Unmasking the obligatory components of nociceptive event-related brain potentials

Journal of Neurophysiology

Volumn 110, Issue 10, 2013, Pages 2312-2324

  Mouraux, A ^a   De Paepe, A L ^b   Marot, E ^a   Plaghki, L ^a   Iannetti, G D ^c   Legrain, V ^a,b  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Event related potentials; Intraepidermal stimulation; Laser evoked potentials; Nociception; Pain; Primary somatosensory cortex

Indexed keywords

ADULT; AROUSAL; ARTICLE; ATTENTION; BRAIN REGION; CINGULATE GYRUS; COGNITION; ELECTROSTIMULATION; EVENT RELATED POTENTIAL; EVOKED SOMATOSENSORY RESPONSE; FEMALE; HUMAN; HUMAN EXPERIMENT; INSULA; MALE; NOCICEPTION; NORMAL HUMAN; PAIN RECEPTOR; PRIORITY JOURNAL; SIGNAL NOISE RATIO; TRANSCUTANEOUS NERVE STIMULATION;

EVENT-RELATED POTENTIALS; INTRAEPIDERMAL STIMULATION; LASER-EVOKED POTENTIALS; NOCICEPTION; PAIN; PRIMARY SOMATOSENSORY CORTEX;

ADULT; ANIMALS; BRAIN; ELECTRIC STIMULATION; EVOKED POTENTIALS, SOMATOSENSORY; FEMALE; HUMANS; MALE; NOCICEPTION; NOCICEPTORS; YOUNG ADULT;

EID: 84887603481     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00137.2013     Document Type: Article

References (76)

1. Baumgartner U, Vogel H, Ohara S, Treede RD, Lenz F. Dipole source analyses of laser evoked potentials obtained from subdural grid recordings from primary somatic sensory cortex. J Neurophysiol 106: 722-730, 2011.
2. Beckmann CF, Smith SA. Probabilistic independent component analysis for functional magnetic resonance imaging. IEEE Trans Med Imaging 23: 137-152, 2004.
3. Bell AJ, Sejnowski TJ. An information-maximization approach to blind separation and blind deconvolution. Neural Comput 7: 1129-1159, 1995.
4. Boly M, Faymonville ME, Schnakers C, Peigneux P, Lambermont B, Phillips C, Lancellotti P, Luxen A, Lamy M, Moonen G, Maquet P, Laureys S. Perception of pain in the minimally conscious state with PET activation: an observational study. Lancet Neurol 7: 1013-1020, 2008.
5. Brooks J, Tracey I. From nociception to pain perception: imaging the spinal and supraspinal pathways. J Anat 207: 19-33, 2005.
6. Bushnell MC, Apkarian AV (Editors). Textbook of Pain. London: Churchill Livingstone, 2005, p. 267-289.
7. Carmon A, Mor J, Goldberg J. Evoked cerebral responses to noxious thermal stimuli in humans. Exp Brain Res 25: 103-107, 1976.
8. Cheng Y, Lin CP, Liu HL, Hsu YY, Lim KE, Hung D, Decety J. Expertise modulates the perception of pain in others. Curr Biol 17: 1708-1713, 2007.
9. Colon E, Nozaradan S, Legrain V, Mouraux A. Steady-state evoked potentials to tag specific components of nociceptive cortical processing. Neuroimage 60: 571-581, 2012.
10. Cruccu G, Aminoff MJ, Curio G, Guerit JM, Kakigi R, Mauguiere F, Rossini PM, Treede RD, Garcia-Larrea L. Recommendations for the clinical use of somatosensory-evoked potentials. Clin Neurophysiol 119: 1705-1719, 2008.
11. Davis PA. Effects of acoustic stimuli on the waking human. J Neurophysiol 2: 494-499, 1939.
12. 2laser stimulation. Clin Neurophysiol 122: 2482-2487, 2011.
13. Delorme A, Makeig S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134: 9-21, 2004.
14. Dum RP, Levinthal DJ, Strick PL. The spinothalamic system targets motor and sensory areas in the cerebral cortex of monkeys. J Neurosci 29: 14223-14235, 2009.
15. Durka PJ, Zygierewicz J, Klekowicz H, Ginter J, Blinowska KJ. On the statistical significance of event-related EEG desynchronization and synchronization in the time-frequency plane. IEEE Trans Biomed Eng 51: 1167-1175, 2004.
16. Frot M, Magnin M, Mauguiere F, Garcia-Larrea L. Cortical representation of pain in primary sensory-motor areas (S1/M1)-a study using intracortical recordings in humans. Hum Brain Mapp 34: 2655-2668, 2013.
17. Fuchs M, Kastner J, Wagner M, Hawes S, Ebersole JS. A standardized boundary element method volume conductor model. Clin Neurophysiol 113: 702-712, 2002.
18. Garcia-Larrea L. Somatosensory volleys and cortical evoked potentials: "first come, first served"? Pain 112: 5-7, 2004.
19. Garcia-Larrea L, Frot M, Valeriani M. Brain generators of laser-evoked potentials: from dipoles to functional significance. Neurophysiol Clin 33: 279-292, 2003.
20. Hu L, Zhang ZG, Hu Y. A time-varying source connectivity approach to reveal human somatosensory information processing. Neuroimage 62: 217-228, 2012.
21. Iannetti GD, Hughes NP, Lee MC, Mouraux A. Determinants of laserevoked EEG responses: pain perception or stimulus saliency? J Neurophysiol 100: 815-828, 2008.
22. Iannetti GD, Mouraux A. From the neuromatrix to the pain matrix (and back). Exp Brain Res 205: 1-12, 2010.
23. Ingvar M. Pain and functional imaging. Philos Trans R Soc Lond B Biol Sci 354: 1347-1358, 1999.
24. Inui K, Tran TD, Hoshiyama M, Kakigi R. Preferential stimulation of Adelta fibers by intra-epidermal needle electrode in humans. Pain 96: 247-252, 2002.
25. Inui K, Tran TD, Qiu Y, Wang X, Hoshiyama M, Kakigi R. A comparative magnetoencephalographic study of cortical activations evoked by noxious and innocuous somatosensory stimulations. Neuroscience 120: 235-248, 2003a.
26. Inui K, Tsuji T, Kakigi R. Temporal analysis of cortical mechanisms for pain relief by tactile stimuli in humans. Cereb Cortex 16: 355-365, 2006.
27. Inui K, Wang X, Qiu Y, Nguyen BT, Ojima S, Tamura Y, Nakata H, Wasaka T, Tran TD, Kakigi R. Pain processing within the primary somatosensory cortex in humans. Eur J Neurosci 18: 2859-2866, 2003b.
28. Jones A. The pain matrix and neuropathic pain. Brain 121: 783-784, 1998.
29. Jung TP, Makeig S, Humphries C, Lee TW, McKeown MJ, Iragui V, Sejnowski TJ. Removing electroencephalographic artifacts by blind source separation. Psychophysiology 37: 163-178, 2000.
30. Kakigi R, Inui K, Tamura Y. Electrophysiological studies on human pain perception. Clin Neurophysiol 116: 743-763, 2005.
31. Kanda M, Nagamine T, Ikeda A, Ohara S, Kunieda T, Fujiwara N, Yazawa S, Sawamoto N, Matsumoto R, Taki W, Shibasaki H. Primary somatosensory cortex is actively involved in pain processing in human. Brain Res 853: 282-289, 2000.
32. Kaube H, Katsarava Z, Kaufer T, Diener H, Ellrich J. A new method to increase nociception specificity of the human blink reflex. Clin Neurophysiol 111: 413-416, 2000.
33. Kenshalo DR, Iwata K, Sholas M, Thomas DA. Response properties and organization of nociceptive neurons in area 1 of monkey primary somatosensory cortex. J Neurophysiol 84: 719-729, 2000.
34. Kunde V, Treede RD. Topography of middle-latency somatosensory evoked potentials following painful laser stimuli and non-painful electrical stimuli. Electroencephalogr Clin Neurophysiol 88: 280-289, 1993.
35. Legatt AD, Kader A. Topography of the initial cortical component of the median nerve somatosensory evoked potential. Relationship to central sulcus anatomy. J Clin Neurophysiol 17: 321-325, 2000.
36. Legrain V, Iannetti GD, Plaghki L, Mouraux A. The pain matrix reloaded: a salience detection system for the body. Prog Neurobiol 93: 111-124, 2011.
37. Legrain V, Mancini F, Sambo CF, Torta DM, Ronga I, Valentini E. Cognitive aspects of nociception and pain: bridging neurophysiology with cognitive psychology. Neurophysiol Clin 42: 325-336, 2012.
38. Liang M, Mouraux A, Chan V, Blakemore C, Iannetti GD. Functional characterisation of sensory ERPs using probabilistic ICA: effect of stimulus modality and stimulus location. Clin Neurophysiol 121: 577-587, 2010.
39. Liang M, Mouraux A, Iannetti GD. Bypassing primary sensory cortices-a direct thalamocortical pathway for transmitting salient sensory information. Cereb Cortex 23: 1-11, 2013.
40. Makeig S, Jung TP, Bell AJ, Ghahremani D, Sejnowski TJ. Blind separation of auditory event-related brain responses into independent components. Proc Natl Acad Sci USA 94: 10979-10984, 1997.
41. Minka TP. Automatic choice of dimensionality for PCA. Adv Neural Inform Process Syst 13: 598-604, 2001.
42. Moisset X, Bouhassira D. Brain imaging of neuropathic pain. Neuroimage 37, Suppl 1: S80-S88, 2007.
43. Mouraux A, Guerit JM, Plaghki L. Refractoriness cannot explain why C-fiber laser-evoked brain potentials are recorded only if concomitant Adelta-fiber activation is avoided. Pain 112: 16-26, 2004.
44. Mouraux A, Iannetti GD. Across-trial averaging of event-related EEG responses and beyond. Magn Reson Imaging 26: 1041-1054, 2008.
45. Mouraux A, Iannetti GD. Nociceptive laser-evoked brain potentials do not reflect nociceptive-specific neural activity. J Neurophysiol 101: 3258-3269, 2009.
46. Mouraux A, Iannetti GD, Colon E, Nozaradan S, Legrain V, Plaghki L. Nociceptive steady-state evoked potentials elicited by rapid periodic thermal stimulation of cutaneous nociceptors. J Neurosci 31: 6079-6087, 2011.
47. Mouraux A, Iannetti GD, Plaghki L. Low intensity intra-epidermal electrical stimulation can activate Adelta-nociceptors selectively. Pain 150: 199-207, 2010.
48. 2laser stimuli in humans. Eur J Pain 7: 189-199, 2003.
49. Nakata H, Tamura Y, Sakamoto K, Akatsuka K, Hirai M, Inui K, Hoshiyama M, Saitoh Y, Yamamoto T, Katayama Y, Kakigi R. Evoked magnetic fields following noxious laser stimulation of the thigh in humans. Neuroimage 42: 858-868, 2008.
50. Ohara S, Crone NE, Weiss N, Treede RD, Lenz FA. Amplitudes of laser evoked potential recorded from primary somatosensory, parasylvian and medial frontal cortex are graded with stimulus intensity. Pain 110: 318-328, 2004a.
51. Ohara S, Crone NE, Weiss N, Treede RD, Lenz FA. Cutaneous painful laser stimuli evoke responses recorded directly from primary somatosensory cortex in awake humans. J Neurophysiol 91: 2734-2746, 2004b.
52. Perchet C, Frot M, Charmarty A, Flores C, Mazza S, Magnin M, Garcia-Larrea L. Do we activate specifically somatosensory thin fibres with the concentric planar electrode? A scalp and intracranial EEG study. Pain 153: 1244-1252, 2012.
53. Peyron R, Frot M, Schneider F, Garcia-Larrea L, Mertens P, Barral FG, Sindou M, Laurent B, Mauguiere F. Role of operculoinsular cortices in human pain processing: converging evidence from PET, fMRI, dipole modeling, and intracerebral recordings of evoked potentials. Neuroimage 17: 1336-1346, 2002.
54. Plaghki L, Mouraux A. How do we selectively activate skin nociceptors with a high power infrared laser? Physiology and biophysics of laser stimulation. Neurophysiol Clin 33: 269-277, 2003.
55. Plaghki L, Mouraux A. EEG and laser stimulation as tools for pain research. Curr Opin Investig Drugs 6: 58-64, 2005.
56. Ploner M, Schmitz F, Freund HJ, Schnitzler A. Differential organization of touch and pain in human primary somatosensory cortex. J Neurophysiol 83: 1770-1776, 2000.
57. Rajan JJ, Rayner PJ. Model order selection for the singular value decomposition and the discrete Karhunen-Loeve transform using a Bayesian approach. IEE Proc Vision Image Signal Process 144: 116-123, 1997.
58. Regan D. Human Brain Electrophysiology: Evoked Potentials and Evoked Magnetic Fields in Science and Medicine. New York: Elsevier, 1989.
59. Schlereth T, Baumgartner U, Magerl W, Stoeter P, Treede RD. Lefthemisphere dominance in early nociceptive processing in the human parasylvian cortex. Neuroimage 20: 441-454, 2003.
60. Singer T, Seymour B, O'Doherty J, Kaube H, Dolan RJ, Frith CD. Empathy for pain involves the affective but not sensory components of pain. Science 303: 1157-1162, 2004.
61. Stern J, Jeanmonod D, Sarnthein J. Persistent EEG overactivation in the cortical pain matrix of neurogenic pain patients. Neuroimage 31: 721-731, 2006.
62. Stowell H. Event related brain potentials and human pain: a first objective overview. Int J Psychophysiol 1: 137-151, 1984.
63. 2laser. J Clin Neurophysiol 10: 513-519, 1993.
64. 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 86: 1499-1503, 2001.
65. Tommerdahl M, Delemos KA, Vierck CJ Jr, Favorov OV, Whitsel BL. Anterior parietal cortical response to tactile and skin-heating stimuli applied to the same skin site. J Neurophysiol 75: 2662-2670, 1996.
66. Treede RD, Kenshalo DR, Gracely RH, Jones AK. The cortical representation of pain. Pain 79: 105-111, 1999.
67. Treede RD, Kunde V. Middle-latency somatosensory evoked potentials after stimulation of the radial and median nerves: component structure and scalp topography. J Clin Neurophysiol 12: 291-301, 1995.
68. Valentini E, Hu L, Chakrabarti B, Hu Y, Aglioti SM, Iannetti GD. The primary somatosensory cortex largely contributes to the early part of the cortical response elicited by nociceptive stimuli. Neuroimage 59: 1571-1581, 2012.
69. 2laser evoked potentials: an intracerebral recording study. Clin Neurophysiol 115: 211-216, 2004.
70. Valeriani M, Betti V, Le Pera D, De Armas L, Miliucci R, Restuccia D, Avenanti A, Aglioti SM. Seeing the pain of others while being in pain: a laser-evoked potentials study. Neuroimage 40: 1419-1428, 2008.
71. Vierck CJ, Whitsel BL, Favorov OV, Brown AW, Tommerdahl M. Role of primary somatosensory cortex in the coding of pain. Pain 154: 334-344, 2013.
72. Wang AL, Mouraux A, Liang M, Iannetti GD. Stimulus novelty, and not neural refractoriness, explains the repetition suppression of laser-evoked potentials. J Neurophysiol 104: 2116-2124, 2010.
73. Wang X, Inui K, Kakigi R. Early cortical activities evoked by noxious stimulation in humans. Exp Brain Res 180: 481-489, 2007.
74. Whitsel BL, Favorov OV, Li Y, Quibrera M, Tommerdahl M. Area 3a neuron response to skin nociceptor afferent drive. Cereb Cortex 19: 349-366, 2009.
75. Whyte J. Clinical implications of the integrity of the pain matrix. Lancet Neurol 7: 979-980, 2008.
76. Woody C. Characterization of an adaptive filter for the analysis of variable latency neuroelectric signals. Med Biol Eng 5: 539-553, 1967.