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Role of glutamate in neuron-glia metabolic coupling^1,2,3,4

¹ From the Brain Mind Institute Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland, and the Center for Psychiatric Neuroscience, DP-CHUV/UNIL Centre de Neurosciences Psychiatriques Département de Psychiatrie/CHUV, Prilly, Switzerland.

² Presented at the "100th Anniversary Symposium of Umami Discovery: The Roles of Glutamate in Taste, Gastrointestinal Function, Metabolism, and Physiology," held in Tokyo, Japan, September 10–13, 2008.

³ Supported by the Swiss National Science Foundation for studies from the author’s laboratory.

⁴ Address correspondence to PJ Magistretti, Brain Mind Institute Ecole Polytechnique Fédérale de Lausanne, AAB 1 33 (Bâtiment AAB), Station 15, CH-1015 Lausanne, Switzerland. E-mail: pierre.magistretti{at}epfl.ch.

The coupling between synaptic activity and glucose utilization (neurometabolic coupling) is a central physiologic principle of brain function that has provided the basis for 2-deoxyglucose-based functional imaging with positron emission tomography. Approximately 10 y ago we provided experimental evidence that indicated a central role of glutamate signaling on astrocytes in neurometabolic coupling. The basic mechanism in neurometabolic coupling is the glutamate-stimulated aerobic glycolysis in astrocytes, such that the sodium-coupled reuptake of glutamate by astrocytes and the ensuing activation of the Na⁺-K⁺ ATPase triggers glucose uptake and its glycolytic processing, which results in the release of lactate from astrocytes. Lactate can then contribute to the activity-dependent fueling of the neuronal energy demands associated with synaptic transmission. Analyses of this coupling have been extended in vivo and have defined the methods of coupling for inhibitory neurotransmission as well as its spatial extent in relation to the propagation of metabolic signals within the astrocytic syncytium. On the basis of a large body of experimental evidence, we proposed an operational model, "the astrocyte-neuron lactate shuttle." A series of results obtained by independent laboratories have provided further support for this model. This body of evidence provides a molecular and cellular basis for interpreting data that are obtained with functional brain imaging studies.

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