  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.
