A theory for how sensorimotor skills are learned and retained in noisy and nonstationary neural circuits

Abstract

During the process of skill learning, synaptic connections in our brains are modified to form motor memories of learned sensorimotor acts. The more plastic the adult brain is, the easier it is to learn new skills or adapt to neurological injury. However, if the brain is too plastic and the pattern of synaptic connectivity is constantly changing, new memories will overwrite old memories, and learning becomes unstable. This trade-off is known as the stability-plasticity dilemma. Here a theory of sensorimotor learning and memory is developed whereby synaptic strengths are perpetually fluctuating without causing instability in motor memory recall, as long as the underlying neural networks are sufficiently noisy and massively redundant. The theory implies two distinct stages of learning - preasymptotic and postasymptotic - because once the error drops to a level comparable to that of the noiseinduced error, further error reduction requires altered network dynamics. A key behavioral prediction derived from this analysis is tested in a visuomotor adaptation experiment, and the resultant learning curves are modeled with a nonstationary neural network. Next, the theory is used to model two-photon microscopy data that show, in animals, high rates of dendritic spine turnover, even in the absence of overt behavioral learning. Finally, the theory predicts enhanced task selectivity in the responses of individual motor cortical neurons as the level of task expertise increases. From these considerations, a unique interpretation of sensorimotor memory is proposed - memories are defined not by fixed patterns of synaptic weights but, rather, by nonstationary synaptic patterns that fluctuate coherently.