Activation of rostral ventromedial medulla neurons by noxious stimulation of Cutaneous and deep craniofacial tissues

Journal of Neurophysiology

Volumn 113, Issue 1, 2015, Pages 14-22

  Khasabov, Sergey G ^a   Malecha, Patrick ^a   Noack, Joseph ^a   Tabakov, Janneta ^a   Okamoto, Keiichiro ^a   Bereiter, David A ^a   Simone, Donald A ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

ATP; Brain stem; Capsaicin; Pain; Pain modulation; Temporomandibular joint

Indexed keywords

ADENOSINE TRIPHOSPHATE; CAPSAICIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONTROLLED STUDY; FACE PAIN; MALE; NERVE CELL STIMULATION; NERVE PROJECTION; NEUROMODULATION; NEUROTRANSMISSION; NOCICEPTIVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; RAT; ROSTRAL VENTROMEDIAL MEDULLA; SPINAL CORD DORSAL HORN; STIMULUS RESPONSE; TAIL; TEMPOROMANDIBULAR JOINT; ACTION POTENTIAL; ANIMAL; EYE; FORELIMB; HINDLIMB; MEDULLA OBLONGATA; MICROELECTRODE; NERVE CELL; NOCICEPTIVE PAIN; PATHOPHYSIOLOGY; PHYSIOLOGY; SKIN; SPRAGUE DAWLEY RAT; STIMULATION;

ACTION POTENTIALS; ADENOSINE TRIPHOSPHATE; ANIMALS; CAPSAICIN; EYE; FACIAL PAIN; FORELIMB; HINDLIMB; MALE; MEDULLA OBLONGATA; MICROELECTRODES; NEURONS; NOCICEPTIVE PAIN; PHYSICAL STIMULATION; RATS, SPRAGUE-DAWLEY; SKIN; TEMPOROMANDIBULAR JOINT;

EID: 84920903578     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00125.2014     Document Type: Article

References (47)

1. Abols IA, Basbaum AI. Afferent connections of the rostral medulla of the cat: a neural substrate for midbrain-medullary interactions in the modulation of pain. J Comp Neurol 201: 285-297, 1981.
2. Aicher SA, Hermes SM, Whittier KL, Hegarty DM. Descending projections from the rostral ventromedial medulla (RVM) to trigeminal and spinal dorsal horns are morphologically and neurochemically distinct. J Chem Neuroanat 43: 103-111, 2012.
3. Basbaum AI, Fields HL. Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry. Annu Rev Neurosci 7: 309-338, 1984.
4. Brink TS, Mason P. Raphe magnus neurons respond to noxious colorectal distension. J Neurophysiol 89: 2506-2515, 2003.
5. Brink TS, Pacharinsak C, Khasabov SG, Beitz AJ, Simone DA. Differential modulation of neurons in the rostral ventromedial medulla by neurokinin-1 receptors. J Neurophysiol 107: 1210-1221, 2012.
6. Chang Z, Okamoto K, Bereiter DA. Differential ascending projections of temporomandibular joint-responsive brainstem neurons to periaqueductal gray and posterior thalamus of male and female rats. Neuroscience 203: 230-243, 2012.
7. Chiang CY, Hu JW, Dostrovsky JO, Sessle BJ. Changes in mechanoreceptive field properties of somatosensory brainstem neurons induced by stimulation of nucleus raphe magnus in cats. Brain Res 485: 371-381, 1989.
8. Chiang CY, Hu JW, Sessle BJ. Parabrachial area and nucleus raphe magnusinduced modulation of nociceptive and nonnociceptive trigeminal subnucleus caudalis neurons activated by cutaneous or deep inputs. J Neurophysiol 71: 2430-2445, 1994.
9. Chiang CY, Hu JW, Sessle BJ. Parabrachial area and nucleus raphe magnusinduced modulation of electrically evoked trigeminal subnucleus caudalis neuronal responses to cutaneous or deep A-fiber and C-fiber inputs. Pain 62: 61-68, 1995.
10. Cleary DR, Heinricher MM. Adaptations in responsiveness of brainstem pain-modulating neurons in acute compared with chronic inflammation. Pain 154: 845-855, 2013.
11. Dostrovsky JO, Shah Y, Gray BG. 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 49: 948-960, 1983.
12. Dowd E, McQueen DS, Chessell IP, Humphrey PP. P2X receptor-mediated excitation of nociceptive afferents in the normal and arthritic rat knee joint. Br J Pharmacol 125: 341-346, 1998.
13. Ellrich J, Messlinger K, Chiang CY, Hu JW. Modulation of neuronal activity in the nucleus raphe magnus by the 5-HT1-receptor agonist naratriptan in rat. Pain 90: 227-231, 2001.
14. Ellrich J, Ulucan C, Schnell C. Are “neutral cells” in the rostral ventromedial medulla subtypes of on-and off-cells? Neurosci Res 38: 419-423, 2000.
15. Fields H, Basbaum AI, Heinricher MM. Central nervous system mechanisms of pain modulation. In: Textbook of Pain, edited by McMahon SB, Koltzenburg M. Edinburgh: Churchill Livingstone, 2006, p. 125-142.
16. Fields HL, Malick A, Burstein R. Dorsal horn projection targets of ON and OFF cells in the rostral ventromedial medulla. J Neurophysiol 74: 1742-1759, 1995.
17. 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.
18. Heinricher MM, Tavares I, Leith JL, Lumb BM. Descending control of nociception: specificity, recruitment and plasticity. Brain Res Rev 60: 214-225, 2009.
19. Hermann DM, Luppi PH, Peyron C, Hinckel P, Jouvet M. Afferent projections to the rat nuclei raphe magnus, raphe pallidus and reticularis gigantocellularis pars alpha demonstrated by iontophoretic application of choleratoxin (subunit b). J Chem Neuroanat 13: 1-21, 1997.
20. 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.
21. Khasabov SG, Brink TS, Schupp M, Noack J, Simone DA. Changes in response properties of rostral ventromedial medulla neurons during prolonged inflammation: modulation by neurokinin-1 receptors. Neuroscience 224: 235-248, 2012.
22. Khasabov SG, Okamoto K, Katagiri A, Simone DA, Bereiter DA. Activation of “NEUTRAL” cells in the RVM by noxious craniofacial stimulation (Abstract). Soc Neurosci Abstr 2013: 461.-04, 2013.
23. 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.
24. Leung CG, Mason P. Physiological survey of medullary raphe and magnocellular reticular neurons in the anesthetized rat. J Neurophysiol 80: 1630-1646, 1998.
25. Maixner W. Temporomandibular joint disorders. In: Functional Pain Syndromes: Presentation and Pathology, edited by Mayer E, Bushnell M. Seattle, WA: IASP, 2009, p. 55-69.
26. 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.
27. Mason P. Physiological identification of pontomedullary serotonergic neurons in the rat. J Neurophysiol 77: 1087-1098, 2009.
28. Mason P. Medullary circuits for nociceptive modulation. Curr Opin Neurobiol 22: 640-645, 2012.
29. Mason P, Gao K, Genzen JR. Serotonergic raphe magnus cell discharge reflects ongoing autonomic and respiratory activities. J Neurophysiol 98: 1919-1927, 2007.
30. Meng ID, Hu JW, Bereiter DA. Parabrachial area and nucleus raphe magnus inhibition of corneal units in rostral and caudal portions of trigeminal subnucleus caudalis in the rat. Pain 87: 241-251, 2000.
31. Miki K, Zhou QQ, Guo W, 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.
32. Okamoto K, Tashiro A, Chang Z, Thompson R, Bereiter DA. Temporomandibular joint-evoked responses by spinomedullary neurons and masseter muscle are enhanced after repeated psychophysical stress. Eur J Neurosci 36: 2025-2034, 2012.
33. Oliveira MC, Parada CA, Veiga MC, Rodrigues LR, Barros SP, Tambeli CH. Evidence for the involvement of endogenous ATP and P2X receptors in TMJ pain. Eur J Pain 9: 87-93, 2005.
34. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. New York: Academic, 2007.
35. Porreca F, Ossipov MH, Gebhart GF. Chronic pain and medullary descending facilitation. Trends Neurosci 25: 319-325, 2002.
36. Potrebic SB, Fields HL, Mason P. Serotonin immunoreactivity is contained in one physiological cell class in the rat rostral ventromedial medulla. J Neurosci 14: 1655-1665, 1994.
37. Ren K, Dubner R. Descending modulation in persistent pain: an update. Pain 100: 1-6, 2002.
38. Sarlani E, Greenspan JD. Evidence for generalized hyperalgesia in temporomandibular disorders patients. Pain 102: 221-226, 2003.
39. Schnell C, Ulucan C, Ellrich J. Atypical on-, off-and neutral cells in the rostral ventromedial medulla oblongata in rat. Exp Brain Res 145: 64-75, 2002.
40. 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 493: 510-523, 2005.
41. Takeshita S, Hirata H, Bereiter DA. Intensity coding by TMJ-responsive neurons in superficial laminae of caudal medullary dorsal horn of the rat. J Neurophysiol 86: 2393-2404, 2001.
42. Tashiro A, Okamoto K, Bereiter DA. Morphine modulation of temporomandibular joint-responsive units in superficial laminae at the spinomedullary junction in female rats depends on estrogen status. Eur J Neurosci 28: 2065-2074, 2008.
43. Thurston CL, Randich A. Effects of vagal afferent stimulation on and OFF cells in the rostroventral medulla: relationships to nociception and arterial blood pressure. J Neurophysiol 67: 180-196, 1992.
44. Watkins LR, Griffin G, Leichnetz GR, Mayer DJ. The somatotopic organization of the nucleus raphe magnus and surrounding brain stem structures as revealed by HRP slow-release gels. Brain Res 181: 1-15, 1980.
45. Wolstencroft JH. Reticulospinal neurons. J Physiol 174: 91-108, 1964.
46. Yu XM, Mense S. Response properties and descending control of rat dorsal horn neurons with deep receptive fields. Neuroscience 39: 823-831, 1990.
47. Yunus MB. Fibromyalgia and overlapping disorders: the unifying concept of central sensitivity syndromes. Semin Arthritis Rheum 36: 339-356, 2007.