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Volume 17, Number 24, Issue of December 15, 1997 pp. 9448-9457

Endogenous Monocarboxylates Sustain Hippocampal Synaptic Function and Morphological Integrity during Energy Deprivation

Received May 6, 1997; revised Sept. 9, 1997; accepted Sept. 30, 1997.

Yukitoshi Izumi1, Ann M. Benz1, Hiroshi Katsuki1, and Charles F. Zorumski1, 2

Departments of 1 Psychiatry and 2 Neurobiology, Washington University School of Medicine, St. Louis, Missouri 63110

The ability to fuel neurons via glycogenolysis is believed to be an important function of glia. Indeed, the slow, rather than immediate, depression of synaptic transmission in hippocampal slices during exogenous glucose deprivation suggests that intrinsic energy reservoirs help to sustain neurotransmission. It is believed that glia fuel neighboring neurons via diffusible monocarboxylates such as pyruvate and lactate, although a role for glucose has been proposed also. Using alpha -cyano-4-hydroxycinnamate (4-CIN) to inhibit monocarboxylate transport and cytochalasin B (CCB) to inhibit glucose transport, we examined the role of glucose and monocarboxylates in supporting the functional and morphological integrity of hippocampal neurons during glucose deprivation. Although 200 µM 4-CIN failed to depress EPSPs supported by 10 mM glucose, pretreatment with 4-CIN accelerated the depression of EPSPs during glucose deprivation. 4-CIN also accelerated the decline in glucose-supported EPSPs after administration of 50 µM CCB, whereas CCB failed to alter the slow decay of pyruvate-supported EPSPs during pyruvate deprivation. 4-CIN did not alter the morphology of pyramidal neurons in the presence of 10 mM glucose but produced significant damage during glucose deprivation or CCB administration. These results suggest that endogenous monocarboxylates rather than glucose maintain neuronal integrity during energy deprivation. Furthermore, EPSPs supported by 2-3.3 mM glucose were sensitive to 4-CIN, suggesting that endogenous monocarboxylates are involved in maintaining neuronal function even under conditions of mild glucose deprivation.

Key words: hippocampus; energy metabolism; glucose transport; pyruvate; lactate; neuroglial interactions




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