Zero net flux estimates of septal extracellular glucose levels and the effects of glucose on septal extracellular GABA levels

European Journal of Pharmacology

Volumn 611, Issue 1-3, 2009, Pages 44-52

  Krebs Kraft, Desiree L ^a   Rauw, Gail ^b   Baker, Glen B ^b   Parent, Marise B ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

GABA; Glucose; in vivo microdialysis; Memory; Muscimol; Septum; Spontaneous alternation; Zero net flux

Indexed keywords

4 AMINOBUTYRIC ACID; GLUCOSE; MUSCIMOL;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXTRACELLULAR FLUID; GLUCOSE BRAIN LEVEL; GLUCOSE INFUSION; HIPPOCAMPUS; MALE; MEMORY DISORDER; MICRODIALYSIS; NONHUMAN; PRIORITY JOURNAL; RAT; SEPTUM PELLUCIDUM; WORKING MEMORY; ZERO NET FLUX METHOD;

ANIMALS; EXTRACELLULAR SPACE; GAMMA-AMINOBUTYRIC ACID; GLUCOSE; HIPPOCAMPUS; MALE; MICRODIALYSIS; MUSCIMOL; RATS; RATS, SPRAGUE-DAWLEY; SEPTUM OF BRAIN;

EID: 67349141388     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2009.03.055     Document Type: Article

References (86)

1. Amoroso S., Schmid-Antomarchi H., Fosset M., and Lazdunski M. Glucose, sulfonylureas, and neurotransmitter release: role of ATP-sensitive K+ channels. Science 247 (1990) 852-854
2. Apelt J., Mehlhorn G., and Schliebs R. Insulin-sensitive GLUT4 glucose transporters are colocalized with GLUT3-expressing cells and demonstrate a chemically distinct neuron-specific localization in rat brain. J. Neurosci. Res. 57 (1999) 693-705
3. Awad N., Gagnon M., Desrochers A., Tsiakas M., and Messier C. Impact of peripheral glucoregulation on memory. Behav. Neurosci. 116 (2002) 691-702
4. Barros L.F., Porras O.H., and Bittner C.X. Why glucose transport in the brain matters for PET. Trends Neurosci. 28 (2005) 117-119
5. Borisyuk R., Denham M., Denham S., and Hoppensteadt F. Computational models of predictive and memory-related functions of the hippocampus. Rev. Neurosci. 10 (1999) 213-232
6. Bunce J.G., Sabolek H.R., and Chrobak J.J. Intraseptal infusion of oxotremorine impairs memory in a delayed-non-match-to-sample radial maze task. Neuroscience 121 (2003) 259-267
7. Bunce J.G., Sabolek H.R., and Chrobak J.J. Intraseptal infusion of the cholinergic agonist carbachol impairs delayed-non-match-to-sample radial arm maze performance in the rat. Hippocampus 14 (2004) 450-459
8. Bunce J.G., Sabolek H.R., and Chrobak J.J. Timing of administration mediates the memory effects of intraseptal carbachol infusion. Neuroscience 127 (2004) 593-600
9. Burke S.P., and Nadler J.V. Effects of glucose deficiency on glutamate/aspartate release and excitatory synaptic responses in the hippocampal CA1 area in vitro. Brain Res. 500 (1989) 333-342
10. Campbell K., Kalen P., Lundberg C., Wictorin K., Rosengren E., and Bjorklund A. Extracellular gamma-aminobutyric acid levels in the rat caudate-putamen: monitoring the neuronal and glial contribution by intracerebral microdialysis. Brain Res. 614 (1993) 241-250
11. Canal C.E., McNay E.C., and Gold P.E. Increases in extracellular fluid glucose levels in the rat hippocampus following an anesthetic dose of pentobarbital or ketamine-xylazine: an in vivo microdialysis study. Physiol. Behav. 84 (2005) 245-250
12. Choeiri C., Staines W., Miki T., Seino S., and Messier C. Glucose transporter plasticity during memory processing. Neuroscience 130 (2005) 591-600
13. Craft S., Dagogo-Jack S.E., Wiethop B.V., Murphy C., Nevins R.T., Fleischman S., Rice V., Newcomer J.W., and Cryer P.E. Effects of hyperglycemia on memory and hormone levels in dementia of the Alzheimer type: a longitudinal study. Behav. Neurosci. 107 (1993) 926-940
14. Craft S., Murphy C., and Wemstrom J. Glucose effects and glucose regulation in memory and nonmemory tasks: the influence of age, sex, regulation, and glucoregulatory response. Psychobiology 22 (1994) 95-105
15. Degroot A., Kornecook T., Quirion R., DeBow S., and Parent M. Glucose increases hippocampal extracellular acetylcholine levels upon activation of septal GABA receptors. Learn. Mem. 979 (2003) 71-77
16. During M.J., Leone P., Davis K.E., Kerr D., and Sherwin R.S. Glucose modulates rat substantia nigra GABA release in vivo via ATP-sensitive potassium channels. J. Clin. Invest. 95 (1995) 2403-2408
17. Elvander E., Schott P., Sandin J., Bjelke B., Kehr J., Yoshitake T., and Ogren S. Intraseptal muscarinic ligands and galanin: influence on hippocampal acetylcholine and cognition. Neuroscience 126 (2004) 541-557
18. Erickson E.J., Watts K.D., and Parent M.B. Septal co-infusions of glucose with a GABAB agonist impair memory. Neurobiol. Learn. Mem. 85 (2006) 66-70
19. Fellows L.K., Boutelle M.G., and Fillenz M. Extracellular brain glucose levels reflect local neuronal activity: a microdialysis study in awake, freely moving rats. J. Neurochem. 59 (1992) 2141-2147
20. Fink K., and Gothert M. 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
21. Fink K., Zentner J., and Gothert M. Increased GABA release in the human brain cortex as a potential pathogenetic basis of hyperosmolar diabetic coma. J. Neurochem. 62 (1994) 1476-1481
22. Fioramonti X., Lorsignol A., Taupignon A., and Penicaud L. A new ATP-sensitive K+ channel-independent mechanism is involved in glucose-excited neurons of mouse arcuate nucleus. Diabetes 53 (2004) 2767-2775
23. Forsyth R., Fray A., Boutelle M., Fillenz M., Middleditch C., and Burchell A. A role for astrocytes in glucose delivery to neurons?. Dev. Neurosci. 18 (1996) 360-370
24. Fray A.E., Boutelle M., and Fillenz M. Extracellular glucose turnover in the striatum of unanaesthetized rats measured by quantitative microdialysis. J. Physiol. 504 Pt 3 (1997) 721-726
25. Gage F.H., Kelly P.A., and Bjorklund A. Regional changes in brain glucose metabolism reflect cognitive impairments in aged rats. J. Neurosci. 4 (1984) 2856-2865
26. Gerber III J.C., Choki J., Brunswick D.J., Reivich M., and Frazer A. The effect of antidepressant drugs on regional cerebral glucose utilization in the rat. Brain Res. 269 (1983) 319-325
27. Gold P.E. Acetylcholine modulation of neural systems involved in learning and memory. Neurobiol. Learn. Mem. 80 (2003) 194-210
28. Gold P.E. Acetylcholine: cognitive and brain functions. Neurobiol. Learn. Mem. 80 (2003) 177
29. Gold P.E., Vogt J., and Hall J.L. Glucose effects on memory: behavioral and pharmacological characteristics. Behav. Neural Biol. 46 (1986) 145-155
30. Gradman T.J., Laws A., Thompson L.W., and Reaven G.M. Verbal learning and/or memory improves with glycemic control in older subjects with non-insulin-dependent diabetes mellitus. J. Am. Geriatr. Soc. 41 (1993) 1305-1312
31. 13C NMR studies of compartmentalized cerebral carbohydrate metabolism. Neurochem. Int. 41 (2002) 143-154
32. Hamberger A.C., Chiang G.H., Nylen E.S., Scheff S.W., and Cotman C.W. Glutamate as a CNS transmitter. I. Evaluation of glucose and glutamine as precursors for the synthesis of preferentially released glutamate. Brain Res. 168 (1979) 513-530
33. Herbison A.E., Heavens R.P., and Dyer R.G. Endogenous release of gamma-aminobutyric acid from the medial preoptic area measured by microdialysis in the anaesthetised rat. J. Neurochem. 55 (1990) 1617-1623
34. Hu M., Watson C.J., Kennedy R.T., and Becker J.B. Estradiol attenuates the K+-induced increase in extracellular GABA in rat striatum. Synapse 59 (2006) 122-124
35. Huang Y.H., Tsai S.J., Huang H.J., and Sim C.B. The effect of acute administration of risperidone on local cerebral glucose utilization in the rat. Eur. J. Pharmacol. 370 (1999) 257-261
36. Izquierdo I., and Medina J.H. Memory formation: the sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol. Learn. Mem. 68 (1997) 285-316
37. Johnson C.T., Olton D.S., Gage III F.H., and Jenko P.G. Damage to hippocampus and hippocampal connections: effects on DRL and spontaneous alternation. J. Comp. Physiol. Psychol. 91 (1977) 508-522
38. Khandelwal P., Beyer C.E., Lin Q., McGonigle P., Schechter L.E., and Bach II A.C. Nanoprobe NMR spectroscopy and in vivo microdialysis: new analytical methods to study brain neurochemistry. J. Neurosci. Methods 133 (2004) 181-189
39. Kimbrell T.A., Ketter T.A., George M.S., Little J.T., Benson B.E., Willis M.W., Herscovitch P., and Post R.M. Regional cerebral glucose utilization in patients with a range of severities of unipolar depression. Biol. Psychiatry 51 (2002) 237-252
40. Korol D.L. Enhancing cognitive function across the life span. Ann. N.Y. Acad. Sci. 959 (2002) 167-179
41. Korol D.L., and Gold P.E. Epinephrine converts long-term potentiation from transient to durable form in awake rats. Hippocampus 18 (2008) 81-91
42. Krebs D.L., and Parent M.B. The enhancing effects of hippocampal infusions of glucose are not restricted to spatial working memory. Neurobiol. Learn. Mem. 83 (2005) 168-172
43. Krebs-Kraft D.L., and Parent M.B. Hippocampal infusions of glucose reverse memory deficits produced by co-infusions of a GABA receptor agonist. Neurobiol. Learn. Mem. 89 (2008) 142-152
44. Lalonde R. The neurological basis of spontaneous alternation. Neurosci. Biobehav. Rev. 26 (2002) 91-104
45. Lee M.K., Graham S.N., and Gold P.E. Memory enhancement with posttraining intraventricular glucose injections in rats. Behav. Neurosci. 102 (1988) 591-595
46. Lonnroth P., Jansson P.A., and Smith U. A microdialysis method allowing characterization of intercellular water space in humans. Am. J. Physiol. 253 (1987) E228-231
47. Lund-Anderson H. Transport of glucose from blood to brain. Physiol. Rev. 59 (1979) 305-352
48. Marighetto A., Micheau J., and Jaffard R. Effects of intraseptally injected glutamatergic drugs on hippocampal sodium-dependent high-affinity choline uptake in "naïve" and "trained" mice. Pharmacol. Biochem. Behav. 49 (1994) 689-699
49. McNay E.C., and Gold P.E. Extracellular glucose concentrations in the rat hippocampus measured by zero-net-flux: effects of microdialysis flow rate, strain, and age. J. Neurochem. 72 (1999) 785-790
50. McNay E.C., and Gold P.E. Age-related differences in hippocampal extracellular fluid glucose concentration during behavioral testing and following systemic glucose administration. J. Geront. A Biol. Sci. Med. Sci. 56 (2001) B66-71
51. McNay E.C., Canal C.E., Sherwin R.S., and Gold P.E. Modulation of memory with septal injections of morphine and glucose: effects on extracellular glucose levels in the hippocampus. Physiol. Behav. 87 (2006) 298-303
52. McNay E.C., Fries T.M., and Gold P.E. Decreases in rat extracellular hippocampal glucose concentration associated with cognitive demand during a spatial task. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 2881-2885
53. McNay E.C., McCarty R.C., and Gold P.E. Fluctuations in brain glucose concentration during behavioral testing: dissociations between brain areas and between brain and blood. Neurobiol. Learn. Mem. 75 (2001) 325-337
54. Meneilly G.S., Cheung E., Tessier D., Yakura C., and Tuokko H. The effect of improved glycemic control on cognitive functions in the elderly patient with diabetes. J. Gerontol. 48 (1993) M117-121
55. Messier C. Glucose improvement of memory: a review. Eur. J. Pharmacol. 490 (2004) 33-57
56. Naor M., Steingruber H.J., Westhoff K., Schottenfeld-Naor Y., and Gries A.F. Cognitive function in elderly non-insulin-dependent diabetic patients before and after inpatient treatment for metabolic control. J. Diabetes Its Complicat. 11 (1997) 40-46
57. Ohtani N., Ohta M., and Sugano T. Microdialysis study of modification of hypothalamic neurotransmitters in streptozotocin-diabetic rats. J. Neurochem. 69 (1997) 1622-1628
58. Pang K.C., and Nocera R. Interactions between 192-IgG saporin and intraseptal cholinergic and GABAergic drugs: role of cholinergic medial septal neurons in spatial working memory. Behav. Neurosci. 113 (1999) 265-275
59. Parent M.B., and Baxter M.G. Septohippocampal acetylcholine: involved in but not necessary for learning and memory?. Learn. Mem. 11 (2004) 9-20
60. Parent M.B., and Gold P.E. Intra-septal infusions of glucose potentiate inhibitory avoidance deficits when co-infused with the GABA agonist muscimol. Brain Res. 745 (1997) 317-320
61. Parent M., Bush D., Rauw G., Master S., Vaccarino F., and Baker G. Analysis of amino acids and catecholamines, 5-hydroxytryptamine and their metabolites in brain areas in the rat using in vivo microdialysis. Methods 23 (2001) 11-20
62. Parent M., Laurey P., Wilkniss S., and Gold P. Intraseptal infusions 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
63. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates, Fourth Edition ed (1998), Academic Press, San Diego
64. Ragozzino M.E., and Gold P.E. Task-dependent effects of intra-amygdala morphine injections: attenuation by intra-amygdala glucose injections. J. Neurosci. 14 (1994) 7478-7485
65. Ragozzino M.E., and 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
66. Ragozzino M.E., Hellems K., Lennartz R.C., and Gold P.E. Pyruvate infusions into the septal area attenuate spontaneous alternation impairments induced by intraseptal morphine injections. Behav. Neurosci. 109 (1995) 1074-1080
67. Ragozzino M.E., Pal S.N., Unick K., Stefani M.R., and Gold P.E. Modulation of hippocampal acetylcholine release and spontaneous alternation scores by intrahippocampal glucose injections. J. Neurosci. 18 (1998) 1595-1601
68. Ragozzino M.E., Parker M.E., and 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
69. Richman C., Dember W., and Kim P. Spontaneous alternation behavior: a review. Curr Psychol. Res. Rev. 5 (1987) 358-391
70. Rodriguez W.A., Horne C.A., Mondragon A.N., and Phelps D.D. Comparable dose-response functions for the effects of glucose and fructose on memory. Behav. Neural Biol. 61 (1994) 162-169
71. Sabolek H.R., Bunce J.G., and Chrobak J.J. Intraseptal tacrine-induced disruptions of spatial memory performance. Behav. Brain Res. 158 (2005) 1-7
72. Schmid-Antomarchi H., Amoroso S., Fosset M., and Lazdunski M. K+ channel openers activate brain sulfonylurea-sensitive K+ channels and block neurosecretion. Proc. Natl. Acad. Sci. U.S.A. 87 (1990) 3489-3492
73. Schroeder J.P., and Packard M.G. Systemic or intra-amygdala injections of glucose facilitate memory consolidation for extinction of drug-induced conditioned reward. Eur. J. Neurosci. 17 (2003) 1482-1488
74. Seeley R.J., and Moran T.H. Principles for interpreting interactions among the multiple systems that influence food intake. Am. J. Physiol. Regul. Integr. Comp. Physiol. 283 (2002) R46-53
75. Shah A.A., and Parent M.B. Septal infusions of glucose or pyruvate, but not fructose, produce avoidance deficits when co-infused with the GABA agonist muscimol. Neurobiol. Learn. Mem. 79 (2003) 243-251
76. Shah A.A., and Parent M.B. Septal infusions of glucose or pyruvate with muscimol impair spontaneous alternation. Brain Res. 996 (2004) 246-250
77. Song Z., Levin B.E., McArdle J.J., Bakhos N., and Routh V.H. Convergence of pre- and postsynaptic influences on glucosensing neurons in the ventromedial hypothalamic nucleus. Diabetes 50 (2001) 2673-2681
78. Stefani M.R., and Gold P.E. Intra-septal injections of glucose and glibenclamide attenuate galanin-induced spontaneous alternation performance deficits in the rat. Brain Res. 813 (1998) 50-56
79. Stefani M.R., and Gold P.E. Intrahippocampal infusions of k-atp channel modulators influence spontaneous alternation performance: relationships to acetylcholine release in the hippocampus. J. Neurosci. 21 (2001) 609-614
80. Stefani M.R., Nicholson G.M., and Gold P.E. ATP-sensitive potassium channel blockade enhances spontaneous alternation performance in the rat: a potential mechanism for glucose-mediated memory enhancement. Neuroscience 93 (1999) 557-563
81. Stevens R., and Cowey A. Effects of dorsal and ventral hippocampal lesions on spontaneous alternation, learned alternation and probability learning in rats. Brain Res. 52 (1973) 203-224
82. Takeda A., Hirate M., Tamano H., and Oku N. Release of glutamate and GABA in the hippocampus under zinc deficiency. J. Neurosci. Res. 72 (2003) 537-542
83. Tossman U., and Ungerstedt U. The effect of apomorphine and pergolide on the potassium-evoked overflow of GABA in rat striatum studied by microdialysis. Eur. J. Pharmacol. 123 (1986) 295-298
84. Vanhanen M., Koivisto K., Karjalainen L., Helkala E.L., Laakso M., Soininen H., and Riekkinen Sr. P. Risk for non-insulin-dependent diabetes in the normoglycaemic elderly is associated with impaired cognitive function. Neuroreport 8 (1997) 1527-1530
85. Wang R., Liu X., Hentges S.T., Dunn-Meynell A.A., Levin B.E., Wang W., and Routh V.H. The regulation of glucose-excited neurons in the hypothalamic arcuate nucleus by glucose and feeding-relevant peptides. Diabetes 53 (2004) 1959-1965
86. Wree A., Goller H.J., and Beck T. Local cerebral glucose utilization in perfusion-fixed rat brains. J. Neurosci. Methods 58 (1995) 143-149