Discrete and differentiated encoding of distinct components of spatial experience occurs within the proximodistal subfields of the dorsoventral axis of the hippocampus.

A multitude of studies have confirmed the essential role of the hippocampus in the acquisition and updating of associative experience. In rodents, spatial memories are dependent on hippocampal information processing and encoding. The role of the dorsal hippocampal pole is well documented, but information about the roles of the intermediate and ventral hippocampus in spatial learning are few and often contradictory. Here, we used fluorescence in situ hybridization (FISH) to identify nuclear expression of the immediate early (IEG) gene, Homer1a, that was triggered by specific spatial learning events in hippocampal neurons of adult male rats. We compared IEG expression in the cornu ammonis (CA) and dentate gyrus (DG) along the proximodistal and dorsoventral hippocampal axis, triggered by novel learning about spatial constellations of large (macroscale), or partially concealed (microscale) objects within a familiar environment. We observed that the dorsal hippocampus predominates with regard to the neuronal encoding of both forms of spatial content information, whereby the distal CA1 (dCA1) and proximal CA3 (pCA3) preferentially encode microscale spatial location. The infrapyramidal blade of the DG, as well as pCA3, encode macroscale information. The intermediate CA shows increased IEG expression in dCA1 triggered by novel microscale information, but the DG of neither the intermediate, nor ventral, hippocampus encode macroscale information. The ventral hippocampus exhibits IEG expression patterns that are unique in comparison to the other two structures: here, both CA1 (proximal and distal) and pCA3 encode macroscale information. Taken together, these findings suggest that the intermediate and ventral hippocampus support spatial memory encoding, but may do so in support of differentiated and distinct aspects of associative learning.