Glutamate and capsaicin effects on trigeminal nociception II: Activation and central sensitization in brainstem neurons with deep craniofacial afferent input

Brain Research

Volumn 1253, Issue , 2009, Pages 48-59

  Lam, David K ^a   Sessle, Barry J ^a   Hu, James W ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Excitatory amino acid; Pain; Temporomandibular joint; TRPV1

Indexed keywords

CAPSAICIN; GLUTAMIC ACID; HALOTHANE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN STEM; CERVICAL SPINAL CORD; CONTROLLED STUDY; DESENSITIZATION; DRUG MECHANISM; DRUG POTENTIATION; DRUG RESPONSE; EVOKED SOMATOSENSORY RESPONSE; MALE; MECHANICAL STIMULATION; MECHANORECEPTOR; NERVE CELL; NERVE CELL EXCITABILITY; NOCICEPTION; NOCICEPTIVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; RAT; SENSITIZATION; SENSORY NERVE; SKIN RECEPTOR; SPRAGUE DAWLEY RAT; TEMPOROMANDIBULAR JOINT; TRIGEMINAL NERVE; TRIGEMINAL NUCLEUS;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; CAPSAICIN; GLUTAMIC ACID; MALE; MICROELECTRODES; NEURONS, AFFERENT; NOCICEPTORS; PHYSICAL STIMULATION; RATS; RATS, SPRAGUE-DAWLEY; SENSORY SYSTEM AGENTS; TEMPOROMANDIBULAR JOINT; TRIGEMINAL CAUDAL NUCLEUS;

RATTUS;

EID: 58249131219     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2008.11.056     Document Type: Article

References (57)

1. Baumann T.K., Simone D.A., Shain C.N., and LaMotte R.H. Neurogenic hyperalgesia: the search for the primary cutaneous afferent fibers that contribute to capsaicin-induced pain and hyperalgesia. J. Neurophysiol. 66 (1991) 212-227
2. Bereiter D.A., Hiraba H., and Hu J.W. Trigeminal subnucleus caudalis beyond homologies with the spinal dorsal horn. Pain 88 (2000) 221-224
3. Bereiter D.A., Okamoto K., and Bereiter D.F. Effect of persistent monoarthritis of the temporomandibular joint region on acute mustard oil-induced excitation of trigeminal subnucleus caudalis neurons in male and female rats. Pain 117 (2005) 58-67
4. Cairns B.E., Sessle B.J., and Hu J.W. Evidence that excitatory amino acid receptors within the temporomandibular joint region are involved in the reflex activation of the jaw muscles. J. Neurosci. 18 (1998) 8056-8064
5. Cairns B.E., Sessle B.J., and Hu J.W. Temporomandibular-evoked jaw muscle reflex: role of brain stem NMDA and non-NMDA receptors. NeuroReport 12 (2001) 1875-1878
6. Cairns B.E., Hu J.W., Arendt-Nielsen L., Sessle B.J., and Svensson P. Sex-related differences in human pain and rat afferent discharge evoked by injection of glutamate into the masseter muscle. J. Neurophysiol. 86 (2001) 782-791
7. Cairns B.E., Svensson P., Wang K., Hupfeld S., Graven-Nielsen T., Sessle B.J., Berde C.B., and Arendt-Nielsen L. Activation of peripheral NMDA receptors contributes to human pain and rat afferent discharges evoked by injection of glutamate into the masseter muscle. J. Neurophysiol. 90 (2003) 2098-2105
8. Cairns B.E., Wang K., Hu J.W., Sessle B.J., Arendt-Nielsen L., and Svensson P. The effect of glutamate-evoked masseter muscle pain on the human jaw-stretch reflex differs in men and women. J. Orofac. Pain 17 (2003) 317-325
9. Cairns B.E., Svensson P., Wang K., Castrillon E., Hupfeld S., Sessle B.J., and Arendt-Nielsen L. Ketamine attenuates glutamate-induced mechanical sensitization of the masseter muscle in human males. Exp. Brain Res. 169 (2006) 467-472
10. Carstens E., Kuenzler N., and Handwerker H.O. Activation of neurons in rat trigeminal subnucleus caudalis by different irritant chemicals applied to oral or ocular mucosa. J. Neurophysiol. 80 (1998) 465-492
11. Docherty R.J., Yeats J.C., Bevan S., and Boddeke H.W. Inhibition of calcineurin inhibits the desensitization of capsaicin-evoked currents in cultured dorsal root ganglion neurones from adult rats. Pflugers Arch. 431 (1996) 828-837
12. Dubner R. Plasticity in central nociceptive pathways. In: Merskey H., Loeser J.D., and Dubner R. (Eds). The Paths of Pain 1975-2005 (2005), IASP Press, Seattle, WA 101-115
13. Dubner R., and Bennett G.J. Spinal and trigeminal mechanisms of nociception. Annu. Rev. Neurosci. 6 (1983) 381-418
14. Dubner R., and Ren K. Brainstem mechanisms of persistent pain following injury. J. Orofac. Pain 18 (2004) 299-305
15. Galan A., and Cervero F. Painful stimuli induce in vivo phosphorylation and membrane mobilization of mouse spinal cord NKCC1 co-transporter. Neuroscience 133 (2005) 245-252
16. Garcia-Nicas E., Laird J.M., and Cervero F. GABAA-receptor blockade reverses the injury-induced sensitization of nociceptor-specific (NS) neurons in the spinal dorsal horn of the rat. J. Neurophysiol. 96 (2006) 661-670
17. Gazerani P., and Arendt-Nielsen L. The impact of ethnic differences in response to capsaicin-induced trigeminal sensitization. Pain 117 (2005) 223-229
18. Gazerani P., Staahl C., Drewes A.M., and Arendt-Nielsen L. The effects of Botulinum Toxin type A on capsaicin-evoked pain, flare, and secondary hyperalgesia in an experimental human model of trigeminal sensitization. Pain 122 (2006) 315-325
19. Ge H.Y., Madeleine P., and Arendt-Nielsen L. Gender differences in pain modulation evoked by repeated injections of glutamate into the human trapezius muscle. Pain 113 (2005) 134-140
20. Hu J.W. Response properties of nociceptive and non-nociceptive neurons in the rat's trigeminal subnucleus caudalis (medullary dorsal horn) related to cutaneous and deep craniofacial afferent stimulation and modulation by diffuse noxious inhibitory controls. Pain 41 (1990) 331-345
21. Hu J.W., Sun K.Q., Vernon H., and Sessle B.J. Craniofacial inputs to upper cervical dorsal horn: implications for somatosensory information processing. Brain Res. 1044 (2005) 93-106
22. Jung J., Shin J.S., Lee S.Y., Hwang S.W., Koo J., Cho H., and Oh U. Phosphorylation of vanilloid receptor 1 by Ca2+/calmodulin-dependent kinase II regulates its vanilloid binding. J. Biol. Chem. 279 (2004) 7048-7054
23. Karlsson U., Sundgren-Andersson A.K., Johansson S., and Krupp J.J. Capsaicin augments synaptic transmission in the rat medial preoptic nucleus. Brain Res. 1043 (2005) 1-11
24. Kosugi M., Nakatsuka T., Fujita T., Kuroda Y., and Kumamoto E. Activation of TRPA1 channel facilitates excitatory synaptic transmission in substantia gelatinosa neurons of the adult rat spinal cord. J. Neurosci. 27 (2007) 4443-4451
25. Lam, D.K., Sessle, B.J., Hu, J.W., 2003. Trigeminal nociceptive neuronal activity modulated by glutamate and capsaicin application to rat TMJ. Program No. 1178. 2003 Abstract Viewer/Itinerary Planner. International Association for Dental Research.
26. Lam D.K., Sessle B.J., Cairns B.E., and Hu J.W. Peripheral NMDA receptor modulation of jaw muscle electromyographic activity induced by capsaicin injection into the temporomandibular joint of rats. Brain Res. 1046 (2005) 68-76
27. Lam D.K., Sessle B.J., Cairns B.E., and Hu J.W. Neural mechanisms of temporomandibular joint and masticatory muscle pain: a possible role for peripheral glutamate receptor mechanisms. Pain Res. Manag. 10 (2005) 145-152
28. Lam, D.K., Sessle, B.J., Hu, J.W., 2008a. Glutamate and capsaicin effects on trigeminal nociception I: activation and peripheral sensitization of deep craniofacial nociceptive afferents. Brain Res. doi:10.1016/j.brainres.2008.11.029.
29. Lam D.K., Sessle B.J., and Hu J.W. Surgical incision can alter capsaicin-induced central sensitization in rat brainstem nociceptive neurons. Neurosci. 156 (2008) 737-747
30. LaMotte R., Shain C.N., Simone D.A., and Tsai E.F. Neurogenic hyperalgesia: psychophysical studies of underlying mechanisms. J. Neurophysiol. 66 (1991) 190-211
31. LaMotte R.H., Lundberg L.E., and Torebjork H.E. Pain, hyperalgesia and activity in nociceptive C units in humans after intradermal injection of capsaicin. J. Physiol. 448 (1992) 749-764
32. Lawand N.B., Willis W.D., and Westlund K.N. Excitatory amino acid receptor involvement in peripheral nociceptive transmission in rats. Eur. J. Pharmacol. 324 (1997) 169-177
33. Merrill A.W., Cuellar J.M., Judd J.H., Carstens M.I., and Carstens E. Effects of TRPA1 agonists mustard oil and cinnamaldehyde on lumbar spinal wide-dynamic range neuronal responses to innocuous and noxious cutaneous stimuli in rats. J. Neurophysiol. 99 (2008) 415-425
34. Mørch C.D., Hu J.W., Arendt-Nielsen L., and Sessle B.J. Convergence of cutaneous, musculoskeletal, dural and visceral afferents onto nociceptive neurons in the first cervical dorsal horn. Eur. J. Neurosci. 26 (2007) 142-154
35. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates, Compact Third Edition (1997), Academic Press, Toronto
36. Pitcher M.H., Price T.J., Entrena J.M., and Cervero F. Spinal NKCC1 blockade inhibits TRPV1-dependent referred allodynia. Mol. Pain 3 (2007) 17
37. Price T.J., Cervero F., and de Koninck Y. Role of cation-chloride-cotransporters (CCC) in pain and hyperalgesia. Curr. Top. Med. Chem. 5 (2005) 547-555
38. Price T.J., Hargreaves K.M., and Cervero F. Protein expression and mRNA cellular distribution of the NKCC1 cotransporter in the dorsal root and trigeminal ganglia of the rat. Brain Res. 1112 (2006) 146-158
39. Rycroft B.K., and Gibb A.J. Inhibitory interactions of calcineurin (phosphatase 2B) and calmodulin on rat hippocampal NMDA receptors. Neuropharmacology 47 (2004) 505-514
40. Sessle B.J. Orofacial pain. In: Merskey H., Loeser J.D., and Dubner R. (Eds). The Paths of Pain 1975-2005 (2005), IASP Press, Seattle 131-150
41. Sessle B.J., Chiang C.Y., and Dostrovsky J.O. Interrelationships between sensorimotor cortex, anterior pretectal nucleus and periaqueductal gray in modulation of trigeminal sensorimotor function in the rat. In: Inoki R., Shigenaga Y., and Tohyama M. (Eds). Processing and inhibition of nociceptive information (1992), Elsevier, Amsterdam 77-82
42. Simone D.A., Sorkin L.A., Oh U., Chung J.M., Owens C., LaMotte R.H., and Willis W.D. Neurogenic hyperalgesia: central correlates in responses of spinothalamic tract neurons. J. Neurophysiol. 66 (1991) 228-246
43. Sohn M.K., Graven-Nielsen T., Arendt-Nielsen L., and Svensson P. Inhibition of motor unit firing during experimental muscle pain in humans. Muscle Nerve 23 (2000) 1219-1226
44. Sohn M.K., Graven-Nielsen T., Arendt-Nielsen L., and Svensson P. Effects of experimental muscle pain on mechanical properties of single motor units in human masseter. Clin. Neurophysiol. 115 (2004) 76-84
45. Svensson P., Cairns B.E., Wang K., Hu J.W., Graven-Nielsen T., Arendt-Nielsen L., and Sessle B.J. Glutamate-evoked pain and mechanical allodynia in the human masseter muscle. Pain. 101 (2003) 221-227
46. Svensson P., Wang K., Arendt-Nielsen L., Cairns B.E., and Sessle B.J. Pain effects of glutamate injections into human jaw or neck muscles. J. Orofac. Pain 19 (2005) 109-118
47. Swope S.L., Moss S.J., Raymond L.A., and Huganir R.L. Regulation of ligand-gated ion channels by protein phosphorylation. Adv. Second Messenger Phosphoprot. Res. 33 (1999) 49-78
48. Takeshita S., Hirata H., and Bereiter D.A. Intensity coding by TMJ-responsive neurons in superficial laminae of caudal medullary dorsal horn of the rat. J. Neurophysiol. 86 (2001) 2393-2404
49. Tang M.L., Haas D.A., and Hu J.W. Capsaicin-induced joint inflammation is not blocked by local anesthesia. Anesth. Prog. 51 (2004) 2-9
50. Tashiro A., Okamoto K., Milam S.B., and Bereiter D.A. Differential effects of estradiol on encoding properties of TMJ units in laminae I and V at the spinomedullary junction in female rats. J. Neurophysiol. 98 (2007) 3242-3253
51. Wang H., Liu R.J., Zhang R.-X., and Qiao J.-T. Peripheral NMDA receptors contribute to the activation of nociceptors: a c-fos expression study in rats. Neurosci. Lett. 221 (1997) 101-104
52. Wang K., Arendt-Nielsen L., and Svensson P. Capsaicin-induced muscle pain alters the excitability of the human jaw-stretch reflex. J. Dent. Res. 81 (2002) 650-654
53. Warncke T., Jørum E., and Stubhaug A. Local treatment with N-methyl-d-aspartate receptor antagonist ketamine inhibits development of secondary hyperalgesia in man by a peripheral action. Neurosci. Lett. 227 (1997) 1-4
54. Woolf C.J., and Salter M.W. Neuronal plasticity: increasing the gain in pain. Science 288 (2000) 1765-1769
55. Woolf C.J., and Ma Q. Nociceptors-noxious stimulus detectors. Neuron 55 (2007) 353-364
56. Yu X.M., Sessle B.J., and Hu J.W. Differential effects of cutaneous and deep application of inflammatory irritant on mechanoreceptive field properties of trigeminal brain stem nociceptive neurons. J. Neurophysiol. 70 (1993) 1704-1707
57. Zanotto K., Merrill A.W., Carstens M.I., and Carstens E. Neurons in superficial trigeminal subnucleus caudalis responsive to oral cooling, menthol and other irritant stimuli. J. Neurophysiol. 97 (2007) 966-978