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The Journal of Neuroscience, February 4, 2009, 29(5):1424-1433; doi:10.1523/JNEUROSCI.4817-08.2009

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Cellular/Molecular
Odor-Evoked Oxygen Consumption by Action Potential and Synaptic Transmission in the Olfactory Bulb

Jérôme Lecoq,^1,2,3 Pascale Tiret,^1,2,3 Marion Najac,^1,2,3 Gordon M. Shepherd,⁴ Charles A. Greer,^5,6 and Serge Charpak^1,2,3

¹Institut National de la Santé et de la Recherche Médicale, U603, ²Centre National de la Recherche Scientifique, Unité Mixte de Recherche 8154, and ³Laboratory of Neurophysiology and New Microscopies, Université Paris Descartes, Paris 75006, France, and Departments of ⁴Neurobiology, ⁵Neurosurgery, and ⁶Neurobiology, Yale University School of Medicine, New Haven, Connecticut 06520

Correspondence should be addressed to Serge Charpak, Institut National de la Santé et de la Recherche Médicale U 603, Laboratory of Neurophysiology, 45 rue des St Pères, 75006 Paris, France. E-mail: Email: serge.charpak{at}univ-paris5.fr

The relationship between metabolism of neuronal activity, microvascular organization, and blood flow dynamics is critical for interpreting functional brain imaging. Here we used the rat dorsal olfactory bulb as a model to determine in vivo the correlation between action potential propagation, synaptic transmission, oxygen consumption, and capillary density during odor stimulation. We find that capillary lumen occupies 3% of the glomerular volume, where synaptic transmission occurs, and only 0.1% of the overlying nerve layer. In glomeruli, odor triggers a local early decrease in tissue oxygen partial pressure that results principally from dendritic activation rather than from firing of axon terminals, transmitter release or astrocyte activation. In the nerve layer, action potential propagation does not generate local changes in tissue oxygen partial pressure. We conclude that capillary density is tightly correlated with the oxidative metabolism of synaptic transmission, and suggest that action potential propagation operates mainly anaerobically.

Key words: neurometabolic coupling; metabolism; oxygen; olfactory bulb; neurovascular coupling; odor

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Received Oct. 7, 2008; revised Dec. 10, 2008; accepted Jan. 2, 2009.

Correspondence should be addressed to Serge Charpak, Institut National de la Santé et de la Recherche Médicale U 603, Laboratory of Neurophysiology, 45 rue des St Pères, 75006 Paris, France. E-mail: Email: serge.charpak{at}univ-paris5.fr

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				K. Thomsen, H. Piilgaard, A. Gjedde, G. Bonvento, and M. Lauritzen Principal Cell Spiking, Postsynaptic Excitation, and Oxygen Consumption in the Rat Cerebellar Cortex J Neurophysiol, September 1, 2009; 102(3): 1503 - 1512. [Abstract] [Full Text] [PDF]

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