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

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...

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Main Authors: Arjen van Ooyen, Andrew Carnell, Sander de Ridder, Bernadetta Tarigan, Huibert D Mansvelder, Fetsje Bijma, Mathisca de Gunst, Jaap van Pelt
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2014-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC3894200?pdf=render
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spelling doaj-bd69f81cc4644c0892dcc70f0cffe43b2020-11-25T01:18:31ZengPublic Library of Science (PLoS)PLoS ONE1932-62032014-01-0191e8585810.1371/journal.pone.0085858Independently outgrowing neurons and geometry-based synapse formation produce networks with realistic synaptic connectivity.Arjen van OoyenAndrew CarnellSander de RidderBernadetta TariganHuibert D MansvelderFetsje BijmaMathisca de GunstJaap van PeltNeuronal 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.http://europepmc.org/articles/PMC3894200?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Arjen van Ooyen
Andrew Carnell
Sander de Ridder
Bernadetta Tarigan
Huibert D Mansvelder
Fetsje Bijma
Mathisca de Gunst
Jaap van Pelt
spellingShingle Arjen van Ooyen
Andrew Carnell
Sander de Ridder
Bernadetta Tarigan
Huibert D Mansvelder
Fetsje Bijma
Mathisca de Gunst
Jaap van Pelt
Independently outgrowing neurons and geometry-based synapse formation produce networks with realistic synaptic connectivity.
PLoS ONE
author_facet Arjen van Ooyen
Andrew Carnell
Sander de Ridder
Bernadetta Tarigan
Huibert D Mansvelder
Fetsje Bijma
Mathisca de Gunst
Jaap van Pelt
author_sort Arjen van Ooyen
title Independently outgrowing neurons and geometry-based synapse formation produce networks with realistic synaptic connectivity.
title_short Independently outgrowing neurons and geometry-based synapse formation produce networks with realistic synaptic connectivity.
title_full Independently outgrowing neurons and geometry-based synapse formation produce networks with realistic synaptic connectivity.
title_fullStr Independently outgrowing neurons and geometry-based synapse formation produce networks with realistic synaptic connectivity.
title_full_unstemmed Independently outgrowing neurons and geometry-based synapse formation produce networks with realistic synaptic connectivity.
title_sort independently outgrowing neurons and geometry-based synapse formation produce networks with realistic synaptic connectivity.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2014-01-01
description 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.
url http://europepmc.org/articles/PMC3894200?pdf=render
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