1. Centre for the Biology of Memory, Norwegian University of Science and Technology, NO-7489 Trondheim, Norway
2. Cognitive Neuroscience Sector, SISSA International School for Advanced Studies, I-34014 Trieste, Italy
3. These authors contributed equally to this work.

Correspondence to: Edvard I. Moser¹ Correspondence and requests for materials should be addressed to E.I.M. (Email: edvard.moser@ntnu.no).

Abstract

A fundamental property of many associative memory networks is the ability to decorrelate overlapping input patterns before information is stored^{1, 2, 3, 4, 5}. In the hippocampus, this neuronal pattern separation is expressed as the tendency of ensembles of place cells⁶ to undergo extensive 'remapping' in response to changes in the sensory or motivational inputs to the hippocampus^{7, 8, 9, 10, 11, 12, 13}. Remapping is expressed under some conditions as a change of firing rates in the presence of a stable place code ('rate remapping')¹⁴, and under other conditions as a complete reorganization of the hippocampal place code in which both place and rate of firing take statistically independent values ('global remapping')¹⁴. Here we show that the nature of hippocampal remapping can be predicted by ensemble dynamics in place-selective grid cells in the medial entorhinal cortex^{15, 16}, one synapse upstream of the hippocampus. Whereas rate remapping is associated with stable grid fields, global remapping is always accompanied by a coordinate shift in the firing vertices of the grid cells. Grid fields of co-localized medial entorhinal cortex cells move and rotate in concert during this realignment. In contrast to the multiple environment-specific representations coded by place cells in the hippocampus, local ensembles of grid cells thus maintain a constant spatial phase structure, allowing position to be represented and updated by the same translation mechanism in all environments encountered by the animal.

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