Replay without sharp wave ripples in a spatial memory task

Sharp-wave ripples in the hippocampus are believed to be a fundamental mechanism for the consolidation of episodic memories. During ripples, hippocampal neurons are re-activated in sequences called replay, which have been hypothesized to reflect episodic memory content. Ripples and replay are usually reported to co-occur, and are commonly thought to reflect the same process. Here we report that, in rats performing an open field spatial memory task, replays readily occur in the complete absence of ripples. Moreover, the occurrence of ripple-less and ripple-containing replays is not random, but precisely organized in terms of virtual space: Ripples are confined to “ripple fields”, which are spatially-restricted areas defined over the virtual locations depicted during replay and independent of the actual location of the animal. Similar to allocentric coding by place fields, ripple fields are independent of the direction of travel, and stable throughout the recording session. Ripple fields track changes to environmental structure caused by the addition or subtraction of barriers to movement, consistent with ripples conveying information about the incorporation of novel experiences. Moreover, ripple fields were matched across different rats experiencing the same barrier configuration, highlighting the robustness of the ripple field spatial code. We hypothesize a new relationship between ripples and replay, in which a subset of replays that is particularly relevant to learning or novelty is paired with ripples, in order to promote its selective broadcast to the rest of the brain for consolidation.