Context-independent expression of spatial code in hippocampus

Hippocampus plays a crucial role in formation and retrieval of spatial memory across mammals and episodic memory in humans. Episodic as well as spatial memories can be retrieved irrespectively of subjects awake behavioral state and independently of its actual spatial context. The nature of hippocampal network activity during such out-context retrieval has not been described so far, though. Theoretically, context-independent spatial memory retrieval suggests a shift from the hippocampal spatial representations coding the actual- to the remembered context. In this study we show in rats that CA3 neuronal population can switch spontaneously across representations and transiently activate another stored familiar spatial pattern without a direct external sensory cuing. This phenomenon qualitatively differs from the well described sharp wave-related pattern reactivations during immobility. Here it occurred under theta oscillatory state during an active exploration and reflected the preceding experience of sudden environment change. The respective out-context coding spikes appeared later in the theta cycle than the in-context ones. Finally, the experience induced as well an emergence of population vectors with a co-expression of both codes segregated into different phases of the theta cycle.