Dynamics of Dentate Gyrus Place Cells and Dentate Spikes Signal Spatial and Nonspatial Changes in Environments

The dentate gyrus (DG) is thought to play a key role in the formation of dissociable memory representations for similar contexts. Neurons in the dentate gyrus (DG) receive highly processed spatial and nonspatial sensory information from the medial and lateral entorhinal cortices, respectively. Changes in spatially tuned firing patterns of DG place cells occur after spatial changes to an environment, but the degree to which DG place cells respond to ethologically relevant nonspatial stimuli is largely unknown. Spatial and nonspatial information is thought to be transmitted to the DG during discrete local field potential events called dentate spikes. Here, we tested the extent to which different spatial and nonspatial stimuli modulate place cell firing patterns and dentate spike dynamics. We performed extracellular recordings of DG place cells and local field potentials in rats of both sexes exploring a familiar spatial environment, in which social stimuli and nonsocial odors of varying ethological relevance were presented, and a novel spatial environment. As expected, DG place cells exhibited different firing patterns between familiar and novel environments. Remarkably, a small population of DG place cells changed their firing patterns when social but not nonsocial stimuli were presented in a familiar environment. Additionally, the occurrence of dentate spikes associated with lateral entorhinal cortex inputs increased during exploration of social but not nonsocial stimuli. Altogether, these results suggest that the DG preferentially responds to social stimuli at neuronal and network levels, providing novel insights into how spatial and nonspatial information is integrated in the DG.