Subdivision-specific responses of neurons in the nucleus of the tractus solitarius to activation of mu-opioid receptors in the rat

Journal of Neurophysiology

Volumn 98, Issue 5, 2007, Pages 3060-3071

  Poole, Sarah L ^a   Deuchars, Jim ^a   Lewis, David I ^a   Deuchars, Susan A ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BRADYKININ; DELTA OPIATE RECEPTOR AGONIST; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; ENKEPHALIN[2,5 DEXTRO PENICILLAMINE]; KAPPA OPIATE RECEPTOR AGONIST; MU OPIATE RECEPTOR; N METHYL N [7 (1 PYRROLIDINYL) 1 OXASPIRO[4.5]DEC 8 YL]BENZENEACETAMIDE;

ANIMAL TISSUE; ARTICLE; AUTONOMIC NERVOUS SYSTEM FUNCTION; BRAIN ELECTROPHYSIOLOGY; BRAIN NERVE CELL; CONTROLLED STUDY; ELECTRON MICROSCOPY; EVOKED RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; HYPERPOLARIZATION; MALE; MICROSCOPY; NEUROANATOMY; NONHUMAN; PATCH CLAMP; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; RECEPTOR UPREGULATION; REFLEX; SOLITARY TRACT NUCLEUS;

ANALGESICS, OPIOID; ANIMALS; ANIMALS, NEWBORN; DRUG INTERACTIONS; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; MALE; MICROSCOPY, IMMUNOELECTRON; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR; RECEPTORS, OPIOID, MU; SOLITARY NUCLEUS; SOMATOSTATIN;

EID: 36249003377     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00755.2007     Document Type: Article

References (61)

1. Aicher SA, Goldberg A, Sharma S, Pickel VM. mu-opioid receptors are present in vagal afferents and their dendritic targets in the medial nucleus tractus solitarius. J Comp Neurol 422: 181-190, 2000.
2. Akil H, Watson SJ, Young E, Lewis ME, Khachaturian H, Walker JM. Endogenous opioids: biology and function. Annu Rev Neurosci 7: 223-255, 1984.
3. Altschuler SM, Bao XM, Bieger D, Hopkins DA, Miselis RR. Viscerotopic representation of the upper alimentary tract in the rat: sensory ganglia and nuclei of the solitary and spinal trigeminal tracts. J Comp Neurol 283: 248-268, 1989.
4. Altschuler SM, Ferenci DA, Lynn RB, Miselis RR. Representation of the cecum in the lateral dorsal motor nucleus of the vagus nerve and commissural subnucleus of the nucleus tractus solitarii in rat. J Comp Neurol 304: 261-274, 1991.
5. Appleyard SM, Bailey TW, Doyle MW, Jin YH, Smart JL, Low MJ, Andresen MC. Proopiomelanocortin neurons in nucleus tractus solitarius are activated by visceral afferents: regulation by cholecystokinin and opioids. J Neurosci 25: 3578-3585, 2005.
6. Arvidsson U, Dado RJ, Riedl M, Lee JH, Law PY, Loh HH, Elde R, Wessendorf MW. delta-Opioid receptor immunoreactivity: distribution in brainstem and spinal cord, and relationship to biogenic amines and enkephalin. J Neurosci 15: 1215-1235, 1995.
7. Browning KN, Kalyuzhny AE, Travagli RA. Opioid peptides inhibit excitatory but not inhibitory synaptic transmission in the rat dorsal motor nucleus of the vagus. J Neurosci 22: 2998-3004, 2002.
8. Browning KN, Kalyuzhny AE, Travagli RA. Mu-opioid receptor trafficking on inhibitory synapses in the rat brain stem. J Neurosci 24: 7344-7352, 2004.
9. Burks TF, Fox DA, Hirning LD, Shook JE, Porreca F. Regulation of gastrointestinal function by multiple opioid receptors. Life Sci 43: 2177-2181, 1988.
10. Cahill CM, Morinville A, Lee MC, Vincent JP, Collier B, Beaudet A. Prolonged morphine treatment targets delta opioid receptors to neuronal plasma membranes and enhances delta-mediated antinociception. J Neurosci 21: 7598-7607, 2001.
11. Caligiorne SM, Santos RA, Campagnole-Santos MJ. Cardiovascular effects produced by bradykinin microinjection into the nucleus tractus solitarii of anesthetized rats. Brain Res 720: 183-190, 1996.
12. Chan RK, Sawchenko PE. Organization and transmitter specificity of medullary neurons activated by sustained hypertension: implications for understanding baroreceptor reflex circuitry. J Neurosci 18: 371-387, 1998.
13. Chen EY, Emerich DF, Bartus RT, Kordower JH. B2 bradykinin receptor immunoreactivity in rat brain. J Comp Neurol 427: 1-18, 2000.
14. Cheng PY, Liu-Chen LY, Chen C, Pickel VM. Immunolabeling of Mu opioid receptors in the rat nucleus of the solitary tract: extrasynaptic plasmalemmal localization and association with Leu5-enkephalin. J Comp Neurol 371: 522-536, 1996.
15. Ciriello J. Brain stem projections of aortic baroreceptor afferent fibers in the rat. Neurosci Lett 36: 37-42, 1983.
16. Deuchars J, Li YW, Kasparov S, Paton JF. Morphological and electrophysiological properties of neurons in the dorsal vagal complex of the rat activated by arterial baroreceptors. J Comp Neurol 417: 233-249, 2000.
17. Deuchars SA, Brooke RE, Deuchars J. Adenosine A1 receptors reduce release from excitatory but not inhibitory synaptic inputs onto lateral horn neurons. J Neurosci 21: 6308-6320, 2001.
18. Deuchars SA, Brooke RE, Frater B, Deuchars J. Properties of interneurones in the intermediolateral cell column of the rat spinal cord: role of the potassium channel subunit Kv3.1. Neuroscience 106: 433-446, 2001.
19. Donoghue S, Felder RB, Jordan D, Spyer KM. The central projections of carotid baroreceptors and chemoreceptors in the cat: a neurophysiological study. J Physiol 347: 397-409, 1984.
20. Donoghue S, Garcia M, Jordan D, Spyer KM. The brain-stem projections of pulmonary stretch afferent neurones in cats and rabbits. J Physiol 322: 353-363, 1982.
21. Emmerson PJ, Liu MR, Woods JH, Medzihradsky F. Binding affinity and selectivity of opioids at mu, delta and kappa receptors in monkey brain membranes. J Pharmacol Exp Ther 271: 1630-1637, 1994.
22. Endoh T. Pharmacological characterization of inhibitory effects of postsynaptic opioid and cannabinoid receptors on calcium currents in neonatal rat nucleus tractus solitarius. Br J Pharmacol 147: 391-401, 2006.
23. Finley JC, Katz DM. The central organization of carotid body afferent projections to the brain stem of the rat. Brain Res 572: 108-116, 1992.
24. Glass MJ, Pickel VM. Alpha(2A)-adrenergic receptors are present in muopioid receptor containing neurons in rat medial nucleus tractus solitarius. Synapse 43: 208-218, 2002.
25. Goodman RR, Snyder SH, Kuhar MJ, Young WS III. Differentiation of delta and mu opiate receptor localizations by light microscopic autoradiography. Proc Natl Acad Sci USA 77: 6239-6243, 1980.
26. Hassen AH, Feuerstein G, Faden AI. Differential cardiovascular effects mediated by mu and kappa opiate receptors in hindbrain nuclei. Peptides 4: 621-625, 1983.
27. Hayakawa T, Takanaga A, Maeda S, Seki M, Yajima Y. Subnuclear distribution of afferents from the oral, pharyngeal and laryngeal regions in the nucleus tractus solitarii of the rat: a study using transganglionic transport of cholera toxin. Neurosci Res 39: 221-232, 2001.
28. Housley GD, Martin-Body RL, Dawson NJ, Sinclair JD. Brain stem projections of the glossopharyngeal nerve and its carotid sinus branch in the rat. Neuroscience 22: 237-250, 1987.
29. Kalia M, Fuxe K, Hokfelt T, Johansson O, Lang R, Ganten D, Cuello C, Terenius L. Distribution of neuropeptide immunoreactive nerve terminals within the subnuclei of the nucleus of the tractus solitarius of the rat. J Comp Neurol 222: 409-444, 1984.
30. Kalia M, Sullivan JM. Brain stem projections of sensory and motor components of the vagus nerve in the rat. J Comp Neurol 211: 248-265, 1982.
31. Kivell BM, Day DJ, McDonald FJ, Miller JH. Developmental expression of mu and delta opioid receptors in the rat brain stem: evidence for a postnatal switch in micro isoform expression. Brain Res Dev Brain Res 148: 185-196, 2004.
32. Kotz CM, Billington CJ, Levine AS. Opioids in the nucleus of the solitary tract are involved in feeding in the rat. Am J Physiol Regulatory Integrative Comp Physiol 272: R1028-R1032, 1997.
33. Lahti RA, Mickelson MM, McCall JM, Von Voigtlander PF. [3H]U-69593 a highly selective ligand for the opioid kappa receptor. Eur J Pharmacol 109: 281-284, 1985.
34. Leslie RA, Gwyn DG, Hopkins DA. The central distribution of the cervical vagus nerve and gastric afferent and efferent projections in the rat. Brain Res Bull 8: 37-43, 1982.
35. Mansour A, Burke S, Pavlic RJ, Akil H, Watson SJ. Immunohistochemical localization of the cloned kappa 1 receptor in the rat CNS and pituitary. Neuroscience 71: 671-690, 1996.
36. Mansour A, Fox CA, Burke S, Meng F, Thompson RC, Akil H, Watson SJ. Mu, delta, and kappa opioid receptor mRNA expression in the rat CNS: an in situ hybridization study. J Comp Neurol 350: 412-438, 1994.
37. Mansour A, Thompson RC, Akil H, Watson SJ. Delta opioid receptor mRNA distribution in the brain: comparison to delta receptor binding and proenkephalin mRNA. J Chem Neuroanat 6: 351-362, 1993.
38. Margolis EB, Hjelmstad GO, Bonci A, Fields HL. Kappa-opioid agonists directly inhibit midbrain dopaminergic neurons. J Neurosci 23: 9981-9986, 2003.
39. Mayne RG, Armstrong WE, Crowley WR, Bealer SL. Cytoarchitectonic analysis of Fos-immunoreactivity in brain stem neurons following visceral stimuli in conscious rats. J Neuroendocrinol 10: 839-847, 1998.
40. Mennicken F, Zhang J, Hoffert C, Ahmad S, Beaudet A, O'Donnell D. Phylogenetic changes in the expression of delta opioid receptors in spinal cord and dorsal root ganglia. J Comp Neurol 465: 349-360, 2003.
41. Milligan CJ, Buckley NJ, Garret M, Deuchars J, Deuchars SA. Evidence for inhibition mediated by coassembly of GABAA and GABAC receptor subunits in native central neurons. J Neurosci 24: 7241-7250, 2004.
42. Morinville A, Cahill CM, Esdaile MJ, Aibak H, Collier B, Kieffer BL, Beaudet A. Regulation of delta-opioid receptor trafficking via mu-opioid receptor stimulation: evidence from mu-opioid receptor knock-out mice. J Neurosci 23: 4888-4898, 2003.
43. Nomura S, Ding YQ, Kaneko T, Li JL, Mizuno N. Localization of muopioid receptor-like immunoreactivity in the central components of the vagus nerve: a light and electron microscope study in the rat. Neuroscience 73: 277-286, 1996.
44. Paton JF, Deuchars J, Li YW, Kasparov S. Properties of solitary tract neurones responding to peripheral arterial chemoreceptors. Neuroscience 105: 231-248, 2001.
45. Paton JF, Foster WR, Schwaber JS. Characteristic firing behavior of cell types in the cardiorespiratory region of the nucleus tractus solitarii of the rat. Brain Res 604: 112-125, 1993.
46. Paton JF, Li YW, Deuchars J, Kasparov S. Properties of solitary tract neurons receiving inputs from the sub-diaphragmatic vagus nerve. Neuroscience 95: 141-153, 2000.
47. Patwardhan AM, Berg KA, Akopain AN, Jeske NA, Gamper N, Clarke WP, Hargreaves KM. Bradykinin-induced functional competence and trafficking of the delta-opioid receptor in trigeminal nociceptors. J Neurosci 25: 8825-8832, 2005.
48. Paxinos G, Watson C. The Rat Brain Atlas in Stereotaxic Coordinates. San Diego, CA: Academic Press, 1998.
49. Privitera PJ, Beckstead RM, Yates P, Walgren R. Autoradiographic localization of [125I-Tyr0]bradykinin binding sites in brains of Wistar-Kyoto and spontaneously hypertensive rats. Cell Mol Neurobiol 23: 805-815, 2003.
50. Quirion R, Zajac JM, Morgat JL, Roques BP. Autoradiographic distribution of mu and delta opiate receptors in rat brain using highly selective ligands. Life Sci 33, Suppl 1: 227-230, 1983.
51. Rhim H, Glaum SR, Miller RJ. Selective opioid agonists modulate afferent transmission in the rat nucleus tractus solitarius. J Pharmacol Exp Ther 264: 795-800, 1993.
52. Rhim H, Miller RJ. Opioid receptors modulate diverse types of calcium channels in the nucleus tractus solitarius of the rat. J Neurosci 14: 7608-7615, 1994.
53. Santos SF, Melnick IV, Safronov BV. Selective postsynaptic inhibition of tonic-firing neurons in substantia gelatinosa by mu-opioid agonist. Anesthesiology 101: 1177-1183, 2004.
54. Shook JE, Kazmierski W, Wire WS, Lemcke PK, Hruby VJ, Burks TF. Opioid receptor selectivity of beta-endorphin in vitro and in vivo: mu, delta and epsilon receptors. J Pharmacol Exp Ther 246: 1018-1025, 1988.
55. Shook JE, Watkins WD, Camporesi EM. Differential roles of opioid receptors in respiration, respiratory disease, and opiate-induced respiratory depression. Am Rev Respir Dis 142: 895-909, 1990.
56. Spyer KM. The central nervous organisation of reflex circulatory control. In: Central Regulation of Autonomic Functions, edited by Loewy AD and Spyer KM. Oxford, UK: Oxford Univ. Press, 1990.
57. Waldhoer M, Bartlett SE, Whistler JL. Opioid receptors. Annu Rev Biochem 73: 953-990, 2004.
58. Xia Y, Haddad GG. Ontogeny and distribution of opioid receptors in the rat brainstem. Brain Res 549: 181-193, 1991.
59. Xie Q, Miki T, Sato K, Itoh M, Takeuchi Y. Evaluation of pulmonary afferent fibers in the nucleus tractus solitarius: a horseradish peroxidase and c-fos like immunohistochemical study in the rat. J Auton Nerv Syst 74: 120-125, 1998.
60. Zhang X, Renehan WE, Fogel R. Vagal innervation of the rat duodenum. J Auton Nerv Syst 79: 8-18, 2000.
61. Zhu W, Pan ZZ. Synaptic properties and postsynaptic opioid effects in rat central amygdala neurons. Neuroscience 127: 871-879, 2004.