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The Journal of Neuroscience, November 7, 2007, 27(45):12242-12254; doi:10.1523/JNEUROSCI.3753-07.2007

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Behavioral/Systems/Cognitive
Stereotypical Bouton Clustering of Individual Neurons in Cat Primary Visual Cortex

Tom Binzegger,^1,2 Rodney J. Douglas,¹ and Kevan A. C. Martin¹

¹Institute of Neuroinformatics, University Zürich and Swiss Federal Institute of Technology Zürich, 8057 Zürich, Switzerland, and ²Henry Wellcome Building, University of Newcastle, Newcastle upon Tyne NE2 4HH, United Kingdom

Correspondence should be addressed to Tom Binzegger, School of Biology, Henry Wellcome Building for Neuroecology, University of Newcastle upon Tyne NE2 4HH, UK. Email: tom.binzegger{at}ncl.ac.uk

In all species examined, with the exception of rodents, the axons of neocortical neurons form boutons in multiple separate clusters. Most descriptions of clusters are anecdotal, so here we developed an objective method for identifying clusters. We applied a mean-shift cluster-algorithm to three-dimensional reconstructions of 39 individual neurons and three thalamic afferents from the cat primary visual cortex. Both spiny (20 of 26) and smooth (7 of 13) neurons formed at least two distinct ellipsoidal clusters (range, 2–7). For all cell types, cluster formation is heterogenous, but is regulated so that cluster size and the number of boutons allocated to a cluster equalize with increasing number of clusters formed by a neuron. The bouton density within a cluster is inversely related to the spatial scale of the axon, resulting in a four times greater density for smooth neurons than for spiny neurons. Thus, the inhibitory action of the smooth neurons is much more concentrated and focal than the excitatory action of spiny neurons. The cluster with the highest number of boutons (primary cluster) was typically located around or above the soma of the parent neuron. The distance to the next cluster was proportional to the diameter of the primary cluster, suggesting that there is an optimal distance and spatial focus of the lateral influence of a neuron. The lateral spread of clustered axons may thus support a spoke-like network architecture that routes signals to localized sites, thereby reducing signal correlation and redundancy.

Key words: bouton patches; axon; HRP; micro-circuit; cluster algorithm; trivariate Gaussian mixture; patch model

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Received March 7, 2007; revised Sept. 20, 2007; accepted Sept. 20, 2007.

Correspondence should be addressed to Tom Binzegger, School of Biology, Henry Wellcome Building for Neuroecology, University of Newcastle upon Tyne NE2 4HH, UK. Email: tom.binzegger{at}ncl.ac.uk

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