Change is ubiquitous in living beings. In particular, the connectome and neural representations can change. Nevertheless, behaviors and memories often persist over long times. In a standard model, associative memories are represented by assemblies of strongly interconnected neurons. For faithful storage these assemblies are assumed to consist of the same neurons over time. Here we propose a contrasting memory model with complete temporal remodeling of assemblies, based on experimentally observed changes of synapses and neural representations. The assemblies drift freely as noisy autonomous network activity and spontaneous synaptic turnover induce neuron exchange. The gradual exchange allows activity-dependent and homeostatic plasticity to conserve the representational structure and keep inputs, outputs, and assemblies consistent. This leads to persistent memory. Our findings explain recent experimental results on temporal evolution of fear memory representations and suggest that memory systems need to be understood in their completeness as individual parts may constantly change.Here is an explanatory graphic from the article:
Assembly drift and persistent memory. (A) At two nearby times a similar ensemble of neurons forms the neural representation of, for example, “apple” (compare the blue-colored assembly neurons at the first and the second time point). At distant times the representation consists of completely different ensembles (blue-colored assembly neurons at the first and the third time point). Due to their gradual change, temporally distant representations are indirectly related via ensembles in the time period between them. (B) Parts of a thread possess the same form of indirect relation: Nearby parts are composed of similar ensembles of fibers, while distant ones consist of different ensembles, which are connected by those in between. (C) The complete change of memory representations still allows for stable behavior. In the schematic, a tasty apple is perceived. At different times, this triggers different ensembles that presently form the representation of “apple”; see A. Assembly activation initiates a reaching movement toward the apple, despite the dissimilarity of the activated neuron ensembles. Memory and behavior are conserved because the gradual change of assembly neurons enables the inputs (green) and outputs (orange) to track the neural representation.