The dynamic brain: Synaptic plasticity on different time scales

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Original Research
01 April 2014
Homeostatic structural plasticity increases the efficiency of small-world networks
Markus Butz
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Arjen van Ooyen
The spatial distribution of newly formed synapses change in dependence on the calcium concentration. In (A,B), each dot represents the Euclidean distances between those neurons that are most likely to form a synaptic connection with each other at this update in connectivity. For this, we took at every update in connectivity in which vacant synaptic elements were available the Euclidean distance of the connection from neuron j to i for which Pformi,j (Equation 7) was maximal. In (C,D), each dot represents the length of that connection (again in terms of the Euclidean distance between the connected neurons) for which synapse deletion was most likely, i.e., Pdeli,j (Equation 6) was maximal for every update in connectivity in which synapses had to be deleted. In (A,C), we plotted the Euclidean distances for synapse formation and deletion over time. The black curve (right y-axis) indicates the course of the calcium concentration [Ca2+]. In (B,D), we plotted synapse formation and deletion in dependence on [Ca2+]. The color code in all panels indicates the density of the dots in the diagrams, with blue and red representing low and high densities of dots, respectively. The figure essentially shows that before calcium reaches the homeostatic set-point ϵ, the distribution for synapse formation is rather Gaussian, following the Kernel function K (Equation 5). The distribution becomes random and scattered, with increased Euclidean distances, when calcium is at the set-point. The stripes in the distribution arise from the fact that not all Euclidean distances are possible due to the grid layout of the network. There is no change in the distribution for synapse deletion.

In networks with small-world topology, which are characterized by a high clustering coefficient and a short characteristic path length, information can be transmitted efficiently and at relatively low costs. The brain is composed of small-world networks, and evolution may have optimized brain connectivity for efficient information processing. Despite many studies on the impact of topology on information processing in neuronal networks, little is known about the development of network topology and the emergence of efficient small-world networks. We investigated how a simple growth process that favors short-range connections over long-range connections in combination with a synapse formation rule that generates homeostasis in post-synaptic firing rates shapes neuronal network topology. Interestingly, we found that small-world networks benefited from homeostasis by an increase in efficiency, defined as the averaged inverse of the shortest paths through the network. Efficiency particularly increased as small-world networks approached the desired level of electrical activity. Ultimately, homeostatic small-world networks became almost as efficient as random networks. The increase in efficiency was caused by the emergent property of the homeostatic growth process that neurons started forming more long-range connections, albeit at a low rate, when their electrical activity was close to the homeostatic set-point. Although global network topology continued to change when neuronal activities were around the homeostatic equilibrium, the small-world property of the network was maintained over the entire course of development. Our results may help understand how complex systems such as the brain could set up an efficient network topology in a self-organizing manner. Insights from our work may also lead to novel techniques for constructing large-scale neuronal networks by self-organization.

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