Reduced stochastic models reveal the mechanisms underlying drifting cell assemblies

In a standard model, associative memories are represented by assemblies of strongly interconnected neurons. It has recently been proposed that these assemblies are not static but drift freely in neural circuits. This explains experimental findings of changing memory representations. On the level of single neurons, assembly drift is reflected by characteristic dynamics: relatively long times of stable assembly membership interspersed with fast transitions. How can we mechanistically understand these dynamics? Here we answer this question by proposing simplified, reduced models. We first construct a random walk model for neuron transitions between assemblies based on the statistics of synaptic weight changes measured in simulations of spiking neural networks exhibiting assembly drift. It shows that neuron transitions between assemblies can be understood as noise-activated switching between metastable states. The random walk's potential landscape and inhomogeneous noise strength induce metastability and thus support assembly maintenance in the presence of ongoing fluctuations. In a second step, we derive an effective random walk model from first principles. In this model, a neuron spikes at a fixed background rate and with an input weight-dependent probability when its current or another assembly reactivates. The model generates neuron transitions between assemblies as well as potentials and inhomogeneous noise similar to spiking networks. The approach can be applied generally to networks of drifting assemblies, irrespective of the employed neuron and synapse models.