Self-organization of a doubly asynchronous irregular network state for spikes and bursts

Abstract

Cortical pyramidal cells (PCs) have a specialized dendritic mechanism for the generation of bursts, suggesting that these events play a special role in cortical information processing. In vivo, bursts occur at a low, but consistent rate. Theory suggests that this network state increases the amount of information they convey. However, because burst activity relies on a threshold mechanism, it is rather sensitive to dendritic input levels. In spiking network models, network states in which bursts occur rarely are therefore typically not robust, but require fine-tuning. Here, we show that this issue can be solved by a homeostatic inhibitory plasticity rule in dendrite-targeting interneurons that is consistent with experimental data. The suggested learning rule can be combined with other forms of inhibitory plasticity to self-organize a network state in which both spikes and bursts occur asynchronously and irregularly at low rate. Finally, we show that this network state creates the network conditions for a recently suggested multiplexed code and thereby indeed increases the amount of information encoded in bursts. Author summary The language of the brain consists of sequences of action potentials. These sequences often contain bursts, short “words” consisting of a few action potentials in rapid succession. Bursts appear to play a special role in the brain. They indicate whether a stimulus was perceived or missed, and they are very effective drivers of synaptic plasticity, the neural substrate of learning. Bursts occur rarely, but consistently, a condition that is thought to maximize the amount of information they can communicate. In our article, we argue that this condition is far from self-evident, but requires very special circumstances. We show that these circumstances can be reached by homeostatic inhibitory plasticity in certain inhibitory neuron types. This may sound complicated, but basically works just like a thermostat. When bursts occur too often, inhibition goes up and suppresses them. When they are too rare, inhibition goes down and thereby increases their number. In computer simulations, we show that this simple mechanism can create circumstances akin to those in the brain, and indeed allows bursts to convey information effectively. Whether this mechanism is indeed used by the brain now remains to be tested by our experimental colleagues.