Changes in response properties of rostral ventromedial medulla neurons during prolonged inflammation: Modulation by neurokinin-1 receptors

Neuroscience

Volumn 224, Issue , 2012, Pages 235-248

  Khasabov, S G ^a   Brink, T S ^a   Schupp, M ^a   Noack, J ^a   Simone, D A ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Descending facilitation; Electrophysiology; Hyperalgesia; Inflammatory pain; Rostral ventromedial medulla

Indexed keywords

NEUROKININ 1 RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CELL STIMULATION; CONTROLLED STUDY; HINDLIMB; HYPERALGESIA; INFLAMMATION; MALE; NERVE CELL; NERVE CELL EXCITABILITY; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; ROSTRAL VENTROMEDIAL MEDULLA NERVE CELL;

ANIMALS; HYPERALGESIA; INFLAMMATION; MALE; MEDULLA OBLONGATA; NEURONS; PAIN; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NEUROKININ-1;

EID: 84866529131     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.08.029     Document Type: Article

References (97)

1. Aimone L.D., Gebhart G.F. Stimulation-produced spinal inhibition from the midbrain in the rat is mediated by an excitatory amino acid neurotransmitter in the medial medulla. J Neurosci 1986, 6:1803-1813.
2. Andrew D., Greenspan J.D. Mechanical and heat sensitization of cutaneous nociceptors after peripheral inflammation in the rat. J Neurophysiol 1999, 82:2649-2656.
3. Basbaum A.I., Fields H.L. Endogenous pain control mechanisms: review and hypothesis. Ann Neurol 1978, 4:451-462.
4. Basbaum A.I., Fields H.L. Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry. Annu Rev Neurosci 1984, 7:309-338.
5. Bederson J.B., Fields H.L., Barbaro N.M. Hyperalgesia during naloxone-precipitated withdrawal from morphine is associated with increased on-cell activity in the rostral ventromedial medulla. Somatosens Mot Res 1990, 7:185-203.
6. Behbehani M.M. Functional characteristics of the midbrain periaqueductal gray. Prog Neurobiol 1995, 46:575-605.
7. Brink T.S., Mason P. Raphe magnus neurons respond to noxious colorectal distension. J Neurophysiol 2003, 89:2506-2515.
8. Brink T.S., Hellman K.M., Lambert A.M., Mason P. Raphe magnus neurons help protect reactions to visceral pain from interruption by cutaneous pain. J Neurophysiol 2006, 96:3423-3432.
9. Brink T.S., Pacharinsak C., Khasabov S.G., Beitz A.J., Simone D.A. Differential modulation of neurons in the rostral ventromedial medulla by neurokinin-1 receptors. J Neurophysiol 2012, 107:1210-1221.
10. Budai D., Khasabov S.G., Mantyh P.W., Simone D.A. NK-1 receptors modulate the excitability of ON cells in the rostral ventromedial medulla. J Neurophysiol 2007, 97:1388-1395.
11. Burgess S.E., Gardell L.R., Ossipov M.H., Malan T.P., Vanderah T.W., Lai J., Porreca F. Time-dependent descending facilitation from the rostral ventromedial medulla maintains, but does not initiate, neuropathic pain. J Neurosci 2002, 22:5129-5136.
12. Cao Y.Q., Mantyh P.W., Carlson E.J., Gillespie A.M., Epstein C.J., Basbaum A.I. Primary afferent tachykinins are required to experience moderate to intense pain. Nature 1998, 392:390-394.
13. Carlson J.D., Maire J.J., Martenson M.E., Heinricher M.M. Sensitization of pain-modulating neurons in the rostral ventromedial medulla after peripheral nerve injury. J Neurosci 2007, 27:13222-13231.
14. Coutinho S.V., Urban M.O., Gebhart G.F. Role of glutamate receptors and nitric oxide in the rostral ventromedial medulla in visceral hyperalgesia. Pain 1998, 78:59-69.
15. Criswell H.E. Analgesia and hyperactivity following morphine microinjection into mouse brain. Pharmacol Biochem Behav 1976, 4:23-26.
16. Donovan-Rodriguez T., Urch C.E., Dickenson A.H. Evidence of a role for descending serotonergic facilitation in a rat model of cancer-induced bone pain. Neurosci Lett 2006, 393:237-242.
17. Dostrovsky J.O., Shah Y., Gray B.G. Descending inhibitory influences from periaqueductal gray, nucleus raphe magnus, and adjacent reticular formation. II. Effects on medullary dorsal horn nociceptive and nonnociceptive neurons. J Neurophysiol 1983, 49:948-960.
18. Dougherty P.M., Palecek J., Paleckova V., 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. J Neurophysiol 1994, 72:1464-1475.
19. Duggan A.W., Morton C.R. Tonic descending inhibition and spinal nociceptive transmission. Prog Brain Res 1988, 77:193-211.
20. Fields H. State-dependent opioid control of pain. Nat Rev Neurosci 2004, 5:565-575.
21. Fields H.L., Heinricher M.M. Anatomy and physiology of a nociceptive modulatory system. Philos Trans R Soc Lond B Biol Sci 1985, 308:361-374.
22. Fields H.L., Bry J., Hentall I., Zorman G. The activity of neurons in the rostral medulla of the rat during withdrawal from noxious heat. J Neurosci 1983, 3:2545-2552.
23. Fields H.L., Heinricher M.M., Mason P. Neurotransmitters in nociceptive modulatory circuits. Annu Rev Neurosci 1991, 14:219-245.
24. Gao K., Kim Y.H., Mason P. Serotonergic pontomedullary neurons are not activated by antinociceptive stimulation in the periaqueductal gray. J Neurosci 1997, 17:3285-3292.
25. 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 2007, 26:2188-2195.
26. Guan Y., Guo W., Zou S.P., Dubner R., Ren K. Inflammation-induced upregulation of AMPA receptor subunit expression in brain stem pain modulatory circuitry. Pain 2003, 104:401-413.
27. Guo W., Robbins M.T., Wei F., Zou S., Dubner R., Ren K. Supraspinal brain-derived neurotrophic factor signaling: a novel mechanism for descending pain facilitation. J Neurosci 2006, 26:126-137.
28. Guo W., Wang H., Watanabe M., Shimizu K., Zou S., LaGraize S.C., Wei F., Dubner R., Ren K. Glial-cytokine-neuronal interactions underlying the mechanisms of persistent pain. J Neurosci 2007, 27:6006-6018.
29. Hamity MV, Hammond DL (2011) Persistent peripheral inflammation increases the number of neurokinin-1 receptor (NK1-R) expressing neurons in the rostral ventromedial medulla (RVM). Neuroscience Meeting Planner Program No. 805.05.
30. Hamity M.V., White S.R., Hammond D.L. 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.
31. Heinricher M.M., Drasner K. Lumbar intrathecal morphine alters activity of putative nociceptive modulatory neurons in rostral ventromedial medulla. Brain Res 1991, 549:338-341.
32. Heinricher M.M., Neubert M.J. Neural basis for the hyperalgesic action of cholecystokinin in the rostral ventromedial medulla. J Neurophysiol 2004, 92:1982-1989.
33. Heinricher M.M., Barbaro N.M., Fields H.L. Putative nociceptive modulating neurons in the rostral ventromedial medulla of the rat: firing of on- and off-cells is related to nociceptive responsiveness. Somatosens Mot Res 1989, 6:427-439.
34. Heinricher M.M., Morgan M.M., Tortorici V., Fields H.L. Disinhibition of off-cells and antinociception produced by an opioid action within the rostral ventromedial medulla. Neuroscience 1994, 63:279-288.
35. Heinricher M.M., Tavares I., Leith J.L., Lumb B.M. Descending control of nociception: specificity, recruitment and plasticity. Brain Res Rev 2009, 60:214-225.
36. Hurley R.W., Hammond D.L. The analgesic effects of supraspinal mu and delta opioid receptor agonists are potentiated during persistent inflammation. J Neurosci 2000, 20:1249-1259.
37. Hurley R.W., Banfor P., Hammond D.L. Spinal pharmacology of antinociception produced by microinjection of mu or delta opioid receptor agonists in the ventromedial medulla of the rat. Neuroscience 2003, 118:789-796.
38. Hylden J.L., Nahin R.L., Traub R.J., Dubner R. Expansion of receptive fields of spinal lamina I projection neurons in rats with unilateral adjuvant-induced inflammation: the contribution of dorsal horn mechanisms. Pain 1989, 37:229-243.
39. Imbe H., Kimura A., Okamoto K., Donishi T., Aikawa F., Senba E., Tamai Y. Activation of ERK in the rostral ventromedial medulla is involved in hyperalgesia during peripheral inflammation. Brain Res 2008, 1187:103-110.
40. Jinks S.L., Carstens E., Antognini J.F. Isoflurane differentially modulates medullary on and off neurons while suppressing hind-limb motor withdrawals. Anesthesiology 2004, 100:1224-1234.
41. Jones S.L., Gebhart G.F. Spinal pathways mediating tonic, coeruleospinal, and raphe-spinal descending inhibition in the rat. J Neurophysiol 1987, 58:138-159.
42. Kaplan H., Fields H.L. Hyperalgesia during acute opioid abstinence: evidence for a nociceptive facilitating function of the rostral ventromedial medulla. J Neurosci 1991, 11:1433-1439.
43. Khasabov S.G., Rogers S.D., Ghilardi J.R., Peters C.M., Mantyh P.W., Simone D.A. Spinal neurons that possess the substance P receptor are required for the development of central sensitization. J Neurosci 2002, 22:9086-9098.
44. Khasabov S.G., Ghilardi J.R., Mantyh P.W., Simone D.A. Spinal neurons that express NK-1 receptors modulate descending controls that project through the dorsolateral funiculus. J Neurophysiol 2005, 93:998-1006.
45. Kovelowski C.J., Ossipov M.H., Sun H., Lai J., Malan T.P., Porreca F. Supraspinal cholecystokinin may drive tonic descending facilitation mechanisms to maintain neuropathic pain in the rat. Pain 2000, 87:265-273.
46. Lagraize S.C., 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. Neuroscience 2010, 171:1341-1356.
47. Li H.S., Monhemius R., Simpson B.A., Roberts M.H. Supraspinal inhibition of nociceptive dorsal horn neurones in the anaesthetized rat: tonic or dynamic?. J Physiol (Lond) 1998, 506(Pt. 2):459-469.
48. Ljungdahl A., Hokfelt T., Nilsson G. Distribution of substance P-like immunoreactivity in the central nervous system of the rat - I. Cell bodies and nerve terminals. Neuroscience 1978, 3:861-943.
49. Marson L., Loewy A.D. Topographic organization of substance P and monoamine cells in the ventral medulla of the cat. J Auton Nerv Syst 1985, 14:271-285.
50. Martin G., Montagne-Clavel J., Oliveras J.L. Involvement of ventromedial medulla "multimodal, multireceptive" neurons in opiate spinal descending control system: a single-unit study of the effect of morphine in the awake, freely moving rat. J Neurosci 1992, 12:1511-1522.
51. Mason P. Physiological identification of pontomedullary serotonergic neurons in the rat. J Neurophysiol 1997, 77:1087-1098.
52. Mason P. Central mechanisms of pain modulation. Curr Opin Neurobiol 1999, 9:436-441.
53. Mason P. Medullary circuits for nociceptive modulation. Curr Opin Neurobiol 2012, 22:640-645.
54. McCreery D.B., Bloedel J.R., Hames E.G. Effects of stimulating in raphe nuclei and in reticular formation on response of spinothalamic neurons to mechanical stimuli. J Neurophysiol 1979, 42:166-182.
55. Meng I.D., Harasawa I. Chronic morphine exposure increases the proportion of on-cells in the rostral ventromedial medulla in rats. Life Sci 2007, 80:1915-1920.
56. Miki K., Zhou Q.Q., 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 2002, 87:750-760.
57. Millan M.J. Descending control of pain. Prog Neurobiol 2002, 66:355-474.
58. Montagne-Clavel J., Oliveras J.L. Are ventromedial medulla neuronal properties modified by chronic peripheral inflammation? A single-unit study in the awake, freely moving polyarthritic rat. Brain Res 1994, 657:92-104.
59. 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.
60. Namjoshi D.R., McErlane S.A., Taepavarapruk N., Soja P.J. Network actions of pentobarbital in the rat mesopontine tegmentum on sensory inflow through the spinothalamic tract. J Neurophysiol 2009, 102:700-713.
61. Neubert M.J., Kincaid W., Heinricher M.M. Nociceptive facilitating neurons in the rostral ventromedial medulla. Pain 2004, 110:158-165.
62. Pacharinsak C., Khasabov S.G., Beitz A.J., Simone D.A. NK-1 receptors in the rostral ventromedial medulla contribute to hyperalgesia produced by intraplantar injection of capsaicin. Pain 2008, 139:34-46.
63. Paik K.S., Nam S.C., Chung J.M. Different classes of cat spinal neurons display differential sensitivity to sodium pentobarbital. J Neurosci Res 1989, 23:107-115.
64. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Academic Press, New York, NY. 4th ed.
65. Pertovaara A., Wei H., Hamalainen M.M. Lidocaine in the rostroventromedial medulla and the periaqueductal gray attenuates allodynia in neuropathic rats. Neurosci Lett 1996, 218:127-130.
66. Porreca F., Ossipov M.H., Gebhart G.F. Chronic pain and medullary descending facilitation. Trends Neurosci 2002, 25:319-325.
67. Potenzieri C., Brink T.S., Pacharinsak C., Simone D.A. Cannabinoid modulation of cutaneous Adelta nociceptors during inflammation. J Neurophysiol 2008, 100:2794-2806.
68. Potrebic S.B., Fields H.L., Mason P. Serotonin immunoreactivity is contained in one physiological cell class in the rat rostral ventromedial medulla. J Neurosci 1994, 14:1655-1665.
69. Pubols L.M., Simone D.A., Bernau N.A., Atkinson J.D. Anesthetic blockade of the dorsolateral funiculus enhances evoked activity of spinal cord dorsal horn neurons. J Neurophysiol 1991, 66:140-152.
70. Ren K., Dubner R. Enhanced descending modulation of nociception in rats with persistent hindpaw inflammation. J Neurophysiol 1996, 76:3025-3037.
71. Ren K., Dubner R. Inflammatory models of pain and hyperalgesia. ILAR J 1999, 40:111-118.
72. Ren K., Hylden J.L., Williams G.M., Ruda M.A., Dubner R. The effects of a non-competitive NMDA receptor antagonist, MK-801, on behavioral hyperalgesia and dorsal horn neuronal activity in rats with unilateral inflammation. Pain 1992, 50:331-344.
73. Roberts J., Ossipov M.H., Porreca F. Glial activation in the rostroventromedial medulla promotes descending facilitation to mediate inflammatory hypersensitivity. Eur J Neurosci 2009, 30:229-241.
74. Saffroy M., Beaujouan J.C., Torrens Y., Besseyre J., Bergstrom L., Glowinski J. Localization of tachykinin binding sites (NK1, NK2, NK3 ligands) in the rat brain. Peptides 1988, 9:227-241.
75. Saffroy M., Torrens Y., Glowinski J., Beaujouan J.C. Autoradiographic distribution of tachykinin NK2 binding sites in the rat brain: comparison with NK1 and NK3 binding sites. Neuroscience 2003, 116:761-773.
76. Sandkuhler J., Fu Q.G., Zimmermann M. Spinal pathways mediating tonic or stimulation-produced descending inhibition from the periaqueductal gray or nucleus raphe magnus are separate in the cat. J Neurophysiol 1987, 58:327-341.
77. Sanoja R., Tortorici V., Fernandez C., Price T.J., Cervero F. Role of RVM neurons in capsaicin-evoked visceral nociception and referred hyperalgesia. Eur J Pain 2010, 14:120.e1-120.e9.
78. Simone D.A., Khasabov S.G., Hamamoto D.T. Changes in response properties of nociceptive dorsal horn neurons in a murine model of cancer pain. Sheng Li Xue Bao 2008, 60:635-644.
79. Soja P.J., Taepavarapruk N., Pang W., Cairns B.E., McErlane S.A., Fragoso M.C. Transmission through the dorsal spinocerebellar and spinoreticular tracts: wakefulness versus thiopental anesthesia. Anesthesiology 2002, 97:1178-1188.
80. Suzuki R., Morcuende S., Webber M., Hunt S.P., Dickenson A.H. Superficial NK1-expressing neurons control spinal excitability through activation of descending pathways. Nat Neurosci 2002, 5:1319-1326.
81. Suzuki R., Rahman W., Hunt S.P., Dickenson A.H. Descending facilitatory control of mechanically evoked responses is enhanced in deep dorsal horn neurones following peripheral nerve injury. Brain Res 2004, 1019:68-76.
82. Suzuki R., Rygh L.J., Dickenson A.H. Bad news from the brain: descending 5-HT pathways that control spinal pain processing. Trends Pharmacol Sci 2004, 25:613-617.
83. Suzuki R., Rahman W., Rygh L.J., Webber M., Hunt S.P., Dickenson A.H. Spinal-supraspinal serotonergic circuits regulating neuropathic pain and its treatment with gabapentin. Pain 2005, 117:292-303.
84. Terayama R., Guan Y., Dubner R., Ren K. Activity-induced plasticity in brain stem pain modulatory circuitry after inflammation. Neuroreport 2000, 11:1915-1919.
85. Terayama R., Dubner R., Ren K. The roles of NMDA receptor activation and nucleus reticularis gigantocellularis in the time-dependent changes in descending inhibition after inflammation. Pain 2002, 97:171-181.
86. Tracey D.J. Ascending and descending pathways in the spinal cord. The rat nervous system 1995, Academic Press, San Diego, New York, Boston, London Sydney, Tokyo, Toronto. G. Paxinos (Ed.).
87. Urban M.O., Gebhart G.F. Supraspinal contributions to hyperalgesia. Proc Natl Acad Sci U S A 1999, 96:7687-7692.
88. Urban M.O., Coutinho S.V., Gebhart G.F. Involvement of excitatory amino acid receptors and nitric oxide in the rostral ventromedial medulla in modulating secondary hyperalgesia produced by mustard oil. Pain 1999, 81:45-55.
89. Urban M.O., Zahn P.K., Gebhart G.F. Descending facilitatory influences from the rostral medial medulla mediate secondary, but not primary hyperalgesia in the rat. Neuroscience 1999, 90:349-352.
90. Vanegas H. To the descending pain-control system in rats, inflammation-induced primary and secondary hyperalgesia are two different things. Neurosci Lett 2004, 361:225-228.
91. Watkins L.R., Wiertelak E.P., Goehler L.E., Mooney-Heiberger K., Martinez J., Furness L., Smith K.P., Maier S.F. Neurocircuitry of illness-induced hyperalgesia. Brain Res 1994, 639:283-299.
92. Watkins L.R., Wiertelak E.P., McGorry M., Martinez J., Schwartz B., Sisk D., Maier S.F. Neurocircuitry of conditioned inhibition of analgesia: effects of amygdala, dorsal raphe, ventral medullary, and spinal cord lesions on antianalgesia in the rat. Behav Neurosci 1998, 112:360-378.
93. Wei F., Guo W., Zou S., Ren K., Dubner R. Supraspinal glial-neuronal interactions contribute to descending pain facilitation. J Neurosci 2008, 28:10482-10495.
94. Wiertelak E.P., Furness L.E., Horan R., Martinez J., Maier S.F., Watkins L.R. Subcutaneous formalin produces centrifugal hyperalgesia at a non-injected site via the NMDA-nitric oxide cascade. Brain Res 1994, 649:19-26.
95. Zhang L., Hammond D.L. Substance P enhances excitatory synaptic transmission on spinally projecting neurons in the rostral ventromedial medulla after inflammatory injury. J Neurophysiol 2009, 102:1139-1151.
96. Zhuo M., Gebhart G.F. Facilitation and attenuation of a visceral nociceptive reflex from the rostroventral medulla in the rat. Gastroenterology 2002, 122:1007-1019.
97. Zhuo M., Sengupta J.N., Gebhart G.F. Biphasic modulation of spinal visceral nociceptive transmission from the rostroventral medial medulla in the rat. J Neurophysiol 2002, 87:2225-2236.