Endomorphin-2-immunoreactive fibers selectively appose serotonergic neuronal somata in the rostral ventral medial medulla

Journal of Comparative Neurology

Volumn 502, Issue 5, 2007, Pages 701-713

  Gu, Ming ^a   Wessendorf, Martin ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

opioid receptor; Analgesia; Hypothalamus; Spinal cord

Indexed keywords

ENDOMORPHIN 2; MU OPIATE RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HYPOTHALAMUS; IMMUNOREACTIVITY; MALE; MEDULLA OBLONGATA; NONHUMAN; PERIKARYON; PRIORITY JOURNAL; RAT; SEROTONINERGIC NERVE CELL; SOLITARY TRACT NUCLEUS; SPINAL CORD;

ANIMALS; CELL COUNT; IMMUNOHISTOCHEMISTRY; MALE; MEDULLA OBLONGATA; NERVE FIBERS; NEURONS; OLIGOPEPTIDES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OPIOID, MU; SEROTONIN; STILBAMIDINES; TRYPTOPHAN HYDROXYLASE;

EID: 34248376565     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21343     Document Type: Article

References (52)

1. Adams JE, Hosobuchi Y. 1977. Technique and technical problems. Neurosurgery 1:196-199.
2. Aicher SA, Mitchell JL, Swanson KC, Zadina JE. 2003. Endomorphin-2 axon terminals contact mu-opioid receptor-containing dendrites in trigeminal dorsal horn. Brain Res 977:190-198.
3. Aimone L, Bauer C, Gebhart G. 1988. Brain-stem relays mediating stimulation-produced antinociception from the lateral hypothalamus in the rat. J Neurosci 8:2652-2663.
4. Akil H, Mayer DJ, Liebeskind JC. 1976. Antagonism of stimulation-produced analgesia by naloxone, a narcotic antagonist. Science 191: 961-962.
5. Arvidsson U, Riedl M, Chakrabarti S, Lee JH, Nakano AH, Dado RJ, Loh HH, Law PY, Wessendorf MW, Elde R. 1995. Distribution and targeting of a mu-opioid receptor (MORI) in brain and spinal cord. J Neurosci 15(5 Pt 1):3328-3341.
6. Bandler R, Tork I. 1987. Midbrain periaqueductal grey region in the cat has afferent and efferent connections with solitary tract nuclei. Neurosci Lett 74:1-6.
7. Barbaro NM, Heinricher MM, Fields HL. 1986. Putative pain modulating neurons in the rostral ventral medulla: reflex-related activity predicts effects of morphine. Brain Res 366:203-210.
8. Beitz AJ. 1982. The nuclei of origin of brain stem enkephalin and substance P projections to the rodent nucleus raphe magnus. Neuroscience 7:2753-2768.
9. Bowker RM, Dilts RP. 1988. Distribution of mu-opioid receptors in the nucleus raphe magnus and nucleus gigantocellularis: a quantitative autoradiographic study. Neurosci Lett 88:247-252.
10. Bowker RM, Westlund KN, Sullivan MC, Coulter JD. 1982. Organization of descending serotonergic projections to the spinal cord. Prog Brain Res 57:239-265.
11. Carstens E, MacKinnon JD, Guinan MJ. 1982. Inhibition of spinal dorsal horn neuronal responses to noxious skin heating by medial preoptic and septal stimulation in the cat. J Neurophysiol 48:981-989.
12. Fardin V, Oliveras JL, Besson JM. 1984. A reinvestigation of the analgesic effects induced by stimulation of the periaqueductal gray matter in the rat. I. The production of behavioral side effects together with analgesia. Brain Res 306:105-123.
13. Fields HL, Vanegas H, Hentall ID, Zorman G. 1983. Evidence that disinhibition of brain stem neurones contributes to morphine analgesia. Nature 306:684-686.
14. Fields HL, Malick A, Burstein R. 1995. Dorsal horn projection targets of ON and OFF cells in the rostral ventromedial medulla. J Neurophysiol 74:1742-1759.
15. Gallager DW, Pert A. 1978. Afferents to brain stem nuclei (brain stem raphe, nucleus reticularis pontis caudalis and nucleus gigantocellularis) in the rat as demonstrated by microiontophoretically applied horseradish peroxidase. Brain Res 144:257-275.
16. Gao K, Mason P. 2000. Serotonergic raphe magnus cells that respond to noxious tail heat are not ON or OFF cells. J Neurophysiol 84:1719-1725.
17. Gao K, Chen DO, Genzen JR, Mason P. 1998. Activation of serotonergic neurons in the raphe magnus is not necessary for morphine analgesia. J Neurosci 18:1860-1868.
18. Hammond DL, Yaksh TL. 1984. Antagonism of stimulation-produced antinociception by intrathecal administration of methysergide or phentolamine. Brain Res 298:329-337.
19. Heinricher MM, Kaplan HJ. 1991. GABA-mediated inhibition in rostral ventromedial medulla: role in nociceptive modulation in the lightly anesthetized rat. Pain 47:105-113.
20. Howard V, Reed MG. 1998. Unbiased stereology: three-dimensional measurement in microscopy. Oxford: BIOS Scientific.
21. Jensen TS, Yaksh TL. 1986a. Comparison of the antinociceptive action of mu and delta opioid receptor ligands in the periaqueductal gray matter, medial and paramedial ventral medulla in the rat as studied by the microinjection technique. Brain Res 372:301-312.
22. Jensen TS, Yaksh TL. 1986b. Examination of spinal monoamine receptors through which brainstem opiate-sensitive systems act in the rat. Brain Res 363:114-127.
23. Kalyuzhny AE, Arvidsson U, Wu W, Wessendorf MW. 1996. mu-Opioid and delta-opioid receptors are expressed in brainstem antinociceptive circuits: studies using immunocytochemistry and retrograde tract-tracing. J Neurosci 16:6490-6503.
24. Lewis JW, Baldrighi G, Akil H. 1987. A possible interface between autonomic function and pain control: opioid analgesia and the nucleus tractus solitarius. Brain Res 424:65-70.
25. Marinelli S, Vaughan CW, Schnell SA, Wessendorf MW, Christie MJ. 2002. Rostral ventromedial medulla neurons that project to the spinal cord express multiple opioid receptor phenotypes. J Neurosci 22:10847-10855.
26. Martin-Schild S, Zadina JE, Gerall AA, Vigh S, Kastin AJ. 1997. Localization of endomorphin-2-like immunoreactivity in the rat medulla and spinal cord. Peptides 18:1641-1649.
27. Martin-Schild S, Gerall AA, Kastin AJ, Zadina JE. 1998. Endomorphin-2 is an endogenous opioid in primary sensory afferent fibers. Peptides 19:1783-1789.
28. Martin-Schild S, Gerall AA, Kastin AJ, Zadina JE. 1999. Differential distribution of endomorphin 1- and endomorphin 2-like immunoreactivities in the CNS of the rodent. J Comp Neurol 405:450-471.
29. Mason P, Back SA, Fields HL. 1992. A confocal laser microscopic study of enkephalin-immunoreactive appositions onto physiologically identified neurons in the rostral ventromedial medulla. J Neurosci 12:4023-4036.
30. Morgan MM, Sohn J-H, Lohof AM, Ben-Eliyahu S, Liebeskind JC. 1989. Characterization of stimulation-produced analgesia from the nucleus tractus solitarius in the rat. Brain Res 486:175-180.
31. Pan ZZ, Williams JT, Osborne PB. 1990. Opioid actions on single nucleus raphe magnus neurons from rat and guinea-pig in vitro. J Physiol 427:519-532.
32. Pan ZZ, Wessendorf MW, Williams JT. 1993. Modulation by serotonin of the neurons in rat nucleus raphe magnus in vitro. Neuroscience 54: 421-429.
33. Paxinos G, Watson C. 1986. The rat brain in stereotaxic coordinates. New York: Academic Press.
34. Pierce TL, Wessendorf MW. 2000. Immunocytochemical mapping of endomorphin-2-immunoreactivity in rat brain. J Chem Neuroanat 18: 181-207.
35. Pierce TL, Grahek MD, Wessendorf MW. 1998. Immunoreactivity for endomorphin-2 occurs in primary afferents in rats and monkey. Neuroreport 9:385-389.
36. Popken GJ, Farel PB. 1997. Sensory neuron number in neonatal and adult rats estimated by means of stereologic and profile-based methods. J Comp Neurol 386:8-15.
37. Potrebic SB, Fields HL, Mason P. 1994. Serotonin immunoreactivity is contained in one physiological cell class in the rat rostral ventromedial medulla. J Neurosci 14(3 Pt 2): 1655-1665.
38. Pretel S, Ruda MA. 1988. Immunocytochemical analysis of noradrenaline, substance P and enkephalin axonal contacts on serotonin neurons in the caudal raphe nuclei of the cat. Neurosci Lett 89:19-24.
39. Rahman W, Suzuki R, Webber M, Hunt SP, Dickenson AH. 2006. Depletion of endogenous spinal 5-HT attenuates the behavioural hypersensitivity to mechanical and cooling stimuli induced by spinal nerve ligation. Pain 123:264-274.
40. Schmued LC, Swanson LW, Sawchenko PE. 1982. Some fluorescent counterstains for neuroanatomical studies. J Histochem Cytochem 30:123-128.
41. Schreff M, Schulz S, Wiborny D, Hollt V. 1998. Immunofluorescent identification of endomorphin-2-containing nerve fibers and terminals in the rat brain and spinal cord. Neuroreport 9:1031-1034.
42. Schwanzel-Fukuda M, Morrell JI, Pfaff DW. 1984. Localization of forebrain neurons which project directly to the medulla and spinal cord of the rat by retrograde tracing with wheat germ agglutinin. J Comp Neurol 226:1-20.
43. Silverman MB, Hermes SM, Zadina JE, Aicher SA. 2005. Mu-opioid receptor is present in dendritic targets of endomorphin-2 axon terminals in the nuclei of the solitary tract. Neuroscience 135:887-896.
44. Skagerberg G, Bjorklund A. 1985. Topographic principles in the spinal projections of serotonergic and non-serotonergic brainstem neurons in the rat. Neuroscience 15:445-480.
45. Suzuki R, Rahman W, Hunt SP, Dickenson AH. 2004. Descending facilitatory control of mechanically evoked responses is enhanced in deep dorsal horn neurones following peripheral nerve injury. Brain Res 1019:68-76.
46. Vanegas H, Barbaro NM, Fields HL. 1984. Tail-flick related activity in medullospinal neurons. Brain Res 321:135-141.
47. Wang H, Wessendorf MW. 1999. Mu- and delta-opioid receptor mRNAs are expressed in spinally projecting serotonergic and nonserotonergic neurons of the rostral ventromedial medulla. J Comp Neurol 404:183-196.
48. Wang QP, Zadina JE, Guan JL, Kastin AJ, Funahashi H, Shioda S. 2002. Endomorphin-2 immunoreactivity in the cervical dorsal horn of the rat spinal cord at the electron microscopic level. Neuroscience 113:593-605.
49. Willcockson WS, Kim J, Shin HK, Chung JM, Willis WD. 1986. Actions of opioids on primate spinothalamic tract neurons. J Neurosci 6:2509-2520.
50. Wu HE, Sun HS, Darpolar M, Leitermann RJ, Kampine JP, Tseng LF. 2003. Dynorphinergic mechanism mediating endomorphin-2-induced antianalgesia in the mouse spinal cord. J Pharmacol Exp Ther 307: 1135-1141.
51. Zadina JE, Hackler L, Ge LJ, Kastin AJ. 1997. A potent and selective endogenous agonist for the mu-opiate receptor. Nature 386:499-502.
52. Zhang L, Sykes KT, Buhler AV, Hammond DL. 2006. Electrophysiological heterogeneity of spinally projecting serotonergic and nonserotonergic neurons in the rostral ventromedial medulla. J Neurophysiol 95:1853-1863.