Dynamic and reversible remapping of network representations in an unchanging environment

Abstract

In response to environmental changes, the medial entorhinal cortex alters its single-cell firing properties. This flexibility in neural coding is hypothesized to support navigation and memory by dividing sensory experience into unique contextual episodes. However, it is unknown how the entorhinal circuit transitions between different representations, particularly when sensory information is not delineated into discrete contexts. Here, we describe spontaneous and abrupt transitions between multiple spatial maps of an unchanging task and environment. These remapping events were synchronized across hundreds of medial entorhinal neurons and correlated with changes in running speed. While remapping altered spatial coding in individual neurons, we show that features of the environment were statistically preserved at the population-level, enabling simple decoding strategies. These findings provoke a reconsideration of how medial entorhinal cortex dynamically represents space and broadly suggest a remarkable capacity for higher-order cortical circuits to rapidly and substantially reorganize their neural representations.