Hippocampal infusions of pyruvate reverse the memory-impairing effects of septal muscimol infusions

European Journal of Pharmacology

Volumn 520, Issue 1-3, 2005, Pages 91-99

  Krebs, Desiree L ^a   Parent, Marise B ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

Author keywords

Glucose; Hippocampus; Metabolism; Muscimol; Pyruvate; Shock avoidance; Spontaneous alternation

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR STIMULATING AGENT; GLUCOSE; MUSCIMOL; PYRUVIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; CONTROLLED STUDY; DRUG INFUSION; GLUCOSE METABOLISM; GLYCOLYSIS; HIPPOCAMPUS; LATENT PERIOD; MALE; MEMORY; MEMORY DISORDER; METABOLITE; NONHUMAN; PRIORITY JOURNAL; RAT; SCORING SYSTEM; SEPTUM PELLUCIDUM; TASK PERFORMANCE; TRAINING;

ANIMALS; AVOIDANCE LEARNING; ELECTROSHOCK; GABA AGONISTS; HIPPOCAMPUS; MALE; MEMORY DISORDERS; MEMORY, SHORT-TERM; MUSCIMOL; PYRUVIC ACID; RATS; RATS, SPRAGUE-DAWLEY; RETENTION (PSYCHOLOGY); SEPTUM OF BRAIN;

EID: 25444484185     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2005.08.007     Document Type: Article

References (69)

1. S. Amoroso, H. Schmid-Antomarchi, M. Fosset, and M. Laduski Glucose, sulfonylureas, and neurotransmitter release: role of ATP-sensitive K+ channels Science 247 1990 852 854
2. C. Arias, T. Montiel, R. Quiroz-Baez, and L. Massieu beta-Amyloid neurotoxicity is exacerbated during glycolysis inhibition and mitochondrial impairment in the rat hippocampus in vivo and in isolated nerve terminals: implications for Alzheimer's disease Exp. Neurol. 176 2002 163 174
3. D. Benton, and S. Nabb Carbohydrate, memory, and mood Nutr. Rev. 61 2003 S61 S67
4. G.J. Biessels, A. Kamal, G.M. Ramakers, I.J. Urban, B.M. Spruijt, D.W. Erklens, and W.H. Gispen Place learning and hippocampal synaptic plasticity in streptozotocin-induced diabetic rats Diabetes 45 1996 1259 1266
5. S. Craft, C. Murphy, and J. Wemstrom Glucose effects on complex memory and nonmemory tasks: the influence of age, sex, and glucoregulatory response Psychobiology 22 1994 95 105
6. S.F. De Boer, J.L. Slangen, and J. Van der Gugten Plasma catecholamine and corticosterone levels during active and passive shock-prod avoidance behavior in rats: effects of chlordiazepoxide Physiol. Behav. 47 1990 1089 1098
7. A. Degroot, and M.B. Parent Increasing acetylcholine levels in the hippocampus or entorhinal cortex attenuate avoidance retention deficits produced by intra-septal infusions of the GABA agonist muscimol Brain Res. 7 2000 293 302
8. A. Degroot, and M.B. Parent Infusions of physostigmine into the hippocampus or entorhinal cortex attenuate avoidance retention deficits produced by intra-septal infusions of the GABA agonist muscimol Brain Res. 7 2001 293 302
9. A. Degroot, and D. Treit Septal GABAergic and hippocampal cholinergic systems interact in the modulation of anxiety Neuroscience 117 2003 493 501
10. A. Degroot, T. Kornecook, R. Quiron, S. DeBow, and M.B. Parent Glucose increases hippocampal extracellular acetylcholine levels upon activation of septal GABA receptors Brain Res. 979 2003 71 77
11. W.N. Dember Spontaneous Alternation Behavior 1989 Springer-Verlag New York, NY
12. V. Dolezal, and S. Tucek Utilization of citrate, acetylcarnitine, acetate, pyruvate and glucose for the synthesis of acetylcholine in the rat brain slices J. Neurochem. 36 1981 1323 1330
13. M. During, P. Leone, K.E. Davis, D. Kerr, and R.S. Sherwin Glucose modulates rat substantia nigra GABA release in vivo via ATP-sensitive potassium channels J. Clin. Invest. 95 1995 2403 2408
14. T.P. Durkin, C. Messier, P. de Boer, and B.H. Westerink 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
15. H. Eichenbaum, A. Fagan, P. Mathews, and N.J. Cohen Hippocampal system dysfunction and odor discrimination learning in rats: impairment or facilitation depending on representational demands Behav. Neurosci. 102 1988 331 339
16. R. Engeset, and R. Ritter Intracerebroventricular 2-DG causes feeding in the absence of other signs of glucoprivation Brain Res. 202 1980 229 233
17. K. Fink, and M. Gothert High d-glucose concentrations increase GABA release but inhibit release of norepinephrine and 5-hydroxytryptamine in rat cerebral cortex Brain Res. 618 1993 220 226
18. K. Fink, J. Zentner, and M. Gothert Increase GABA release in the human brain cortex as a potential pathogenic basis of hyperosmolar diabetic coma J. Neurochem. 62 1994 1476 1481
19. J. Flood, A. Mooradian, and J. Morley Characteristics of learning and memory in streptozotocin-induced diabetic mice Diabetes 39 1990 1391 1398
20. G.E. Gibson, R. Jope, and J.P. Blass Decreased synthesis of acetylcholine accompanying impaired oxidation of pyruvic acid in rat brain minces Biochem. J. 148 1975 17 23
21. P.E. Gold The role of glucose in regulating brain and cognition Am. J. Clin. Nutr. 61 1995 S987 S995
22. G. Guillazo-Blanch, R. Nadal, A. Vale-Martinez, M. Marti-Nicolovius, R. Arevalo, and I. Morgado-Bernal Effects of fimbria lesions on trace two-way active avoidance acquisition and retention in rats Neurobiol. Learn. Mem. 78 2002 406 425
23. Z. Guo, J. Lee, M. Lane, and M. Mattson Iodoacetate protects hippocampal neurons against excitotoxic and oxidative injury: involvement of heat-shock proteins and Bcl-2 J. Neurochem. 79 2001 361 370
24. L. Hertz, and G. Dienel Energy metabolism in the brain D.S. Dwyer Glucose Metabolism in the Brain 2002 Academic Press New York, NY 2 81
25. G. Johnston GABA chemistry: analogs of GABA as therapeutic and investigational agents D.L. Martin R.W. Olsen GABA in the Nervous System: The View at Fifty Years 2000 Lippincott, Williams, & Wilkins Philadephia 65 80
26. C.T. Johnston, D.S. Olton, F.H. Gage, and P.G. Jenko Damage to hippocampus and hippocampal connections: effects of DRL and spontaneous alternation J. Comp. Physiol. Psychol. 91 1977 508 522
27. M. Kawahara, M. Kato-Negishi, and Y. Kuroda Pyruvate blocks zinc-induced neurotoxicity in immortalized hypothalamic neurons Cell. Mol. Neurobiol. 22 2002 87 93
28. S.R. Kopf, and C.M. Baratti Memory-improving actions of glucose: involvement of a central cholinergic muscarinic mechanism Behav. Neural Biol. 62 1994 237 243
29. S.R. Kopf, M.L. Buchholzer, M. Hilger, K. Loffelhoz, and J. Klein Glucose plus choline improve passive avoidance behaviour and increase hippocampal acetylcholine release in mice Neuroscience 103 2001 365 371
30. D.L. Korol, and P.E. Gold Glucose, memory, and aging Am. J. Clin. Nutr. 67 1998 764S 771S
31. D.L. Krebs, and M.B. Parent The enhancing effects of hippocampal infusions of glucose are not restricted to spatial working memory Neurobiol. Learn. Mem. 83 2005 168 172
32. R. Lalonde The neurobiological basis of spontaneous alternation Neurosci. Biobehav. Rev. 26 2002 91 104
33. P. Lefresne, P. Guynet, and J. Glowinski Acetylcholine synthesis from (2-14 C) pyruvate in rat striatal slices J. Neurochem. 20 1973 1083 1097
34. P. Leung, and R. Bryant Autobiographical memory in diabetes mellitus patients J. Psychosom. Res. 49 2000 435 438
35. A. Li, Y. Oomura, K. Sasaki, I. Tooyama, K. Hanai, H. Kimura, and T. Hori A single pre-training glucose injection induces memory facilitation in rodents performing various tasks: contribution of acidic fibroblast growth factor Neuroscience 85 1998 785 794
36. R.H. Lovely, N.E. Grossen, S.A. Moot, R.H. Bauer, and J.J. Peterson Hippocampal lesions and inhibition of avoidance behavior J. Comp. Physiol. Psychol. 77 1971 345 352
37. T.R. Mabry, P.E. Gold, and R. McCarty Age-related changes in plasma catecholamine responses to acute swim stress Neurobiol. Learn. Mem. 63 1995 260 268
38. C.S. Malcolm, K.R. Benwell, H. Lamb, D. Bebbington, and R.H. Porter Characterization of iodoacetate-mediated neurotoxicity in vitro using primary cultures of rat cerebellar granule cells Free Radic. Biol. Med. 28 2000 102 107
39. I. Martinez, G.L. Quirarte, S. Diaz-Cintra, C. Quiroz, and R.A. Prado-Alcala Effects of lesions of hippocampal fields CA1 and CA3 on acquisition of inhibitory avoidance Neuropsychobiology 46 2002 97 103
40. L. Massieu, N. Gomez-Roman, and T. Montiel In vivo potentiation of glutamate-mediated neuronal damage after chronic administration of the glycolysis inhibitor iodoacetate Exp. Neurol. 165 2000 257 267
41. E.A. Mazzio, and K.F. Soliman Cytoprotection of pyruvic acid and reduced beta-nicotinamide adenine dinucleotide against hydrogen peroxide toxicity in neuroblastoma cells Neurochem. Res. 28 2003 733 741
42. R.J. McDonald, and N.M. White Information acquired by the hippocampus interferes with acquisition of the amygdala-based conditioned-cue preference in the rat Hippocampus 5 1995 189 197
43. J.L. McGaugh The amygdala modulates the consolidation of memories of emotionally arousing experiences Annu. Rev. Neurosci. 27 2004 185 191
44. C. Messier, and M. Gagnon Glucose regulation and brain aging J. Nutr. Health Aging 4 2000 208 213
45. A.H. Nagahara, and J.L. McGaugh Muscimol infused into the medial septal area impairs long-term memory but not short-term memory in inhibitory avoidance, water maze place learning and rewarded alternation tasks Brain Res. 591 1992 54 61
46. A.H. Nagahara, J.D. Brioni, and J.L. McGaugh Effects of intraseptal infusion of muscimol on inhibitory avoidance and spatial learning: differential effects of pretraining and posttraining administration Psychobiology 20 1992 198 204
47. N. Ohtani, M. Ohta, and T. Sugano Microdialysis study of modification of hypothalamic neurotransmitter in streptozotocin-diabetic rats J. Neurochem. 69 1997 1622 1628
48. M.B. Parent, and P.E. Gold Intra-septal infusions of glucose potentiate inhibitory avoidance deficits when co-infused with the GABA agonist muscimol Brain Res. 745 1997 317 320
49. M.B. Parent, P.T. Laurey, S. Wilkniss, and P.E. Gold Intraseptal infusion of muscimol impair spontaneous alternation performance: infusions of glucose into the hippocampus, but not the medial septum, reverse the deficit Neurobiol. Learn. Mem. 68 1997 75 85
50. M.W. Parsons, and P.E. Gold Glucose enhancement of memory in elderly humans: an inverted-U dose response curve Neurobiol. Aging 13 1992 401 404
51. G. Paxinos, and C. Watson The Rat Brain in Stereotaxic Coordinates 1986 Springer-Verlag New York, NY
52. F. Pavone, F. Capone, M. Battaglia, and M. Sansone Shuttle-box avoidance learning in mice: improvement by combined glucose and tacrine Neurobiol. Learn. Mem. 69 1998 204 210
53. M.E. Ragozzino, and P.E. Gold Glucose injections into the medial septum reverse the effects of intraseptal morphine infusion on hippocampal acetylcholine output and memory Neuroscience 68 1995 981 988
54. M.E. Ragozzino, G. Arankowshy-Sandoval, and P.E. Gold Glucose attenuates the effect of combined muscarinic-nicotine receptor blockade on spontaneous alternation Eur. J. Pharmacol. 256 1994 31 36
55. M.E. Ragozzino, K.L. Hellems, R.C. Lennartz, and P.E. Gold Pyruvate infusion into the septal area attenuate spontaneous alternation impairments induced by intraseptal morphine injections Behav. Neurosci. 109 1995 1074 1080
56. M.E. Ragozzino, K.E. Unick, and P.E. Gold Hippocampal acetylcholine release during memory testing in rats: augmentation by glucose Proc. Natl. Acad. Sci. 93 1996 4693 4698
57. M.E. Ragozzino, S.N. Pal, K. Unick, M.R. Stefani, and P.E. Gold Modulation of hippocampal acetylcholine release and spontaneous alternation scores by intrahippocampal glucose injections J. Neurosci. 18 1998 1595 1601
58. S. Rahner-Welsch, J. Vogel, and W. Kushinsky Regional congruence and divergence of glucose transporters (GLUT-1) and capillaries in rat brains J. Cereb. Blood Flow Metab. 15 1995 681 686
59. C.M. Ryan, and M. Geckle Why is learning and memory dysfunction in Type 2 diabetes limited to older adults? Diabetes Metab. Res. Rev. 16 2000 308 315
60. C. Ryan, A. Vega, and A. Drash Cognitive deficits in adolescents who developed diabetes early in life Pediatrics 75 1995 921 927
61. A.A. Shah, and M.B. Parent Septal infusions of glucose or pyruvate, but not fructose, produce avoidance deficits when co-infused with the GABA receptor agonist muscimol Neurobiol. Learn. Mem. 79 2003 243 251
62. A.A. Shah, and M.B. Parent Septal infusions of glucose or pyruvate with muscimol impair spontaneous alternation Brain Res. 996 2004 246 250
63. M.R. Stefani, and P.E. Gold Intra-septal injections of glucose and glibenclamide attenuate galanin-induced spontaneous alternation performance deficits in the rat Brain Res. 813 1998 50 56
64. M.R. Stefani, and P.E. Gold Intrahippocampal infusions of K-ATP channel modulators influence spontaneous alternation performance: relationships to acetylcholine release in the hippocampus J. Neurosci. 21 2001 609 614
65. M.R. Stefani, G.M. Nicholson, and P.E. Gold ATP-sensitive potassium channel blockade enhances spontaneous alternation performance in the rat: a potential mechanism for glucose mediate memory enhancement Neuroscience 93 1999 557 563
66. S.I. Sunran-Lea, J.K. Foster, P. Durlach, and C. Perez The effect of retrograde and anterograde glucose administration on memory performance in healthy young adults Behav. Brain Res. 134 2002 505 516
67. A. Takahaski, H. Ishimaru, Y. Ikarashi, E. Kishi, and Y. Maruyana Hypothalamic cholinergic activity and 2-deoxyglucose-induced hyperglycemia Brain Res. Bull. 43 1997 65 68
68. K. Takata, H. Hirano, and M. Kasahara Transport of glucose across the blood-tissue barriers Int. Rev. Cytol. 172 1997 1 53
69. K. Van der Borght, P. Meerlo, P.G. Luiten, B.J. Eggen, and E.A. Van der Zee Effects of active shock avoidance learning on hippocampal neurogenesis and plasma levels of corticosterone Behav. Brain Res. 157 2005 23 30