To determine how hippocampal backprojections influence spatially periodic firing in grid cells, we recorded neural activity in the medial entorhinal cortex (MEC) of rats after temporary inactivation of the hippocampus. We report two major changes in entorhinal grid cells. First, hippocampal inactivation gradually and selectively extinguished the grid pattern. Second, the same grid cells that lost their grid fields acquired substantial tuning to the direction of the rat's head. This transition in firing properties was contingent on a drop in the average firing rate of the grid cells and could be replicated by the removal of an external excitatory drive in an attractor network model in which grid structure emerges by velocity-dependent translation of activity across a network with inhibitory connections. These results point to excitatory drive from the hippocampus, and possibly other regions, as one prerequisite for the formation and translocation of grid patterns in the MEC.
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- Supplementary Text and Figures (9M)
Supplementary Figures 1–8
- Supplementary Video 1 (24M)
External input is large enough (100% hippocampal activity). This corresponds to an external input to the right of the transition in Fig. 8b. In this case, the activity on the neuronal sheet is a hexagonal grid. When the animal moves, this activity is translated on the network and follows the movement of the animal without being distorted. The resulting activity at the single cell levels is a hexagonal grid and thus high grid score.
- Supplementary Video 2 (24M)
External input is below the transition. In this case, most of the time the activity on the neuronal sheet is still grid like, but the grid changes size, amplitude and orientation as it tries to follow the animals movement sometime turning into stripe patterns (see e.g. t = 0:16). The peak activity also substantially changes between different time steps. Consequently, no grid firing will be observed at the single cell level and substantially low grid scores are found.