Modulation of paratrigeminal nociceptive neurons following temporomandibular joint inflammation in rats

Experimental Neurology

Volumn 214, Issue 2, 2008, Pages 209-218

  Yamazaki, Yoko ^a   Ren, Ke ^b   Shimada, Masahiko ^a   Iwata, Koichi ^c  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b UNIVERSITY OF MARYLAND DENTAL SCHOOL   (United States)

^c NIHON UNIVERSITY   (Japan)

Author keywords

Complete Freund's adjuvant; Fos; Hyperalgesia; Nociceptive neuron; Pa5; TMJ; Trigeminal nerve; Vagus nerve

Indexed keywords

FLUOROGOLD; FREUND ADJUVANT; PROTEIN FOS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ARTHRALGIA; ARTHRITIS; ARTICLE; AUTONOMIC NERVOUS SYSTEM; CELL FUNCTION; CELL LABELING; CELL POPULATION; COLD SENSITIVITY; CONTROLLED STUDY; EXPERIMENTAL RAT; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; MALE; NERVE CELL; NEUROMODULATION; NOCICEPTION; NOCICEPTIVE STIMULATION; NONHUMAN; PAIN; PAIN THRESHOLD; PARABRACHIAL NUCLEUS; PARATRIGEMINAL NOCICEPTIVE NEURON; PRIORITY JOURNAL; RAT; SINGLE UNIT ACTIVITY; STIMULUS RESPONSE; TEMPOROMANDIBULAR JOINT DISORDER; TEMPOROMANDIBULAR JOINT INFLAMMATION; TRIGEMINAL NERVE; TRIGEMINAL NUCLEUS; VAGUS NERVE; VAGUS NERVE STIMULATION;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; COLD TEMPERATURE; ELECTRIC STIMULATION; FREUND'S ADJUVANT; HOT TEMPERATURE; HYPERALGESIA; INFLAMMATION; MALE; NEURONS; NOCICEPTORS; PAIN THRESHOLD; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; TEMPOROMANDIBULAR JOINT DISORDERS; TRIGEMINAL NUCLEI; VAGUS NERVE;

EID: 56349156480     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2008.08.005     Document Type: Article

References (48)

1. Balan J.A., Caous C.A., Yu Y.G., and Lindsey C.J. Barosensitive neurons in the rat tractus solitarius and paratrigeminal nucleus: a new model for medullary, cardiovascular reflex regulation. Can. J. Physiol. Pharmacol. 82 (2004) 474-484
2. Bereiter D.A., Bereiter D.F., and Ramos M. Vagotomy prevents morphine-induced reduction in Fos-like immunoreactivity in trigeminal spinal nucleus produced after TMJ injury in a sex-dependent manner. Pain 96 (2002) 205-213
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. Bereiter D.A., Cioffi J.L., Bereiter D.F., Zardeneta G., and Milam S.B. Local blockade of integrins in the temporomandibular joint region reduces Fos-positive neurons in trigeminal subnucleus caudalis of female rats produced by jaw movement. Pain 125 (2006) 65-73
5. Bush F.M., Whitehill J.M., and Martelli M.F. Pain assessment in temporomandibular disorders. Cranio 7 (1989) 137-143
6. Bossut D.F., and Maixner W. Effect of cardiac vagus afferent electrostimulation on the responses of trigeminal and trigeminothalamic neurons to noxious orofacial stimulation. Pain 65 (1996) 101-109
7. Boucher Y., Simons C.T., Cuellar J.M., Jung S.W., Carstens M.I., and Carstens E. Activation of brain stem neurons by irritant chemical stimulation of the throat assessed by c-fos immunohistochemistry. Exp. Brain Res. 148 (2003) 211-218
8. 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
9. Caous C.A., Buck H.S., and Lindsey C.J. Neuronal connections of the paratrigeminal nucleus: a topographic analysis of neurons projecting to bulber, pontine and thalamic nuclei related to cardiovascular, respiratory and sensory functions. Auton. Neurosci. Basic Clin. 94 (2001) 14-24
10. Carstens E., Saxe I., and Ralph R. Brainstem neurons expressing c-Fos immunoreactivity following irritant chemical stimulation of the rat's tongue. Neuroscience 69 (1995) 939-953
11. Chandler M.J., Hobbs S.F., Bolser D.C., and Foreman R.D. Effect of vagus afferent stimulation on cervical spinothalamic tract neurons in monkeys. Pain 44 (1991) 81-87
12. Hains B.C., and Waxman S.G. Activated microglia contribute to the maintenance of chronic pain after spinal cord injury. J. Neurosci. 26 (2006) 4308-4317
13. Hansdottir R., and Bakke M. Joint tenderness, jaw opening, chewing velocity, and bite force in patients with temporomandibular joint pain and matched healthy control subjects. J. Orofacial Pain 18 (2004) 108-113
14. Hargreaves K., Dubner R., Brown F., Flores C., and Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32 (1988) 77-78
15. Hathaway C.B., Hu J.W., and Bereiter D.A. Distribution of Fos-like immunoreactivity in the caudal brainstem of the rat following noxious chemical stimulation of the temporomandibular joint. J. Comp. Neurol. 356 (1995) 444-456
16. Hu J.W., Sessle B.J., Raboisson P., Dallel R., and Woda A. Stimulation of craniofacial muscle afferents induces prolonged facilitatory effects in trigeminal nociceptive brain-stem neurones. Pain 48 (1992) 53-60
17. Imbe H., and Ren K. Orofacial deep and cutaneous tissue inflammation differentially upregulates preprodynorphin mRNA in the trigeminal and paratrigeminal nuclei of the rat. Mol. Brain Res. 67 (1999) 87-97
18. Imbe H., Iwata K., Zhou Q.Q., Zou S., Dubner R., and Ren K. Orofacial deep and cutaneous tissue inflammation and trigeminal neuronal activation. Implications for persistent temporomandibular pain. Cells Tissues Organs 169 (2001) 238-247
19. Iwata K., Kanda K., Tsuboi Y., Kitajima K., and Sumino R. Fos induction in the medullary dorsal horn and C1 segment of the spinal cord by acute inflammation in aged rats. Brain Res. 678 (1995) 127-139
20. Iwata K., Tashiro A., Tsuboi Y., Imai T., Sumino R., Morimoto T., Dubner R., and Ren K. Medullary dorsal horn neuronal activity in rats with persistent temporomandibular joint and perioral inflammation. J. Neurophysiol. 82 (1999) 1244-1253
21. Jacquin M.F., Chiaia N.L., and Rhoades R.W. Trigeminal projections to contralateral dorsal horn: central extent, peripheral origins, and plasticity. Somatosens. Mot. Res. 7 (1990) 153-183
22. Koepp J., Lindsey C.J., Motta E.M., and Rae G.A. Role of the paratrigeminal nucleus in nocifensive responses of rats to chemical, thermal and mechanical stimuli applied to the hind paw. Pain 122 (2006) 235-244
23. Korszun A., Hinderstein B., and Wong M. Comorbidity of depression with chronic facial pain and temporomandibular disorders. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 82 (1996) 496-500
24. Korszun A., Young E.A., Singer K., Carlson N.E., Brown M.B., and Crofford L. Basal circadian cortisol secretion in women with temporomandibular disorders. J. Dent. Res. 81 4 (2002) 279-283
25. 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
26. Lapa R.C.R.S., and Watanabe I. Synaptic contacts established by inferior alveolar nerve fibres in the paratrigeminal nucleus: an electron microscopic study in the rat. Arch. Oral Biol. 50 (2005) 73-79
27. Ness T.J., Fillingim R.B., Randich A., Backensto E.M., and Faught E. Low intensity vagal nerve stimulation lowers human thermal pain thresholds. Pain 86 (2000) 81-85
28. Ogawa A., Ren K., Tsuboi Y., Morimoto T., Sato T., and Iwata K. A new model of experimental parotitis in rats and its implication for trigeminal nociception. Exp. Brain Res. 152 (2003) 307-316
29. Oliveira M.C., Parada C.A., Veiga M.C., Rodrigues L.R., Barros S.P., and Tambeli C.H. Evidence for the involvement of endogenous ATP and P2X receptors in TMJ pain. Eur. J. Pain 9 (2005) 87-93
30. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates. Second ed. (1986), Academic Press, New York
31. Quinn J.H., and Bazan N.G. Identification of prostaglandin E2 and leukotriene B4 in the synovial fluid of painful, dysfunctional temporomandibular joints. J. Oral Maxillofac. Surg. 48 (1990) 968-971
32. Randich A., and Gebhart G.F. Vagal afferent modulation of nociception. Brain Res. Rev. 17 (1992) 77-99
33. Ren K., Zhuo M., Randich A., and Gebhart G.F. Vagal afferent stimulation-produced effects on nociception in capsaicin-treated rats. J. Neurophysiol. 69 (1993) 1530-1540
34. Roveroni R.C., Parada C.A., Cecilia M., Veiga F.A., and Tambeli C.H. Development of a behavioral model of TMJ pain in rats: the TMJ formalin test. Pain 94 (2001) 185-191
35. Rutherfurd S.D., Widdop R.E., Sannajust F., Louis W.J., and Gundlach A.L. Expression of c-fos and NGFI-A messenger RNA in the medulla oblongata of the anaesthetized rat following stimulation of vagal and cardiovascular afferents. Brain Res. Mol. Brain Res. 13 (1992) 301-312
36. Sato T., Kitagawa J., Ren K., Tanaka H., Tanabe A., Watanabe T., Mitsuhashi Y., and Iwata K. Activation of trigeminal intranuclear pathway in rats with temporomandibular joint inflammation. J. Oral Sci. 47 (2005) 65-69
37. Schaible H.G., and Schmidt R.F. Time course of mechanosensitivity changes in articular afferents during a developing experimental arthritis. J. Neurophysiol. 60 (1988) 2180-2195
38. Schellhas K.P., Wilkes C.H., and Baker C.C. Facial pain, headache, and temporomandibular joint inflammation. Headache 29 (1989) 229-232
39. Shimizu K., Asano M., Kitagawa J., Ogiso B., Ren K., Oki H., Matsumoto M., and Iwata K. Phosphorylation of extracellular signal-regulated kinase in medullary and upper cervical cord neurons following noxious tooth pulp stimulation. Brain Res. 1072 (2006) 99-109
40. Suwanprathes P., Ngu M., Ing A., and Hunt G. c-Fos immunoreactivity in the brain after esophageal acid stimulation. Am. J. Med. 115 (2003) 31S-38S
41. 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
42. Thurston C.L., and Randich A. Responses of on and off cells in the rostral ventral medulla to stimulation of vagal afferents and changes in mean arterial blood pressure in intact and cardiopulmonary deafferented rats. Pain. 62 (1995) 19-38
43. Ushiyama T., Nakatsu T., Yamane S., Tokutake H., Wakabayashi H., Ishimura K., and Maeta H. Heart rate variability for evaluating surgical stress and development of postoperative complications. Clin. Exp. Hypertens. 30 (2008) 45-55
44. Yu Y.G., and Lindsey C.J. Baroreceptor-sensitive neurons in the rat paratrigeminal nucleus. Auton. Neurosci. Basic Clin. 105 (2003) 25-34
45. Yu Y.G., Caous C.A., Balan A.C., Rae G.A., and Lindsey C.J. Cardiovascular responses to sciatic nerve stimulation are blocked by paratrigeminal nucleus lesion. Auton. Neurosci. Basic Clin. 98 (2002) 70-74
46. Xie Y.F., Zhang S., Chiang C.Y., Hu J.W., Dostrovsky J.O., and Sessle B.J. Involvement of glia in central sensitization in trigeminal subnucleus caudalis (medullary dorsal horn). Brain Behav. Immun. 21 (2007) 634-641
47. Zhou Q.Q., Imbe H., Dubner R., and Ren K. Persistent Fos protein expression after orofacial deep or cutaneous tissue inflammation in rats: implications for persistent orofacial pain. J. Comp. Neurol. 412 (1999) 276-291
48. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16 (1983) 109-110