Purely STDP-based assembly dynamics: stability, learning, overlaps, drift and aging

Abstract

AbstractMemories may be encoded in the brain via strongly interconnected groups of neurons, called assemblies. The concept of Hebbian plasticity suggests that these assemblies are generated through synaptic plasticity, strengthening the recurrent connections within select groups of neurons that receive correlated stimulation. To remain stable in absence of such stimulation, the assemblies need to be self-reinforcing under the plasticity rule. Previous models of such assembly maintenance require additional mechanisms of fast homeostatic plasticity often with biologically implausible timescales. Here we provide a model of neuronal assembly generation and maintenance purely based on spike-timing-dependent plasticity (STDP) between excitatory neurons. It uses irregularly and stochastically spiking neurons and STDP that depresses connections of uncorrelated neurons. We find that assemblies do not grow beyond a certain size, because temporally imprecisely correlated spikes dominate the plasticity in large assemblies. Assemblies in the model can be learned or spontaneously emerge. The model allows for prominent, stable overlap structures between static assemblies. Further, assemblies can drift, particularly according to a novel, transient overlap-based mechanism. Finally the model indicates that assemblies grow in the aging brain, where connectivity decreases.Author summaryIt is widely assumed that memories are represented by ensembles of nerve cells that have strong interconnections with each other. It is to date not clear how such strongly interconnected nerve cell ensembles form, persist, change and age. Here we show that already a basic rule for activity-dependent synaptic strength plasticity can explain the learning or spontaneous formation and the stability of assemblies. In particular, it is not necessary to explicitly keep the overall total synaptic strength of a neuron nearly constant, a constraint that was incorporated in previous models in a manner inconsistent with current experimental knowledge. Furthermore, our model achieves the challenging task of stably maintaining many overlaps between assemblies and generating the experimentally observed drift of memory representations. Finally, the model predicts that if the number of synaptic connections in the brain decreases, as observed during aging, the size of the neuron ensembles underlying memories increases. This may render certain memories in the aging brain more robust and prominent but also less specific.