Analysis of hyperalgesia time courses in humans after painful electrical high-frequency stimulation identifies a possible transition from early to late LTP-like pain plasticity

Pain

Volumn 152, Issue 7, 2011, Pages 1532-1539

  Pfau, Doreen B ^a   Klein, Thomas ^a   Putzer, Daniel ^b   Pogatzki Zahn, Esther M ^b   Treede, Rolf Detlef ^a   Magerl, Walter ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY HOSPITAL MÜNSTER   (Germany)

Author keywords

Central sensitization; Chronic pain; Early LTP; Late LTP; Long term potentiation; LTP; LTP1; LTP2; Persistent pain; Secondary hyperalgesia

Indexed keywords

ADULT; ALLODYNIA; ARTICLE; DYNAMIC MECHANICAL ALLODYNIA; ELECTROSTIMULATION; FEMALE; HUMAN; HUMAN EXPERIMENT; HYPERALGESIA; LONG TERM POTENTIATION; MALE; NOCICEPTION; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; SENSITIZATION; SKIN STIMULATION;

ADULT; BIOPHYSICAL PROCESSES; ELECTRIC STIMULATION; FEMALE; HUMANS; HYPERALGESIA; LIKELIHOOD FUNCTIONS; LONG-TERM POTENTIATION; MALE; PAIN MEASUREMENT; PAIN THRESHOLD; STATISTICS AS TOPIC; TIME FACTORS; YOUNG ADULT;

EID: 79958754583     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2011.02.037     Document Type: Article

References (49)

1. Abel T, Nguyen PV. Regulation of hippocampus-dependent memory by cyclic AMP-dependent protein kinase. Prog Brain Res 2008;169:97-115. (Pubitemid 351454062)
2. Abraham WC. How long will long-term potentiation last? Phil Trans R Soc Lond B Biol Sci 2003;358:735-44.
3. Abraham WC, Logan B, Greenwood JM, Dragunow M. Induction and experience-dependent consolidation of stable long-term potentiation lasting months in the hippocampus. J Neurosci 2002;22:9626-34. (Pubitemid 35356205)
4. Anderson TW. R.A. Fisher and multivariate analysis. Stat Sci 1996;11:20-34.
5. Basbaum AI, Braz JM, Ossipov MH, Porreca F. The endogenous neuromodulation system. In: Krames ES, Peckham PH, Rezai AR, editors. Neuromodulation. Amsterdam: Elsevier; 2009. p. 303-12.
6. Baumgärtner U, Magerl W, Klein T, Hopf HC, Treede RD. Neurogenic hyperalgesia versus painful hypoalgesia: two distinct mechanisms of neuropathic pain. Pain 2002;96:141-51. (Pubitemid 34272290)
7. Bear MF, Malenka RC. Synaptic plasticity: LTP and LTD. Curr Opin Neurobiol 1994;4:389-99. (Pubitemid 24194277)
8. Bliss TV, Gardner-Medwin AR. Long-lasting potentiation of synaptic transmission in the dentate area of the unanaestetized rabbit following stimulation of the perforant path. J Physiol 1973;232:357-74.
9. Bramham CR, Alme MN, Bittins M, Kuipers SD, Nair RR, Pai B, Panja D, Schubert M, Soule J, Tiron A, Wibrand K. The arc of synaptic memory. Exp Brain Res 2010;200:125-40.
10. Cooke SF, Bliss TV. Plasticity in the human central nervous system. Brain 2006;129:1659-73. (Pubitemid 43999401)
11. Hansen N, Klein T, Magerl W, Treede RD. Psychophysical evidence for long-term potentiation of C-fiber and Adelta-fiber pathways in humans by analysis of pain descriptors. J Neurophysiol 2007;97:2559-63. (Pubitemid 46411185)
12. Ikeda H, Heinke B, Ruscheweyh R, Sandkühler J. Synaptic plasticity in spinal lamina I projection neurons that mediate hyperalgesia. Science 2003;299:1237-40. (Pubitemid 36237466)
13. Inui K, Tran TD, Hoshiyama M, Kakigi R. Preferential stimulation of A delta fibers by intra-epidermal needle electrode in humans. Pain 2002;96:247-52. (Pubitemid 34327870)
14. Ji RR, Kohno T, Moore KA, Woolf CJ. Central sensitization and LTP: do pain and memory share similar mechanisms? Trends Neurosci 2003;26:696-705.
15. Jung K, Rottmann S, Ellrich J. Long-term depression of spinal nociception and pain in man: influence of varying stimulation parameters. Eur J Pain 2009;13:161-70.
16. Klein T, Magerl W, Treede RD. Perceptual correlate of nociceptive long-term potentiation (LTP) in humans shares the time course of early-LTP. J Neurophysiol 2006;96:3551-5. (Pubitemid 44837897)
17. Klein T, Magerl W, Rolke R, Treede RD. Human surrogate models of neuropathic pain. Pain 2005;115:227-33. (Pubitemid 40725278)
18. Klein T, Stahn S, Magerl W, Treede RD. The role of heterosynaptic facilitation in long-term potentiation (LTP) of human pain sensation. Pain 2008;139:507-19.
19. Klein T, Magerl W, Hopf HC, Sandkühler J, Treede RD. Perceptual correlates of nociceptive long-term potentiation and long-term depression in humans. J Neurosci 2004;24:964-71. (Pubitemid 38146607)
20. Klein T, Magerl W, Nickel U, Hopf HC, Sandkühler J, Treede RD. Effects of the NMDA-receptor antagonist ketamine on perceptual correlates of long-term potentiation within the nociceptive system. Neuropharmacology 2007;52:655-61. (Pubitemid 46123376)
21. Koltzenburg M, Lundberg LE, Torebjörk HE. Dynamic and static components of mechanical hyperalgesia in human hairy skin. Pain 1992;51:207-19.
22. Koltzenburg M, Torebjörk HE, Wahren LK. Nociceptor modulated central sensitization causes mechanical hyperalgesia in acute chemogenic and chronic neuropathic pain. Brain 1994;117:579-91. (Pubitemid 24225905)
23. LaMotte RH, Shain CN, Simone DA, Tsai EF. Neurogenic hyperalgesia: psychophysical studies of underlying mechanisms. J Neurophysiol 1991;66:190-211.
24. Latremoliere A, Woolf CJ. Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J Pain 2009;10:895-926.
25. Liu XG, Morton CR, Azkue JJ, Zimmermann M, Sandkühler J. Long-term depression of C-fibre-evoked spinal field potentials by stimulation of primary afferent A delta-fibres in the adult rat. Eur J Neurosci 1998;10:3069-75.
26. Magerl W, Klein T. Experimental human models of neuropathic pain. Handb Clin Neurol 2006;81:503-16.
27. Magerl W, Wilk SH, Treede RD. Secondary hyperalgesia and perceptual wind-up following intradermal injection of capsaicin in humans. Pain 1998;74:257-68. (Pubitemid 28081612)
28. Magerl W, Fuchs PN, Meyer RA, Treede RD. Roles of capsaicin-insensitive nociceptors in cutaneous pain and secondary hyperalgesia. Brain 2001;124:1754-64. (Pubitemid 32845437)
29. Magerl W, Ali Z, Ellrich J, Meyer RA, Treede RD. C- and A delta-fiber components of heat-evoked cerebral potentials in healthy human subjects. Pain 1999;82:127-37. (Pubitemid 29317525)
30. Malenka RC, Bear MF. LTP and LTD: an embarrassment of riches. Neuron 2004;44:5-21. (Pubitemid 39348827)
31. Nguyen PV, Abel T, Kandel ER. Requirement of a critical period of transcription for induction of a late phase of LTP. Science. 1994;265:1104-7. (Pubitemid 24293080)
32. Nilsson HJ, Schouenborg J. Differential inhibitory effect on human nociceptive skin senses induced by local stimulation of thin cutaneous fibers. Pain 1999;80:103-12. (Pubitemid 29151694)
33. Pastalkova E, Serrano P, Pinkhasova D, Wallace E, Fenton AA, Sacktor TC. Storage of spatial information by the maintenance mechanism of LTP. Science 2006;313:1141-4.
34. Pertovaara A. A neuronal correlate of secondary hyperalgesia in the rat spinal dorsal horn is submodality selective and facilitated by supraspinal influence. Exp Neurol 1998;149:193-202. (Pubitemid 28091028)
35. Plath N, Ohana O, Dammermann B, Errington ML, Schmitz D, Gross C, Mao X, Engelsberg A, Mahlke C, Welzl H, Kobalz U, Stawrakakis A, Fernandez E, Waltereit R, Bick-Sander A, Therstappen E, Cooke SF, Blanquet V, Wurst W, Salmen B, Bosl MR, Lipp HP, Grant SG, Bliss TV, Wolfer DP, Kuhl D. Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories. Neuron 2006;52:437-44. (Pubitemid 44755254)
36. Racine RJ, Milgram NW, Hafner S. Long-term potentiation phenomena in the rat limbic forebrain. Brain Res 1983;260:217-31. (Pubitemid 13181989)
37. Raja SN, Campbell JN, Meyer RA. Evidence for different mechanisms of primary and secondary hyperalgesia following heat injury to the glabrous skin. Brain 1984;107:1179-88. (Pubitemid 15182103)
38. Randic M, Jiang MC, Cerne R. Long-term potentiation and long-term depression of primary afferent neurotransmission in the rat spinal cord. J Neurosci 1993;13:5228-41. (Pubitemid 24001008)
39. Sacktor TC. PKMzeta, LTP maintenance, and the dynamic molecular biology of memory storage. Prog Brain Res 2008;169:27-40.
40. Sandkühler J. Models and mechanisms of hyperalgesia and allodynia. Physiol Rev 2009;89:707-58.
41. Schmelz M, Schmid R, Handwerker HO, Torebjörk HE. Encoding of burning pain from capsaicin-treated human skin in two categories of unmyelinated nerve fibres. Brain 2000;123:560-71. (Pubitemid 30099540)
42. Schmidt R, Schmelz M, Forster C, Ringkamp M, Torebjörk HE, Handwerker H. Novel classes of responsive and unresponsive C nociceptors in human skin. J Neurosci 1995;15:333-41.
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 1991;66:228-46.
44. Wang Y, Wu J, Wu Z, Lin Q, Yue Y, Fang L. Regulation of AMPA receptors in spinal nociception. Mol Pain 2010;6:5.
45. Woolf CJ. Evidence for a central component of post-injury pain hypersensitivity. Nature 1983;306:686-8. (Pubitemid 14201852)
46. Yang HW, Hu XD, Zhang HM, Xin WJ, Li MT, Zhang T, Zhou LJ, Liu XG. Roles of CaMKII, PKA, and PKC in the induction and maintenance of LTP of C-fiber-evoked field potentials in rat spinal dorsal horn. J Neurophysiol 2004;91:1122-33. (Pubitemid 38250397)
47. Yashiro K, Philpot BD. Regulation of NMDA receptor subunit expression and its implications for LTD, LTP, and metaplasticity. Neuropharmacology 2008;55:1081-94.
48. You HJ, Tjolsen A, Arendt-Nielsen L. High-frequency conditioning electrical stimulation evokes supraspinal independent long-term depression but not long-term potentiation of the spinal withdrawal reflex in rats. Brain Res 2006;1090:116-22. (Pubitemid 43817940)
49. Ziegler EA, Magerl W, Meyer RA, Treede RD. Secondary hyperalgesia to punctate mechanical stimuli. Central sensitization to A-fibre nociceptor input. Brain 1999;122:2245-57.