Peripheral Inflammation Undermines the Plasticity of the Isolated Spinal Cord

Behavioral Neuroscience

Volumn 122, Issue 1, 2008, Pages 233-249

  Hook, Michelle A ^a   Huie, John R ^a   Grau, James W ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

Author keywords

capsaicin; central sensitization; instrumental learning; recovery of function; spinal cord injury

Indexed keywords

CAPSAICIN; NALTREXONE;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CONVALESCENCE; ELECTROSTIMULATION; INFLAMMATION; LEARNING DISORDER; MALE; NERVE CELL PLASTICITY; NOCICEPTION; NONHUMAN; RAT; SENSITIZATION; SPINAL CORD; SPINAL CORD DORSAL HORN; SPINAL CORD INJURY; VERTEBRA;

ANALYSIS OF VARIANCE; ANIMALS; CAPSAICIN; CONDITIONING (PSYCHOLOGY); DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRIC STIMULATION; INFLAMMATION; LEARNING DISORDERS; MALE; NALTREXONE; NARCOTIC ANTAGONISTS; NEURONAL PLASTICITY; PAIN THRESHOLD; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; SENSORY SYSTEM AGENTS; SPINAL CORD INJURIES; TIME FACTORS; TOUCH;

EID: 40749097184     PISSN: 07357044     EISSN: None     Source Type: Journal    
DOI: 10.1037/0735-7044.122.1.233     Document Type: Article

References (64)

1. Barthelemy D., Leblond H., Provencher J., and Rossignol S. Nonlocomotor and locomotor hindlimb responses evoked by electrical microstimulation of the lumbar cord in spinalized cats. Journal of Neurophysiology 96 (2006) 3273-3292
2. Baumbauer K.M., Young E.E., Hoy Jr. K.C., France J.L., and Joynes R.L. Intrathecal infusions of anisomycin impact the learning deficit but not the learning effect observed in spinal rats that have received instrumental training. Behavioural Brain Research 173 (2006) 299-309
3. Baumbauer K.M., Young E.E., Hoy Jr. K.C., and Joynes R.L. Intrathecal administration of neurokinin 1 and neurokinin 2 receptor antagonists undermines the savings effect in spinal rats seen in an instrumental learning paradigm. Behavioral Neuroscience 121 (2007) 186-199
4. Bigbee A.J., Crown E.D., Ferguson A.R., Roy R.R., Tillakaratne N.J.K., Tobin A.J., et al. Two chronic motor training paradigms differentially alter the potential to perform a novel motor learning task in spinally transected rats. Behavioural Brain Research 180 (2007) 95-101
5. Bolding K.A., Hook M.A., Ferguson A.R., and Grau J.W. The general protein kinase C inhibitor, bisindolylmaleimide-I, dose-dependently prevents a shock-induced behavioral deficit in spinalized rats. Abstract Viewer/Itinerary Planner [CD-ROM] (2003), Society for Neuroscience, Washington, DC
6. Castro-Lopes J.M., Tavares I., Tolle T.R., and Coimbra A. Carrageenan-induced inflammation of the hind foot provokes arise of GABA-immunoreactive cells in the rat spinal cord that is prevented by peripheral neurectomy or neonatal capsaicin treatment. Pain 56 (1994) 193-201
7. Coderre T.J., and Melzack R. Increased pain sensitivity following heat injury involves a central mechanism. Behavioural Brain Research 15 (1985) 259-262
8. Crown E.D., Ferguson A.R., Joynes R.L., and Grau J.W. Instrumental learning within the spinal cord: IV. Induction and retention of the behavioral deficit observed after noncontingent shock. Behavioral Neuroscience 116 (2002) 1032-1051
9. Crown E.D., Ferguson A.R., Joynes R.L., and Grau J.W. Instrumental learning within the spinal cord. II. Evidence for central mediation. Physiology and Behavior 77 (2002) 259-267
10. Crown E.D., and Grau J.W. Preserving and restoring behavioral potential within the spinal cord using an instrumental training paradigm. Journal of Neurophysiology 86 (2001) 845-855
11. Dougherty P.M., Palecek J., Paleckova V., Sorkin L.S., and Willis W.D. 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. Journal of Neuroscience 12 (1992) 3025-3041
12. Dougherty P.M., Palecek J., Paleckova V., and Willis W.D. Neurokinin 1 and 2 antagonists attenuate the responses and NK1 antagonists prevent the sensitization of primate spinothalamic tract neurons after intradermal capsaicin. Journal of Neurophysiology 72 (1994) 1464-1475
13. Draisci G., Kajander K.C., Dubner R., Bennett G.J., and Iadarola M.J. Up-regulation of opioid gene expression in spinal cord evoked by experimental nerve injuries and inflammation. Brain Research 560 (1991) 186-192
14. Dubner R., and Ruda M.A. Activity-dependent neuronal plasticity following tissue injury and inflammation. Trends in Neuroscience 15 (1992) 96-103
15. Edgerton V.R., Roy R.R., and de Leon R.D. Neural Darwinism in the mammalian spinal cord. In: Patterson M.M., and Grau J.W. (Eds). Spinal cord plasticity: Alterations in reflex function (2001), Kluwer Academic, Boston 185-206
16. Edgerton V.R., Roy R.R., de Leon R.D., Tillakaratne N., and Hodgson J.A. Does motor learning occur in the spinal cord?. Neuroscientist 3 (1997) 287-294
17. Edgerton V.R., Roy R.R., Hodgson J.A., Gregor R.J., and De Guzman C.P. Recovery of full weight-supporting locomotion of the hindlimbs after complete thoracic spinalization of adult and neonatal cats. In Restorative neurology, plasticity of motoneuronal connections (1991), Elselvier, New York 405-418
18. Edgerton V.R., Tillakaratne N.J., Bigbee A.J., de Leon R.D., and Roy R.R. Plasticity of the spinal neural circuitry after injury. Annual Review of Neuroscience 27 (2004) 145-167
19. Fang L., Wu J., Lin Q., and Willis W.D. Calcium-calmodulin-dependent protein kinase II contributes to spinal cord central sensitization. Journal of Neuroscience 22 (2002) 4196-4204
20. Fang L., Wu J., Zhang X., Lin Q., and Willis W.D. Increased phosphorylation of the GluR1 subunit of spinal cord alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionate receptor in rats following intradermal injection of capsaicin. Neuroscience 122 (2003) 237-245
21. Ferguson A.R., Crown E.D., and Grau J.W. Nociceptive plasticity inhibits adaptive learning in the spinal cord. Neuroscience 141 (2006) 421-431
22. Ferguson A.R., Washburn S.N., Crown E.D., and Grau J.W. GABAA receptor activation is involved in non-contingent shock inhibition of instrumental conditioning in spinal rat. Behavioral Neuroscience 117 (2003) 799-812
23. Forssberg H., and Grillner S. The locomotion of the acute spinal cat injected with clonidine i. v. Brain Research 50 (1973) 184-186
24. Gómez-Pinilla F., Huie J.R., Ying Z., Ferguson A., Crown E.D., Baumbauer K.M., Edgerton V.R., and Grau J.W. BDNF and learning: Evidence that instrumental training promotes learning within the spinal cord by up-regulating BDNF expression. Neuroscience 148 (2007) 893-906
25. Grau J.W., Barstow D.G., and Joynes R.L. Instrumental learning within the spinal cord: I. Behavioral properties. Behavioral Neuroscience 112 (1998) 1366-1386
26. Grau J.W., Crown E.D., Ferguson A.R., Washburn S.N., Hook M.A., and Miranda R.C. Instrumental Learning Within the Spinal Cord: Underlying Mechanisms and Implications for Recovery After Injury. Behavioral and Cognitive Neuroscience Reviews 5 (2006) 1-48
27. Grau J.W., and Hook M.A. Spinal neurons exhibit a surprising capacity to learn and a hidden vulnerability when freed from the brain's control. Current Neurology and Neuroscience Reports 6 (2006) 177-180
28. Grillner S. Control of locomotion in bipeds, tetrapods, and fish. In: Brookhart J.M., and Mountcastle V.B. (Eds). Handbook of physiology. The nervous system II (1981), American Physiological Society, Bethseda, MD 1179-1236
29. Hodgson J.A., Roy R.R., de Leon R., Dobkin B., and Edgerton V.R. Can the mammalian lumbar spinal cord learn a motor task?. Medicine and Science in Sports and Exercise 26 (1994) 1491-1497
30. Hook M.A., and Grau J.W. An animal model of functional electrical stimulation: Evidence that the central nervous system modulates the consequences of training. Spinal Cord 45 (2007) 702-712
31. Huie J.R., Gomez-Pinilla F., Ying Z., Edgerton V.R., and Grau J.W. BDNF enables learning in the rat spinal cord. Program No. 175.16. 2005 Abstract Viewer/Itinerary Planner (2005), Society for Neuroscience, Washington, DC
32. Huie J.R., Hoy K.C., Miranda R.A., and Grau J.W. Instrumental learning in the spinalized rat: A therapeutic effect of BDNF. 2007 Abstract Viewer/Itinerary Planner (2007), Society for Neuroscience, Washington, DC
33. Igwe O.J., and Chronwall B.M. Hyperalgesia induced by peripheral inflammation is mediated by protein kinase C betaII isozyme in the rat spinal cord. Neuroscience 104 (2001) 875-890
34. Joynes R.L., Ferguson A.R., Crown E.D., Patton B.C., and Grau J.W. Instrumental learning within the spinal cord: V. Evidence the behavioral deficit observed after noncontingent nociceptive stimulation reflects an intraspinal modification. Behavioral Brain Research 141 (2003) 159-170
35. Joynes R.L., and Grau J.W. Instrumental learning within the spinal cord: III. Prior exposure to noncontingent shock induces a behavioral deficit that is blocked by an opioid antagonist. Neurobiology of Learning and Memory 82 (2004) 35-51
36. Joynes R.L., Janjua K., and Grau J.W. Instrumental learning within the spinal cord: VI. The NMDA receptor antagonist, AP5, disrupts the acquisition and maintenance of an acquired flexion response. Behavioral Brain Research 154 (2004) 431-438
37. Kajander K.C., Sahara Y., Iadarola M.J., and Bennett G.J. Dynorphin increases in the dorsal spinal cord in rats with a painful peripheral neuropathy. Peptides 11 (1990) 719-728
38. Kawasaki Y., Kohno T., Zhuang Z.Y., Brenner G.J., Wang H., Van Der Meer C., et al. Ionotropic and metabotropic receptors, protein kinase A, protein kinase C, and Src contribute to C-fiber-induced ERK activation and cAMP response element-binding protein phosphorylation in dorsal horn neurons, leading to central sensitization. Journal of Neuroscience 24 (2004) 8310-8321
39. LaMotte R.H., Shain C.N., Simone D.A., and Tsai E.F. Neurogenic hyperalgesia: Psychophysical studies of underlying mechanisms. Journal of Neurophysiology 66 (1991) 190-211
40. Langlet C., Leblond H., and Rossignol S. Mid-lumbar segments are needed for the expression of locomotion in chronic spinal cats. Journal of Neurophysiology 93 (2005) 2474-2488
41. Lavrov I., Gerasimenko Y.P., Ichiyama R.M., Courtine G., Zhong H., Roy R.R., et al. Plasticity of spinal cord reflexes after a complete transection in adult rats: Relationship to stepping ability. Journal of Neurophysiology 96 (2006) 1699-1710
42. Lin Q., Peng Y.B., and Willis W.D. Possible role of protein kinase C in the sensitization of primate spinothalamic tract neurons. Journal of Neuroscience 16 (1996) 3026-3034
43. Liu G.T., Ferguson A.R., Crown E.D., Bopp A.C., Miranda R.C., and Grau J.W. Instrumental learning within the rat spinal cord: Localization of the essential neural circuit. Behavioral Neuroscience 119 (2005) 538-547
44. Mannion R.J., Costigan M., Decosterd I., Amaya F., Ma Q.P., Holstege J.C., et al. Neurotrophins: Peripherally and centrally acting modulators of tactile stimulus-induced inflammatory pain hypersensitivity. Proceedings of the National Academy of Sciences USA 96 (1999) 9385-9390
45. Neugebauer V., Chen P.S., and Willis W.D. Groups II and III metabotropic glutamate receptors differentially modulate brief and prolonged nociception in primate STT cells. Journal of Neurophysiology 84 (2000) 2998-3009
46. Neumann S., Doubell T.P., Leslie T., and Woolf C.J. Inflammatory pain hypersensitivity mediated by phenotypic switch in myelinated primary sensory neurons. Nature 384 (1996) 360-364
47. Patton B.C., Hook M.A., Ferguson A.R., Crown E.D., and Grau J.W. The behavioral deficit observed following noncontingent shock in spinalized rats is prevented by the protein synthesis inhibitor cycloheximide. Behavioral Neuroscience 118 (2004) 653-658
48. Rossignol S., Chau C., Brustein E., Belanger M., Barbeau H., and Drew T. Locomotor capacities after complete and partial lesions of the spinal cord. Acta neurobiologiae experimentalis 56 (1996) 449-463
49. Simone D.A., Baumann T.K., and LaMotte R.H. Dose-dependent pain and mechanical hyperalgesia in humans after intradermal injection of capsaicin. Pain 38 (1989) 99-107
50. Simone D.A., Sorkin L.S., Oh U., Chung J.M., Owens C., LaMotte R.H., et al. Neurogenic hyperalgesia: Central neural correlates in responses of spinothalamic tract neurons. Journal of Neurophysiology 66 (1991) 228-246
51. Sluka K.A., Rees H., Chen P.S., Tsuruoka M., and Willis W.D. Inhibitors of G-proteins and protein kinases reduce the sensitization to mechanical stimulation and the desensitization to heat of spinothalamic tract neurons induced by intradermal injection of capsaicin in the primate. Experimental Brain Research 115 (1997) 15-24
52. Sluka K.A., Willis W.D., and Westlund K.N. Joint inflammation and hyperalgesia are reduced by spinal bicuculline. Neuroreport 5 (1993) 109-112
53. Sluka K.A., Willis W.D., and Westlund K.N. Inflammationinducedrelease of excitatory amino acids is prevented by spinal administration of a GABAA but not by a GABAB receptor antagonist in rats. The Journal of Pharmacology and Experimental Therapeutics 271 (1994) 76-82
54. Soliman A.C., Yu J.S., and Coderre T.J. mGlu and NMDA receptor contributions to capsaicin-induced thermal and mechanical hypersensitivity. Neuropharmacology 48 (2005) 325-332
55. Washburn S.N., Maultsby M.L., and Grau J.W. The K2 opioid receptor agonist GR89696 has both adverse and beneficial effects on spinal cord plasticity. Program No. 396.19. 2005 Abstract Viewer/Itinerary Planner (2005), Society for Neuroscience, Washington, DC
56. Wernig A., Muller S., Nanassy A., and Cagol E. Laufband therapy based on 'rules of spinal locomotion' is effective in spinal cord injured persons. European Journal of Neuroscience 7 (1995) 823-829
57. Willis W.D. Role of neurotransmitters in sensitization of pain responses. Annals of the New York Academy of the Sciences 933 (2001) 142-156
58. Willis W.D. Long-term potentiation in spinothalamic neurons. Brain Research Reviews 40 (2002) 202-214
59. Woolf C.J. Evidence for a central component of post-injury pain hypersensitivity. Nature 306 (1983) 686-688
60. Yaksh T.L., and Rudy T.A. Chronic catheterization of the spinal subarachnoid space. Physiology and Behavior 17 (1976) 1031-1036
61. Young E.E., Baumbauer K.M., Elliot A., and Joynes R.L. The impact of neonatal injury on spinally mediated instrumental learning in adult rats. Behavioral Neuroscience (2007)
62. Zhou Y., Li G.D., and Zhao Z.Q. State-dependent phosphorylation of epsilon-isozyme of protein kinase C in adult rat dorsal root ganglia after inflammation and nerve injury. Journal of Neurochemistry 85 (2003) 571-580
63. Zou X., Lin Q., and Willis W.D. Role of protein kinase A in phosphorylation of NMDA receptor 1 subunits in dorsal horn and spinothalamic tract neurons after intradermal injection of capsaicin in rats. Neuroscience 115 (2002) 775-786
64. Zou X., Lin Q., and Willis W.D. Effect of protein kinase C blockade on phosphorylation of NR1 in dorsal horn and spinothalamic tract cells caused by intradermal capsaicin injection in rats. Brain Research 1020 (2004) 95-105