MEMORY TRACE OF A BUTTERFLY ENCOUNTER

Episodic memory is necessary for animals to adapt to the dynamically changing world. A substantial body of research has described how the hippocampus updates its representation of the external world in response to novel cues. However, the mechanisms enabling the parallel processing and the integration of familiar spatial information and novel transient information is still unclear. In this study, we developed a novel paradigm in which head-fixed mice run on a cue-enriched treadmill and occasionally encounter a butterfly dummy controlled by 3-motor axes, and we recorded neuronal responses in hippocampal CA1 and CA3 regions using silicon probes. We found that the first encounter with the butterfly instantly remodeled the activity patterns of place cells. While the prior encoding of treadmill belt locations was still be observed at the level of gamma-scale population vectors, new population vectors emerged during the butterfly encounters and multiplexed with spatial information. Furthermore, a neural network model of competitive learning replicated the range of place cell responses and revealed a parallel development of engrams for both spatial environments and butterfly encounters. These results demonstrate the existence of hippocampal memory traces for single encounter events and provide insights into the neural network mechanisms that support the ‘one-shot’ memory encoding of experiences.