Decreases in Rat Extracellular Hippocampal Glucose Concentration Associated with Cognitive Demand During a Spatial Task

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2000 Mar 8

PMID 10706633

Citations 132

Authors

E C McNay

T M Fries

P E Gold

Affiliations

Soon will be listed here.

Abstract

Using in vivo microdialysis, we measured hippocampal extracellular glucose concentrations in rats while they performed spontaneous alternation tests of spatial working memory in one of two mazes. Extracellular glucose levels in the hippocampus decreased by 32% below baseline during the test period on the more complex maze, but by a maximum of 11% on the less complex maze. Comparable decreases were not observed in samples taken from rats tested on the more complex maze but with probes located near but outside of the hippocampus. Systemic glucose fully blocked any decrease in extracellular glucose and enhanced alternation on the more complex maze. These findings suggest that cognitive activity can deplete extracellular glucose in the hippocampus and that exogenous glucose administration reverses the depletion while enhancing task performance.

Citing Articles

Mitochondrial pyruvate transport regulates presynaptic metabolism and neurotransmission.

Tiwari A, Myeong J, Hashemiaghdam A, Stunault M, Zhang H, Niu X Sci Adv. 2024; 10(46):eadp7423.

PMID: 39546604 PMC: 11567002. DOI: 10.1126/sciadv.adp7423.

Concentrations of glutamate and -acetylaspartate detected by magnetic resonance spectroscopy in the rat hippocampus correlate with hippocampal-dependent spatial memory performance.

Duarte J Front Mol Neurosci. 2024; 17:1458070.

PMID: 39219740 PMC: 11362093. DOI: 10.3389/fnmol.2024.1458070.

WNKs regulate mouse behavior and alter central nervous system glucose uptake and insulin signaling.

Jaykumar A, Binns D, Taylor 4th C, Anselmo A, Birnbaum S, Huber K bioRxiv. 2024; .

PMID: 38915673 PMC: 11195145. DOI: 10.1101/2024.06.09.598125.

Mind the Metabolic Gap: Bridging Migraine and Alzheimer's disease through Brain Insulin Resistance.

Del Moro L, Pirovano E, Rota E Aging Dis. 2024; 15(6):2526-2553.

PMID: 38913047 PMC: 11567252. DOI: 10.14336/AD.2024.0351.

An Integrated Perspective of Effort and Perception of Effort.

Halperin I, Vigotsky A Sports Med. 2024; 54(8):2019-2032.

PMID: 38909350 PMC: 11329614. DOI: 10.1007/s40279-024-02055-8.

References

Wenk G . An hypothesis on the role of glucose in the mechanism of action of cognitive enhancers. Psychopharmacology (Berl). 1989; 99(4):431-8. DOI: 10.1007/BF00589888. View

Kirkby R, Stein D, Kimble R, Kimble D . Effects of hippocampal lesions and duration of sensory input on spontaneous alternation. J Comp Physiol Psychol. 1967; 64(2):342-5. DOI: 10.1037/h0088012. View

Harada M, Okuda C, Sawa T, Murakami T . Cerebral extracellular glucose and lactate concentrations during and after moderate hypoxia in glucose- and saline-infused rats. Anesthesiology. 1992; 77(4):728-34. DOI: 10.1097/00000542-199210000-00017. View

Stevens R, Cowey A . Effects of dorsal and ventral hippocampal lesions on spontaneous alternation, learned alternation and probability learning in rats. Brain Res. 1973; 52:203-24. DOI: 10.1016/0006-8993(73)90659-8. View

Sokoloff L, Reivich M, Kennedy C, Des Rosiers M, PATLAK C, Pettigrew K . The [14C]deoxyglucose method for the measurement of local cerebral glucose utilization: theory, procedure, and normal values in the conscious and anesthetized albino rat. J Neurochem. 1977; 28(5):897-916. DOI: 10.1111/j.1471-4159.1977.tb10649.x. View

Ragozzino M, Unick K, Gold P . Hippocampal acetylcholine release during memory testing in rats: augmentation by glucose. Proc Natl Acad Sci U S A. 1996; 93(10):4693-8. PMC: 39341. DOI: 10.1073/pnas.93.10.4693. View

Sarter M, Bodewitz G, Stephens D . Attenuation of scopolamine-induced impairment of spontaneous alteration behaviour by antagonist but not inverse agonist and agonist beta-carbolines. Psychopharmacology (Berl). 1988; 94(4):491-5. DOI: 10.1007/BF00212843. View

Ragozzino M, PARKER M, Gold P . Spontaneous alternation and inhibitory avoidance impairments with morphine injections into the medial septum. Attenuation by glucose administration. Brain Res. 1992; 597(2):241-9. DOI: 10.1016/0006-8993(92)91480-3. View

Winocur G, Gagnon S . Glucose treatment attenuates spatial learning and memory deficits of aged rats on tests of hippocampal function. Neurobiol Aging. 1998; 19(3):233-41. DOI: 10.1016/s0197-4580(98)00057-8. View

10.

Stone W, Walser B, Gold S, Gold P . Scopolamine- and morphine-induced impairments of spontaneous alternation performance in mice: reversal with glucose and with cholinergic and adrenergic agonists. Behav Neurosci. 1991; 105(2):264-71. DOI: 10.1037//0735-7044.105.2.264. View

11.

Benton D, Owens D . Blood glucose and human memory. Psychopharmacology (Berl). 1993; 113(1):83-8. DOI: 10.1007/BF02244338. View

12.

Messier C, Gagnon M . Glucose regulation and cognitive functions: relation to Alzheimer's disease and diabetes. Behav Brain Res. 1996; 75(1-2):1-11. DOI: 10.1016/0166-4328(95)00153-0. View

13.

Pellerin L, Magistretti P . Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci U S A. 1994; 91(22):10625-9. PMC: 45074. DOI: 10.1073/pnas.91.22.10625. View

14.

McNay E, Gold P . Extracellular glucose concentrations in the rat hippocampus measured by zero-net-flux: effects of microdialysis flow rate, strain, and age. J Neurochem. 1999; 72(2):785-90. DOI: 10.1046/j.1471-4159.1999.720785.x. View

15.

Pacteau C, Einon D, Sinden J . Early rearing environment and dorsal hippocampal ibotenic acid lesions: long-term influences on spatial learning and alternation in the rat. Behav Brain Res. 1989; 34(1-2):79-96. DOI: 10.1016/s0166-4328(89)80092-0. View

16.

Sokoloff L, Takahashi S, Gotoh J, Driscoll B, Law M . Contribution of astroglia to functionally activated energy metabolism. Dev Neurosci. 1996; 18(5-6):344-52. View

17.

Stone W, Rudd R, Gold P . Glucose attenuation of atropine-induced deficits in paradoxical sleep and memory. Brain Res. 1995; 694(1-2):133-8. DOI: 10.1016/0006-8993(95)00810-d. View

18.

Gold P . Role of glucose in regulating the brain and cognition. Am J Clin Nutr. 1995; 61(4 Suppl):987S-995S. DOI: 10.1093/ajcn/61.4.987S. View

19.

Korol D, Gold P . Glucose, memory, and aging. Am J Clin Nutr. 1998; 67(4):764S-771S. DOI: 10.1093/ajcn/67.4.764S. View

20.

Messier C, White N . Memory improvement by glucose, fructose, and two glucose analogs: a possible effect on peripheral glucose transport. Behav Neural Biol. 1987; 48(1):104-27. DOI: 10.1016/s0163-1047(87)90634-0. View