Pinprick-evoked brain potentials: A novel tool to assess central sensitization of nociceptive pathways in humans

Journal of Neurophysiology

Volumn 110, Issue 5, 2013, Pages 1107-1116

  Iannetti, G D ^a   Baumgartner U ^b   Tracey, I ^c   Treede, R D ^b   Magerl, W ^b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Central sensitization; Electrophysiology; Human; Neuropathic pain; Pain

Indexed keywords

CAPSAICIN;

ADULT; ARTICLE; BRAIN DEPTH STIMULATION; CLINICAL ARTICLE; ELECTROPHYSIOLOGY; FEMALE; HUMAN; HYPERALGESIA; MALE; NEUROPATHIC PAIN; PINPRICK EVOKED BRAIN POTENTIAL; PRIORITY JOURNAL; SENSITIZATION; SOMATOSENSORY SYSTEM; SPINOTHALAMIC TRACT;

EID: 84883405912     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00774.2012     Document Type: Article

References (56)

1. Andrew D, Craig AD. Quantitative responses of spinothalamic lamina I neurones to graded mechanical stimulation in the cat. J Physiol 545: 913-931, 2002.
2. Andrew D, Greenspan JD. Modality-specific hyper-responsivity of regenerated cat cutaneous nociceptors. J Physiol 516: 897-906, 1999.
3. Baumann TK, Simone DA, Shain CN, LaMotte RH. Neurogenic hyperalgesia: the search for the primary cutaneous afferent fibers that contribute to capsaicin-induced pain and hyperalgesia. J Neurophysiol 66: 212-227, 1991.
4. Baumgärtner U, Magerl W, Klein T, Hopf HC, Treede RD. Neurogenic hyperalgesia versus painful hypoalgesia: two distinct mechanisms of neuropathic pain. Pain 96: 141-151, 2002.
5. Bentley DE, Watson A, Treede RD, Barrett G, Youell PD, Kulkarni B, Jones AK. Differential effects on the laser evoked potential of selectively attending to pain localisation versus pain unpleasantness. Clin Neurophysiol 115: 1846-1856, 2004.
6. Bromm B, Treede RD. Laser-evoked cerebral potentials in the assessment of cutaneous pain sensitivity in normal subjects and patients. Rev Neurol (Paris) 147: 625-643, 1991.
7. Casey KL, Beydoun A, Boivie J, Sjolund B, Holmgren H, Leijon G, Morrow TJ, Rosen I. Laser-evoked cerebral potentials and sensory function in patients with central pain. Pain 64: 485-491, 1996.
8. 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, 2008a.
9. Cruccu G, Anand P, Attal N, Garcia-Larrea L, Haanpaa M, Jorum E, Serra J, Jensen TS. EFNS guidelines on neuropathic pain assessment. Eur J Neurol 11: 153-162, 2004.
10. Cruccu G, Gronseth G, Alksne J, Argoff C, Brainin M, Burchiel K, Nurmikko T, Zakrzewska JM. AAN-EFNS guidelines on trigeminal neuralgia management. Eur J Neurol 15: 1013-1028, 2008b.
11. 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.
12. Djouhri L, Lawson SN. Abeta-fiber nociceptive primary afferent neurons: a review of incidence and properties in relation to other afferent A-fiber neurons in mammals. Brain Res Brain Res Rev 46: 131-145, 2004.
13. Fields HL, Rowbotham M, Baron R. Postherpetic neuralgia: irritable nociceptors and deafferentation. Neurobiol Dis 5: 209-227, 1998.
14. 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 110: 133-145, 1999.
15. Garcia-Larrea L, Convers P, Magnin M, Andre-Obadia N, Peyron R, Laurent B, Mauguiere F. Laser-evoked potential abnormalities in central pain patients: the influence of spontaneous and provoked pain. Brain 125: 2766-2781, 2002.
16. Garcia-Larrea L, Frot M, Valeriani M. Brain generators of laser-evoked potentials: from dipoles to functional significance. Neurophysiol Clin 33: 279-292, 2003.
17. Greenspan JD, McGillis SL. Stimulus features relevant to the perception of sharpness and mechanically evoked cutaneous pain. Somatosens Motor Res 8: 137-147, 1991.
18. Greffrath W, Baumgartner U, Treede RD. Peripheral and central components of habituation of heat pain perception and evoked potentials in humans. Pain 132: 301-311, 2007.
19. Hardy JD, Woolf HG, Goodell H. Experimental evidence on the nature of cutaneous hyperalgesia. J Clin Invest 115-140, 1952.
20. Iannetti GD, Hughes NP, Lee MC, Mouraux A. Determinants of laserevoked EEG responses: pain perception or stimulus saliency? J Neurophysiol 100: 815-828, 2008.
21. Iannetti GD, Zambreanu L, Cruccu G, Tracey I. Operculoinsular cortex encodes pain intensity at the earliest stages of cortical processing as indicated by amplitude of laser-evoked potentials in humans. Neuroscience 131: 199-208, 2005.
22. Jensen TS, Baron R, Haanpaa M, Kalso E, Loeser JD, Rice AS, Treede RD. A new definition of neuropathic pain. Pain 152: 2204-2205, 2011.
23. Jörum E, Warncke T, Stubhaug A. Cold allodynia and hyperalgesia in neuropathic pain: the effect of N-methyl-D-aspartate (NMDA) receptor antagonist ketamine-a double-blind, cross-over comparison with alfentanil and placebo. Pain 101: 229-235, 2003.
24. Jung TP, Makeig S, Westerfield M, Townsend J, Courchesne E, Sejnowski TJ. Analysis and visualization of single-trial event-related potentials. Hum Brain Mapp 14: 166-185, 2001.
25. Klein T, Magerl W, Rolke R, Treede RD. Human surrogate models of neuropathic pain. Pain 115: 227-233, 2005.
26. LaMotte RH, Shain CN, Simone DA, Tsai EF. Neurogenic hyperalgesia: psychophysical studies of underlying mechanisms. J Neurophysiol 66: 190-211, 1991.
27. Lavand'homme PM, Roelants F, Waterloos H, Collet V, De Kock MF. An evaluation of the postoperative antihyperalgesic and analgesic effects of intrathecal clonidine administered during elective cesarean delivery. Anesth Analg 107: 948-955, 2008.
28. Lawson SN. Phenotype and function of somatic primary afferent nociceptive neurones with C-, Adelta-or Aalpha/beta-fibres. Exp Physiol 87: 239-244, 2002.
29. Legrain V, Guerit JM, Bruyer R, Plaghki L. Attentional modulation of the nociceptive processing into the human brain: selective spatial attention, probability of stimulus occurrence, and target detection effects on laser evoked potentials. Pain 99: 21-39, 2002.
30. Lewis T. Experiments relating to cutaneous hyperalgesia and its spread through somatic nerves. Clin Sci 373-421, 1936.
31. Madsen CS, Johnsen B, Fuglsang-Frederiksen A, Jensen TS, Finnerup NB. The effect of nerve compression and capsaicin on contact heat-evoked potentials related to Adelta-and C-fibers. Neuroscience 223: 92-101, 2012a.
32. Madsen CS, Johnsen B, Fuglsang-Frederiksen A, Jensen TS, Finnerup NB. Increased contact heat pain and shortened latencies of contact heat evoked potentials following capsaicin-induced heat hyperalgesia. Clin Neurophysiol 123: 1429-1436, 2012b.
33. Magerl W, Fuchs PN, Meyer RA, Treede RD. Roles of capsaicin-insensitive nociceptors in cutaneous pain and secondary hyperalgesia. Brain 124: 1754-1764, 2001.
34. Magerl W, Wilk SH, Treede RD. Secondary hyperalgesia and perceptual wind-up following intradermal injection of capsaicin in humans. Pain 74: 257-268, 1998.
35. Maier C, Baron R, Tolle TR, Binder A, Birbaumer N, Birklein F, Gierthmuhlen J, Flor H, Geber C, Huge V, Krumova EK, Landwehrmeyer GB, Magerl W, Maihofner C, Richter H, Rolke R, Scherens A, Schwarz A, Sommer C, Tronnier V, Uceyler N, Valet M, Wasner G, Treede RD. Quantitative sensory testing in the German Research Network on Neuropathic Pain (DFNS): somatosensory abnormalities in 1236 patients with different neuropathic pain syndromes. Pain 150: 439-450, 2010.
36. Maxwell SE. Sample size and multiple regression analysis. Psychol Methods 5: 434-458, 2000.
37. Meyer RA, Treede RD. Mechanisms of secondary hyperalgesia: a role for myelinated nociceptors in punctate hyperalgesia. In: Hyperalgesia: Molecular Mechanisms and Clinical Implications, edited by Brune K, Handwerker HO. Seattle, WA: IASP, 2004.
38. Mouraux A, Iannetti GD. Across-trial averaging of event-related EEG responses and beyond. Magn Reson Imaging 26: 1041-1054, 2008.
39. Mouraux A, Iannetti GD. Nociceptive laser-evoked brain potentials do not reflect nociceptive-specific neural activity. J Neurophysiol 101: 3258-3269, 2009.
40. Mouraux A, Iannetti GD, Plaghki L. Low intensity intra-epidermal electrical stimulation can activate Adelta-nociceptors selectively. Pain 150: 199-207, 2010.
41. 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, 2004.
42. Ringkamp M, Peng YB, Wu G, Hartke TV, Campbell JN, Meyer RA. Capsaicin responses in heat-sensitive and heat-insensitive A-fiber nociceptors. J Neurosci 21: 4460-4468, 2001.
43. Simone DA, Sorkin LS, Oh U, Chung JM, Owens C, LaMotte RH, Willis WD. Neurogenic hyperalgesia: central neural correlates in responses of spinothalamic tract neurons. J Neurophysiol 66: 228-246, 1991.
44. Slugg RM, Meyer RA, Campbell JN. Response of cutaneous A-and C-fiber nociceptors in the monkey to controlled-force stimuli. J Neurophysiol 83: 2179-2191, 2000.
45. Spiegel J, Hansen C, Baumgartner U, Hopf HC, Treede RD. Sensitivity of laser-evoked potentials versus somatosensory evoked potentials in patients with multiple sclerosis. Clin Neurophysiol 114: 992-1002, 2003.
46. Spiegel J, Hansen C, Treede RD. Clinical evaluation criteria for the assessment of impaired pain sensitivity by thulium-laser evoked potentials. Clin Neurophysiol 111: 725-735, 2000.
47. Stiasny-Kolster K, Magerl W, Oertel WH, Moller JC, Treede RD. Static mechanical hyperalgesia without dynamic tactile allodynia in patients with restless legs syndrome. Brain 127: 773-782, 2004.
48. Szolcsanyi J, Anton F, Reeh PW, Handwerker HO. Selective excitation by capsaicin of mechano-heat sensitive nociceptors in rat skin. Brain Res 446: 262-268, 1988.
49. Tarkka IM, Treede RD. Equivalent electrical source analysis of pain-related somatosensory evoked potentials elicited by a CO2 laser. J Clin Neurophysiol 10: 513-519, 1993.
50. Torebjork HE, Lundberg LE, LaMotte RH. Central changes in processing of mechanoreceptive input in capsaicin-induced secondary hyperalgesia in humans. J Physiol 448: 765-780, 1992.
51. Treede RD, Kief S, Holzer T, Bromm B. Late somatosensory evoked cerebral potentials in response to cutaneous heat stimuli. Electroencephalogr Clin Neurophysiol 70: 429-441, 1988.
52. Treede RD, Lorenz J, Baumgärtner U. Clinical usefulness of laser-evoked potentials. Neurophysiol Clin 33: 303-314, 2003.
53. Treede RD, Meyer RA, Campbell JN. Myelinated mechanically insensitive afferents from monkey hairy skin: heat-response properties. J Neurophysiol 80: 1082-1093, 1998.
54. Valeriani M, Arendt-Nielsen L, Le Pera D, Restuccia D, Rosso T, De Armas L, Maiese T, Fiaschi A, Tonali P, Tinazzi M. Short-term plastic changes of the human nociceptive system following acute pain induced by capsaicin. Clin Neurophysiol 114: 1879-1890, 2003.
55. Wu Q, Garcia-Larrea L, Mertens P, Beschet A, Sindou M, Mauguiere F. Hyperalgesia with reduced laser evoked potentials in neuropathic pain. Pain 80: 209-214, 1999.
56. Ziegler EA, Magerl W, Meyer RA, Treede RD. Secondary hyperalgesia to punctate mechanical stimuli. Central sensitization to A-fibre nociceptor input. Brain 122: 2245-2257, 1999.