Intracerebroventricular insulin enhances memory in a passive-avoidance task

Physiology and Behavior

Volumn 68, Issue 4, 2000, Pages 509-514

  Park, Collin R ^a   Seeley, Randy J ^b   Craft, Suzanne ^c,d   Woods, Stephen C ^b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF CINCINNATI MEDICAL CENTER   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^d Education and Clinical Center   (United States)

Author keywords

Insulin; Intracerebroventricular; Memory; Passive avoidance

Indexed keywords

INSULIN;

ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; CONTROLLED STUDY; DRUG EFFECT; MALE; MEMORY; NONHUMAN; PASSIVE AVOIDANCE; PERFORMANCE; PRIORITY JOURNAL; RAT; TRAINING;

EID: 0034012731     PISSN: 00319384     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0031-9384(99)00220-6     Document Type: Article

References (52)

1. Craft S., Dagogo-Jack S.E., Wiethop B.V., Murphy C., Nevins R.T., Fleischman S., Rice V., Newcomer J.W., 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.
2. Craft S., Newcomer J., Kanne S., Dagogo-Jack S., Cryer P., Sheline Y., Luby J., Dagogo-Jack A., Alderson A. Memory improvement following induced hyperinsulinemia in Alzheimer's disease. Neurobiol Aging. 17:1996;123-130.
3. Hoyer S., Nitsch R., Oesterreich K. Predominant abnormality in cerebral glucose utilization in late-onset dementia of the Alzheimer type. a cross-sectional comparison against advanced late-onset and incipient early-onset cases J Neural Transm. 3:1991;1-14.
4. Frölich L., Blum-Degen D., Bernstein H.G., Englesberger S., Humrich J., Laufer S., Muschner D., Thalheimer A., Hoyer S., Beckmann H., Riederer P. Insulin and insulin receptors in the brain in aging and in sporadic Alzheimer's disease. J Neural Transm. 105:1998;423-438.
5. Richardson J.T.E. Cognitive function in diabetes mellitus. Neurosci Biobehav Rev. 14:1990;385-388.
6. Debons A.F., Krimsky I., From A. A direct action of insulin on the hypothalamic satiety center. Am J Physiol. 219:1970;938-943.
7. Hoyer S., Henneberg N., Knapp S., Lannert H., Martin M.L. Brain glucose metabolism is controlled by amplification and desensitization of the neuronal insulin receptor. Ann NY Acad Sci. 777:1996;374-379.
8. Plaschke K., Hoyer S. Action of the diabetogenic drug streptozotocin on glycolytic and glycogenolytic metabolism in adult rat brain cortex and hippocampus. Int J Dev Neurosci. 11:1993;477-483.
9. Woods S.C., Figlewicz-Lattemann D.P., Schwartz M.W., Porte D. Jr. A re-assessment of the regulation of adiposity and appetite by the brain insulin system. Int J Obes. 14:1990;69-76.
10. Chavez M., Kaiyala K., Madden L.J., Schwartz M.W., Woods S.C. Intraventricular insulin and the level of maintained body weight in rats. Behav Neurosci. 100:1995;528-531.
11. Schwartz M.W., Figlewicz D.P., Baskin D.G., Woods S.C., Porte D. Jr. Insulin in the brain. a hormonal regulator of energy balance Endocr Rev. 13:1992;387-414.
12. Oomura Y. Significance of glucose, insulin, and free fatty acid on the hypothalamic feeding and satiety neurons. Novin D., Wyrwicka W., Bray G. Hunger. Basic Mechanisms and Clinical Implications:1975;145-157 Raven Press, New York.
13. Palovcik R.A., Phillips M.I., Kappy M.S., Raizada M.K. Insulin inhibits pyramidal neurons in hippocampal slices. Brain Res. 309:1984;187-191.
14. Phillips M.I., Palovcik R.A. Dose-response testing of peptides by hippocampal brain slice recording. Methods Enzymol. 168:1989;129-144.
15. Havrankova J., Roth J., Brownstein M. Insulin receptors are widely distributed in the central nervous system of the rat. Nature. 272:1978;827-829.
16. Unger J.W., Livingston J.N., Moss A.M. Insulin receptors in the central nervous system. localization, signalling mechanisms and functional aspects Prog Neurobiol. 36:1991;343-362.
17. Baskin D.G., Sipols A.J., Schwartz M.W., White M.F. Immunocytochemical detection of insulin receptor substrate-1 (IRS-1) in rat brain. colocalization with phosphotyrosine Regul Pept. 48:1993;257-266.
18. 125I-insulin binding sites in the rat hypothalamus by quantitative autoradiography. Neurosci Lett. 70:1986;17-22.
19. Baskin D.G., Schwartz M.W., Sipols A.J., D'Alessio D.A., Goldstein B.J., White M.F. Insulin receptor substrate-1 (IRS-1) expression in rat brain. Endocrinology. 134:1994;1952-1955.
20. Kopf S.R., Baratti C.M. Memory modulation by post-training glucose or insulin remains evident at long retention intervals. Neurobiol Learn Mem. 65:1996;189-191.
21. Schwarzberg H., Bernstein H.G., Reiser M., Gunther O. Intracerebroventricular administration of insulin attenuates retrieval of a passive avoidance responce in rats. Neuropeptides. 13:1989;79-81.
22. Tamasi G.C., Drenick E.J. Resistance to insulin convulsions in fasted mice. Endocrinology. 92:1973;1277-1279.
23. Blanchard J.G., Duncan P.M. Effect of combinations of insulin, glucose and scopolamine on radial arm maze performance. Pharmacol Biochem Behav. 58:1997;209-214.
24. Schwartz M.W., Sipols A.J., Kahn S.E., Lattemann D.P., Taborsky G.J. Jr., Bergman R.N., Woods S.C., Porte D. Jr. Kinetics and specificity of insulin uptake from plasma into cerebrospinal fluid. Am J Physiol. 259:1990;E378-E383.
25. Bourne D.W.A., Triggs E.J., Eadie M.J. Pharmacokinetics for the Non-mathematical. 1986;MTP Press Ltd, Lancaster. pp. 41-45.
26. Meek JL, Neff NH. Is cerebrospinal fluid the major avenue for the removal of 5-hydroxyindoleacetic acid from the brain? Neuropharmacology 1973;12497-9.
27. Manin M., Broer Y., Balage M., Rostene W., Grizard J. Metabolic clearance of insulin from the cerebrospinal fluid in the anesthetized rat. Peptides. 11:1990;5-12.
28. Ono T., Steffens A.B., Sasaki K. Influence of peripheral and intracerebroventricular glucose and insulin infusions on peripheral and cerebrospinal fluid glucose and insulin levels. Physiol Behav. 30:1983;301-306.
29. Lorenzini C.A., Baldi E., Bucherelli C., Sacchetti B., Tassoni G. Role of dorsal hippocampus in acquisition, consolidation and retrieval of rat's passive avoidance response. a tetrodotoxin functional inactivation study Brain Res. 730:1996;32-39.
30. Lorenzini C.A., Baldi E., Bucherelli C., Sacchetti B., Tassoni G. Role of ventral hippocampus in acquisition, consolidation and retrieval of rat's passive avoidance response memory trace. Brain Res. 768:1997;242-248.
31. Gold P.E., Hall J.L. Posttraining glucose effects on memory. behavioral and pharmacological characteristics Behav Neural Biol. 46:1986;145.
32. 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.
33. Messier C. Object recognition in mice. Improvement of memory by glucose Neurobiol Learn Mem. 67:1997;172-175.
34. Hall J.L., Gonder-Frederick L.A., Chewning W.W., Silveira J., Gold P.E. Glucose enhancement of performance on memory tests in young and aged humans. Neuropsychologia. 27:1989;1129-1138.
35. Lee M.K., Graham S.N., Gold P.E. Memory enhancement with posttraining intraventricular glucose injections in rats. Behav Neurosci. 102:1988;591-595.
36. Henneberg N., Hoyer S. Short-term or long-term intracerebroventricular (i.c.v.) infusion of insulin exhibits a discrete anabolic effect on cerebral energy metabolism in the rat. Neurosci Lett. 175:1994;153-156.
37. Ragozzino M.E., Pal S.N., Unick K., Stefani M.R., Gold P.E. Modulation of hippocampal acetylcholine release and spontaneous alternation scores by intrahippocampal glucose injections. J Neurosci. 18:1998;1595-1601.
38. Ragozzino M.E., Unick K.E., Gold P.E. Hippocampal acetylcholine release during memory testing in rats. augmentation by glucose Proc Natl Acad Sci USA. 93:1996;4693-4698.
39. Liu L., Brown J.C. III, Webster W.W., Morrisett R.A., Monaghan D.T. Insulin potentiates N-methyl-D-aspartate receptor activity in Xenopus oocytes and rat hippocampus. Neurosci Lett. 192:1995;5-8.
40. + channel by insulin in rat skeletal muscle fibers. Biochem Biophys Res Commun. 232:1977;536-539.
41. Shapiro E., Brown S.D., Saltiel A.R., Schwartz J.H. Short-term action of insulin on Aplysia neurons. generation of a possible novel modulator of ion channels J Neurobiol. 22:1991;55-62.
42. 2+ pool and of neuropeptide secretion. Nature. 385:1997;343-346.
43. Nie L., Kanzaki M., Shibata H., Kojima I. Activation of calcium-permeable cation channel by insulin in Chinese hamster ovary cells expressing human insulin receptors. Endocrinology. 139:1998;179-188.
44. A receptors to postsynaptic domains by insulin. Nature. 388:1997;686-690.
45. Biessels G.-J., Kamal A., Ramakers G.M., Urban I.J., Spruijt B.M., Erkelens D.W., Gispen W.H. Place learning and hippocampal synaptic plasticity in streptozotocin-induced diabetic rats. Diabetes. 45:1996;1259-1266.
46. Biessels G.-J., Kamal A., Urban I.J., Spruijt B.M., Erkelens D.W., Gispen W.H. Water maze learning and hippocampal synaptic plasticity in streptozotocin-diabetic rats. effects of insulin treatment Brain Res. 800:1998;125-135.
47. Figlewicz D.P., Szot P. Insulin stimulates membrane phospholipid metabolism by enhancing endogenous alpha-1-adrenergic activity in the rat hippocampus. Brain Res. 550:1991;101-107.
48. Figlewicz D.P., Szot P., Greenwood M.R.C. Insulin stimulates inositol incorporation in hippocampus of lean but not obese Zucker rats. Physiol Behav. 47:1990;325-330.
49. Tsukahara H., Gordienko D.V., Tonshoff B., Gelato M.C., Goligorsky M.S. Direct demonstration of insulin-like growth factor-I-induced nitric oxide production by endothelial cells. Kidney Int. 45:1994;598-604.
50. Akers R.F., Routtenberg A. Brain protein phosphorylation in vitro. selective substrate action of insulin Life Sci. 35:1984;809-813.
51. Giorgino F., Almahfouz A., Goodyear L.J., Smith R.J. Glucocorticoid regulation of insulin receptor and substrate IRS-1 tyrosine phosphorylation in rat skeletal muscle in vivo. J Clin Invest. 91:1993;2020-2030.
52. Chavez M., Seeley R.J., Green P.K., Wilkinson C.W., Schwartz M.W., Woods S.C. Arenalectomy increases sensitivity to central insulin. Physiol Behav. 62:1997;631-634.