A cortical-hippocampal communication undergoes rebalancing after new learning

The brain's ability to consolidate a wide range of memories while maintaining their distinctiveness across experiences remains poorly understood. Sharp-wave ripples, neural oscillations that occur predominantly within CA1 of the hippocampus during immobility and sleep, have been shown to play a critical role in the consolidation process. More recently, evidence has uncovered functional heterogeneity of pyramidal neurons within distinct sublayers of CA1 that display unique properties during ripples, potentially contributing to memory specificity. Despite this, it remains unclear exactly how ripples shift the activity of CA1 neuronal populations to accommodate the consolidation of specific memories and how sublayer differences manifest. Here, we studied interactions between the anterior cingulate cortex (ACC) and CA1 neurons during ripples and discovered a reorganization of their communication following learning. Notably, this reorganization appeared specifically for CA1 superficial (CA1sup) sublayer neurons. Utilizing a generalized linear model decoder, we demonstrate the pre-existence of ACC-to-CA1sup communication, which is suppressed during new learning and subsequent sleep suggesting that ACC activity may reallocate the contribution of CA1sup neurons during memory acquisition and consolidation. Further supporting this notion, we found that optogenetic stimulations of the ACC preferentially suppressed CA1sup interneurons while activating a unique subset of CA1 interneurons. Overall, these findings highlight a possible role of the ACC in rebalancing CA1 neuronal populations' contribution to ripple contents surrounding learning.