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The Journal of Neuroscience, September 5, 2007, 27(36):9790-9800; doi:10.1523/JNEUROSCI.1415-07.2007

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Cellular/Molecular
An Energy Budget for the Olfactory Glomerulus

Janna C. Nawroth,^1,3 Charles A. Greer,³ Wei R. Chen,³ Simon B. Laughlin,² and Gordon M. Shepherd³

¹Master Program Molecular Biotechnology, Institute of Pharmacy and Molecular Biotechnology, University of Heidelberg, D-69120 Heidelberg, Germany, ²Department of Zoology, Cambridge University, Cambridge CB2 3EJ, United Kingdom, and ³Department of Neurobiology, Yale University School of Medicine, New Haven, Connecticut 06510

Correspondence should be addressed to Dr. Gordon M. Shepherd, Department of Neurobiology, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06510. Email: gordon.shepherd{at}yale.edu

Energy demands are becoming recognized as an important constraint on neural signaling. The olfactory glomerulus provides a well defined system for analyzing this question. Odor stimulation elicits high-energy demands in olfactory glomeruli where olfactory axons converge onto dendrites of olfactory bulb neurons. We performed a quantitative analysis of the energy demands of each type of neuronal element within the glomerulus. This included the volumes of each element, their surface areas, and ion loads associated with membrane potentials and synaptic activation as constrained by experimental observations. In the resting state, there was a high-energy demand compared with other brain regions because of the high density of neural elements. The activated state was dominated by the energy demands of action potential propagation in afferent olfactory sensory neurons and their synaptic input to dendritic tufts, whereas subsequent dendritic potentials and dendrodendritic transmission contributed only a minor share of costs. It is proposed therefore that afferent input and axodendritic transmission account for the strong signals registered by 2-deoxyglucose and functional magnetic resonance imaging, although postsynaptic dendrites comprise at least one-half of the volume of the glomerulus. The results further suggest that presynaptic inhibition of the axon terminals by periglomerular cells plays an important role in limiting the range of excitation of the postsynaptic cells. These results provide a new quantitative basis for interpreting olfactory bulb activation patterns elicited by odor stimulation.

Key words: olfactory bulb; sensory processing; energy consumption; brain metabolism; functional imaging; fMRI; postsynaptic; presynaptic mechanisms; odor map

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Received March 29, 2007; revised July 18, 2007; accepted July 21, 2007.

Correspondence should be addressed to Dr. Gordon M. Shepherd, Department of Neurobiology, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06510. Email: gordon.shepherd{at}yale.edu

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