Querying hippocampal replay with subcortical inputs

Abstract: During sleep, the hippocampus recapitulates neuronal patterns corresponding to behavioral trajectories during previous experiences. This hippocampal replay supports the formation of long-term memories. Yet, whether replay originates within the hippocampal circuitry or is initiated by extrahippocampal inputs is unknown. Here, I review recent findings regarding the organization of neuronal activity upstream to the hippocampus, in the head-direction (HD) and grid cell networks. I argue that hippocampal activity is under the influence of primary spatial signals, which originate from subcortical structures and set the stage for memory replay. In turn, hippocampal replay resets the HD network activity to select a new direction for the next replay event. This reciprocal interaction between the HD network and the hippocampus may be essential in providing meaning to hippocampal activity, specifically by training decoders of hippocampal sequences. Neuronal dynamics in thalamo-hippocampal loops may thus be instrumental for memory processes during sleep.