Independently outgrowing neurons and geometry-based synapse formation produce networks with realistic synaptic connectivity

PLoS One. 2014 Jan 16;9(1):e85858. doi: 10.1371/journal.pone.0085858. eCollection 2014.

Abstract

Neuronal signal integration and information processing in cortical networks critically depend on the organization of synaptic connectivity. During development, neurons can form synaptic connections when their axonal and dendritic arborizations come within close proximity of each other. Although many signaling cues are thought to be involved in guiding neuronal extensions, the extent to which accidental appositions between axons and dendrites can already account for synaptic connectivity remains unclear. To investigate this, we generated a local network of cortical L2/3 neurons that grew out independently of each other and that were not guided by any extracellular cues. Synapses were formed when axonal and dendritic branches came by chance within a threshold distance of each other. Despite the absence of guidance cues, we found that the emerging synaptic connectivity showed a good agreement with available experimental data on spatial locations of synapses on dendrites and axons, number of synapses by which neurons are connected, connection probability between neurons, distance between connected neurons, and pattern of synaptic connectivity. The connectivity pattern had a small-world topology but was not scale free. Together, our results suggest that baseline synaptic connectivity in local cortical circuits may largely result from accidentally overlapping axonal and dendritic branches of independently outgrowing neurons.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Shape
  • Cells, Cultured
  • Computer Simulation*
  • Dendrites / physiology
  • Models, Biological*
  • Nerve Net / cytology
  • Neurons / physiology*
  • Pyramidal Tracts / cytology
  • Rats
  • Software
  • Synapses / physiology*

Grants and funding

This work was supported by the BIO-ICT project SECO (grant number 216593) of the 7th Framework Programme of the European Union, and the NETFORM project (grant number 635.100.017) of the Computational Life Sciences program of the Netherlands Organization for Scientific Research. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.