Multiple Maps of the Same Spatial Context Can Stably Coexist in the Mouse Hippocampus

Abstract

Hippocampal place cells selectively fire when an animal traverses a particular location and are considered a neural substrate of spatial memory. Place cells were shown to change their activity patterns (remap) across different spatial contexts but to maintain their spatial tuning in a fixed familiar context. Here, we show that mouse hippocampal neurons can globally remap, forming multiple distinct representations (maps) of the same familiar environment, without any apparent changes in sensory input or behavior. Alternations between maps occurred only across separate visits to the environment, implying switching between distinct stable attractors in the hippocampal network. Importantly, the different maps were spatially informative and persistent over weeks, demonstrating that they can be reliably stored and retrieved from long-term memory. Taken together, our results suggest that a memory of a given spatial context could be associated with multiple distinct neuronal representations, rather than just one.

Keywords: attractor; calcium imaging; cognitive map; hippocampus; memory; navigation; place cells; remapping.