Ionic currents underlying the response of rat dorsal vagal neurones to hypoglycaemia and chemical anoxia

Journal of Physiology

Volumn 579, Issue 3, 2007, Pages 691-702

  Balfour, Robert H ^a,b   Trapp, Stefan ^a,b  

^a CHELSEA AND WESTMINSTER HOSPITAL   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ADENOSINE TRIPHOSPHATASE (POTASSIUM); CHLORIDE CHANNEL; POTASSIUM CHANNEL; GLUCOSE; INWARDLY RECTIFYING POTASSIUM CHANNEL;

ANIMAL CELL; ANOXIA; ARTICLE; BRAIN MITOCHONDRION; CELL MEMBRANE DEPOLARIZATION; CHANNEL GATING; CONTROLLED STUDY; ELECTRIC POTENTIAL; ENZYME INHIBITION; FEMALE; HYPERPOLARIZATION; HYPOGLYCEMIA; ION CURRENT; MALE; MEMBRANE CURRENT; METABOLIC INHIBITION; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL RESPIRATION; NERVE CONDUCTION; NONHUMAN; POTASSIUM CONDUCTANCE; PRIORITY JOURNAL; RAT; SPRAGUE DAWLEY RAT; VAGUS NERVE DORSAL NUCLEUS; ANIMAL TISSUE; BRAIN HYPOXIA; CELL SUBPOPULATION; CHOLINERGIC NERVE CELL; DORSAL VAGAL NERVE CELL; GLUCOSE METABOLISM; ION TRANSPORT; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE STEADY POTENTIAL; SMALL INWARD CURRENT; VAGUS NERVE;

ACTION POTENTIALS; ADENOSINE TRIPHOSPHATE; ANIMALS; ANOXIA; BRAIN STEM; CHEMORECEPTORS; ENERGY METABOLISM; FEMALE; GLUCOSE; HYPOGLYCEMIA; MALE; MITOCHONDRIA; NA(+)-K(+)-EXCHANGING ATPASE; ORGAN CULTURE TECHNIQUES; POTASSIUM; POTASSIUM CHANNELS, INWARDLY RECTIFYING; RATS; RATS, SPRAGUE-DAWLEY; VAGUS NERVE;

EID: 33947189587     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2006.126094     Document Type: Article

References (49)

1. Ashcroft FM (1988). Adenosine 5′-triphosphate-sensitive potassium channels. Annu Rev Neurosci 11, 97-118.
2. + channels. Pflugers Arch 415, 479-483.
3. Balfour RH, Hansen AM & Trapp S (2006). Neuronal responses to transient hypoglycaemia in the dorsal vagal complex of the rat brainstem. J Physiol 570, 469-484.
4. Ballanyi K, Doutheil J & Brockhaus J (1996). Membrane potentials and microenvironment of rat dorsal vagal cells in vitro during energy depletion. J Physiol 495, 769-784.
5. 2+ during metabolic activation of K ATP channels in spontaneously active dorsal vagal neurons in medullary slices. Eur J Neurosci 10, 2574-2585.
6. Borg MA, Tamborlane WV, Shulman GI & Sherwin RS (2003). Local lactate perfusion of the ventromedial hypothalamus suppresses hypoglycemic counterregulation. Diabetes 52, 663-666.
7. Buckler KJ, Williams BA & Honore E (2000). An oxygen-, acid- and anaesthetic-sensitive TASK-like background potassium channel in rat arterial chemoreceptor cells. J Physiol 525, 135-142.
8. + channels mediate inhibition of orexin neurons by glucose. Neuron 50, 711-722.
9. + conductance. J Physiol 548, 731-743.
10. Cowan AI & Martin RL (1992). Ionic basis of membrane potential changes induced by anoxia in rat dorsal vagal motoneurones. J Physiol 455, 89-109.
11. Cowan AI & Martin RL (1995). Simultaneous measurement of pH and membrane potential in rat dorsal vagal motoneurons during normoxia and hypoxia: A comparison in bicarbonate and HEPES buffers. J Neurophysiol 74, 2713-2721.
12. + channels in glucose-sensing in the rat solitary tract nucleus. Neurosci Lett 278, 77-80.
13. Dunn-Meynell AA, Routh VH, Kang L, Gaspers L & Levin BE (2002). Glucokinase is the likely mediator of glucosensing in both glucose-excited and glucose-inhibited central neurons. Diabetes 51, 2056-2065.
14. Erdemli G, Xu YZ & Krnjevic K (1998). Potassium conductance causing hyperpolarization of CA1 hippocampal neurons during hypoxia. J Neurophysiol 80, 2378-2390.
15. Ferreira M Jr, Browning KN, Sahibzada N, Verbalis JG, Gillis RA & Travagli RA (2001). Glucose effects on gastric motility and tone evoked from the rat dorsal vagal complex. J Physiol 536, 141-152.
16. Hille B (2001). Ion Channals of Excitable Membranes. Sinauer Associates, Inc., Sunderland.
17. + channels mediate effects of 5-HT and extracellular pH in rat dorsal vagal neurones in vitro. J Physiol 568, 145-154.
18. Kang L, Dunn-Meynell AA, Routh VH, Gaspers LD, Nagata Y, Nishimura T, Eiki J, Zhang BB & Levin BE (2006). Glucokinase is a critical regulator of ventromedial hypothalamic neuronal glucosensing. Diabetes 55, 412-420.
19. Krnjevic K & Xu Y (1990). Mechanisms underlying anoxic hyperpolarization of hippocampal neurons. Can J Physiol Pharmacol 68, 1609-1613.
20. Laughton WB & Powley TL (1987). Localization of efferent function in the dorsal motor nucleus of the vagus. Am J Physiol Regul Integr Comp Physiol 252, R13-R25.
21. Liss B & Roeper J (2001). Molecular physiology of neuronal K-ATP channels. Mol Membr Biol 18, 117-127.
22. Martin RL (1999). Block of rapid depolarization induced by in vitro energy depletion of rat dorsal vagal motoneurones. J Physiol 519, 131-141.
23. + channels in the hypothalamus are essential for the maintenance of glucose homeostasis. Nat Neurosci 4, 507-512.
24. Mizuno Y & Oomura Y (1984). Glucose responding neurons in the nucleus tractus solitarius of the rat: In vitro study. Brain Res 307, 109-116.
25. Mobbs CV, Kow LM & Yang XJ (2001). Brain glucose-sensing mechanisms: ubiquitous silencing by aglycemia vs. hypothalamic neuroendocrine responses. Am J Physiol Endocrinol Metab 281, E649-E654.
26. Niki I, Ashcroft FM & Ashcroft SJ (1989). The dependence on intracellular ATP concentration of ATP-sensitive K-channels and of Na,K-ATPase in intact HIT-T15 β-cells. FEBS Lett 257, 361-364.
27. Oomura Y, Ono T, Ooyama H & Wayner MJ (1969). Glucose and osmosensitive neurones of the rat hypothalamus. Nature 222, 282-284.
28. Oomura Y, Ooyama H, Sugimori M, Nakamura T & Yamada Y (1974). Glucose inhibition of the glucose-sensitive neurone in the rat lateral hypothalamus. Nature 247, 284-286.
29. Powley TL (2000). Vagal circuitry mediating cephalic-phase responses to food. Appetite 34, 184-188.
30. ATP channel activity in dorsal vagal neurons of juvenile rats in situ during metabolic disturbances. Brain Res 1017, 137-145.
31. Ritter RC, Slusser PG & Stone S (1981). Glucoreceptors controlling feeding and blood glucose: Location in the hindbrain. Science 213, 451-452.
32. Routh VH (2002). Glucose-sensing neurons: Are they physiologically relevant?Physiol Behav 76, 403-413.
33. Sakura H, Ashcroft SJ, Terauchi Y, Kadowaki T & Ashcroft FM (1998). Glucose modulation of ATP-sensitive K-currents in wild-type, homozygous and heterozygous glucokinase knock-out mice. Diabetologia 41, 654-659.
34. +-ATPase in rat auditory thalamus. J Physiol 502, 375-385.
35. Silver IA & Erecinska M (1998). Glucose-induced intracellular ion changes in sugar-sensitive hypothalamic neurons. J Neurophysiol 79, 1733-1745.
36. Song Z, Levin BE, McArdle JJ, Bakhos N & Routh VH (2001). Convergence of pre- and postsynaptic influences on glucosensing neurons in the ventromedial hypothalamic nucleus. Diabetes 50, 2673-2681.
37. Song Z & Routh VH (2005). Differential effects of glucose and lactate on glucosensing neurons in the ventromedial hypothalamic nucleus. Diabetes 54, 15-22.
38. Spanswick D, Smith MA, Groppi VE, Logan SD & Ashford ML (1997). Leptin inhibits hypothalamic neurons by activation of ATP-sensitive potassium channels. Nature 390, 521-525.
39. + channels in hypothalamic neurons of lean, but not obese rats. Nat Neurosci 3, 757-758.
40. Talley EM, Solorzano G, Lei Q, Kim D & Bayliss DA (2001). CNS distribution of members of the two-pore-domain (KCNK) potassium channel family. J Neurosci 21, 7491-7505.
41. Thomas RC (1972). Electrogenic sodium pump in nerve and muscle cells. Physiol Rev 52, 563-594.
42. ATP channel mediation of anoxia-induced outward current in rat dorsal vagal neurons in vitro. J Physiol 487, 37-50.
43. Travagli RA, Hermann GE, Browning KN & Rogers RC (2006). Brainstem circuits regulating gastric function. Annu Rev Physiol 68, 279-305.
44. Williams BA & Buckler KJ (2004). Biophysical properties and metabolic regulation of a TASK-like potassium channel in rat carotid body type 1 cells. Am J Physiol Lung Cell Mol Physiol 286, L221-L230.
45. Wu X, Gao J, Yan J, Owyang C & Li Y (2004). Hypothalamus-brain stem circuitry responsible for vagal efferent signaling to the pancreas evoked by hypoglycemia in rat. J Neurophysiol 91, 1734-1747.
46. Wyatt CN & Buckler KJ (2004). The effect of mitochondrial inhibitors on membrane currents in isolated neonatal rat carotid body type I cells. J Physiol 556, 175-191.
47. Yamada K, Ji JJ, Yuan H, Miki T, Sato S, Horimoto N, Shimizu T, Seino S & Inagaki N (2001). Protective role of ATP-sensitive potassium channels in hypoxia-induced generalized seizure. Science 292, 1543-1546.
48. Yang XJ, Kow LM, Funabashi T & Mobbs CV (1999). Hypothalamic glucose sensor: Similarities to and differences from pancreatic β-cell mechanisms. Diabetes 48, 1763-1772.
49. Yang XJ, Kow LM, Pfaff DW & Mobbs CV (2004). Metabolic pathways that mediate inhibition of hypothalamic neurons by glucose. Diabetes 53, 67-73.