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The Journal of Neuroscience, February 1, 2000, 20(3):1199-1207

Four-Dimensional Neuronal Signaling by Nitric Oxide: A Computational Analysis

Andrew Philippides, Phil Husbands, and Michael O'Shea

Sussex Centre for Neuroscience, School of Biological Sciences, University of Sussex, Brighton, East Sussex, BN1 9QG, United Kingdom

Nitric oxide (NO) is now recognized as a transmitter of neurons that express the neuronal isoform of the enzyme nitric oxide synthase. NO, however, violates some of the key tenets of chemical transmission, which is classically regarded as occurring at points of close apposition between neurons. It is the ability of NO to diffuse isotropically in aqueous and lipid environments that has suggested a radically different form of signaling in which the transmitter acts four-dimensionally in space and time, affecting volumes of the brain containing many neurons and synapses. Although "volume signaling" clearly challenges simple connectionist models of neural processing, crucial to its understanding are the spatial and temporal dynamics of the spread of NO within the brain. Existing models of NO diffusion, however, have serious shortcomings because they represent solutions for "point-sources," which have no physical dimensions. Methods for overcoming these difficulties are presented here, and results are described that show how NO spreads from realistic neural architectures with both simple symmetrical and irregular shapes. By highlighting the important influence of the geometry of NO sources, our results provide insights into the four-dimensional spread of a diffusing messenger. We show for example that reservoirs of NO that accumulate in volumes of the nervous system where NO is not synthesized contribute significantly to the temporal and spatial dynamics of NO spread.

Key words: nitric oxide; diffusion; nitric oxide synthase; computational modeling; volume signaling; guanylyl cyclase

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Copyright © 2000 Society for Neuroscience  0270-6474/00/2031199-09$05.00/0

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