A simple rule for axon outgrowth and synaptic competition generates realistic connection lengths and filling fractions

TY - JOUR

T1 - A simple rule for axon outgrowth and synaptic competition generates realistic connection lengths and filling fractions

AU - Kaiser, Marcus

AU - Hilgetag, Claus C

AU - van Ooyen, Arjen

PY - 2009/12

Y1 - 2009/12

N2 - 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.

AB - 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.

KW - Animals

KW - Axons

KW - Cell Enlargement

KW - Computer Simulation

KW - Macaca

KW - Models, Anatomic

KW - Models, Neurological

KW - Morphogenesis

KW - Synapses

KW - Journal Article

KW - Research Support, Non-U.S. Gov't

U2 - 10.1093/cercor/bhp071

DO - 10.1093/cercor/bhp071

M3 - SCORING: Journal article

C2 - 19435708

VL - 19

SP - 3001

EP - 3010

JO - CEREB CORTEX

JF - CEREB CORTEX

SN - 1047-3211

IS - 12

ER -