A few strong connections: optimizing information retention in neuronal avalanches

Abstract

Abstract Background How living neural networks retain information is still incompletely understood. Two prominent ideas on this topic have developed in parallel, but have remained somewhat unconnected. The first of these, the "synaptic hypothesis," holds that information can be retained in synaptic connection strengths, or weights, between neurons. Recent work inspired by statistical mechanics has suggested that networks will retain the most information when their weights are distributed in a skewed manner, with many weak weights and only a few strong ones. The second of these ideas is that information can be represented by stable activity patterns. Multineuron recordings have shown that sequences of neural activity distributed over many neurons are repeated above chance levels when animals perform well-learned tasks. Although these two ideas are compelling, no one to our knowledge has yet linked the predicted optimum distribution of weights to stable activity patterns actually observed in living neural networks. Results Here, we explore this link by comparing stable activity patterns from cortical slice networks recorded with multielectrode arrays to stable patterns produced by a model with a tunable weight distribution. This model was previously shown to capture central features of the dynamics in these slice networks, including neuronal avalanche cascades. We find that when the model weight distribution is appropriately skewed, it correctly matches the distribution of repeating patterns observed in the data. In addition, this same distribution of weights maximizes the capacity of the network model to retain stable activity patterns. Thus, the distribution that best fits the data is also the distribution that maximizes the number of stable patterns. Conclusions We conclude that local cortical networks are very likely to use a highly skewed weight distribution to optimize information retention, as predicted by theory. Fixed distributions impose constraints on learning, however. The network must have mechanisms for preserving the overall weight distribution while allowing individual connection strengths to change with learning.