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.
Short-term plasticity (STP) denotes changes in synaptic strength that last up to tens of seconds. It is generally thought that STP impacts information transfer across synaptic connections and may thereby provide neurons with, for example, the ability to detect input coherence, to maintain stability and to promote synchronization. STP is due to a combination of mechanisms, including vesicle depletion and calcium accumulation in synaptic terminals. Different forms of STP exist, depending on many factors, including synapse type. Recent evidence shows that synapse dependence holds true even for connections that originate from a single presynaptic cell, which implies that postsynaptic target cell type can determine synaptic short-term dynamics. This arrangement is surprising, since STP itself is chiefly due to presynaptic mechanisms. Target-specific synaptic dynamics in addition imply that STP is not a bug resulting from synapses fatiguing when driven too hard, but rather a feature that is selectively implemented in the brain for specific functional purposes. As an example, target-specific STP results in sequential somatic and dendritic inhibition in neocortical and hippocampal excitatory cells during high-frequency firing. Recent studies also show that the Elfn1 gene specifically controls STP at some synapse types. In addition, presynaptic NMDA receptors have been implicated in synapse-specific control of synaptic dynamics during high-frequency activity. We argue that synapse-specific STP deserves considerable further study, both experimentally and theoretically, since its function is not well known. We propose that synapse-specific STP has to be understood in the context of the local circuit, which requires combining different scientific disciplines ranging from molecular biology through electrophysiology to computer modeling.