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Original Research ARTICLE

Deciphering neuron-glia compartmentalization in cortical energy metabolism

Renaud Jolivet¹*, Pierre J. Magistretti^2,3 and Bruno Weber¹

Institute of Pharmacology and Toxicology, University of Zurich, Zurich, Switzerland

Brain Mind Institute, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland

Center for Psychiatric Neuroscience, University of Lausanne and CHUV, Lausanne, Switzerland

Energy demand is an important constraint on neural signaling. Several methods have been proposed to assess the energy budget of the brain based on a bottom-up approach in which the energy demand of individual biophysical processes are first estimated independently and then summed up to compute the brain’s total energy budget. Here, we address this question using a novel approach that makes use of published datasets that reported average cerebral glucose and oxygen utilization in humans and rodents during different activation states. Our approach allows us (1) to decipher neuron-glia compartmentalization in energy metabolism and (2) to compute a precise state-dependent energy budget for the brain. Under the assumption that the fraction of energy used for signaling is proportional to the cycling of neurotransmitters, we find that in the activated state, most of the energy (∼80%) is oxidatively produced and consumed by neurons to support neuron-to-neuron signaling. Glial cells, while only contributing for a small fraction to energy production (∼6%), actually take up a significant fraction of glucose (50% or more) from the blood and provide neurons with glucose-derived energy substrates. Our results suggest that glycolysis occurs for a significant part in astrocytes whereas most of the oxygen is utilized in neurons. As a consequence, a transfer of glucose-derived metabolites from glial cells to neurons has to take place. Furthermore, we find that the amplitude of this transfer is correlated to (1) the activity level of the brain; the larger the activity, the more metabolites are shuttled from glia to neurons and (2) the oxidative activity in astrocytes; with higher glial pyruvate metabolism, less metabolites are shuttled from glia to neurons. While some of the details of a bottom-up biophysical approach have to be simplified, our method allows for a straightforward assessment of the brain’s energy budget from macroscopic measurements with minimal underlying assumptions.

Keywords:

astrocyte-neuron interactions, brain energy metabolism, brain energy budget, glucose, oxygen

Citation:

Jolivet R, Magistretti PJ and Weber B (2009). Deciphering neuron-glia compartmentalization in cortical energy metabolism. Front. Neuroenerg. 1:4. doi: 10.3389/neuro.14.004.2009

Received:

02 February 2009;

Paper pending published:

28 April 2009;

Accepted:

22 June 2009;

Published online:

09 July 2009.

Edited by:

Rolf Gruetter, Ecole Polytechnique FÃƒÂƒÃ‚Â©dÃƒÂƒÃ‚Â©rale de Lausanne, Switzerland

Reviewed by:

Kevin L. Behar, Yale University, School of Medicine, Department of Diagnostic Radiology, Yale Magnetic Resonance Center, USA
Helle S. Waagepetersen, University of Copenhagen, Denmark
Albert Gjedde, Aarhus University Hospital, Denmark

© 2009 Jolivet, Magistretti and Weber. This is an open-access article subject to an exclusive license agreement between the authors and the Frontiers Research Foundation, which permits unrestricted use, distribution, and reproduction in any medium, provided the original authors and source are credited.

*Correspondence:

Renaud Jolivet, University Hospital Zurich, Nuclear Medicine, Rämistrasse 100, CH-8091, Zürich, Switzerland. e-mail: renaud.jolivet@a3.epfl.ch