Sparse-to-dense coding transformation between hippocampal areas CA3 and CA1

The hippocampus is crucial for spatial memory and navigation. It contains place cells1–7: spatially selective neurons found in areas CA1 and CA3—two distinct hippocampal subregions with substantially different anatomical connectivity8. Previous studies have found highly similar spatial coding between CA1 and CA3 place cells3,9–11. This raises the question of why two subregions that form consecutive processing stages would exhibit identical neural coding. Here we hypothesized that the lack of differences between CA1 and CA3 spatial coding is due to the experimental paradigm: using small arenas. We tested this hypothesis by simultaneously recording from CA1 and CA3 neurons in bats flying in flight tunnels up to 200 m in length. We identified highly distinct neural coding in CA1 and CA3: whereas CA1 neurons exhibited dense spatial coding, consisting of multiple place fields12, CA3 neurons exhibited ultrasparse spatial coding, consisting predominantly of single place fields. Despite this marked difference, the sizes of place fields were very similar between the two subregions, across 5 different environment sizes ranging from 6 m to 200 m. Using a neural-network model, we show that such a sparse-to-dense transformation can facilitate fast learning of new spatial maps. We also found that in a large multicompartment environment, place cells were strongly modulated by trajectory history—a contextual effect (retrospective coding) that could last for over 100 m. Together, by using large naturalistic environments, we identified a CA3-to-CA1 coding transformation that serves to reformat spatial information into a more efficient, compressed neural code. The hippocampus exhibits a CA3-to-CA1 coding transformation that combines fast learning with an efficient, compressed neural code.