Flexible encoding of objects and space in single cells of the dentate gyrus

Abstract

The hippocampus is involved in the formation of memories that require associations among stimuli to construct representations of space and the items and events within that space. Neurons in the dentate gyrus (DG), an initial input region of the hippocampus, have robust spatial tuning, but it is unclear how nonspatial information may be integrated with spatially modulated firing at this stage. We recorded from the DG of 21 adult mice as they foraged for food in an environment that contained discrete objects. By classifying recorded DG cells into putative granule cells and mossy cells, we examined how the addition or displacement of objects affected the spatial firing of these DG cell types. We found DG cells with multiple firing fields at a fixed distance and direction from objects (landmark vector cells) as well as cells that exhibited localized changes in spatial firing when objects in the environment were manipulated. When mice were exposed to a second environment with the same objects, DG spatial maps were completely reorganized, suggesting standard global remapping, and a largely different subset of cells responded to object manipulations. Together, these data reveal the capacity of DG cells to detect small changes in the environment, while preserving a stable spatial representation of the overall context.