Perceptual Correlates of Nociceptive Long-Term Potentiation and Long-Term Depression in Humans

Journal of Neuroscience

Volumn 24, Issue 4, 2004, Pages 964-971

  Klein, Thomas ^a   Magerl, Walter ^a   Hopf, Hanns Christian ^a   Sandkühler, Jürgen ^b   Treede, Rolf Detlef ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

Central sensitization; Hyperalgesia; Neuropathic pain; Pain; Pain memory; Spinal cord

Indexed keywords

ADULT; ALLODYNIA; ARTICLE; ELECTROSTIMULATION; FEMALE; HUMAN; HYPERALGESIA; HYPOALGESIA; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; MECHANICAL PROBE; NERVE CELL PLASTICITY; NEUROPATHIC PAIN; NOCICEPTION; NOCICEPTIVE STIMULATION; NORMAL HUMAN; PAIN; PAIN ASSESSMENT; PEPTIDERGIC NERVOUS SYSTEM; PRIORITY JOURNAL; SENSORY NERVE; TACTILE STIMULATION;

ADULT; ANALYSIS OF VARIANCE; CONDITIONING (PSYCHOLOGY); ELECTRIC STIMULATION; FEMALE; FOREARM; HIPPOCAMPUS; HUMANS; LONG-TERM DEPRESSION (PHYSIOLOGY); LONG-TERM POTENTIATION; MALE; MIDDLE AGED; NEOCORTEX; NEURONAL PLASTICITY; NOCICEPTORS; PAIN; PAIN MEASUREMENT; PAIN THRESHOLD; SENSITIVITY AND SPECIFICITY; SKIN; SPINAL CORD; SYNAPTIC TRANSMISSION;

EID: 0742322851     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1222-03.2004     Document Type: Article

References (63)

1. Ali Z, Meyer RA, Campbell JN (1996) Secondary hyperalgesia to mechanical but not heat stimuli following a capsaicin injection in hairy skin. Pain 68:401-411.
2. Artola A, Singer W (1993) Long-term depression of excitatory synaptic transmission and its relationship to long-term potentiation. Trends Neurosci 16:480-487.
3. Bailey CH, Giustetto M, Huang YY, Hawkins RD, Kandel ER (2000) Is heterosynaptic modulation essential for stabilizing Hebbian plasticity and memory? Nat Rev Neurosci 1:11-20.
4. Baumgärtner U, Magerl W, Klein T, Hopf HC, Treede R-D (2002) Neurogenic hyperalgesia versus painful hypoalgesia: two distinct mechanisms of neuropathic pain. Pain 96:141-151.
5. Bliss TVP, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
6. Brain SD, Williams TJ (1988) Substance P regulates the vasodilator activity of calcitonin gene-related peptide. Nature 335:73-75.
7. Bütefisch CM, Davis BC, Sawaki L, Kopylev L, Classen J, Cohen LG (2000) Mechanisms of use-dependent plasticity in the human motor cortex. Proc Natl Acad Sci USA 97:3661-3665.
8. Chen J, Sandkühler J (2000) Induction of homosynaptic long-term depression at spinal synapses of sensory Aδ-fibers requires activation of metabotropic glutamate receptors. Neuroscience 98:141-148.
9. Dougherty PM, Willis WD (1991) Enhancement of spinothalamic neuron responses to chemical and mechanical stimuli following combined micro-iontophoretic application of N-methyl-D-aspartic acid and substance P. Pain 47:85-93.
10. Dougherty PM, Willis WD, Lenz FA (1998) Transient inhibition of responses to thermal stimuli of spinal sensory tract neurons in monkeys during sensitization by intradermal capsaicin. Pain 77:129-136.
11. Duggan AW, Riley RC, Mark MA, MacMillan SJ, Schaible HG (1995) Afferent volley patterns and the spinal release of immunoreactive substance P in the dorsal horn of the anaesthetized spinal cat. Neuroscience 65:849-858.
12. Fields HL, Rowbotham M, Baron R (1998) Postherpetic neuralgia: irritable nociceptors and deafferentation. Neurobiol Dis 5:209-227.
13. Garrison DW, Foreman RD (1996) Effects of transcutaneous nerve stimulation (TENS) on spontaneous and noxiously evoked dorsal horn cell activity in cats with transacted spinal cords. Neurosci Lett 216:125-128.
14. Gozariu M, Bragard D, Willer JC, Le Bars D (1997) Temporal summation of C-fiber afferent inputs: competition between facilitatory and inhibitory effects on C-fiber reflex in the rat. J Neurophysiol 78:3165-3179.
15. Greenspan JD, McGillis SL (1994) Thresholds for the perception of pressure, sharpness, and mechanically evoked cutaneous pain: effects of laterality and repeated testing. Somatosens Mot Res 11:311-317.
16. Herrero JF, Laird JMA, Lopez-Garcia JA (2000) Wind-up of spinal cord neurones and pain sensation: much ado about something? Prog Neurobiol 61:169-203.
17. Hunt SP, Mantyh PW (2001) The molecular dynamics of pain control. Nat Rev Neurosci 2:83-91.
18. Ikeda H, Sandkühler J (2003) Two forms of synaptic long-term potentiation in ascending pathways. Soc Neurosci Abstr 29:131.
19. Ikeda H, Heinke B, Ruscheweyh R, Sandkühler J (2003) Synaptic plasticity in spinal lamina I projection neurons that mediate hyperalgesia. Science 299:1237-1240.
20. Illich PA, Walters ET (1997) Mechanosensory neurons innervating Aplysia siphon encode noxious stimuli and display nociceptive sensitization. J Neurosci 17:459-469.
21. Inui K, Tran TD, Hoshiyama M, Kakigi R (2002) Preferential stimulation of Adelta fibers by intra-epidermal needle electrode in humans. Pain 96:247-252.
22. Kandel ER (2001) The molecular biology of memory storage: a dialogue between genes and synapses. Science 294:1030-1038.
23. Kemp N, Bashir ZI (2001) Long-term depression: a cascade of induction and expression mechanisms. Prog Neurobiol 65:339-365.
24. Khasabov SG, Rogers SD, Ghilardi JR, Peters CM, Mantyh PW, Simone DA (2002) Spinal neurons that possess the substance P receptor are required for the development of central sensitization. J Neurosci 22:9086-9098.
25. Kilo S, Schmelz M, Koltzenburg M, Handwerker HO (1994) Different patterns of hyperalgesia induced by experimental inflammation in human skin. Brain 117:385-396.
26. Klein T, Magerl W, Hopf H-C, Sandkühler J, Mantzke U, Treede R-D (2002) Long-term potentiation of human pain perception. Tenth World Congress on Pain, San Diego, August.
27. Koppert W, Dern SK, Sittl R, Albrecht S, Schuttler J, Schmelz M (2001) A new model of electrically evoked pain and hyperalgesia in human skin: the effects of intravenous alfentanil, S(+)-ketamine, and lidocaine. Anesthesiology 95:395-402.
28. Laird JMA, Roza C, DeFelipe C, Hunt SP, Cervero F (2001) Role of central and peripheral tachykinin NK1 receptors in capsaicin-induced pain and hyperalgesia in mice. Pain 90:97-103.
29. LaMotte RH, Shain CN, Simone DA, Tsai E-FP (1991) Neurogenic hyperalgesia: psychophysical studies of underlying mechanisms. J Neurophysiol 66:190-211.
30. Leem JW, Willis WD, Weller SC, Chung JM (1993) Differential activation and classification of cutaneous afferents in the rat. J Neurophysiol 70:2411-2424.
31. Liu H, Brown JL, Jasmin L, Maggio JE, Vigna SR, Mantyh PW, Basbaum AI (1994) Synaptic relationship between substance P and the substance P receptor: light and electron microscopic characterization of the mismatch between neuropeptides and their receptors. Proc Natl Acad Sci USA 91:1009-1013.
32. Liu X-G, Sandkühler J (1997) Characterization of long-term potentiation of C-fiber-evoked potentials in spinal dorsal horn of adult rat: essential role of NK1 and NK2 receptors. J Neurophysiol 78:1973-1982.
33. Magerl W, Wilk SH, Treede R-D (1998) Secondary hyperalgesia and perceptual wind-up following intradermal injection of capsaicin in humans. Pain 74:257-268.
34. Magerl W, Fuchs PN, Meyer RA, Treede R-D (2001) Roles of capsaicin-insensitive nociceptors in pain and secondary hyperalgesia. Brain 124:1754-1764.
35. Malinow R (1994) LTP: desperately seeking resolution. Science 266:1195-1196.
36. Mantyh PW, Rogers SD, Honore P, Allen BJ, Ghilardi JR, Li J, Daughters RS, Lappi DA, Wiley RG, Simone DA (1997) Inhibition of hyperalgesia by ablation of lamina I spinal neurons expressing the substance P receptor. Science 278:275-279.
37. Mayer DJ, Price DD, Becker DP (1975) Neurophysiological characterization of the anterolateral spinal cord neurons contributing to pain perception in man. Pain 1:51-58.
38. Meyer RA, Davis KD, Cohen RH, Treede R-D, Campbell JN (1991) Mechanically insensitive afferents (MIAs) in cutaneous nerves of monkey. Brain Res 561:252-261.
39. Miletic G, Miletic V (2000) Long-term changes in sciatic-evoked A-fiber dorsal horn field potentials accompany loose ligation of the sciatic nerve in rats. Pain 84:353-359.
40. Mizuno T, Kanazawa I, Sakurai M (2001) Differential induction of LTP and LTD is not determined solely by instantaneous calcium concentration: an essential involvement of a temporal factor. Eur J Neurosci 14:701-708.
41. Nilsson H-J, Schouenborg J (1999) Differential inhibitory effect on human nociceptive skin senses induced by local stimulation of thin cutaneous fibers. Pain 80:103-112.
42. Nitsche MA, Paulus W (2001) Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology 57:1899-1901.
43. North RB, Kidd DH, Zahurak M, James CS, Long DM (1993) Spinal cord stimulation for chronic, intractable pain: experience over two decades. Neurosurgery 32:384-395.
44. Pertovaara A (1998) A neuronal correlate of secondary hyperalgesia in the rat spinal dorsal horn is submodality selective and facilitated by supraspinal influence. Exp Neurol 149:193-202.
45. Porreca F, Ossipov MH, Gebhart GF (2002) Chronic pain and medullary descending facilitation. Trends Neurosci 25:319-325.
46. Randic M, Jiang MC, Cerne R (1993) Long-term potentiation and long-term depression of primary afferent neurotransmission in the rat spinal cord. J Neurosci 13:5228-5241.
47. Sandkühler J (2000a) Learning and memory in pain pathways. Pain 88:113-118.
48. Sandkühler J (2000b) Long-lasting analgesia following TENS and acupuncture: spinal mechanisms beyond gate control. In: Proceedings of the Ninth World Congress on Pain. Progress in Pain Research and Management, Vol 16 (Devor M, Rowbotham M, Wiesenfeld-Hallin Z, eds), pp 359-369. Seattle: International Association for the Study of Pain.
49. Sandkühler J, Chen JG, Cheng G, Randic M (1997) Low-frequency stimulation of afferent AS-fibers induces long-term depression at primary afferent synapses with substantia gelatinosa neurons in the rat. J Neurosci 17:6483-6491.
50. Schmidt R, Schmelz M, Forster C, Ringkamp M, Torebjörk E, Handwerker H (1995) Novel classes of responsive and unresponsive C nociceptors in human skin. J Neurosci 15:333-341.
51. Simone DA, Sorkin LS, Oh U, Chung JM, Owens C, LaMotte RH, Willis WD (1991) Neurogenic hyperalgesia: central neural correlates in responses of spinothalamic tract neurons. J Neurophysiol 66:228-246.
52. Suzuki R, Morcuende S, Webber M, Hunt SP, Dickenson AH (2002) Superficial NK1-expressing neurons control spinal excitability through activation of descending pathways. Nat Neurosci 5:1319-1326.
53. Svendsen F, Tjolsen A, Hole K (1998) AMPA and NMDA receptor-dependent spinal LTP after nociceptive tetanic stimulation. NeuroReport 9:1185-1190.
54. Thompson SW, Dray A, Urban L (1994) Injury-induced plasticity of spinal reflex activity: NK1 neurokinin receptor activation and enhanced A- and C-fiber mediated responses in the rat spinal cord in vitro. J Neurosci 14:3672-3687.
55. Treede R-D, Kunde V (1995) Middle-latency somatosensory evoked potentials after stimulation of the radial and median nerves: component structure and scalp topography. I Clin Neurophysiol 12:291-301.
56. Treede R-D, Meyer RA, Raja SN, Campbell JN (1992) Peripheral and central mechanisms of cutaneous hyperalgesia. Prog Neurobiol 38:397-421.
57. Walters ET (1994) Injury-related behavior and neuronal plasticity: an evolutionary perspective on sensitization, hyperalgesia, and analgesia. Int Rev Neurobiol 36:325-427.
58. Weidner C, Schmelz M, Schmidt R, Hammarberg B, Orstavik K, Hilliges M, Torebjörk HE, Handwerker HO (2002) Neural signal processing: the underestimated contribution of peripheral human C-fibers. J Neurosci 22:6704-6712.
59. Willer JC (1977) Comparative study of perceived pain and nociceptive flexion reflex in man. Pain 3:69-80.
60. Willis WD (2002) Long-term potentiation in spinothalamic neurons. Brain Res Brain Res Rev 40:202-214.
61. Woolf CJ (1996) Windup and central sensitization are not equivalent. Pain 66:105-108.
62. Woolf CJ, Salter MW (2000) Neuronal plasticity: increasing the gain in pain. Science 288:1765-1769.
63. Ziegler EA, Magerl W, Meyer RA, Treede R-D (1999) Secondary hyperalgesia to punctate mechanical stimuli: central sensitization to A-fiber nociceptor input. Brain 122:2245-2257.