Modulation of memory with septal injections of morphine and glucose: Effects on extracellular glucose levels in the hippocampus

Physiology and Behavior

Volumn 87, Issue 2, 2006, Pages 298-303

  McNay, Ewan C ^a   Canal, Clinton E ^b   Sherwin, Robert S ^a   Gold, Paul E ^b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Glucose; Hippocampus; Medial septum; Memory; Morphine; Spontaneous alternation

Indexed keywords

GLUCOSE; MARKER; MORPHINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; EXTRACELLULAR FLUID; HIPPOCAMPUS; MALE; MEMORY; MEMORY DISORDER; NONHUMAN; PRIORITY JOURNAL; RAT; TASK PERFORMANCE;

EID: 31944444064     PISSN: 00319384     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.physbeh.2005.10.016     Document Type: Article

References (60)

1. D. Benton, and S. Nabb Carbohydrate, memory, and mood Nutr Rev 61 2003 S61 S67
2. Gold PE. Glucose and age-related changes in memory. Neurobiol Aging in press.
3. D.L. Korol Enhancing cognitive function across the life span Ann N Y Acad Sci 959 2002 167 179
4. E.C. McNay, and P.E. Gold Food for thought: fluctuations in brain extracellular glucose provide insight into the mechanisms of memory modulation Behav Cog Neurosci Rev 1 2002 264 280
5. C. Messier Glucose improvement of memory: a review Eur J Pharmacol 490 2004 33 57
6. R. Lalonde The neurobiological basis of spontaneous alternation Neurosci Biobehav Rev 26 2002 91 104
7. E.C. McNay, T.M. Fries, and P.E. Gold Decreases in rat extracellular hippocampal glucose concentration associated with cognitive demand during a spatial task PNAS 97 2000 2881 2885
8. E.C. McNay, and P.E. Gold 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
9. E.C. McNay, and P.E. Gold Age-related differences in hippocampal extracellular fluid glucose concentration during behavioral testing and following systemic glucose administration J. Gerontol., Ser. A, Biol. Sci. Med. Sci. 56 2001 B66 B71
10. E.C. McNay, R.C. McCarty, and P.E. Gold Fluctuations in brain glucose concentration during behavioral testing: dissociations between brain areas and between brain and blood Neurobiol Learn Mem 75 2001 325 337
11. S.J. Watson, J.D. Barchas, and C.H. Li β-Lipotropin: localization of cells and axons in rat brain by immunocytochemistry PNAS 74 1977 5155 5158
12. M.H. Millan, M.J. Millan, and R. Przewlocki Lesions of the hypothalamic arcuate nucleus modify discrete brain and pituitary pools of dynorphin in addition to b-endorphin in the rat Neurosci Lett 48 1984 149 154
13. M. Alreja, M. Wu, W. Liu, J.B. Atkins, C. Leranth, and M. Shanabrough Muscarinic tone sustains impulse flow in the septohippocampal GABA but not cholinergic pathway: implications for learning and memory J Neurosci 20 2000 8103 8110
14. E. Elvander, P.A. Schott, J. Sandin, B. Bjelke, J. Kehr, and T. Yoshitake Intraseptal muscarinic ligands and galanin: influence on hippocampal acetylcholine and cognition Neuroscience 126 2004 541 557
15. H.R. Sabolek, J.G. Bunce, and J.J. Chrobak Intraseptal tacrine can enhance memory in cognitively impaired young rats Neuroreport 15 2004 181 183
16. 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 agonist muscimol Neurobiol Learn Mem 79 2003 243 251
17. A.A. Shah, and M.B. Parent Septal infusions of glucose or pyruvate with muscimol impair spontaneous alternation Brain Res 996 2004 246 250
18. Y. Asaka, M.A. Seager, A.L. Griffin, and S.D. Berry Medial septal microinfusion of scopolamine disrupts hippocampal activity and trace jaw movement conditioning Behav Neurosci 114 2000 1068 1077
19. C. Xu, K.A. Michelsen, M. Wu, E. Morozova, P. Panula, and M. Alreja Histamine innervation and activation of septohippocampal GABAergic neurones: involvement of local ACh release J Physiol 561 Pt 3 2004 657 670
20. S.A. Farr, K. Uezu, J.F. Flood, and J.E. Morley Septo-hippocampal drug interactions in post-trial memory processing Brain Res 847 1999 221 230
21. M.B. Parent, P.T. Laurey, S. Wilkniss, and P.E. Gold 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
22. A.L. Markowska, D.S. Olton, and B. Givens Cholinergic manipulations in the medial septal area: age-related effects on working memory and hippocampal electrophysiology J Neurosci 15 1995 2063 2073
23. J.D. Brioni, M.W. Decker, L.P. Gamboa, I. Izquierdo, and J.L. McGaugh Muscimol injections in the medial septum impair spatial learning Brain Res 522 1990 227 234
24. J.J. Chrobak, R.W. Stackman, and T.J. Walsh Intraseptal administration of muscimol produces dose-dependent memory impairments in the rat Behav Neural Biol 52 1989 357 369
25. E.C. McNay, and P.E. Gold Memory modulation across neural systems: intra-amygdala glucose reverses deficits caused by intraseptal morphine on a spatial task but not on an aversive task J Neurosci 18 1998 3853 3858
26. C.P. Talley, G. Arankowsky-Sandoval, R. McCarty, and P.E. Gold Attenuation of morphine-induced behavioral changes in rodents by d- and l-glucose Neurobiol Learn Mem 71 1989 62 79
27. M.E. Ragozzino, and P.E. Gold Glucose injections into the medial septum reverse the effects of intraseptal morphine infusions on hippocampal acetylcholine output and memory Neuroscience 68 1995 981 988
28. M.E. Ragozzino, K. Hellems, R.C. Lennartz, and P.E. Gold Pyruvate infusions into the septal area attenuate spontaneous alternation impairments induced by intraseptal morphine injections Behav Neurosci 109 1995 1074 1080
29. M.E. Ragozzino, M.E. Parker, and P.E. Gold Spontaneous alternation and inhibitory avoidance impairments with morphine injections into the medial septum. Attenuation by glucose administration Brain Res 597 1992 241 249
30. R.Q. Wan, B.S. Givens, and D.S. Olton Opioid modulation of working memory: intraseptal, but not intraamygdaloid, infusions of beta-endorphin impair performance in spatial alternation Neurobiol Learn Mem 63 1995 74 86
31. E. Bostock, M. Gallagher, and R.A. King Effects of opioid microinjections into the medial septal area on spatial memory in rats Behav Neurosci 102 1988 643 652
32. E. Costa, P. Panula, H.K. Thompson, and D.L. Cheney The transsynaptic regulation of the septal-hippocampal cholinergic neurons Life Sci 32 1983 165 179
33. L.K. Gorman, K. Pang, K.M. Frick, B. Givens, and D.S. Olton Acetylcholine release in the hippocampus: effects of cholinergic and GABAergic compounds in the medial septal area Neurosci Lett 166 1994 199 202
34. G.S. Simon, and W.L. Dewey Narcotics and diabetes: I. The effects of streptozotocin-induced diabetes on the antinociceptive potency of morphine J Pharmacol Exp Ther 218 1981 318 323
35. D.A. Brase, C.R. Ward, P.S. Bey, and W.L. Dewey Antagonism of the morphine-induced locomotor activation of mice by fructose: comparison with other opiates and sugars, and sugar effects on brain morphine Life Sci 49 1991 727 734
36. L.J. Pellegrino, A.S. Pellegrino, and A.J. Cushman A stereotaxic atlas of the rat brain 1979 Plenum New York
37. H. Benveniste, and N.H. Diemer Cellular reactions to implantation of a microdialysis tube in the rat hippocampus Acta Neuropathol 74 1987 234 238
38. D.J. Beracochea, and R. Jaffard Effects of ibotenic lesions of mammillary bodies on spontaneous and rewarded spatial alternation in mice J Cogn Neurosci 2 1990 133 140
39. M.E. Ragozzino, G.L. Wenk, and P.E. Gold Glucose attenuates morphine-induced decrease in hippocampal acetylcholine output: an in vivo microdialysis study in rats Brain Res 655 1994 77 82
40. M. Sarter, G. Bodewitz, and D.N. Stephens Attenuation of scopolamine-induced impairment of spontaneous alteration behaviour by antagonist but not inverse agonist and agonist beta-carbolines Psychopharmacology 94 1988 491 495
41. W.N. Dember Spontaneous alternation behavior 1989 Springer-Verlag New York
42. P.E. Gold Modulation of emotional and non-emotional memories: same pharmacological systems, different neuroanatomical systems J.L. McGaugh N.M. Weinberger G.S. Lynch Brain and memory: modulation and mediation of neural plasticity 1995 Oxford Press New York 41 74
43. E.C. McNay, and R.S. Sherwin Effect of recurrent hypoglycemia on spatial cognition and cognitive metabolism in normal and diabetic rats Diabetes 53 2004 418 425
44. D. Barrett, J. Shumake, D. Jones, and F. Gonzales-Lima Metabolic mapping of mouse brain activity after extinction of a conditioned emotional response J Neurosci 23 2003 5740 5749
45. B. Bontempi, R. Jaffard, and C. Destrade Differential temporal evolution of post-training changes in regional brain glucose metabolism induced by repeated spatial discrimination training in mice: visualization of the memory consolidation process? Eur J Neurosci 8 1996 2348 2360
46. 14C]2- deoxyglucose uptake in the glomerular layer of the rat olfactory bulb following early odor preference learning J Comp Neurol 376 1996 557 566
47. 14C]2-deoxyglucose uptake in subcortical and cortical structures during memory consolidation of an operant training in mice Behav Neural Biol 56 1991 43 61
48. P.E. Gold Drug enhancement of memory in aged rodents and humans M.E. Carroll J.B. Overmier Animal research and human health: advancing human welfare through behavioral science 2001 American Psychological Association Washington, DC 293 304
49. T.R. Mabry, P.E. Gold, and R. McCarty Age-related changes in plasma catecholamine and glucose responses of F-344 rats to footshock as in inhibitory avoidance training Neurobiol Learn Mem 64 1995 146 155
50. J.L. Hall, and P.E. Gold The effects of training, epinephrine, and glucose injections on plasma glucose levels in rats Behav Neural Biol 46 1986 156 176
51. S. Leutgeb, J.K. Leutgeb, C.A. Barnes, E.I. Moser, B.L. McNaughton, and M.-B. Moser Independent codes for spatial and episodic memory in hippocampal neuronal ensembles Science 309 2005 619 623
52. 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-mediated memory enhancement Neuroscience 93 1999 557 563
53. M.R. Stefani, and P.E. Gold Intra-hippocampal infusions of K-ATP channel modulators influence spontaneous alternation performance: relationships to acetylcholine release in the hippocampus J Neurosci 21 2001 609 614
54. A. Rashidy-Pour ATP-sensitive potassium channels mediate the effects of a peripheral injection of glucose on memory storage in an inhibitory avoidance task Behav Brain Res 126 2001 43 48
55. M. Narita, K. Takamori, N. Kawashima, M. Funada, J. Kamei, and T. Suzuki Activation of central ATP-sensitive potassium channels produces the antinociception and spinal noradrenaline turnover-enhancing effect in mice Psychopharmacology 113 1993 11 14
56. M. Ocaña, E. Del Pozo, M. Barrios, and M.M. Baeyens Subgroups among opioid receptor agonists distinguished by ATP-sensitive K1 channel acting drugs Br J Pharmacol 114 1995 1296 1302
57. R.B. Raffa, and R.P. Martinez The 'glibenclamide-shift' of centrally-acting antinociceptive agents in mice Brain Res 677 1995 277 282
58. Y. Uchida, K. Saito, T. Ohnishi, S. Maeda, T. Matsuya, and R. Inoki Antagonism by glibenclamide of the effect of morphine in hippocampal preparations Neurosci Lett 162 1993 14 16
59. M.E. Ragozzino, S.N. Pal, K. Unick, M.R. Stefani, and P.E. Gold Modulation of hippocampal acetylcholine release and of memory by intrahippocampal glucose injections J Neurosci 18 1998 1595 1601
60. 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