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

• MeSH
• Memory, Episodic * MeSH
• Hippocampus MeSH
• Rats MeSH
• Humans MeSH
• Gastropoda * MeSH
• Cues MeSH
• Spatial Memory MeSH
• Mental Recall MeSH
• Mammals MeSH
• Animals MeSH
• Check Tag
• Rats MeSH
• Humans MeSH
• Animals MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH

Retrieval of stored network activity pattern has been shown as a competitive transition from one attractor state to another, orchestrated by local theta oscillation. However, the fine nature of this process that is considered as substrate of memory recall is not clear. We found that hippocampal network recall is characterized by hyperactivity in the CA3 place cell population, associated with an "overexpression" of the retrieved network pattern. The overexpression was based on recruitment of cells from the same (recalled) spatial representation with low expected firing probability at the given position. We propose that increased place cell activation during state transitions might facilitate pattern completion towards the retrieved network state and stabilize its expression in the network. Furthermore, we observed frequent mixing of both activity patterns at the temporal level of a single theta cycle. On a sub-theta cycle scale, we found signs of segregation that might correspond to a gamma oscillation patterning, as well as occasional mixing at intervals of less than 5 milliseconds. Such short timescale coactivity might induce plasticity mechanisms, leading to associations across the two originally decorrelated network activity states.

• MeSH
• Action Potentials physiology   MeSH
• CA3 Region, Hippocampal physiopathology   MeSH
• Models, Neurological * MeSH
• Animals MeSH
• Check Tag
• Animals MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH