Replay without sharp wave ripples in a spatial memory task

Abstract

Sharp-wave ripples and hippocampal replay are widely viewed as inseparable components of episodic memory consolidation, with ripples broadcasting the episodic content carried by replay sequences. Here, we show that in male rats performing an open-field spatial memory task, replay can occur in the absence of ripples. Replays with and without ripples were organized in virtual space: ripples were confined to discrete “ripple fields,” spatially restricted regions defined over the virtual locations depicted during replay and independent of the rat’s location. Ripple fields were direction-independent, stable within sessions, and adapted to environmental changes induced by barriers. Ripple fields were matched across animals exposed to the same environment, revealing a conserved spatial code. These results indicate that ripples and replay are distinct but coordinated processes, with ripples selectively tagging a subset of replays linked to learning or novelty. We propose that this coupling enables targeted broadcast of salient experiences for consolidation.