Grid cell co-activity patterns remain stable across different behavioral states and experiences

Grid cells in the medial entorhinal cortex have been well studied while animals are exploring their environment; however, what they do when an animal is not navigating is less clear. Other cell types in the entorhinal-hippocampal network appear to have memory-related activity when an animal is inactive, so what grid cells do during quiescence is an important question. If grid cells show activity similar to place cells during rest and sleep, then it would imply that grid cells play an active role in memory functions rather than simply providing current sensory information to the hippocampus. Models have been proposed that make testable predictions about grid cell activity when spatial input is absent. The continuous attractor network model of grid cell pattern formation posits that grid cell patterning is a result of network connections between grid cells. As a result of this connectivity, these models hypothesize that grid cell co-activity patterns should be the same during sleep as during active navigation. In my first study, I investigated how spike time correlations between grid cell pairs during sleep compared to spike time correlations between the same grid cell pairs during waking activity. I found that the same correlation patterns were present regardless of whether spatial information was available to grid cells (i.e., during active navigation) or whether sensory input was absent (i.e., during sleep). These results support the continuous attractor network model hypothesis. In my second study, I examined whether novel experience changed grid cell co-activity patterns during active waking behaviors, rest, and sleep. I found that spike time correlations between grid cell pairs remained stable across behavioral states regardless of experience. In my last study, I looked at organized sequences of firing in grid cell ensembles to examine whether small changes in correlations led to detectable changes in more complex ensemble representations of experience. I found that grid cell ensemble activity did not appear to be influenced by different behaviors or novel experience. Taken together, these results suggest that grid cells are part of a low-dimensional, continuous attractor network and that grid cell activity patterns during sleep reflect connections in the grid cell network rather than representing specific experiences.