Grid-Cell Activity on Linear Tracks Indicates Purely Translational Remapping of 2D Firing Patterns at Movement Turning Points

Grid cells in rodent medial entorhinal cortex are thought to play a critical role for spatial navigation. When the animal is freely moving in an open arena the firing fields of each grid cell tend to form a hexagonal lattice spanning the environment. For movements along a linear track the cells seem to respond differently. They show multiple firing fields that are not periodically arranged and whose shape and position change when the running direction is reversed. In addition, peak firing rates vary widely from field to field. Measured along one running direction only, firing fields are, however, compatible with a slice through a two-dimensional (2D) hexagonal pattern. It is an open question, whether this is also true if leftward and rightward runs are jointly considered. By analyzing data from 15 male Long–Evans rats, we show that a single hexagonal firing pattern explains the linear-track data if translational shifts of the pattern are allowed at the movement turning points. A rotation or scaling of the grid is not required. The agreement is further improved if the peak firing rates of the underlying 2D grid fields can vary from field to field, as suggested by recent studies. These findings have direct consequences for experiments using linear tracks in virtual reality.

SIGNIFICANCE STATEMENT Various types of neurons support spatial navigation. Their response properties are often studied in reduced settings and might change when the animal can freely explore its environment. Grid cells in rodents, for example, exhibit seemingly irregular firing fields when animal movement is restricted to a linear track but highly regular patterns in two-dimensional (2D) arenas. We show that linear-track responses of a cell for both leftward and rightward running directions can be explained as cuts through a single hexagonal pattern if translational remapping is allowed at movement turning points; neither rotations nor scale transformations are needed. These results provide a basis to quantify grid-cell activity in 1D virtual reality and could help to detect and categorize grid cells without experiments in 2D environments.