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Cerebral Cortex Advance Access originally published online on May 12, 2009
Cerebral Cortex 2009 19(12):3001-3010; doi:10.1093/cercor/bhp071
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© The Author 2009. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

A Simple Rule for Axon Outgrowth and Synaptic Competition Generates Realistic Connection Lengths and Filling Fractions

Marcus Kaiser1,2, Claus C. Hilgetag3,4 and Arjen van Ooyen5

1 School of Computing Science, Newcastle University, Newcastle upon Tyne NE1 7RU, UK, 2 Institute of Neuroscience, Newcastle University, Newcastle upon Tyne NE2 4HH, UK, 3 School of Engineering and Science, Jacobs University Bremen, 28759 Bremen, Germany, 4 Department of Health Sciences, Sargent College, Boston University, Boston MA 02215, USA, 5 Department of Integrative Neurophysiology, Center for Neurogenomics and Cognitive Research, VU University Amsterdam, 1081 HV Amsterdam, the Netherlands

Address correspondence to Dr Marcus Kaiser, School of Computing Science, Newcastle University, Claremont Tower, Newcastle upon Tyne NE1 7RU, UK. Email: m.kaiser{at}ncl.ac.uk.

Neural connectivity at the cellular and mesoscopic level appears very specific and is presumed to arise from highly specific developmental mechanisms. However, there are general shared features of connectivity in systems as different as the networks formed by individual neurons in Caenorhabditis elegans or in rat visual cortex and the mesoscopic circuitry of cortical areas in the mouse, macaque, and human brain. In all these systems, connection length distributions have very similar shapes, with an initial large peak and a long flat tail representing the admixture of long-distance connections to mostly short-distance connections. Furthermore, not all potentially possible synapses are formed, and only a fraction of axons (called filling fraction) establish synapses with spatially neighboring neurons. We explored what aspects of these connectivity patterns can be explained simply by random axonal outgrowth. We found that random axonal growth away from the soma can already reproduce the known distance distribution of connections. We also observed that experimentally observed filling fractions can be generated by competition for available space at the target neurons—a model markedly different from previous explanations. These findings may serve as a baseline model for the development of connectivity that can be further refined by more specific mechanisms.

Key Words: axon growth • cortical networks • filling fraction • neural competition • neural networks


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