An animal's spatial location within its environment is represented by place (O'Keefe & Dostrovsky, 1971) and grid cells (Hafting et al., 2005) in the hippocampal formation (HF). The HF also plays a major role in detecting environmental novelty, a function designed to create new representations or update old ones. Exploration of novel environments leads to the formation of new spatial representations ("remapping") (Muller & Kubie, 1987), which are long-lasting and depend on NMDA receptors. A key question concerns the mechanisms by which novelty is detected and how HF spatial representations are created or modified. Here we show that environmental novelty causes expansion of the spatial firing patterns of grid cells and a concomitant reduction in their spatial regularity and in the frequency of the theta-band modulation of their firing rate. This latter change is consistent with the oscillatory interference model of grid cell firing (Burgess et al., 2007). Grid scale and regularity change back towards their canonical values as the environment becomes familiar over subsequent days of experience. Novelty-induced grid expansion would produce a major mismatch with other spatial inputs (e.g. boundary-related cells, which do not remap (Solstad et al., 2008)) potentially driving place cell remapping. Furthermore the scale expansion questions the widely-assumed role of grid cells in providing a fixed metric for navigation in all environments.

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