Trigeminal-Rostral Ventromedial Medulla circuitry is involved in orofacial hyperalgesia contralateral to tissue injury

Molecular Pain

Volumn 8, Issue , 2012, Pages

  Chai, Bryan ^a,b   Guo, Wei ^a,b   Wei, Feng ^a,b   Dubner, Ronald ^a,b   Ren, Ke ^a,b  

^a UNIVERSITY OF MARYLAND DENTAL SCHOOL   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

Author keywords

Descending modulation; IL 1 ; Pain; Rat; Serotonin; Substance P; Vi Vc transition zone

Indexed keywords

2 [1 IMINO 2 (2 METHOXYPHENYL)ETHYL] 7,7 DIPHENYLPERHYDROISOINDOL 4 ONE; 3 [3,5 BIS(TRIFLUOROMETHYL)BENZYLOXY] 2 PHENYLPIPERIDINE; AZASETRON; FREUND ADJUVANT; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1BETA; NEUROKININ 1 RECEPTOR; SEROTONIN; SEROTONIN 3 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN STEM INJURY; CONTROLLED STUDY; FACE PAIN; FEMALE; HYPERALGESIA; MALE; MASSETER MUSCLE; MYELENCEPHALON; NERVE CELL NETWORK; NEUROMODULATION; NEUROPATHOLOGY; NONHUMAN; OROFACIAL HYPERALGESIA; PRIORITY JOURNAL; RAT; RECEPTOR BLOCKING; ROSTRAL VENTROMEDIAL MEDULLA; SEROTONIN RELEASE; TRIGEMINAL NUCLEUS;

ANIMALS; FACIAL PAIN; FREUND'S ADJUVANT; HYPERALGESIA; INJECTIONS; INTRALAMINAR THALAMIC NUCLEI; MALE; MEDULLA OBLONGATA; MODELS, BIOLOGICAL; NERVE NET; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, INTERLEUKIN-1; RECEPTORS, NEUROKININ-1; RECEPTORS, SEROTONIN, 5-HT3; REPRODUCIBILITY OF RESULTS; SEROTONIN; TRIGEMINAL CAUDAL NUCLEUS; VENTROMEDIAL HYPOTHALAMIC NUCLEUS;

EID: 84867662299     PISSN: None     EISSN: 17448069     Source Type: Journal    
DOI: 10.1186/1744-8069-8-78     Document Type: Article

References (52)

1. Fernández-de-Las-Peñas C, Galan-del-Rio F, Fernandez-Carnero J, Pesquera J, Arendt-Nielsen L, Svensson P. Bilateral widespread mechanical pain sensitivity in women with myofascial temporomandibular disorder: evidence of impairment in central nociceptive processing. J Pain 2009, 10:1170-1178. 10.1016/j.jpain.2009.04.017, 19592309.
2. Fernández-de-Las-Peñas C, Galan-del-Rio F, Ortega-Santiago R, Jimenez-Garcia R, Arendt-Nielsen L, Svensson P. Bilateral thermal hyperalgesia in trigeminal and extra-trigeminal regions in patients with myofascial temporomandibular disorders. Exp Brain Res 2010, 202:171-179. 10.1007/s00221-009-2121-x, 20013256.
3. Dubner R, Bennett GJ. Spinal and trigeminal mechanisms of nociception. Annu Rev Neurosci 1983, 6:381-418. 10.1146/annurev.ne.06.030183.002121, 6132587.
4. Sessle BJ. Acute and chronic craniofacial pain: brainstem mechanisms of nociceptive transmission and neuroplasticity, and their clinical correlates. Crit Rev Oral Biol Med 2000, 11:57-91. 10.1177/10454411000110010401, 10682901.
5. Dubner R, Ren K. Brainstem mechanisms of persistent pain following injury. J Orofacial Pain 2004, 18:299-305.
6. Tashiro A, Okamoto K, Bereiter DA. Chronic inflammation and estradiol interact through MAPK activation to affect TMJ nociceptive processing by trigeminal caudalis neurons. Neuroscience 2009, 164(4):1813. 10.1016/j.neuroscience.2009.09.058, 2813765, 19786077.
7. Miyamoto M, Tsuboi Y, Takamiya K, Huganir R, Kondo M, Shinoda M, Oi Y, Iwata K. Involvement of GluR2 and GluR3 subunit C-termini in the trigeminal spinal subnucleus caudalis and C1-C2 neurons in trigeminal neuropathic pain. Neurosci Lett 2011, 491(1):8-12. 10.1016/j.neulet.2010.12.060, 3130337, 21215292.
8. Imbe H, Dubner R, Ren K. Masseteric inflammation-induced fos protein expression in the trigeminal interpolaris/caudalis transition zone: Contribution of somatosensory-vagal-adrenal integration. Brain Res 1999, 845:165-175. 10.1016/S0006-8993(99)01913-7, 10536195.
9. Zhou Q, Imbe H, Dubner R, Ren K. Persistent fos protein expression after orofacial deep or cutaneous tissue inflammation in rats: Implications for persistent orofacial pain. J Comp Neurol 1999, 412:276-291. 10.1002/(SICI)1096-9861(19990920)412:2<276::AID-CNE7>3.0.CO;2-9, 10441756.
10. Ro JY, Harriott A, Crouse U, Capra NF. Innocuous jaw movements increase c-fos expression in trigeminal sensory nuclei produced by masseter muscle inflammation. Pain 2003, 104:539-548. 10.1016/S0304-3959(03)00093-9, 12927626.
11. Ren K, Dubner R. The role of trigeminal interpolaris-caudalis transition zone in persistent orofacial pain. Int Rev Neurobiol 2011, 97:207-225. 3257052, 21708312.
12. Shimizu K, Chai B, LaGraize SC, Wei F, Dubner R, Ren K. Microinjection of IL-1beta into the trigeminal transition zone produces bilateral NMDA receptor dependent orofacial hyperalgesia involving descending circuitry. Open Pain J 2009, 2:76-83. 2835306, 20221418.
13. Shimizu K, Guo W, Wang H, Zou S, LaGraize SC, Iwata K, Dubner R, Ren K. Differential involvement of trigeminal transition zone and laminated subnucleus caudalis in orofacial deep and cutaneous hyperalgesia: the effects of interleukin-10 and glial inhibitors. Mol Pain 2009, 5:75. 10.1186/1744-8069-5-75, 2806354, 20025765.
14. Sugiyo S, Takemura M, Dubner R, Ren K. Trigeminal transition zone/rostral ventromedial medulla connections and facilitation of orofacial hyperalgesia after masseter inflammation in rats. J Comp Neurol 2005, 493:510-523. 10.1002/cne.20797, 16304628.
15. Maeno H, Kiyama H, Tohyama M. Distribution of the substance P receptor (NK-1 receptor) in the central nervous system. Brain Res Mol Brain Res 1993, 18:43-58.
16. Nakaya Y, Kaneko T, Shigemoto R, Nakanishi S, Mizuno N. Immunohistochemical localization of substance P receptor in the central nervous system of the adult rat. J Comp Neurol 1994, 347:249-274. 10.1002/cne.903470208, 7814667.
17. Saffroy M, Torrens Y, Glowinski J, Beaujouan JC. Autoradiographic distribution of tachykinin NK2 binding sites in the rat brain: comparison with NK1 and NK3 binding sites. Neuroscience 2000, 116:761-773.
18. Schafer MK, Nohr D, Krause JE, Weihe E. Inflammation-induced upregulation of NK1 receptor mRNA in dorsal horn neurones. Neuroreport 1993, 4:1007-1010. 10.1097/00001756-199308000-00003, 8241452.
19. McCarson KE, Krause JE. NK-1 and NK-3 type tachykinin receptor mRNA expression in the rat spinal cord dorsal horn is increased during adjuvant or formalin-induced nociception. J Neurosci 1994, 14:712-720.
20. Suzuki R, Morcuende S, Webber M, Hunt SP, Dickenson AH. Superficial NK1-expressing neurons control spinal excitability through activation of descending pathways. Nat Neurosci 2002, 5:1319-1326. 10.1038/nn966, 12402039.
21. Budai D, Khasabov SG, Mantyh PW, Simone DA. NK-1 receptors modulate the excitability of ON cells in the rostral ventromedial medulla. J Neurophysiol 2007, 97:1388-1395.
22. Pacharinsak C, Khasabov SG, Beitz AJ, Simone DA. NK-1 receptors in the rostral ventromedial medulla contribute to hyperalgesia produced by intraplantar injection of capsaicin. Pain 2008, 139:34-46. 10.1016/j.pain.2008.02.032, 18407414.
23. Hamity MV, White SR, Hammond DL. Effects of neurokinin-1 receptor agonism and antagonism in the rostral ventromedial medulla of rats with acute or persistent inflammatory nociception. Neuroscience 2010, 165:902-913. 10.1016/j.neuroscience.2009.10.064, 2815160, 19892001.
24. LaGraize SC, Guo W, Yang K, Wei F, Ren K, Dubner R. NK-1 tachykinin receptors in the rostral ventromedial medulla mediate descending facilitation of inflammatory hyperalgesia linked to 5-HT3, NMDA and GABAA receptor dependent spinal circuitry. Neuroscience 2010, 71(4):1341-1356.
25. Brink TS, Pacharinsak C, Khasabov SG, Beitz AJ, Simone DA. Differential modulation of neurons in the rostral ventromedial medulla by neurokin-1 receptors. J Neurophysiol 2012, 107(4):1210-1221. 10.1152/jn.00678.2011, 22031765.
26. Wei F, Dubner R, Zou S, Ren K, Bai G, Wei D, Guo W. Molecular depletion of descending serotonin unmasks its novel facilitatory role in the development of persistent pain. J Neurosci 2010, 30:8624-8636. 10.1523/JNEUROSCI.5389-09.2010, 2902253, 20573908.
27. Chen Y, Oatway MA, Weaver LC. Blockade of the 5-HT3 receptor for days causes sustained relief from mechanical allodynia following spinal cord injury. J Neuro Res 2008, 87(2):418-424.
28. Oatway MA, Chen Y, Weaver LC. The 5-HT3 receptor facilitates mechanical allodynia following spinal cord injury. Pain 2004, 110:259-268. 10.1016/j.pain.2004.03.040, 15275776.
29. Rahman W, Suzuki R, Webber M, Hunt SP, Dickenson AH. Depletion of endogenous spinal 5-HT attenuates the behavioural hypersensitivity to mechanical and cooling stimuli induced by spinal nerve ligation. Pain 2006, 123:264-274. 10.1016/j.pain.2006.02.033, 16644129.
30. Doucet E, Latrémolière A, Darmon M, Hamon M, Emerit MB. Immunolabelling of the 5-HT 3B receptor subunit in the central and peripheral nervous systems in rodents. Eur J Neurosci 2007, 26:355-366. 10.1111/j.1460-9568.2007.05659.x, 17650111.
31. Zeitz KP, Guy N, Malmberg AB, Dirajlal S, Martin WJ, Sun L, Bonhaus DW, Stucky CL, Julius D, Basbaum AI. The 5-HT3 subtype of serotonin receptor contributes to nociceptive processing via a novel subset of myelinated and unmyelinated nociceptors. J Neurosci 2002, 22:1010-1019.
32. Mayer DJ, Wolfle TL, Akil H, Carder B, Liebeskind JC. Analgesia from electrical stimulation in the brainstem of the rat. Science 1971, 174(4016):1351-1354. 10.1126/science.174.4016.1351, 5167502.
33. Fields HL, Heinricher MM, Mason P. Neurotransmitters in nociceptive modulatory circuits. Annu Rev Neurosci 1991, 14:219-245. 10.1146/annurev.ne.14.030191.001251, 1674413.
34. Fang FG, Haws CM, Drasner K, Williamson A, Fields HL. Opioid peptides (DAGO-enkephalin, dynorphin A(1-13), BAM 22P) microinjected into the rat brainstem: comparison of their antinociceptive effect and their effect on neuronal firing in the rostral ventromedial medulla. Brain Res 1989, 501(1):116-128. 10.1016/0006-8993(89)91033-0, 2572306.
35. Boyer JS, Morgan MM, Craft RM. Microinjection of morphine into the rostral ventromedial medulla produces greater antinociception in male compared to female rats. Brain Res 1998, 796(1-2):315-318.
36. Guan Y, Guo W, Zou SP, Dubner R, Ren K. Inflammation-induced upregulation of AMPA receptor subunit expression in brain stem pain modulatory circuitry. Pain 2003, 104(1-2):401-413.
37. Guan Y, Guo W, Robbins MT, Dubner R, Ren K. Changes in AMPA receptor phosphorylation in the rostral ventromedial medulla after inflammatory hyperalgesia in rats. Neurosci Lett 2004, 366(2):201-205. 10.1016/j.neulet.2004.05.051, 15276247.
38. Wiertelak EP, Roemer B, Maier SF, Watkins LR. Comparison of the effects of nucleus tractus solitarius and ventral medial medulla lesions on illness-induced and subcutaneous formalin induced hyperalgesias. Brain Res 1997, 748:143-150. 10.1016/S0006-8993(96)01289-9, 9067455.
39. Urban MO, Gebhart GF. Supraspinal contributions to hyperalgesia. Proc Natl Acad Sci U S A 1999, 96:7687-7692. 10.1073/pnas.96.14.7687, 33602, 10393881.
40. Ren K, Dubner R. Descending modulation in persistent pain: an update. Pain 2002, 100(1-2):1-6.
41. Porreca F, Ossipov MH, Gebhart GF. Chronic pain and medullary descending facilitation. Trends Neurosci 2002, 25(6):319-325. 10.1016/S0166-2236(02)02157-4, 12086751.
42. Heinricher MM, Tavares I, Leith JL, Lumb BM. Descending control of nociception: specificity, recruitment and plasticity. Brain Res Rev 2009, 60:214-225. 10.1016/j.brainresrev.2008.12.009, 2894733, 19146877.
43. Guo W, Wang H, Watanabe M, Shimizu K, Zou S, LaGraize SC, Wei F, Dubner R, Ren K. Glial-cytokine-neuronal interactions underlying the mechanisms of persistent pain. J Neurosci 2007, 27:6006-6018. 10.1523/JNEUROSCI.0176-07.2007, 2676443, 17537972.
44. Zhang L, Hammond DL. Substance P enhances excitatory transmission on spinally projecting neurons in the rostral ventromedial medulla after inflammatory injury. J Neurophysiol 2009, 102(2):1139-1151. 10.1152/jn.91337.2008, 2724368, 19494188.
45. Dogrul A, Ossipov MH, Porreca F. Differential mediation of descending pain facilitation and inhibition by spinal 5HT-3 and 5HT-7 receptors. Brain Res 2009, 1280:52-59.
46. Svensson CI, Tran TK, Fitzsimmons B, Yaksh TL, Hua XY. Descending serotonergic facilitation of spinal ERK activation and pain behavior. FEBS Lett 2006, 580:6629-6634. 10.1016/j.febslet.2006.11.012, 2291024, 17113581.
47. Vanegas H, Schaible H-G. Descending control of persistent pain: inhibitory or facilitatory?. Brain Res Rev 2004, 46:295-309. 10.1016/j.brainresrev.2004.07.004, 15571771.
48. Ren K, Dubner R. Enhanced descending modulation of nociception in rats with persistent hindpaw inflammation. J Neurophysiol 1996, 76:3025-3037.
49. Terayama R, Guan Y, Dubner R, Ren K. Activity-induced plasticity in brain stem pain modulatory circuitry after inflammation. Neuroreport 2000, 11:1915-1919. 10.1097/00001756-200006260-00022, 10884043.
50. Bardin L. The complex role of serotonin and 5-HT receptors in chronic pain. Behav Pharmacol 2011, 22(5-6):390-404.
51. Paxinos G, Watson C. The rat brain in stereotaxic coordinates 2005, Amsterdam: Elsevier, 5.
52. Ren K. An improved method for assessing mechanical allodynia in the rat. Physiol Behav 1999, 67:711-716. 10.1016/S0031-9384(99)00136-5, 10604842.