Central nociceptive sensitization vs. Spinal cord training: Opposing forms of plasticity that dictate function after complete spinal cord injury

Frontiers in Physiology

Volumn 3 OCT, Issue , 2012, Pages

  Ferguson, Adam R ^a   Russell Huie, J ^a   Crown, Eric D ^b   Grau, James W ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b ABBOTT LABORATORIES   (United States)

^c TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Nociception; Pain; Plasticity; Recovery of function; Spinal cord injury; Spinal cord learning

Indexed keywords

EID: 84870910840     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2012.00396     Document Type: Article

References (87)

1. Abbadie, C., Taylor, B. K., Peterson, M. A., and Basbaum, A. I. (1997). Differential contribution of the two phases of the formalin test to the pattern of c-fos expression in the rat spinal cord: studies with remifentanil and lidocaine. Pain 69, 101-110.
2. Alvarez-Vega, M., Baamonde, A., Gutierrez, M., Hidalgo, A., and Menendez, L. (2000). Intrathecal N-methyl-D-aspartate (NMDA) induces paradoxical analgesia in the tail-flick test in rats. Pharmacol. Biochem. Behav. 65, 621-625.
3. Barbeau, H., and Rossignol, S. (1987). Recovery of locomotion after chronic spinalization in the adult cat. Brain Res. 412, 84-95.
4. Baumbauer, K. M., Hoy, K. C. Jr., Huie, J. R., Hughes, A. J., Woller, S. A., Puga, D. A., et al. (2008). Timing in the absence of supraspinal input I: variable, but not fixed, spaced stimulation of the sciatic nerve undermines spinally-mediated instrumental learning. Neuroscience 155, 1030-1047.
5. Baumbauer, K. M., Huie, J. R., Hughes, A. J., and Grau, J. W. (2009). Timing in the absence of supraspinal input II: regularly spaced stimulation induces a lasting alteration in spinal function that depends on the NMDA receptor, BDNF release, and protein synthesis. J. Neurosci. 29, 14383-14393.
6. Baumbauer, K. M., Young, E. E., Hoy, K. C. Jr., and Joynes, R. L. (2007). Neurokinin receptors modulate the impact of uncontrollable stimulation on adaptive spinal plasticity. Behav. Neurosci. 121, 1082-1094.
7. Beattie, E. C., Stellwagen, D., Morishita, W., Bresnahan, J. C., Ha, B. K., Von Zastrow, M., et al. (2002). Control of synaptic strength by glial TNFalpha. Science 295, 2282-2285.
8. Bjorkman, R., Hallman, K. M., Hedner, J., Hedner, T., and Henning, M. (1994). Acetaminophen blocks spinal hyperalgesia induced by NMDA and substance P. Pain 57, 259-264.
9. Bliss, T. V., and Lomo, T. (1973). Long-lasting potentiation of synap-tic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. 232, 331-356.
10. Bouyer, L. J., and Rossignol, S. (2003). Contribution of cutaneous inputs from the hindpaw to the control of locomotion. I. Intact cats. J. Neurophysiol. 90, 3625-3639.
11. Bouyer, L. J., Whelan, P. J., Pearson, K. G., and Rossignol, S. (2001). Adaptive locomotor plasticity in chronic spinal cats after ankle extensors neurectomy. J. Neurosci. 21, 3531-3541.
12. Braiz, J. M., and Bausbaum, A. I. (2010). Differential ATF3 expression in dorsal root ganglion neurons reveals the profile of primary afferents engaged by diverse noxious chemical stimuli. Pain 150, 290-301.
13. Bregman, B. S., Diener, P. S., McAtee, M., Dai, H. N., and James, C. (1997). Intervention strategies to enhance anatomical plasticity and recovery of function after spinal cord injury. Adv. Neurol. 72, 257-275.
14. Buerger, A. A., and Fennessy, A. (1970). Learning of leg position in chronic spinal rats. Nature 225, 751-752.
15. Caudle, K. L., Brown, E. H., Shum-Siu, A., Burke, D. A., Magnuson, T. S., Voor, M. J., et al. (2011). Hindlimb immobilization in a wheelchair alters functional recovery following contusive spinal cord injury in the adult rat. Neurorehabil. Neural Repair 25, 729-739.
16. Choi, J. I., Svensson, C. I., Koehrn, F. J., Bhuskute, A., and Sorkin, L. S. (2010). Peripheral inflammation induces tumor necrosis factor dependent AMPA receptor trafficking and Akt phosphorylation in spinal cord in addition to pain behavior. Pain 149, 243-253.
17. Coderre, T. J. (2001). "Noxious stimulus-induced plasticity in spinal cord dorsal horn: evidence and insights on mechanisms obtained using the formalin test," in Spinal Cord Plasticity: Alterations in Reflex Function, eds M. M. Patterson and J. W. Grau (Boston, MA: Kluwer Academic), 163-183.
18. Coderre, T. J., and Melzack, R. (1992). The contribution of excitatory amino acids to central sensitization and persistent nociception after formalin-induced tissue injury. J. Neurosci. 12, 3665-3670.
19. Crown, E. D., Ferguson, A. R., Joynes, R. L., and Grau, J. W. (2002a). Instrumental learning within the spinal cord: IV. Induction and retention of the behavioral deficit observed after noncontin-gent shock. Behav. Neurosci. 116, 1032-1051.
20. Crown, E. D., Ferguson, A. R., Joynes, R. L., and Grau, J. W. (2002b). Instrumental learning within the spinal cord. II. Evidence for central mediation. Physiol. Behav. 77, 259-267.
21. Crown, E. D., and Grau, J. W. (2001). Preserving and restoring behavioral potential within the spinal cord using an instrumental training paradigm. J. Neurophysiol. 86, 845-855.
22. Crown, E. D., Gwak, Y. S., Ye, Z., Johnson, K. M., and Hulsebosch, C. E. (2008). Activation of p38 MAP kinase is involved in central neuropathic pain following spinal cord injury. Exp. Neurol. 213, 257-267.
23. Crown, E. D., Ye, Z., Johnson, K. M., Xu, G. Y., McAdoo, D. J., and Hulsebosch, C. E. (2006). Increases in the activated forms of ERK 1/2, p38 MAPK, and CREB are correlated with the expression of at-level mechanical allodynia following spinal cord injury. Exp. Neurol. 199, 397-407.
24. Crown, E. D., Ye, Z., Johnson, K. M., Xu, G. Y., McAdoo, D. J., Westlund, K. N., et al. (2005). Upregulation of the phosphorylated form of CREB in spinothalamic tract cells following spinal cord injury: relation to central neuropathic pain. Neurosci. Lett. 384, 139-144.
25. Czeschik, J. C., Hagenacker, T., Schafers, M., and Busselberg, D. (2008). TNF-alpha differentially modulates ion channels of nociceptive neurons. Neurosci. Lett. 434, 293-298.
26. Dawson, V. L., Dawson, T. M., Bartley, D. A., Uhl, G. R., and Snyder, S. H. (1993). Mechanisms of nitric oxide-mediated neurotoxicity in primary brain cultures. J. Neurosci. 13, 2651-2661.
27. De Leon, R. D., Hodgson, J. A., Roy, R. R., and Edgerton, V. R. (1998). Locomotor capacity attributable to step training versus spontaneous recovery after spinalization in adult cats. J. Neurophysiol. 79, 1329-1340.
28. Dickenson, A. H., and Sullivan, A. F. (1991). NMDA receptors and central hyperalgesic states. Pain 46, 344-346.
29. Dougherty, P. M., Palecek, J., Paleckova, V., Sorkin, L. S., and Willis, W. D. (1992). The role of NMDA and non-NMDA excitatory amino acid receptors in the excitation of primate spinothalamic tract neurons by mechanical, chemical, thermal, and electrical stimuli. J. Neurosci. 12, 3025-3041.
30. Dubuisson, D., and Dennis, S. G. (1977). The formalin test: a quantitative study of the analgesic effects of morphine, meperidine, and brain stem stimulation in rats and cats. Pain 4, 161-174.
31. Edgerton, V. R., and Roy, R. R. (2009). Activity-dependent plasticity of spinal locomotion: implications for sensory processing. Exerc. Sport Sci. Rev. 37, 171-178.
32. Edgerton, V. R., Roy, R. R., Hodgson, J. A., Prober, R. J., de Guzman, C. P., and de Leon, R. (1992). Potential of adult mammalian lumbosacral spinal cord to execute and acquire improved locomotion in the absence of supraspinal input. J. Neurotrauma 9(Suppl. 1), S119-S128.
33. Ferguson, A. R., Bolding, K. A., Huie, J. R., Hook, M. A., Santillano, D. R., Miranda, R. C., et al. (2008a). Group I metabotropic glutamate receptors control metaplasticity of spinal cord learning through a protein kinase C-dependent mechanism. J. Neurosci. 28, 11939-11949.
34. Ferguson, A. R., Christensen, R. N., Gensel, J. C., Miller, B. A., Sun, F., Beattie, E. C., et al. (2008b). Cell death after spinal cord injury is exacerbated by rapid TNF alpha-induced trafficking of GluR2-lacking AMPARs to the plasma membrane. J. Neurosci. 28, 11391-11400.
35. Ferguson, A. R., Crown, E. D., and Grau, J. W. (2006). Nociceptive plasticity inhibits adaptive learning in the spinal cord. Neuroscience 141, 421-431.
36. Ferguson, A. R., Huie, J. R., Crown, E. D., Baumbauer, K. M., Hook, M. A., Garraway, S. M., et al. (2012). Maladaptive spinal plasticity opposes spinal learning and recovery in spinal cord injury. Front. Physiol. 3:399. doi: 10.3389/fphys.2012.00399
37. Fisher, K., and Coderre, T. J. (1996). The contribution of metabotropic glutamate receptors (mGluRs) to formalin-induced nociception. Pain 68, 255-263.
38. Fitzgerald, L. A., and Thompson, R. F. (1967). Classical conditioning of the hindlimb flexion reflex in the acute spinal cat. Psychon. Sci. 8, 213-214.
39. Frigon, A., and Rossignol, S. (2009). Partial denervation of ankle extensors prior to spinalization in cats impacts the expression of locomotion and the phasic modulation of reflexes. Neuroscience 158, 1675-1690.
40. Genovese, T., Mazzon, E., Crisafulli, C., Di Paola, R., Muia, C., Bramanti, P., et al. (2006). Immunomodulatory effects of etanercept in an experimental model of spinal cord injury. J. Pharmacol. Exp. Ther. 316, 1006-1016.
41. Giroux, N., Reader, T. A., and Rossignol, S. (2001). Comparison of the effect of intrathecal administration of clonidine and yohimbine on the locomotion of intact and spinal cats. J. Neurophysiol. 85, 2516-2536.
42. Giuliani, C. A., and Smith, J. L. (1987). Stepping behaviors in chronic spinal cats with one hindlimb deafferented. J. Neurosci. 7, 2537-2546.
43. Grau, J. W., Barstow, D. G., and Joynes, R. L. (1998). Instrumental learning within the spinal cord: I. Behavioral properties. Behav. Neurosci. 112, 1366-1386.
44. Grau, J. W., Crown, E. D., Ferguson, A. R., Washburn, S. N., Hook, M. A., and Miranda, R. C. (2006). Instrumental learning within the spinal cord: underlying mechanisms and implications for recovery after injury. Behav. Cogn. Neurosci. Rev. 5, 191-239.
45. Grau, J. W., Huie, J. R., Garraway, S. M., Hook, M. A., Crown, E. D., Baumbauer, K. M., et al. (2012). Impact of behavioral control on the processing of nociceptive stimulation. Front. Physiol. 3:262. doi: 10.3389/fphys.2012.00262
46. Grau, J. W., Washburn, S. N., Hook, M. A., Ferguson, A. R., Crown, E. D., Garcia, G., et al. (2004). Uncontrollable stimulation undermines recovery after spinal cord injury. J. Neurotrauma 21, 1795-1817.
47. Grillner, S., McClellan, A., Sigvardt, K., Wallen, P., and Wilen, M. (1981). Activation of NMDA-receptors elicits "fictive locomotion" in lamprey spinal cord in vitro. Acta Physiol. Scand. 113, 549-551.
48. Haley, J. E., Sullivan, A. F., and Dickenson, A. H. (1990). Evidence for spinal N-methyl-D-aspartate receptor involvement in prolonged chemical nociception in the rat. Brain Res. 518, 218-226.
49. Hook, M. A., Huie, J. R., and Grau, J. W. (2008). Peripheral inflammation undermines the plasticity of the isolated spinal cord. Behav. Neurosci. 122, 233-249.
50. Horridge, G. A. (1962). Learning of leg position by headless insects. Nature 193, 697-698.
51. Huie, J. R., Garraway, S. M., Baumbauer, K. M., Hoy, K. C. Jr., Beas, B. S., Montgomery, K. S., et al. (2012a). Brain-derived neurotrophic factor promotes adaptive plasticity within the spinal cord and mediates the beneficial effects of controllable stimulation. Neuroscience 200C, 74-90.
52. Huie, J. R., Baumbauer, K. M., Lee, K. H., Bresnahan, J. C., Beattie, M. S., Ferguson, A. R., et al. (2012b). Glial tumor necrosis factor alpha (TNFalpha) generates meta-plastic inhibition of spinal learning. PLoS ONE 7:e39751. doi: 10.1371/ journal.pone.0039751
53. Hunskaar, S., and Hole, K. (1987). The formalin test in mice: dissociation between inflammatory and non-inflammatory pain. Pain 30, 103-114.
54. Ikeda, H., Kusudo, K., Ryu, P. D., and Murase, K. (2003). Effects of corticotropin-releasing factor on plasticity of optically recorded neuronal activity in the substantia gelatinosa of rat spinal cord slices. Pain 106, 197-207.
55. Ji, R. R., Kohno, T., Moore, K. A., and Woolf, C. J. (2003). Central sensitization and LTP: do pain and memory share similar mechanisms? Trends Neurosci. 26, 696-705.
56. Jindrich, D. L., Joseph, M. S., Otoshi, C. K., Wei, R. Y., Zhong, H., Roy, R. R., et al. (2009). Spinal learning in the adult mouse using the Horridge paradigm. J. Neurosci. Methods 182, 250-254.
57. Joynes, R. L., Ferguson, A. R., Crown, E. D., Patton, B. C., and Grau, J. W. (2003). Instrumental learning within the spinal cord: V. Evidence the behavioral deficit observed after noncontingent nociceptive stimulation reflects an intraspinal modification. Behav. Brain Res. 141, 159-170.
58. Keppel, G., and Wickens, T. D. (2004). Design and Analysis. A Researcher's Handbook, 4th Edn. Upper Saddle River, NJ: Prentice-Hall.
59. Kim, H. W., Roh, D. H., Yoon, S. Y., Seo, H. S., Kwon, Y. B., Han, H. J., et al. (2008). Activation of the spinal sigma-1 receptor enhances NMDA-induced pain via PKC- and PKA-dependent phosphorylation of the NR1 subunit in mice. Br. J. Pharmacol. 154, 1125-1134.
60. Koh, J. Y., and Choi, D. W. (1988). Cultured striatal neurons containing NADPH-diaphorase or acetyl-cholinesterase are selectively resistant to injury by NMDA receptor agonists. Brain Res. 446, 374-378.
61. Le Bars, D., Gozariu, M., and Cadden, S. W. (2001). Animal models of nociception. Pharmacol. Rev. 53, 597-652.
62. Lovely, R. G., Gregor, R. J., Roy, R. R., and Edgerton, V. R. (1986). Effects of training on the recovery of full-weight-bearing stepping in the adult spinal cat. Exp. Neurol. 92, 421-435.
63. Marchand, F., Tsantoulas, C., Singh, D., Grist, J., Clark, A. K., Bradbury, E. J., et al. (2009). Effects of Etanercept and Minocycline in a rat model of spinal cord injury. Eur. J. Pain 13, 673-681.
64. Menendez, L., Hidalgo, A., and Baamonde, A. (1997). Spinal calmodulin inhibitors reduce N-methyl-D-aspartate- and septide-induced nociceptive behavior. Eur. J. Pharmacol. 335, 9-14.
65. Milligan, E. D., Twining, C., Chacur, M., Biedenkapp, J., O'Connor, K., Poole, S., et al. (2003). Spinal glia and proinflammatory cytokines mediate mirror-image neuropathic pain in rats. J. Neurosci. 23, 1026-1040.
66. Mills, C. D., Johnson, K. M., and Hulsebosch, C. E. (2002). Group I metabotropic glutamate receptors in spinal cord injury: roles in neuroprotection and the development of chronic central pain. J. Neurotrauma 19, 23-42.
67. Park, C. K., Lu, N., Xu, Z. Z., Liu, T., Serhan, C. N., and Ji, R. R. (2011). Resolving TRPV1- and TNF-alpha-mediated spinal cord synaptic plasticity and inflammatory pain with neuroprotectin D1. J. Neurosci. 31, 15072-15085.
68. Petruska, J. C., Ichiyama, R. M., Jindrich, D. L., Crown, E. D., Tansey, K. E., Roy, R. R., et al. (2007). Changes in motoneuron properties and synaptic inputs related to step training after spinal cord transection in rats. J. Neurosci. 27, 4460-4471.
69. Raigorodsky, G., and Urca, G. (1987). Intrathecal N-methyl-D-aspartate (NMDA) activates both nociceptive and antinociceptive systems. Brain Res. 422, 158-162.
70. Raineteau, O., and Schwab, M. E. (2001). Plasticity of motor systems after incomplete spinal cord injury. Nat. Rev. Neurosci. 2, 263-273.
71. Roh, D. H., Seo, H. S., Yoon, S. Y., Song, S., Han, H. J., Beitz, A. J., et al. (2009). Activation of spinal alpha-2 adrenoceptors, but not mu-opioid receptors, reduces the intrathecal N-methyl-D-aspartate-induced increase in spinal NR1 subunit phosphorylation and nociceptive behaviors in the rat. Anesth. Analg. 110, 622-629.
72. Rossignol, S., Barriere, G., Frigon, A., Barthelemy, D., Bouyer, L., Provencher, J., et al. (2008). Plasticity of locomotor sensorimo-tor interactions after peripheral and/or spinal lesions. Brain Res. Rev. 57, 228-240.
73. Sandkuhler, J., Benrath, J., Brechtel, C., Ruscheweyh, R., and Heinke, B. (2000). Synaptic mechanisms of hyperalgesia. Prog. Brain Res. 129, 81-100.
74. Sato, E., Takano, Y., Kuno, Y., Takano, M., and Sato, I. (2003). Involvement of spinal tyrosine kinase in inflammatory and N-methyl-D-aspartate-induced hyperalgesia in rats. Eur. J. Pharmacol. 468, 191-198.
75. Thompson, R. F., and Spencer, W. A. (1966). Habituation: a model phenomenon for the study of neuronal substrates of behavior. Psychol. Rev. 73, 16-43.
76. Villanueva, N., Lastra, A., Hidalgo, A., Baamonde, A., and Menendez, L. (2002). Spinal nociceptin inhibits septide but not N-methyl-D- aspartate-induced nociceptive behavior in rats. Eur. J. Pharmacol. 445, 83-86.
77. Wheeler-Aceto, H., and Cowan, A. (1991). Standardization of the rat paw formalin test for the evaluation of analgesics. Psychopharmacology (Berl.) 104, 35-44.
78. Woolf, C. J. (1983). Evidence for a central component of post-injury pain hypersensitivity. Nature 306, 686-688.
79. Woolf, C. J. (2007). Central sensitization: uncovering the relation between pain and plasticity. Anesthesiology 106, 864-867.
80. Woolf, C. J., and Salter, M. W. (2000). Neuronal plasticity: increasing the gain in pain. Science 288, 1765-1769.
81. Woolf, C. J., and Thompson, S. W. (1991). The induction and maintenance of central sensitization is dependent on N-methyl-D-aspartic acid receptor activation; implications for the treatment of post-injury pain hypersensitivity states. Pain 44, 293-299.
82. Xu, Z. Z., Zhang, L., Liu, T., Park, J. Y., Berta, T., Yang, R., et al. (2010). Resolvins RvE1 and RvD1 attenuate inflammatory pain via central and peripheral actions. Nat. Med. 16, 592-597, (1p following 597).
83. Yamamoto, T., and Yaksh, T. L. (1992). Comparison of the antinociceptive effects of pre- and posttreatment with intrathecal morphine and MK801, an NMDA antagonist, on the formalin test in the rat. Anesthesiology 77, 757-763.
84. Yashpal, K., Fisher, K., Chabot, J. G., and Coderre, T. J. (2001). Differential effects of NMDA and group I mGluR antagonists on both nociception and spinal cord protein kinase C translocation in the formalin test and a model of neuropathic pain in rats. Pain 94, 17-29.
85. Yoon, S. Y., Roh, D. H., Seo, H. S., Kang, S. Y., Moon, J. Y., Song, S., et al. (2010). An increase in spinal dehydroepiandrosterone sulfate (DHEAS) enhances NMDA-induced pain via phosphorylation of the NR1 subunit in mice: involvement of the sigma-1 receptor. Neuropharmacology 59, 460-467.
86. Young, E. E., Baumbauer, K. M., Hillyer, J. E., Patterson, A. M., Hoy, K. C. Jr., Mintz, E. M., et al. (2008). The neonatal injury-induced spinal learning deficit in adult rats: central mechanisms. Behav. Neurosci. 122, 589-600.
87. Zhang, L., Berta, T., Xu, Z. Z., Liu, T., Park, J. Y., and Ji, R. R. (2011). TNF-alpha contributes to spinal cord synaptic plasticity and inflammatory pain: distinct role of TNF receptor subtypes 1 and 2. Pain 152, 419-427.