Differential modulation of neurons in the rostral ventromedial medulla by neurokinin-1 receptors

Journal of Neurophysiology

Volumn 107, Issue 4, 2012, Pages 1210-1221

  Brink, Thaddeus S ^a   Pacharinsak, Cholawat ^a,b   Khasabov, Sergey G ^a   Beitz, Alvin J ^b   Simone, Donald A ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Descending facilitation; Electrophysiology; Hyperalgesia; Nociception; Pain facilitation; Pain modulation; Raphe magnus; Substance p

Indexed keywords

3 [3,5 BIS(TRIFLUOROMETHYL)BENZYLOXY] 2 PHENYLPIPERIDINE; CAPSAICIN; NEUROKININ 1 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EVOKED RESPONSE; EXCITATION; HEAT SENSATION; HYPERALGESIA; MALE; MECHANICAL STIMULATION; MEDULLA OBLONGATA; NERVE CELL; NERVE CELL INHIBITION; NEUROANATOMY; NEUROMODULATION; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; RAT; ROSTRAL VENTROMEDIAL MEDULLA;

ACTION POTENTIALS; AFFERENT PATHWAYS; ANALYSIS OF VARIANCE; ANIMALS; CAPSAICIN; HYPERALGESIA; MALE; MEDULLA OBLONGATA; NEURONS; NOCICEPTION; PAIN THRESHOLD; PATCH-CLAMP TECHNIQUES; PHYSICAL STIMULATION; PIPERIDINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NEUROKININ-1; SENSORY SYSTEM AGENTS;

EID: 84856982459     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00678.2011     Document Type: Article

References (76)

1. Bederson JB, Fields HL, Barbaro NM. Hyperalgesia during naloxone-precipitated withdrawal from morphine is associated with increased on-cell activity in the rostral ventromedial medulla. Somatosens Mot Res 7: 185- 203, 1990.
2. Bee LA, Dickenson AH. Rostral ventromedial medulla control of spinal sensory processing in normal and pathophysiological states. Neuroscience 147: 786-793, 2007.
3. Brink TS, Hellman KM, Lambert AM, Mason P. Raphe magnus neurons help protect reactions to visceral pain from interruption by cutaneous pain. J Neurophysiol 96: 3423-3432, 2006.
4. Brink TS, Mason P. Raphe magnus neurons respond to noxious colorectal distension. J Neurophysiol 89: 2506-2515, 2003.
5. Budai D, Khasabov SG, Mantyh PW, Simone DA. NK-1 receptors modulate the excitability of ON cells in the rostral ventromedial medulla. J Neuro-physiol 97: 1388-1395, 2007.
6. Burgess SE, Gardell LR, Ossipov MH, Malan TP Jr, Vanderah TW, Lai J, Porreca F. Time-dependent descending facilitation from the rostral ventromedial medulla maintains, but does not initiate, neuropathic pain. J Neurosci 22: 5129-5136, 2002.
7. Carlson JD, Maire JJ, Martenson ME, Heinricher MM. Sensitization of pain-modulating neurons in the rostral ventromedial medulla after peripheral nerve injury. J Neurosci 27: 13222-13231, 2007.
8. Cervero F. Spinal cord hyperexcitability and its role in pain and hyperalgesia. Exp Brain Res 196: 129-137, 2009.
9. Coutinho SV, Urban MO, Gebhart GF. Role of glutamate receptors and nitric oxide in the rostral ventromedial medulla in visceral hyperalgesia. Pain 78: 59-69, 1998.
10. Donovan-Rodriguez T, Urch CE, Dickenson AH. Evidence of a role for descending serotonergic facilitation in a rat model of cancer-induced bone pain. Neurosci Lett 393: 237-242, 2006.
11. Fields HL. Pain modulation: expectation, opioid analgesia and virtual pain. Prog Brain Res 122: 245-253, 2000.
12. Fields HL, Bry J, Hentall I, Zorman G. The activity of neurons in the rostral medulla of the rat during withdrawal from noxious heat. J Neurosci 3: 2545-2552, 1983.
13. Gao K, Mason P. Serotonergic raphe magnus cells that respond to noxious tail heat are not ON or OFF cells. J Neurophysiol 84: 1719-1725, 2000.
14. Gilchrist HD, Allard BL, Simone DA. Enhanced withdrawal responses to heat and mechanical stimuli following intraplantar injection of capsaicin in rats. Pain 67: 179-188, 1996.
15. Goncalves L, Almeida A, Pertovaara A. Pronociceptive changes in response properties of rostroventromedial medullary neurons in a rat model of peripheral neuropathy. Eur J Neurosci 26: 2188-2195, 2007.
16. 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 366: 201-205, 2004.
17. Guan Y, Guo W, Zou SP, Dubner R, Ren K. Inflammation-induced upregu-lation of AMPA receptor subunit expression in brain stem pain modulatory circuitry. Pain 104: 401-413, 2003.
18. Guan Y, Terayama R, Dubner R, Ren K. Plasticity in excitatory amino acid receptor-mediated descending pain modulation after inflammation. J Pharmacol Exp Ther 300: 513-520, 2002.
19. Guo W, Robbins MT, Wei F, Zou S, Dubner R, Ren K. Supraspinal brain-derived neurotrophic factor signaling: a novel mechanism for descending pain facilitation. J Neurosci 26: 126-137, 2006.
20. 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 165: 902-913, 2010.
21. Heinricher MM, Neubert MJ. Neural basis for the hyperalgesic action of cholecystokinin in the rostral ventromedial medulla. J Neurophysiol 92: 1982-1989, 2004.
22. Heinricher MM, Tavares I, Leith JL, Lumb BM. Descending control of nociception: specificity, recruitment and plasticity. Brain Res Rev 60: 214-225, 2009.
23. Hernandez N, Vanegas H. Encoding of noxious stimulus intensity by putative pain modulating neurons in the rostral ventromedial medulla and by simultaneously recorded nociceptive neurons in the spinal dorsal horn of rats. Pain 91: 307-315, 2001.
24. Hurley RW, Hammond DL. Contribution of endogenous enkephalins to the enhanced analgesic effects of supraspinal mu opioid receptor agonists after inflammatory injury. J Neurosci 21: 2536-2545, 2001.
25. Imbe H, Okamoto K, Okamura T, Kumabe S, Nakatsuka M, Aikawa F, Iwai-Liao Y, Senba E. Effects of peripheral inflammation on activation of ERK in the rostral ventromedial medulla. Brain Res 1063: 151-158, 2005.
26. Imbe H, Okamoto K, Aikawa F, Kimura A, Donishi T, Tamai Y, Iwai-Liao Y, Senba E. Effects of peripheral inflammation on activation of p38 mitogen-activated protein kinase in the rostral ventromedial medulla. Brain Res 1134: 131-139, 2007.
27. Jiang M, Behbehani MM. Physiological characteristics of the projection pathway from the medial preoptic to the nucleus raphe magnus of the rat and its modulation by the periaqueductal gray. Pain 94: 139-147, 2001.
28. Jinks SL, Carstens E, Antognini JF. Isoflurane differentially modulates medullary on and off neurons while suppressing hind-limb motor withdrawals. Anesthesiology 100: 1224-1234, 2004.
29. Kaplan H, Fields HL. Hyperalgesia during acute opioid abstinence: evidence for a nociceptive facilitating function of the rostral ventromedial medulla. J Neurosci 11: 1433-1439, 1991.
30. Khasabov SG, Ghilardi JR, Mantyh PW, Simone DA. Spinal neurons that express NK-1 receptors modulate descending controls that project through the dorsolateral funiculus. J Neurophysiol 93: 998-1006, 2005.
31. Khasabov SG, Rogers SD, Ghilardi JR, Peters CM, Mantyh PW, Simone DA. Spinal neurons that possess the substance P receptor are required for the development of central sensitization. J Neurosci 22: 9086-9098, 2002.
32. Kincaid W, Neubert MJ, Xu M, Kim CJ, Heinricher MM. Role for medullary pain facilitating neurons in secondary thermal hyperalgesia. J Neurophysiol 95: 33-41, 2006.
33. Kovelowski CJ, Ossipov MH, Sun H, Lai J, Malan TP, Porreca F. Supraspinal cholecystokinin may drive tonic descending facilitation mechanisms to maintain neuropathic pain in the rat. Pain 87: 265-273, 2000.
34. Lagraize SC, Guo W, Yang K, Wei F, Ren K, Dubner R. Spinal cord mechanisms mediating behavioral hyperalgesia induced by neurokinin-1 tachykinin receptor activation in the rostral ventromedial medulla. Neuro-science 171: 1341-1356, 2010.
35. LaMotte RH, Shain CN, Simone DA, Tsai EF. Neurogenic hyperalgesia: psychophysical studies of underlying mechanisms. J Neurophysiol 66: 190-211, 1991.
36. Leung CG, Mason P. Effects of isoflurane concentration on the activity of pontomedullary raphe and medial reticular neurons in the rat. Brain Res 699: 71-82, 1995.
37. Li YW, Bayliss DA. Presynaptic inhibition by 5-HT1B receptors of glutama-tergic synaptic inputs onto serotonergic caudal raphe neurones in rat. J Physiol 510: 121-134, 1998.
38. Mantyh PW, Rogers SD, Honore P, Allen BJ, Ghilardi JR, Li J, Daughters RS, Lappi DA, Wiley RG, Simone DA. Inhibition of hyperalgesia by ablation of lamina I spinal neurons expressing the substance P receptor. Science 278: 275-279, 1997.
39. Marson L, Loewy AD. Topographic organization of substance P and mono-amine cells in the ventral medulla of the cat. J Auton Nerv Syst 14: 271-285, 1985.
40. Mason P. Contributions of the medullary raphe and ventromedial reticular region to pain modulation and other homeostatic functions. Annu Rev Neurosci 24: 737-777, 2001.
41. Mason P. Ventromedial medulla: pain modulation and beyond. J Comp Neurol 493: 2-8, 2005.
42. Mason P. Physiological identification of pontomedullary serotonergic neurons in the rat. J Neurophysiol 77: 1087-1098, 1997.
43. Meng ID, Harasawa I. Chronic morphine exposure increases the proportion of on-cells in the rostral ventromedial medulla in rats. Life Sci 80: 1915- 1920, 2007.
44. Miki K, Zhou QQ, Guo W, Guan Y, Terayama R, Dubner R, Ren K. Changes in gene expression and neuronal phenotype in brain stem pain modulatory circuitry after inflammation. J Neurophysiol 87: 750-760, 2002.
45. Mohrland JS, Gebhart GF. Effects of focal electrical stimulation and morphine microinjection in the periaqueductal gray of the rat mesencephalon on neuronal activity in the medullary reticular formation. Brain Res 201: 23-37, 1980.
46. Montagne-Clavel J, Oliveras JL. Are ventromedial medulla neuronal properties modified by chronic peripheral inflammation? A single-unit study in the awake, freely moving polyarthritic rat. Brain Res 657: 92-104, 1994.
47. Neubert MJ, Kincaid W, Heinricher MM. Nociceptive facilitating neurons in the rostral ventromedial medulla. Pain 110: 158-165, 2004.
48. Nichols ML, Allen BJ, Rogers SD, Ghilardi JR, Honore P, Luger NM, Finke MP, Li J, Lappi DA, Simone DA, Mantyh PW. Transmission of chronic nociception by spinal neurons expressing the substance P receptor. Science 286: 1558-1561, 1999.
49. Pacharinsak C, Khasabov SG, Beitz AJ, Simone DA. NK-1 receptors in the rostral ventromedial medulla contribute to hyperalgesia produced by intra-plantar injection of capsaicin. Pain 139: 34-46, 2008.
50. Paik KS, Nam SC, Chung JM. Different classes of cat spinal neurons display differential sensitivity to sodium pentobarbital. J Neurosci Res 23: 107-115, 1989.
51. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. Amsterdam: Elsevier Academic, 2005.
52. Pertovaara A, Wei H, Hamalainen MM. Lidocaine in the rostroventromedial medulla and the periaqueductal gray attenuates allodynia in neuropathic rats. Neurosci Lett 218: 127-130, 1996.
53. Pinto M, Sousa M, Lima D, Tavares I. Participation of /n-opioid, GABAB, and NK1 receptors of major pain control medullary areas in pathways targeting the rat spinal cord: implications for descending modulation of nociceptive transmission. J Comp Neurol 510: 175-187, 2008.
54. Porreca F, Ossipov MH, Gebhart GF. Chronic pain and medullary descending facilitation. Trends Neurosci 25: 319-325, 2002.
55. Ren K, Dubner R. Enhanced descending modulation of nociception in rats with persistent hindpaw inflammation. J Neurophysiol 76: 3025-3037, 1996.
56. Roberts J, Ossipov MH, Porreca F. Glial activation in the rostral ventromedial medulla promotes descending facilitation to mediate inflammatory hpersensitivity. Eur J Neurosci 30: 229-241, 2009.
57. Saffroy M, Beaujouan JC, Torrens Y, Besseyre J, Bergstrom L, Glowinski J. Localization of tachykinin binding sites (NK1, NK2, NK3 ligands) in the rat brain. Peptides 9: 227-241, 1988.
58. 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 116: 761-773, 2003.
59. Sanoja R, Tortorici V, Fernandez C, Price TJ, Cervero F. Role of RVM neurons in capsaicin-evoked visceral nociception and referred hyperalgesia. Eur J Pain 14: 120.e121-120.e129, 2010.
60. Simone DA, Baumann TK, LaMotte RH. Dose-dependent pain and mechanical hyperalgesia in humans after intradermal injection of capsaicin. Pain 38: 99-107, 1989.
61. Simone DA, Ngeow JY, Putterman GJ, LaMotte RH. Hyperalgesia to heat after intradermal injection of capsaicin. Brain Res 418: 201-203, 1987.
62. Simone DA, Sorkin LS, Oh U, Chung JM, Owens C, LaMotte RH, Willis WD. Neurogenic hyperalgesia: central neural correlates in responses of spinothalamic tract neurons. J Neurophysiol 66: 228-246, 1991.
63. Soja PJ, Taepavarapruk N, Pang W, Cairns BE, McErlane SA, Fragoso MC. Transmission through the dorsal spinocerebellar, and spinoreticular tracts: wakefulness versus thiopental anesthesia. Anesthesiology 97: 1178- 1188, 2002.
64. Suzuki R, Hunt SP, Dickenson AH. The coding of noxious mechanical and thermal stimuli of deep dorsal horn neurones is attenuated in NK1 knockout mice. Neuropharmacology 45: 1093-1100, 2003.
65. Suzuki R, Morcuende S, Webber M, Hunt SP, Dickenson AH. Superficial NK1-expressing neurons control spinal excitability through activation of descending pathways. Nat Neurosci 5: 1319-1326, 2002.
66. Suzuki R, Rahman W, Hunt SP, Dickenson AH. Descending facilitatory control of mechanically evoked responses is enhanced in deep dorsal horn neurones following peripheral nerve injury. Brain Res 1019: 68-76, 2004a.
67. Suzuki R, Rygh LJ, Dickenson AH. Bad news from the brain: descending 5-HT pathways that control spinal pain processing. Trends Pharmacol Sci 12: 613-617, 2004b.
68. Todd AJ, Puskar Z, SPike RV, Hughes C, Watt C, Forrest L. Projection neurons in lamina I of rat spinal cord with the neurokinin 1 receptor are selectively innervated by substance P-containing afferents and respond to noxious stimulation. J Neurosci 22: 4103-4113, 2002.
69. Vanderah TW, Suenaga NM, Ossipov MH, Malan TP Jr, Lai J, Porreca F. Tonic descending facilitation from the rostral ventromedial medulla mediates opioid-induced abnormal pain and antinociceptive tolerance. J Neurosci 21: 279-286, 2001.
70. Vanegas H, Schaible HG. Descending control of persistent pain: inhibitory or facilitatory? Brain Res Brain Res Rev 46: 295-309, 2004.
71. Watkins LR, Wiertelak EP, Goehler LE, Mooney-Heiberger K, Martinez J, Furness L, Smith KP, Maier SF. Neurocircuitry of illness-induced hyperalgesia. Brain Res 639: 283-299, 1994.
72. Wei F, Guo W, Zou S, Ren K, Dubner R. Supraspinal glial-neuronal interactions contribute to descending pain facilitation. J Neurosci 28: 10482-10495, 2008.
73. Xie JY, Herman DS, Stiller CO, Gardell LR, Ossipov MH, Lai J, Porreca F, Vanderah TW. Cholecystokinin in the rostral ventromedial medulla mediates opioid-induced hyperalgesia and antinociceptive tolerance. J Neu-rosci 25: 409-416, 2005.
74. Xu M, Kim CJ, Neubert MJ, Heinricher MM. NMDA receptor-mediated activation of medullary pro-nociceptive neurons is required for secondary thermal hyperalgesia. Pain 127: 253-262, 2007.
75. Zhang L, Hammond DL. Substance P enhances excitatory synaptic transmission on spinally projecting neurons in the rostral ventromedial medulla after inflammatory injury. J Neurophysiol 102: 1139-1151, 2009.
76. Zhuo M, Sengupta JN, Gebhart GF. Biphasic modulation of spinal visceral nociceptive transmission from the rostroventral medial medulla in the rat. J Neurophysiol 87: 2225-2236, 2002.