Plasticity in the brainstem vagal circuits controlling gastric motor function triggered by corticotropin releasing factor

Journal of Physiology

Volumn 592, Issue 20, 2014, Pages 4591-4605

  Browning, Kirsteen N ^a   Babic, Tanja ^a   Toti, Luca ^a   Holmes, Gregory M ^a   Coleman, F Holly ^a   Travagli, R Alberto ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2',3' DIDEOXYADENOSINE; ADENYLATE CYCLASE; CORTICOTROPIN RELEASING FACTOR; CYCLIC AMP DEPENDENT PROTEIN KINASE; GLUTAMATE DECARBOXYLASE 67; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; NITRIC OXIDE; OXYTOCIN; OXYTOCIN RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR; ADENYLATE CYCLASE INHIBITOR; CYCLIC AMP;

ACUTE STRESS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONNECTOME; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; GABAERGIC TRANSMISSION; GASTRIC TONE; IN VITRO STUDY; IN VIVO STUDY; INHIBITORY POSTSYNAPTIC POTENTIAL; MALE; NERVE CELL PLASTICITY; NONHUMAN; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SIGNAL TRANSDUCTION; STOMACH MOTILITY; STOMACH PARAMETERS; VAGUS NERVE; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN STEM; CYTOLOGY; DRUG EFFECTS; GENETICS; INNERVATION; METABOLISM; MOTONEURON; PHYSIOLOGY; SPRAGUE DAWLEY RAT; STOMACH; STOMACH EMPTYING;

ADENYLYL CYCLASE INHIBITORS; ANIMALS; BRAIN STEM; CORTICOTROPIN-RELEASING HORMONE; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; EXCITATORY POSTSYNAPTIC POTENTIALS; GABAERGIC NEURONS; GASTRIC EMPTYING; INHIBITORY POSTSYNAPTIC POTENTIALS; MOTOR NEURONS; NEURONAL PLASTICITY; NITRIC OXIDE; OXYTOCIN; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OXYTOCIN; STOMACH; VAGUS NERVE;

EID: 84912054826     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2014.278192     Document Type: Article

References (48)

1. Babic T, Browning KN & Travagli RA (2011). Differential organization of excitatory and inhibitory synapses within the rat dorsal vagal complex. Am J Physiol Gastrointest Liver Physiol 300, G21-G32.
2. Babygirija R, Bulbul M, Cerjak D, Ludwig K & Takahashi T (2011). Sustained acceleration of colonic transit following chronic homotypic stress in oxytocin knockout mice. Neurosci Lett 495, 77-81.
3. Babygirija R, Bulbul M, Yoshimoto S, Ludwig K & Takahashi T (2012). Central and peripheral release of oxytocin following chronic homotypic stress in rats. Auton Neurosci 167, 56-60.
4. Babygirija R, Zheng J, Bulbul M, Cerjak D, Ludwig K & Takahashi T (2010a). Sustained delayed gastric emptying during repeated restraint stress in oxytocin knockout mice. J Neuroendocrinol 22, 1181-1186.
5. Babygirija R, Zheng J, Ludwig K & Takahashi T (2010b). Central oxytocin is involved in restoring impaired gastric motility following chronic repeated stress in mice. Am J Physiol Regul Integr Comp Physiol 298, R157-R165.
6. Berthoud HR, Sutton GM, Townsend RL, Patterson LM & Zheng H (2006). Brainstem mechanisms integrating gut-derived satiety signals and descending forebrain information in the control of meal size. Physiol Behav 89, 517-524.
7. Blake CB & Smith BN (2014). cAMP-dependent insulin modulation of synaptic inhibition in neurons of the dorsal motor nucleus of the vagus is altered in diabetic mice. Am J Physiol Regul Integr Comp Physiol (in press; DOI: 10.1152/ajpregu.00138.2014).
8. Browning KN, Kalyuzhny AE & Travagli RA (2004). μ-Opioid receptor trafficking on inhibitory synapses in the rat brainstem. J Neurosci 24, 9344-9352.
9. Browning KN, Renehan WE & Travagli RA (1999). Electrophysiological and morphological heterogeneity of rat dorsal vagal neurones which project to specific areas of the gastrointestinal tract. J Physiol 517, 521-532.
10. 1A receptors via activation of a second messenger pathway in the rat dorsal vagal complex. J Physiol 531, 425-435.
11. Browning KN & Travagli RA (2007). Functional organization of presynaptic metabotropic glutamate receptors in vagal brainstem circuits. J Neurosci 27, 8979-8988.
12. Browning KN & Travagli RA (2009). Modulation of inhibitory neurotransmission in brainstem vagal circuits by NPY and PYY is controlled by cAMP levels. Neurogastroenterol Motil 21, 1309-e126.
13. Browning KN, Zheng Z, Gettys TW & Travagli RA (2006). Vagal afferent control of opioidergic effects in rat brainstem circuits. J Physiol 575, 761-776.
14. Buckinx R, Adriaensen D, Nassauw LV & Timmermans JP (2011). Corticotrophin-releasing factor, related peptides, and receptors in the normal and inflamed gastrointestinal tract. Front Neurosci 5, 54.
15. Bulbul M, Babygirija R, Ludwig K & Takahashi T (2010). Central oxytocin attenuates augmented gastric postprandial motility induced by restraint stress in rats. Neurosci Lett 479, 302-306.
16. Chang HY, Mashimo H & Goyal RK (2003). Musings on the Wanderer: What's new in our understanding of vago-vagal reflex? IV. Current concepts of vagal efferent projections to the gut. Am J Physiol Gastrointest Liver Physiol 284, G357-G366.
17. Drucker DJ (2006). The biology of incretin hormones. Cell Metab 3, 153-165.
18. Dufresne M, Seva C & Fourmy D (2006). Cholecystokinin and gastrin receptors. Physiol Rev 86, 805-847.
19. Flanagan LM, Olson BR, Sved AF, Verbalis JG & Stricker EM (1992). Gastric motility in conscious rats given oxytocin and an oxytocin antagonist centrally. Brain Res 578, 256-260.
20. Fujimiya M & Inui A (2001). Peptidergic regulation of gastrointestinal motility in rodents. Peptides 21, 1565-1582.
21. Garrick T, Veiseh A, Sierra A, Weiner H & Tache Y (1988). Corticotropin-releasing factor acts centrally to suppress stimulated gastric contractility. Reg Pept 21, 173-181.
22. Goyal RK & Rattan S (1980). VIP as a possible neurotransmitter of non-cholinergic non-adrenergic inhibitory neurons. Nature 288, 378-380.
23. Grudt TJ, Williams JT & Travagli RA (1995). Inhibition by 5-hydroxytryptamine and noradrenaline in substantia gelatinosa of guinea-pig spinal trigeminal nucleus. J Physiol 485, 113-120.
24. Heymann-Monnikes I, Tache Y, Trauner M, Weiner H & Garrick T (1991). CRF microinjected into the dorsal vagal complex inhibits TRH analog- and kainic acid-stimulated gastric contractility in rats. Brain Res 554, 139-144.
25. Holmes GM, Browning KN, Babic T, Fortna SR, Coleman FH & Travagli RA (2013). Vagal afferent fibres determine the oxytocin-induced modulation of gastric tone. J Physiol 591, 3081-3100.
26. Holmes GM, Browning KN, Tong M, Qualls-Creekmore E & Travagli RA (2009). Vagally mediated effects of glucagon-like peptide 1: in vitro and in vivo gastric actions. J Physiol 587, 4749-4759.
27. Krowicki ZK & Hornby PJ (1996). Contribution of acetylcholine, vasoactive intestinal polypeptide and nitric oxide to CNS-evoked vagal gastric relaxation in the rat. Neurogastroenterol Motil 8, 307-317.
28. Lenz HJ, Raedler A, Greten H, Vale WW & Rivier JE (1988). Stress-induced gastrointestinal secretory and motor responses in rats are mediated by endogenous corticotropin-releasing factor. Gastroenterol 95, 1510-1517.
29. Lewis MW, Hermann GE, Rogers RC & Travagli RA (2002). In vitro and in vivo analysis of the effects of corticotropin releasing factor on rat dorsal vagal complex. J Physiol 543, 135-146.
30. Llewellyn-Smith IJ, Kellett DO, Jordan D, Browning KN & Travagli RA (2012). Oxytocin-immunoreactive innervation of identified neurons in the rat dorsal vagal complex. Neurogastroenterol Motil 24, e136-e146.
31. Martinez V, Rivier J, Wang L & Tache Y (1997). Central injecton of a new corticotropin-releasing factor (CRF) antagonist, astressin, blocks CRF- and stress-related alterations of gastric and colonic motor function. J Pharmacol Exp Therap 280, 754-760.
32. Mayo KE, Miller LJ, Bataille D, Dalle S, Goke B, Thorens B & Drucker DJ (2003). International Union of Pharmacology. XXXV. The glucagon receptor family. Pharmacol Rev 55, 167-194.
33. Monnikes H, Schmidt BG, Raybould HE & Tache Y (1992). CRF in the paraventricular nucleus mediates gastric and colonic motor response to restraint stress. Am J Physiol Gastrointest Liver Physiol 262, G137-G143.
34. Onaka T, Takayanagi Y & Yoshida M (2012). Roles of oxytocin neurones in the control of stress, energy metabolism, and social behaviour. J Neuroendocrinol 24, 587-598.
35. Peters JH, McDougall SJ, Kellett DO, Jordan D, Llewellyn-Smith IJ & Andresen MC (2008). Oxytocin enhances cranial visceral afferent synaptic transmission to the solitary tract nucleus. J Neurosci 28, 11731-11740.
36. Richar P, Moos F & Freund-Mercier M-J (1991). Central effects of oxytocin. Physiol Rev 71, 331-370.
37. Rinaman L (1998). Oxytocinergic inputs to the nucleus of the solitary tract and dorsal motor nucleus of the vagus in neonatal rats. J Comp Neurol 399, 101-109.
38. A receptors in rat hindbrain nuclei controlling gastric motor function. Neurogastroenterol Motil 10, 305-313.
39. Stengel A & Tache Y (2008). Neuroendocrine control of the gut during stress: corticotropin-releasing factor signaling pathways in the spotlight. Annu Rev Physiol 71, 219-239.
40. Swanson LW & Kuypers HG (1980). 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 194, 555-570.
41. Tache Y, Goto Y & Gunion MW (1983). Inhibition of gastric acid secretion in rats by intracerebral injection of corticotropin-releasing factor. Science 222, 935-937.
42. Tache Y, Maeda-Hagiwara M & Turkelson CM (1987). Central nervous system action of corticotropin-releasing factor to inhibit gastric emptying in rats. Am J Physiol Gastrointest Liver Physiol 253, G241-G245.
43. Tache Y & Million M (2006). Central corticotropin-releasing factor and the hypothalamic-pituitary-adrenal axis in gastrointestinal physiology. In Physiology of the Gastrointestinal Tract, ed. Johnson LR, pp. 791-816. Academic Press.
44. Travagli RA, Hermann GE, Browning KN & Rogers RC (2006). Brainstem circuits regulating gastric function. Annu Rev Physiol 68, 279-305.
45. Tsukamoto K, Nakade Y, Mantyh C, Ludwig K, Pappas TN & Takahashi T (2006). Peripherally administered CRF stimulates colonic motility via central CRF receptors and vagal pathways in conscious rats. Am J Physiol Regul Integr Comp Physiol 290, R1537-R1541.
46. Veening JG, de Jong T & Barendregt HP (2010). Oxytocin-messages via the cerebrospinal fluid: behavioral effects; a review. Physiol Behav 101, 193-210.
47. Voorn P & Buijs RM (1983). 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 270, 169-173.
48. Zheng J, Babygirija R, Bulbul M, Cerjak D, Ludwig K & Takahashi T (2010). Hypothalamic oxytocin mediates adaptation mechanism against chronic stress in rats. Am J Physiol Gastrointest Liver Physiol 299, G946-G953.