Tone Ho
Institute of Physiology, National Yang-Ming University Department of Medical Research and Education, Taipei Veterans General Hospital, Taipei, Taiwan
Yung-Yang Lin*
Institute of Physiology, National Yang-Ming University Institute of Brain Science, National Yang-Ming University Institute of Clinical Medicine, National Yang-Ming University Department of Medical Research and Education, Taipei Veterans General Hospital, Taipei, Taiwan
Department of Medical Research and Education, and Department of Neurology, Taipei Veterans General Hospital, No.201, Sec.2, Shih-Pai Rd., Taipei 112, Taiwan.
Rights & Permissions[Opens in a new window]


HTML view is not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

This study is aimed to explore the frequency characteristics of pain-evoked neuromagnetic responses in the secondary somatosensory (SII) cortices.


Thulium-laser nociceptive stimuli to the left hand dorsum of 10 right-handed healthy adults. The pain stimuli were rated as mild, moderate, and severe levels according to subjects' reports on a 10-point visual analog scale. We analyzed their cortical responses with wavelet-based frequency analyses and equivalent current dipole (ECD) modeling.


For each pain level, we found an increase of theta (4-8 Hz) and alpha (8-13 Hz) power in bilateral SII areas at 180-210 ms after stimulus onset. The power was larger for the moderate than for the mild pain level (p < 0.05), but there was no statistical power difference of these oscillations between moderate and severe pain stimulus conditions (p = 0.7). Within the SII area, we did not observe particular difference in theta and alpha ECD locations between varying pain level conditions.


The 4-13 Hz activities, peaking from 180 to 210 ms, are oscillatory correlates of SII activation in response to nociceptive stimulation, but their power may code the magnitude of pain stimuli only up to moderate level, as rated subjectively. This measure could be potentially used to evaluate SII activation in further pain studies.



Le but de cette étude était d'explorer les caractéristiques des fréquences des réponses neuromagnétiques évoquées par la douleur dans les cortex somatosensitifs secondaires (SII).


Des stimuli nociceptifs au laser-thulium ont été appliqués à la face dorsale de la main gauche de 10 adultes droitiers en bonne santé. Les stimuli douloureux étaient évalués comme étant légers, modérés ou sévères par les sujets au moyen d'une échelle analogue visuelle de 10 points. Nous avons analysé leurs réponses corticales au moyen d'analyses fréquentielles par ondelettes et de modélisation d'un dipôle de courant équivalent (DCÉ).


Pour chaque niveau de douleur, nous avons observé une augmentation de puissance thêta (4-8 Hz) et alpha (8-13 Hz) dans les aires SI bilatérales, 180 à 210 ms après le début du stimulus. La puissance était plus grande lors de la douleur modérée par rapport à la douleur légère (p < 0,05), mais il n'y avait pas de différence statistique dans la puissance de ces oscillations entre la douleur modérée ou sévère (p = 0,7). Nous n'avons pas observé de différence particulière dans la localisation DCÉ thêta et alpha dans la zone SII selon les niveaux de douleur.


Les activités 4- 13 Hz, dont le pic était observé entre 180 et 210 ms, sont des corrélats oscillatoires de l'activation au niveau du SII en réponse à une stimulation nociceptive, mais leur puissance peut témoigner de l'ampleur de stimuli douloureux seulement jusqu'à un niveau modéré, évalué subjectivement. Cette mesure pourrait potentiellement être utilisée pour évaluer l'activation SII dans des études ultérieures sur la douleur.

Research Article
Copyright © The Canadian Journal of Neurological 2008


1. Mor, J, Carmon, A. Laser emitted radiant heat for pain research. Pain. 1975; 1: 2337.CrossRefGoogle ScholarPubMed
2. Bromm, B, Jahnke, MT, Treede, RD. Responses of human cutaneous afferents to CO2 laser stimuli causing pain. Exp Brain Res. 1984; 55: 15866.CrossRefGoogle ScholarPubMed
3. Bromm, B, Treede, RD. Laser-evoked cerebral potentials in the assessment of cutaneous pain sensitivity in normal subjects and patients. Rev Neurol (Paris). 1991; 147: 62543.Google Scholar
4. Kakigi, R, Koyama, S, Hoshiyama, M, Kitamura, Y, Shimojo, M, Watanabe, S. Pain-related magnetic fields following painful CO2 laser stimulation in man. Neurosci Lett. 1995; 192: 458.CrossRefGoogle ScholarPubMed
5. Kakigi, R, Koyama, S, Hoshiyama, M, Kitamura, Y, Shimojo, M, Watanabe, S. Pain-related brain responses following CO2 laser stimulation: magnetoencephalographic studies. Electro-encephalogr Clin Neurophysiol Suppl. 1996; 47: 11120.Google ScholarPubMed
6. Chen, WT, Yuan, RY, Shih, YH, Yeh, TC, Hung, DL, Wu, ZA, et al. Neuromagnetic SII responses do not fully reflect pain scale. Neuroimage. 2006; 31: 6706.CrossRefGoogle Scholar
7. Forss, N, Raij, TT, Seppa, M, Hari, R. Common cortical network for first and second pain. Neuroimage. 2005; 24: 13242.CrossRefGoogle ScholarPubMed
8. Timmermann, L, Ploner, M, Haucke, K, Schmitz, F, Baltissen, R, Schnitzler, A. Differential coding of pain intensity in the human primary and secondary somatosensory cortex. J Neurophysiol. 2001; 86: 1499503.CrossRefGoogle ScholarPubMed
9. Apkarian, AV, Darbar, A, Krauss, BR, Gelnar, PA, Szeverenyi, NM. Differentiating cortical areas related to pain perception from stimulus identification: temporal analysis of fMRI activity. J Neurophysiol. 1999; 81: 295663.CrossRefGoogle ScholarPubMed
10. Kwan, CL, Crawley, AP, Mikulis, DJ, Davis, KD. An fMRI study of the anterior cingulate cortex and surrounding medial wall activations evoked by noxious cutaneous heat and cold stimuli. Pain. 2000; 85: 35974.CrossRefGoogle ScholarPubMed
11. Peyron, R, Garcia-Larrea, L, Gregoire, MC, Convers, P, Richard, A, Lavenne, F, et al. 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. 2000; 84: 7787.CrossRefGoogle Scholar
12. Talbot, JD, Marrett, S, Evans, AC, Meyer, E, Bushnell, MC, Duncan, GH. Multiple representations of pain in human cerebral cortex. Science. 1991; 251: 13558.CrossRefGoogle ScholarPubMed
13. Kakigi, R, Inui, K, Tamura, Y. Electrophysiological studies on human pain perception. Clin Neurophysiol. 2005; 116: 74363.CrossRefGoogle ScholarPubMed
14. Basar, E. Brain function and oscillations. Integrative brain functions. Vol. I. Berlin: 1998.Google Scholar
15. Basar, E. Brain function and oscillations. Integrative brain functions. Vol. II. Berlin: 1999.Google Scholar
16. Basar, E, Basar-Eroglu, C, Karakas, S, Schurmann, M. Oscillatory brain theory: a new trend in neuroscience. IEEE Eng Med Biol Mag. 1999; 18: 5666.CrossRefGoogle ScholarPubMed
17. Basar, E, Basar-Eroglu, C, Karakas, S, Schurmann, M. Brain oscillations in perception and memory. Int J Psychophysiol. 2000; 35: 95124.CrossRefGoogle ScholarPubMed
18. Basar, E, Ozgoren, M, Karakas, S, Basar-Eroglu, C. Super-synergy in the brain: grandmother percept is manifested by multiple oscillations. Int J Bifurcat Chaos. 2004; 14: 138.CrossRefGoogle Scholar
19. Klopp, J, Halgren, E, Marinkovic, K, Nenov, V. Face-selective spectral changes in the human fusiform gyrus. Clin Neurophysiol. 1999; 110: 67682.CrossRefGoogle ScholarPubMed
20. Quian Quiroga, R, Sakowitz, OW, Basar, E, Schurmann, M. Wavelet transform in the analysis of the frequency composition of evoked potentials. Brain Res Brain Res Protoc. 2001; 8: 1624.CrossRefGoogle ScholarPubMed
21. Yordanova, J, Devrim, M, Kolev, V, Ademoglu, A, Demiralp, T. Multiple time-frequency components account for the complex functional reactivity of P300. Neuroreport. 2000; 11: 1097103.CrossRefGoogle ScholarPubMed
22. Yordanova, J, Kolev, V, Rosso, OA, Schürmann, M, Sakowitz, OW, Ozgören, M, et al. Wavelet entropy analysis of event-related potentials indicates modality-independent theta dominance. J Neurosci Methods. 2002; 117: 99109.CrossRefGoogle ScholarPubMed
23. Sarnthein, J, Stern, J, Aufenberg, C, Rousson, V, Jeanmonod, D. Increased EEG power and slowed dominant frequency in patients with neurogenic pain. Brain. 2006; 129: 5564.CrossRefGoogle ScholarPubMed
24. Stern, J, Jeanmonod, D, Sarnthein, J. Persistent EEG overactivation in the cortical pain matrix of neurogenic pain patients. Neuroimage. 2006; 31: 72131.CrossRefGoogle ScholarPubMed
25. Hauck, M, Lorenz, J, Engel, AK. Attention to painful stimulation enhances gamma-band activity and synchronization in human sensorimotor cortex. J Neurosci. 2007; 27:92707.CrossRefGoogle ScholarPubMed
26. Samar, VJ, Swartz, KP, Raghuveer, MR. Multiresolution analysis of event-related potentials by wavelet decomposition. Brain Cogn. 1995; 27: 398438.CrossRefGoogle ScholarPubMed
27. Price, DD, McGrath, PA, Rafii, A, Buckingham, B. The validation of visual analogue scales as ratio scale measures for chronic and experimental pain. Pain. 1983; 17:4556.CrossRefGoogle ScholarPubMed
28. Gracely, RH. Studies of pain in human subjects. In: Wall, PD, Melzack, R, editors. Textbook of pain, 4th ed. Edinburgh: Churchill Livingstone; 1999. p. 385407.Google Scholar
29. Hämäläinen, M, R, Hari, Ilmoniemi, RJ, Knuutila, J, Lounasmaa, OV. Magnetoencephalography - theory, instrumentation, and application to noninvasive studies of the working human brain. Rev Mod Phys. 1993; 65: 41397.CrossRefGoogle Scholar
30. Kronland-Martinet, R, Morlet, J, Grossmann, A. Analysis of sound patterns through wavelet transforms. Int J Patt Recogn Art Intell. 1987; 1: 273302.CrossRefGoogle Scholar
31. Grossman, A, Kronland-Martinet, R, Morlet, J. Reading and understanding continuous wavelets transforms. Wavelets, timefrequency methods and phase space. Berlin: Springer-Verlag; 1989. p. 220.Google Scholar
32. Hsiao, FJ, Lin, YY, Hsieh, JC, Wu, ZA, Ho, LT, Chang, Y. Oscillatory characteristics of face-evoked neuromagnetic responses. Int J Psychophysiol. 2006; 61: 11320.CrossRefGoogle ScholarPubMed
33. Jensen, O, Gelfand, J, Kounios, J, Lisman, JE. Oscillations in the alpha band (9-12 Hz) increase with memory load during retention in a short-term memory task. Cereb Cortex. 2002; 12: 87782.CrossRefGoogle Scholar
34. Lachaux, JP, Rodriguez, E, Martinerie, J, Varela, FJ. Measuring phase synchrony in brain signals. Hum Brain Mapp. 1999; 8: 194208.3.0.CO;2-C>CrossRefGoogle ScholarPubMed
35. Lin, YY, Hsiao, FJ, Shih, YH, Yiu, CH, Yen, DJ, Kwan, SY, et al. Plastic phase-locking and magnetic mismatch response to auditory deviants in temporal lobe epilepsy. Cereb Cortex. 2007; 17: 251625.CrossRefGoogle ScholarPubMed
36. Rodriguez, E, George, N, Lachaux, JP, Martinerie, J, Renault, B, Varela, FJ. Perception’s shadow: long-distance synchronization of human brain activity. Nature. 1999; 397: 4303.CrossRefGoogle ScholarPubMed
37. Tallon-Baudry, C, Bertrand, O, Delpuech, C, Pernier, J. Stimulus specificity of phase-locked and non-phase-locked 40 Hz visual responses in human. J Neurosci. 1996; 16: 42409.CrossRefGoogle ScholarPubMed
38. Tallon-Baudry, C, Bertrand, O, Peronnet, F, Pernier, J. Induced gamma-band activity during the delay of a visual short-term memory task in humans. J Neurosci. 1998; 18: 424454.CrossRefGoogle ScholarPubMed
39. Chen, AC, Herrmann, CS. Perception of pain coincides with the spatial expansion of electroencephalographic dynamics in human subjects. Neurosci Lett. 2001; 297: 1836.CrossRefGoogle ScholarPubMed
40. Bromm, B, Meier, W, Scharein, E. Pre-stimulus/post-stimulus relations in EEG spectra and their modulations by an opioid and an antidepressant. Electroencephalogr Clin Neurophysiol. 1989; 73: 18897.CrossRefGoogle ScholarPubMed
41. Mouraux, A, Guerit, JM, Plaghki, L. Non-phase locked electroencephalogram (EEG) responses to CO2 laser skin stimulations may reflect central interactions between A partial partial differential- and C-fibre afferent volleys. Clin Neurophysiol. 2003; 114: 71022.CrossRefGoogle ScholarPubMed
42. Mouraux, A, Plaghki, L. Single-trial detection of human brain responses evoked by laser activation of Adelta-nociceptors using the wavelet transform of EEG epochs. Neurosci Lett. 2004; 361: 2414.CrossRefGoogle ScholarPubMed
43. Backonja, M, Howland, EW, Wang, J, Smith, J, Salinsky, M, Cleeland, CS. Tonic changes in alpha power during immersion of the hand in cold water. Electroencephalogr Clin Neurophysiol. 1991; 79: 192203.CrossRefGoogle ScholarPubMed
44. Chang, PF, Arendt-Nielsen, L, Graven-Nielsen, T, Svensson, P, Chen, AC. Different EEG topographic effects of painful and nonpainful intramuscular stimulation in man. Exp Brain Res. 2001; 141: 195203.CrossRefGoogle Scholar
45. Chen, AC, Dworkin, SF, Haug, J, Gehrig, J. Topographic brain measures of human pain and pain responsivity. Pain. 1989; 37: 12941.CrossRefGoogle ScholarPubMed
46. Chen, AC, Rappelsberger, P. Brain and human pain: topographic EEG amplitude and coherence mapping. Brain Topogr. 1994; 7: 12940.CrossRefGoogle ScholarPubMed
47. Ferracuti, S, Seri, S, Mattia, D, Cruccu, G. Quantitative EEG modifications during the Cold Water Pressor Test: hemispheric and hand differences. Int J Psychophysiol. 1994; 17: 2618.CrossRefGoogle ScholarPubMed
48. Veerasarn, P, Stohler, CS. The effect of experimental muscle pain on the background electrical brain activity. Pain. 1992; 49: 34960.CrossRefGoogle ScholarPubMed
49. Babiloni, C, Babiloni, F, Carducci, F, Cincotti, F, Rosciarelli, F, Arendt-Nielsen, L, et al. Human brain oscillatory activity phase-locked to painful electrical stimulations: a multi-channel EEG study. Hum Brain Mapp. 2002; 15: 11223.CrossRefGoogle ScholarPubMed
50. Narici, L, Forss, N, Jousmaki, V, Peresson, M, Hari, R. Evidence for a 7- to 9-Hz “sigma” rhythm in the human SII cortex. Neuroimage. 2001; 13: 6628.CrossRefGoogle ScholarPubMed
51. Bromm, B, Chen, AC. Brain electrical source analysis of laser evoked potentials in response to painful trigeminal nerve stimulation. Electroencephalogr Clin Neurophysiol. 1995; 95: 1426.CrossRefGoogle ScholarPubMed
52. Valeriani, M, Rambaud, L, Mauguiere, F. Scalp topography and dipolar source modelling of potentials evoked by CO2 laser stimulation of the hand. Electroencephalogr Clin Neurophysiol. 1996; 100: 34353.CrossRefGoogle ScholarPubMed
53. Nakamura, Y, Paur, R, Zimmermann, R, Bromm, B. Attentional modulation of human pain processing in the secondary somatosensory cortex: a magnetoencephalographic study. Neurosci Lett. 2002; 328: 2932.CrossRefGoogle ScholarPubMed
54. Raij, TT, Vartiainen, NV, Jousmaki, V, Hari, R. Effects of interstimulus interval on cortical responses to painful laser stimulation. J Clin Neurophysiol. 2003; 20: 739.CrossRefGoogle ScholarPubMed
55. Watanabe, S, Kakigi, R, Koyama, S, Hoshiyama, M, Kaneoke, Y. Pain processing traced by magnetoencephalography in the human brain. Brain Topogr. 1998; 10: 25564.CrossRefGoogle ScholarPubMed
56. Coghill, RC, Gilron, I, Iadarola, MJ. Hemispheric lateralization of somatosensory processing. J Neurophysiol. 2001; 85: 260212.CrossRefGoogle ScholarPubMed
57. Coghill, RC, Sang, CN, Maisog, JM, Iadarola, MJ. Pain intensity processing within the human brain: a bilateral, distributed mechanism. J Neurophysiol. 1999; 82: 193443.CrossRefGoogle ScholarPubMed
58. Knecht, S, Kunesch, E, Schnitzler, A. Parallel and serial processing of haptic information in man: effects of parietal lesions on sensorimotor hand function. Neuropsychologia. 1996; 34: 66987.CrossRefGoogle ScholarPubMed
59. Stein, BE, Price, DD, Gazzaniga, MS. Pain perception in a man with total corpus callosum transection. Pain. 1989; 38: 516.CrossRefGoogle Scholar
60. Valeriani, M, Restuccia, D, Barba, C, Le Pera, D, Tonali, P, Mauguiere, F. Sources of cortical responses to painful CO2 laser skin stimulation of the hand and foot in the human brain. Clin Neurophysiol. 2000; 111: 110312.CrossRefGoogle Scholar
61. Frot, M, Garcia-Larrea, L, Guenot, M, Mauguiere, F. Responses of the supra-sylvian (SII) cortex in humans to painful and innocuous stimuli. A study using intra-cerebral recordings. Pain. 2001; 94: 6573.CrossRefGoogle ScholarPubMed
62. Frot, M, Rambaud, L, Guenot, M, Mauguiere, F. Intracortical recordings of early pain-related CO2-laser evoked potentials in the human second somatosensory (SII) area. Clin Neurophysiol. 1999; 110: 13345.CrossRefGoogle ScholarPubMed
63. Lenz, FA, Rios, M, Chau, D, Krauss, GL, Zirh, TA, Lesser, RP. Painful stimuli evoke potentials recorded from the parasylvian cortex in humans. J Neurophysiol. 1998; 80: 207788.CrossRefGoogle ScholarPubMed
64. Peyron, R, Frot, M, Schneider, F, Garcia-Larrea, L, Mertens, P, Barral, FG, et al. Role of operculoinsular cortices in human pain processing: converging evidence from PET, fMRI, dipole modeling, and intracerebral recordings of evoked potentials. Neuroimage. 2002; 17: 133646.CrossRefGoogle ScholarPubMed
65. Vogel, H, Port, JD, Lenz, FA., Solaiyappan, M, Krauss, G, Treede, RD. Dipole source analysis of laser-evoked subdural potentials recorded from parasylvian cortex in humans. J Neurophysiol. 2003; 89: 305160.CrossRefGoogle ScholarPubMed
66. Bromm, B, Lorenz, J, Scharein, E. Dipole source analysis of brain activity in the assessment of pain. Recent advances in clinical neurophysiology. Amsterdam: Elsevier; 1996. p. 32835.Google Scholar
67. Kanda, M, Nagamine, T, Ikeda, A, Ohara, S, Kunieda, T, Fujiwara, N, et al. Primary somatosensory cortex is actively involved in pain processing in humans. Brain Res. 2000; 853: 2829.CrossRefGoogle Scholar
68. Ploner, M, Schmitz, F, Freund, HJ, Schnitzler, A. Parallel activation of primary and secondary somatosensory cortices in human pain processing. J Neurophysiol. 1999; 81: 31004.CrossRefGoogle ScholarPubMed
69. Schlereth, T, Baumgartner, U, Magerl, W, Stoeter, P, Treede, RD. Left-hemisphere dominance in early nociceptive processing in the human parasylvian cortex. Neuroimage. 2003; 20: 44154.CrossRefGoogle ScholarPubMed
70. Tarkka, IM, Treede, RD. Equivalent electrical source analysis of pain-related somatosensory evoked potentials elicited by a CO2 laser. J Clin Neurophysiol. 1993; 10: 5139.CrossRefGoogle ScholarPubMed