Oxytocin-immunoreactive innervation of identified neurons in the rat dorsal vagal complex

Neurogastroenterology and Motility

Volumn 24, Issue 3, 2012, Pages

  Llewellyn Smith, I J ^a   Kellett, D O ^b   Jordan, D ^b   Browning, K N ^c   Travagli, R A ^c  

^a FLINDERS UNIVERSITY   (Australia)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

Dorsal motor nucleus of the vagus; Immunoreactivity; Nucleus of the solitary tract; Stomach; Tyrosine hydroxylase; Ultrastructure

Indexed keywords

CHOLINE ACETYLTRANSFERASE; DEOXYGLUCOSE; OXYTOCIN; PROTEIN C FOS; TYROSINE 3 MONOOXYGENASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; AREA POSTREMA; ARTICLE; DENDRITE; FEMALE; GASTROINTESTINAL TRACT FUNCTION; ILEUM; IMMUNOPEROXIDASE STAINING; IMMUNOREACTIVITY; MALE; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SOLITARY TRACT NUCLEUS; STOMACH; VAGUS NERVE DORSAL NUCLEUS; VAGUS NERVE STIMULATION; VARICOSIS;

ANIMALS; AREA POSTREMA; DEOXYGLUCOSE; FEMALE; GASTROINTESTINAL TRACT; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; NEURONS; OXYTOCIN; RATS; RATS, SPRAGUE-DAWLEY; SOLITARY NUCLEUS; VAGUS NERVE;

EID: 84856780604     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/j.1365-2982.2011.01851.x     Document Type: Article

References (66)

1. Andresen MC, Kunze DL. Nucleus tractus solitarius - gateway to neural circulatory control. Annu Rev Physiol 1994; 56: 93-116.
2. Travagli RA, Hermann GE, Browning KN, Rogers RC. Brainstem circuits regulating gastric function. Annu Rev Physiol 2006; 68: 279-305.
3. Hornby PJ. Receptors and transmission in the brain-gut axis. II. Excitatory amino acid receptors in the brain-gut axis. Am J Physiol Gastrointest Liver Physiol 2001; 280: G1055-60.
4. Browning KN, Travagli RA. Plasticity of vagal brainstem circuits in the control of gastric function. Neurogastroenterol Motil 2010; 22: 1154-63.
5. Andresen MC, Paton JFR. The nucleus of the solitary tract: processing information from viscerosensory afferents. In: Llewellyn-Smith IJ, Verberne AJM, eds. Central Regulation of Autonomic Functions, 2nd edn. New York: Oxford University Press, 2011: 23-46.
6. Bailey TW, Hermes SM, Andresen MC, Aicher SA. Cranial visceral afferent pathways through the nucleus of the solitary tract to caudal ventrolateral medulla or paraventricular hypothalamus: target-specific synaptic reliability and convergence patterns. J Neurosci 2006; 26: 11893-902.
7. Bonham AC, Chen CY, Sekizawa S, Joad JP. Plasticity in the nucleus tractus solitarius and its influence on lung and airway reflexes. J Appl Physiol 2006; 101: 322-7.
8. Jin YH, Bailey TW, Li BY, Schild JH, Andresen MC. Purinergic and vanilloid receptor activation releases glutamate from separate cranial afferent terminals in nucleus tractus solitarius. J Neurosci 2004; 24: 4709-17.
9. Fox EA, Powley TL. Longitudinal columnar organization within the dorsal motor nucleus represents separate branches of the abdominal vagus. Brain Res 1985; 341: 269-82.
10. Shapiro RE, Miselis RR. The central organization of the vagus nerve innervating the stomach of the rat. J Comp Neurol 1985; 238: 473-88.
11. Norgren R, Smith GP. Central distribution of subdiaphragmatic vagal branches in the rat. J Comp Neurol 1988; 273: 207-23.
12. Berthoud HR, Carlson NR, Powley TL. Topography of efferent vagal innervation of the rat gastrointestinal tract. Am J Physiol 1991; 260: R200-7.
13. Voorn P, Buijs RM. An immuno-electronmicroscopical study comparing vasopressin, oxytocin, substance P and enkephalin containing nerve terminals in the nucleus of the solitary tract of the rat. Brain Res 1983; 270: 169-73.
14. Higa KT, Mori E, Viana FF, Morris M, Michelini LC. Baroreflex control of heart rate by oxytocin in the solitary-vagal complex. Am J Physiol Regul Integr Comp Physiol 2002; 282: R537-45.
15. Blevins JE, Eakin TJ, Murphy JA, Schwartz MW, Baskin DG. Oxytocin innervation of caudal brainstem nuclei activated by cholecystokinin. Brain Res 2003; 993: 30-41.
16. Peters JH, McDougall SJ, Kellett DO, Jordan D, Llewellyn-Smith IJ, Andresen MC. Oxytocin enhances cranial visceral afferent synaptic transmission to the solitary tract nucleus. J Neurosci 2008; 28: 11731-40.
17. Saper CB, Loewy AD, Swanson LW, Cowan WM. Direct hypothalamo-autonomic connections. Brain Res 1976; 117: 305-12.
18. Swanson LW, Kuypers HG. The paraventricular nucleus of the hypothalamus: cytoarchitectonic subdivisions and organization of projections to the pituitary, dorsal vagal complex, and spinal cord as demonstrated by retrograde fluorescence double-labeling methods. J Comp Neurol 1980; 194: 555-70.
19. Richard P, Moos F, Freund-Mercier MJ. Central effects of oxytocin. Physiol Rev 1991; 71: 331-70.
20. Flanagan LM, Olson BR, Sved AF, Verbalis JG, Stricker EM. Gastric motility in conscious rats given oxytocin and an oxytocin antagonist centrally. Brain Res 1992; 578: 256-60.
21. Rinaman L. Oxytocinergic inputs to the nucleus of the solitary tract and dorsal motor nucleus of the vagus in neonatal rats. J Comp Neurol 1998; 399: 101-9.
22. Verbalis JG, McCann MJ, McHale CM, Stricker EM. Oxytocin secretion in response to cholecystokinin and food: differentiation of nausea from satiety. Science 1986; 232: 1417-9.
23. Tribollet E, Charpak S, Schmidt A, Dubois-Dauphin M, Dreifuss JJ. Appearance and transient expression of oxytocin receptors in fetal, infant, and peripubertal rat brain studied by autoradiography and electrophysiology. J Neurosci 1989; 9: 1764-73.
24. Raggenbass M, Dreifuss JJ. Mechanism of action of oxytocin in rat vagal neurones: induction of a sustained sodium-dependent current. J Physiol 1992; 457: 131-42.
25. Fujimiya M, Inui A. Peptidergic regulation of gastrointestinal motility in rodents. Peptides 2000; 21: 1565-82.
26. Olson BR, Drutarosky MD, Chow MS, Hruby VJ, Stricker EM, Verbalis JG. Oxytocin and an oxytocin agonist administered centrally decrease food intake in rats. Peptides 1991; 12: 113-8.
27. Siaud P, Puech R, Assenmacher I, Alonso G. Microinjection of oxytocin into the dorsal vagal complex decreases pancreatic insulin secretion. Brain Res 1991; 546: 190-4.
28. Dreifuss JJ, Raggenbass M, Charpak S, Dubois-Dauphin M, Tribollet E. A role of central oxytocin in autonomic functions: its action in the motor nucleus of the vagus nerve. Brain Res Bull 1988; 20: 765-70.
29. Tribollet E, Barberis C, Jard S, Dubois-Dauphin M, Dreifuss JJ. Localization and pharmacological characterization of high affinity binding sites for vasopressin and oxytocin in the rat brain by light microscopic autoradiography. Brain Res 1988; 442: 105-18.
30. Windle RJ, Kershaw YM, Shanks N, Wood SA, Lightman SL, Ingram CD. Oxytocin attenuates stress-induced c-fos mRNA expression in specific forebrain regions associated with modulation of hypothalamo-pituitary-adrenal activity. J Neurosci 2004; 24: 2974-82.
31. Neumann ID. Brain oxytocin: a key regulator of emotional and social behaviours in both females and males. J Neuroendocrinol 2008; 20: 858-65.
32. Zheng J, Babygirija R, Bulbul M, Cerjak D, Ludwig K, Takahashi T. Hypothalamic oxytocin mediates adaptation mechanism against chronic stress in rats. Am J Physiol Gastrointest Liver Physiol 2010; 299: G946-53.
33. Babygirija R, Zheng J, Ludwig K, Takahashi T. Central oxytocin is involved in restoring impaired gastric motility following chronic repeated stress in mice. Am J Physiol Regul Integr Comp Physiol 2010; 298: R157-65.
34. Camilleri M, Malagelada JR, Kao PC, Zinsmeister AR. Gastric and autonomic responses to stress in functional dyspepsia. Dig Dis Sci 1986; 31: 1169-77.
35. Geeraerts B, Vandenberghe J, Van OL et al. Influence of experimentally induced anxiety on gastric sensorimotor function in humans. Gastroenterology 2005; 129: 1437-44.
36. Thumshirn M. Pathophysiology of functional dyspepsia. Gut 2002; 51(Suppl 1): i63-6.
37. Tack J, Lee KJ. Pathophysiology and treatment of functional dyspepsia. J Clin Gastroenterol 2005; 39: S211-6.
38. Jones GA, Llewellyn-Smith IJ, Jordan D. Physiological, pharmacological, and immunohistochemical characterisation of juxtacellularly labelled neurones in rat nucleus tractus solitarius. Auton Neurosci 2002; 98: 12-6.
39. Jeggo RD, Kellett DO, Wang Y, Ramage AG, Jordan D. The role of central 5-HT3 receptors in vagal reflex inputs to neurones in the nucleus tractus solitarius of anaesthetized rats. J Physiol 2005; 566: 939-53.
40. Llewellyn-Smith IJ, DiCarlo SE, Collins HL, Keast JR. Enkephalin-immunoreactive interneurons extensively innervate sympathetic preganglionic neurons regulating the pelvic viscera. J Comp Neurol 2005; 488: 278-89.
41. Llewellyn-Smith IJ, Schreihofer AM, Guyenet PG. Distribution and amino acid content of enkephalin-immunoreactive inputs onto juxtacellularly labelled bulbospinal barosensitive neurons in rat rostral ventrolateral medulla. Neuroscience 2001; 108: 307-22.
42. Llewellyn-Smith IJ, Martin CL, Arnolda LF, Minson JB. Retrogradely transported CTB-saporin kills sympathetic preganglionic neurons. NeuroReport 1999; 10: 307-12.
43. Ritter S, Llewellyn-Smith IJ, Dinh TT. Subgroups of hindbrain catecholamine neurons are selectively activated by 2-deoxy-D-glucose induced metabolic challenge. Brain Res 1998; 805: 41-54.
44. Pilowsky P, Llewellyn-Smith IJ, Lipski J, Chalmers J. Substance P immunoreactive boutons form synapses with feline sympathetic preganglionic neurons. J Comp Neurol 1992; 320: 121-35.
45. Sawchenko PE, Swanson LW. Immunohistochemical identification of neurons in the paraventricular nucleus of the hypothalamus that project to the medulla or to the spinal cord in the rat. J Comp Neurol 1982; 205: 260-72.
46. Siaud P, Denoroy L, Assenmacher I, Alonso G. Comparative immunocytochemical study of the catecholaminergic and peptidergic afferent innervation to the dorsal vagal complex in rat and guinea pig. J Comp Neurol 1989; 290: 323-35.
47. Raggenbass M, Dubois-Dauphin M, Charpak S, Dreifuss JJ. Neurons in the dorsal motor nucleus of the vagus nerve are excited by oxytocin in the rat but not in the guinea pig. Proc Natl Acad Sci USA 1987; 84: 3926-30.
48. Mantella RC, Rinaman L, Vollmer RR, Amico JA. Cholecystokinin and D-fenfluramine inhibit food intake in oxytocin-deficient mice. Am J Physiol Regul Integr Comp Physiol 2003; 285: R1037-45.
49. Ritter S, Dinh TT, Li AJ. Hindbrain catecholamine neurons control multiple glucoregulatory responses. Physiol Behav 2006; 89: 490-500.
50. Gue M. Effect of stress on gastrointestinal motility. In: Johnson LR, Barrett KE, Merchant JL, Ghishan FK, Said HM, Wood JD, eds. Physiology of the Gastrointestinal Tract. London: Academic Press, 2006: 781-90.
51. Nakade Y, Tsuchida D, Fukuda H, Iwa M, Pappas TN, Takahashi T. Restraint stress delays solid gastric emptying via a central CRF and peripheral sympathetic neuron in rats. Am J Physiol Regul Integr Comp Physiol 2005; 288: R427-32.
52. Tache Y, Martinez V, Million M, Wang L. Stress and the gastrointestinal tract III. Stress-related alterations of gut motor function: role of brain corticotropin-releasing factor receptors. Am J Physiol Gastrointest Liver Physiol 2001; 280: G173-7.
53. Tache Y, Bonaz B. Corticotropin-releasing factor receptors and stress-related alterations of gut motor function. J Clin Invest 2007; 117: 33-40.
54. Nakade Y, Tsuchida D, Fukuda H, Iwa M, Pappas TN, Takahashi T. Restraint stress augments postprandial gastric contractions but impairs antropyloric coordination in conscious rats. Am J Physiol Regul Integr Comp Physiol 2006; 290: R616-24.
55. Bulbul M, Babygirija R, Ludwig K, Takahashi T. Central oxytocin attenuates augmented gastric postprandial motility induced by restraint stress in rats. Neurosci Lett 2010; 479: 302-6.
56. Troncon LE, Thompson DG, Ahluwalia NK, Barlow J, Heggie L. Relations between upper abdominal symptoms and gastric distension abnormalities in dysmotility like functional dyspepsia and after vagotomy. Gut 1995; 37: 17-22.
57. Holtmann G, Goebell H, Jockenhoevel F, Talley NJ. Altered vagal and intestinal mechanosensory function in chronic unexplained dyspepsia. Gut 1998; 42: 501-6.
58. Tack J. Neurophysiologic mechanisms of gastric reservoir function. In: Johnson LR, Barrett KE, Merchant JL, Ghishan FK, Said HM, Wood JD, eds. Physiology of the Gastrointestinal Tract. London: Academic Press, 2006: 927-34.
59. Lewis MW, Hermann GE, Rogers RC, Travagli RA. In vitro and in vivo analysis of the effects of corticotropin releasing factor on rat dorsal vagal complex. J Physiol 2002; 543: 135-46.
60. Browning KN, Travagli RA. Modulation of Brainstem Vagal Inhibitory Circuits in Response to Application of CRF and Oxytocin. In Vitro Studies. San Diego (CA): Gastroenterology Digestive Diseases Week, 2008.
61. Banihashemi L, Rinaman L. Repeated brief postnatal maternal separation enhances hypothalamic gastric autonomic circuits in juvenile rats. Neuroscience 2010; 165: 265-77.
62. Oreland S, Gustafsson-Ericson L, Nylander I. Short- and long-term consequences of different early environmental conditions on central immunoreactive oxytocin and arginine vasopressin levels in male rats. Neuropeptides 2010; 44: 391-8.
63. Liu LS, Winston JH, Shenoy MM, Song GQ, Chen JD, Pasricha PJ. A rat model of chronic gastric sensorimotor dysfunction resulting from transient neonatal gastric irritation. Gastroenterology 2008; 134: 2070-9.
64. Llewellyn-Smith IJ, Martin CL, Fenwick NM, DiCarlo SE, Lujan HL, Schreihofer AM. VGLUT1 and VGLUT2 innervation in autonomic regions of intact and transected rat spinal cord. J Comp Neurol 2007; 503: 741-67.
65. Llewellyn-Smith IJ, Pilowsky P, Minson JB, Chalmers J. Synapses on axons of sympathetic preganglionic neurons in rat and rabbit spinal cord. J Comp Neurol 1995; 354: 193-208.
66. Fenwick NM, Martin CL, Llewellyn-Smith IJ. Immunoreactivity for cocaine- and amphetamine-regulated transcript in rat sympathetic preganglionic neurons projecting to sympathetic ganglia and the adrenal medulla. J Comp Neurol 2006; 495: 422-33.