ATP-sensitive potassium channel blockade enhances spontaneous alternation performance in the rat: A potential mechanism for glucose-mediated memory enhancement

Neuroscience

Volumn 93, Issue 2, 1999, Pages 557-563

  Stefani, M R ^a   Nicholson, G M ^a   Gold, P E ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Glucose; K ATP; Memory; Opioids; Rat; Septum

Indexed keywords

ADENOSINE TRIPHOSPHATE; GLIBENCLAMIDE; GLUCOSE; MORPHINE; POTASSIUM CHANNEL; POTASSIUM CHANNEL BLOCKING AGENT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CONTROLLED STUDY; HISTOLOGY; HYPOTHESIS; INTRACEREBRAL DRUG ADMINISTRATION; LEARNING; MALE; MEMORY; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BRAIN; GLUCOSE; GLYBURIDE; HYPOGLYCEMIC AGENTS; MALE; MAZE LEARNING; MEMORY; MICROINJECTIONS; MORPHINE; NARCOTICS; POTASSIUM CHANNEL BLOCKERS; POTASSIUM CHANNELS; POTASSIUM CHANNELS, INWARDLY RECTIFYING; PSYCHOMOTOR PERFORMANCE; RATS; RATS, SPRAGUE-DAWLEY; SEPTAL NUCLEI;

EID: 0032777487     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(99)00128-1     Document Type: Article

References (68)

1. Ämmälä C., Moorhouse A., Gribble F., Ashfield R., Proks P., Smith P.A., Sadura H., Coles B., Ashcroft S.J.H., Ashcroft F.M. Promiscuous coupling between the sulphonylurea receptor and inwardly rectifying potassium channels. Nature. 379:1996;545-548.
2. + channels. Science. 247:1990;852-854.
3. Andersen B.J., Marmarou A. Functional compartmentalization of energy production in neural tissue. Brain Res. 585:1992;190-195.
4. Ashcroft F.M. Adenosine 5′-triphosphate-sensitive potassium channels. A. Rev. Neurosci. 11:1988;97-118.
5. ATP channels. Science. 282:1998;1141-1144.
6. Bielarczyk H., Szutowicz A. Evidence for the regulatory function of synaptoplasmic acetyl-CoA in acetylcholine synthesis in nerve endings. Biochem. J. 262:1989;377-380.
7. Blaker W.D., Peruzzi G., Costa E. Behavioral and neurochemical differentiation of specific projections in the septal-hippocampal cholinergic pathway of the rat. Proc. natn. Acad. Sci. U.S.A. 81:1984;1880-1882.
8. Bostock E., Gallagher M., King R.A. Effects of opioid microinjections into the medial septal area on spatial memory in rats. Behav. Neurosci. 102:1988;643-652.
9. Brase D.A., Han Y.-H., Dewey W.L. Effects of glucose and diabetes on binding of naloxone and dihydromorphine to opiate receptors in mouse brain. Diabetes. 36:1987;1173-1177.
10. + channels in pancreatic β-cells: spare-channel hypothesis. Diabetes. 37:1988;495-498.
11. During M.J., Leone P., Davis K.E., Kerr D., Sherwin R.S. Glucose modulates rat substantia nigra GABA release in vivo via ATP-sensitive potassium channels. J. clin. Invest. 95:1995;2403-2408.
12. Durkin T.P., Messier C., de Boer P., Westerink B.H.C. Raised glucose levels enhance scopolamine-induced acetylcholine overflow from the hippocampus: an in vivo microdialysis study in the rat. Behav. Brain Res. 49:1992;181-188.
13. Fellows L.K., Boutelle M.G., Fillenz M. ATP-sensitive potassium channels and local energy demands in the rat hippocampus: an in vivo study. J. Neurochem. 61:1993;949-954.
14. Flood J.F., Smith G.E., Cherkin A. Memory enhancement: supra-additive effect of subcutaneous cholinergic drug combinations in mice. Psychopharmacology. 86:1985;61-67.
15. Frankhuijzen A.L., Jansen F.P., Schoffelmeer A.N.M., Mulder A.H. μ-Opioid receptor-mediated inhibition of the release of radiolabelled noradrenaline and acetylcholine from rat amygdala slices. Neurochem. Int. 19:1991;543-548.
16. Gibson G.E., Jope R., Blass J.P. Decreased synthesis of acetylcholine accompanying impaired oxidation of pyruvic acid in rat brain minces. Biochem. J. 148:1975;17-23.
17. Givens B.S., Olton D.S. Cholinergic and GABAergic modulation of medial septal area: effect on working memory. Behav. Neurosci. 6:1990;849-855.
18. Gold P.E. Glucose modulation of memory storage processing. Behav. neural Biol. 45:1986;342-349.
19. Gold P.E. Role of glucose in regulating the brain and cognition. Am. J. clin. Nutr., Suppl. 61:1995;987S-995S.
20. + channels and adenylate cyclase. Naunyn-Schmiedeberg's Arch. Pharmac. 345:1992;627-632.
21. Inagaki N., Gonoi T., Clement J.P. IV, Namba N., Inazawa J., Gonzalez G., Aguilar-Bryan L., Seino S., Bryan J. Reconstitution of IKATP: an inward rectifier subunit plus the sulfonylurea receptor. Science. 270:1995;1166-1170.
22. Khawaja X., Green I.C. Studies on the effects of glucose in vitro and of the glycaemic state in vivo on the binding characteristics of mu, delta and kappa opiate receptors in mouse brain. Life Sci. 50:1992;1273-1281.
23. - channel current that is activated by cell swelling, cAMP, and glyburide in insulin-secreting cells. Diabetes. 44:1995;1461-1466.
24. Kopf S.R., Baratti C.M. Memory-improving actions of glucose: involvement of a central cholinergic muscarinic mechanism. Behav. neural Biol. 62:1994;237-243.
25. Kopf S.R., Baratti C.M. Effects of posttraining administration of glucose on retention of a habituation response in mice: participation of a central cholinergic mechanism. Neurobiol. Learn. Mem. 65:1996;253-260.
26. Lee K., Dixon A.K., Rowe I.C.M., Ashford M.L.J., Richardson P.J. The high-affinity sulphonylurea receptor regulates KATP channels in nerve terminals of the rat motor cortex. J. Neurochem. 66:1996;2562-2571.
27. Lee M.K., Graham S.N., Gold P.E. Memory enhancement with post-training intraventricular glucose injections in rats. Behav. Neurosci. 4:1988;591-595.
28. Lewis L.D., Ljunggren B., Ratcheson R.A., Siesjö B.K. Cerebral energy state in insulin-induced hypoglycemia, related to blood glucose and to EEG. J. Neurochem. 23:1974;673-679.
29. Matsumoto M., Yoshioka M., Togashi H., Mitsugu H., Tochihara M., Ikeda T., Smith C.B., Saito H. Mu-opioid receptors modulate noradrenaline release from the rat hippocampus as measured by brain microdialysis. Brain Res. 636:1994;1-8.
30. Messier C., Destrade C. Improvement of memory for an operant response by post-training glucose in mice. Behav. Brain Res. 31:1988;185-191.
31. Messier C., Durkin T., Mrabet O., Destrade C. Memory-improving action of glucose: indirect evidence for a facilitation of hippocampal acetylcholine synthesis. Behav. Brain Res. 39:1990;135-143.
32. Messier C., White N.M. Contingent and non-contingent actions of sucrose and saccharin reinforcers: effects on taste preference and memory. Physiol. Behav. 32:1984;195-203.
33. Messier C., White N.M. Memory improvement by glucose, fructose, and two glucose analogs: a possible effect on peripheral glucose transport. Behav. neural Biol. 48:1987;104-127.
34. Micheau J., Messier C., Jaffard R. Glucose enhancement of scopolamine-induced increase of hippocampal high-affinity choline uptake in mice: relation to plasma glucose level. Brain Res. 685:1995;99-104.
35. + channels in the central nervous system: autoradiographic analysis of their distribution and ontogenesis, and of their localization in mutant mice cerebellum. Brain Res. 519:1990;29-43.
36. Narita M., Takamori K., Kawashima N., Funada M., Kamei J., Suzuki T., Misawa M., Nagase H. Activation of central ATP-sensitive potassium channels produces the antinociception and spinal noradrenaline turnover-enhancing effect in mice. Psychopharmacology. 113:1993;11-14.
37. Nies A. S. and Spielberg S. P. (1996) Principles of therapeutics. In Goodman and Gilman's The Pharmacological Basis of Therapeutics, 9th edn (eds Hardman J. G. and Limbird E.), pp. 43-62. McGraw-Hill, New York.
38. + channel-acting drugs. Br. J. Pharmac. 114:1995;1296-1302.
39. Olton D. S., Handelmann G. E. and Walker J. A. (1981) Spatial memory and food searching strategies. In Foraging Behavior: Ecological, Ethological, and Psychological Approaches (eds Kamil A. C. and Sargent T. D.), pp. 333-354. Garland STPM, New York.
40. Panten U., Schwanstecher M., Schwanstecher C. Sulfonylurea receptors and mechanism of sulfonylurea action. Expl clin. Endocr. 104:1996;1-9.
41. Parsons M.W., Gold P.E. Scopolamine-induced deficits in spontaneous alternation performance: attenuation with lateral ventricle injections of glucose. Behav. neural Biol. 57:1992;90-92.
42. Paxinos G. and Watson C. (1986) The Rat Brain in Stereotaxic Coordinates, 2nd edn. Academic, San Diego.
43. + channels. Brain Res. 650:1994;146-148.
44. Raffa R.B., Martinez R.P. The 'glibenclamide-shift' of centrally-acting antinociceptive agents in mice. Brain Res. 677:1995;277-282.
45. Ragozzino M.E., Gold P.E. Glucose effects on mecamylamine-induced memory deficits and decreases in locomotor activity in mice. Behav. neural Biol. 56:1991;271-282.
46. Ragozzino M.E., Gold P.E. Glucose injections into the medial septum reverse the effects of intraseptal morphine infusions on hippocampal acetylcholine output and memory. Neuroscience. 68:1995;981-988.
47. Ragozzino M.E., Parker M.E., Gold P.E. Spontaneous alternation and inhibitory avoidance impairments with morphine injections into the medial septum. Attenuation by glucose administration. Brain Res. 597:1992;241-249.
48. Ragozzino M.E., Arankowsky-Sandoval G., Gold P.E. Glucose attenuates the effect of combined muscarinic-nicotinic receptor blockade on spontaneous alternation. Eur. J. Pharmac. 256:1994;31-36.
49. Ragozzino M.E., Wenk G.L., Gold P.E. Glucose attenuates a morphine-induced decrease in hippocampal acetylcholine output: an in vivo microdialysis study in rats. Brain Res. 655:1994;77-82.
50. Ragozzino M.E., Hellems K., Lennartz R.C., Gold P.E. Pyruvate infusions into the septal area attenuate spontaneous alternation impairments induced by intraseptal morphine injections. Behav. Neurosci. 109:1995;1074-1080.
51. Ragozzino M.E., Unick K.E., Gold P.E. Hippocampal acetylcholine release during memory testing in rats: augmentation by glucose. Proc. natn. Acad. Sci. U.S.A. 93:1996;4693-4698.
52. Ragozzino M.E., Pal S.N., Unick K., Stefani M.R., Gold P.E. Modulation of hippocampal acetylcholine release and of memory by intrahippocampal glucose injections. J. Neurosci. 18:1998;1595-1601.
53. Resine T. and Pasternak G. (1995) Opioid analgesics and antagonists. In Goodman and Gilman's The Pharmacological Basis of Therapeutics, 9th edn (eds Hardman J. G. and Limbird E.), pp. 521-555. McGraw-Hill, New York.
54. Sarter M., Bodewitz G., Stephens D.N. Attenuation of scopolamine-induced impairment of spontaneous alternation behavior by antagonist but not inverse agonist and agonist β-carbolines. Psychopharmacology. 94:1988;491-495.
55. Schultz B.D., DeRoos A.D.G., Venglairik C.J., Singh A.K., Frizzell R.A., Bridges R.J. Glibenclamide blockade of CFTR chloride channels. Am. J. Physiol. 271:1996;L192-L200.
56. ATP channels. Science. 282:1998;1138-1141.
57. Simon G.S., Dewey W.L. Narcotics and diabetes. I. The effects of streptozotocin-induced diabetes on the antinociceptive potency of morphine. J. Pharmac. exp. Ther. 218:1981;318-323.
58. Singh I.S., Chatterjee T.K., Ghosh J.J. Modification of morphine antinociceptive response by blood glucose status: possible involvement of cellular energetics. Eur. J. Pharmac. 90:1983;437-439.
59. Stefani M.R., Ragozzino M.E., Thompson P.K., Hellems K., Lennartz R.C., Gold P.E. Regulation of spontaneous alternation performance in the rat by glucose: a role for glycolysis. Soc. Neurosci. Abstr. 20:1994;1763.
60. Stefani M.R., Gold P.E. Impairment of spontaneous alternation performance in the rat by intra-septal injection of the K-ATP channel openers galanin and lemakalim. Soc. Neurosci. Abstr. 23:1997;2128.
61. Stone W.S., Walser B., Gold S.D., Gold P.E. Scopolamine- and morphine-induced impairments of spontaneous alternation performance in mice: reversal with glucose and with cholinergic and adrenergic agonists. Behav. Neurosci. 105:1991;264-271.
62. Tanaka T., Yoshida M., Yokoo H., Mizoguchi K., Tanaka M. The role of ATP-sensitive potassium channels in striatal dopamine release: an in vivo microdialysis study. Pharmac. Biochem. Behav. 52:1995;831-835.
63. - conductance. Circulation Res. 77:1995;417-423.
64. + channels in the absence of the sulphonylurea receptor. Nature. 387:1997;179-183.
65. Uchida Y., Saito K., Ohnishi T., Maeda S., Matsuya T., Inoki R. Antagonism by glibenclamide of the effect of morphine in hippocampal preparations. Neurosci. Lett. 162:1993;14-116.
66. Wenk G. An hypothesis on the role of glucose in the mechanism of action of cognitive enhancers. Psychopharmacology. 99:1989;31-483.
67. White N. M. (1991) Peripheral and central memory enhancing actions of glucose. In Peripheral Signalling of the Brain: Role in Neural-Immune Interactions, Learning and Memory (eds Frederickson R. C. A., McGaugh J. L. and Felten D. L.), pp. 421-443. Hogrefe & Huber, Toronto.
68. Zini S., Tremblay E., Pollard H., Moreau J., Ben-Ari Y. Regional distribution of sulfonylurea receptors in the brain of rodent and primate. Neuroscience. 55:1993;1085-1091.