Orientation selectivity enhances context generalization and generative predictive coding in the hippocampus.

ABSTRACT

We learn and remember multiple new experiences throughout the day. The neural principles enabling continuous rapid learning and formation of distinct representations of numerous sequential experiences without major interference are not understood. To understand this process, here we interrogated ensembles of hippocampal place cells as rats explored 15 novel linear environments interleaved with sleep sessions over continuous 16 h periods. Remarkably, we found that a population of place cells were selective to environment orientation and topology. This orientation selectivity property biased the network-level discrimination and re/mapping between multiple environments. Novel environmental representations emerged rapidly as more generic, but repeated experience within the environments subsequently enhanced their discriminability. Generalization of prior experience with different environments consequently improved network predictability of future novel environmental representations via strengthened generative predictive codes. These coding schemes reveal a high-capacity, high-efficiency neuronal framework for rapid representation of numerous sequential experiences with optimal discrimination-generalization balance and reduced interference.