Hippocampal and anterior cingulate cortex contribution to the processing of recently-acquired and remotely stored spatial memories in rats trained during preadolescence

Abstract

Preadolescent development is characterized by a reorganization of connectivity within and between brain regions that coincides with the emergence of more complex behaviors. The hippocampus is one such region that undergoes extensive preadolescent remodeling and as this process continues, spatial memory functions emerge. The current work investigated whether preadolescent spatial memories persist beyond 24 h and stabilize into the postadolescent period as remote memories supported by cortical networks in the anterior cingulate cortex (ACC). Male Long Evans rats were trained on the Morris water maze at different time frames from postnatal day (P) 18–26 and compared to P50 rats. Testing occurred at either a recent (24 h) or remote (3 weeks) timepoint. Spatial learning was evident in all age groups (P18, P20, P22, P24 and P50) across the 3 training days but only the P22 and P24 groups showed spatial learning that matched the P50 group. In light of this, the only group to show intact remote (3 week) memory was the P50 group. Spaced training in the P18 group did not improve retention at the recent or remote testing intervals. The P18 and P50 groups tested at 24 h showed more CA1 hippocampal c-Fos labeling than groups tested at 3 weeks. The P50 group tested at 3 weeks showed elevated c-Fos labeling in the anterior cingulate (ACC) compared to the P18 group tested at 3 weeks and the P50 group tested at 24 h. Spaced training in the P18 group was associated with elevated c-Fos labeling in the ACC at the 3-week test. Groups trained at P20, 22, and 24 showed more c-Fos labelling in the ACC than in the CA1. Results suggest that while spatial information processing emerges around P18/P20, remote spatial retention and the neural substrates that support retention are not in place until after P26 in rats.