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Periodic Report Summary 1 - MEMORYCODES (Time and experience dependent evolution of hippocampal memory codes)

The main objective of the project to characterize time and experience dependent evolution of hippocampal memory codes. We wish understand the relationship between experience (e.g. learning), passage of time, and stability or dynamics in hippocampal neural codes for long-term spatial memory. We have recently published our results from the first part of the project (Rubin, Geva, Sheintuch, Ziv, eLife, Dec 2015). In this work, titled “hippocampal ensemble dynamics timestamp events in long-term memory”, we investigated the question of how time is encoded in episodic memory. The capacity to remember temporal relationships between different events is essential to episodic memory, but little has been known about its underlying mechanisms. We performed time-lapse imaging of thousands of neurons over weeks in the hippocampal CA1 of mice as they repeatedly visited two distinct environments. Longitudinal analysis exposed ongoing environment-independent evolution of episodic representations, despite stable place field locations and constant remapping between the two environments. These dynamics time-stamped experienced events via neuronal ensembles that had cellular composition and activity patterns unique to specific points in time. Temporally close episodes shared a common timestamp regardless of the spatial context in which they occurred. Temporally remote episodes had distinct timestamps, even if they occurred within the same spatial context. Our results suggest that days-scale hippocampal ensemble dynamics could support the formation of a mental timeline in which experienced events could be mnemonically associated or dissociated based on their temporal distance. One of this project’s questions is “What are the mechanisms that drive ensemble dynamics and time coding over timescales of days?”. One potential mechanism at the network level is adult neurogenesis in the dentate gyrus (two synapses upstream to CA1) which takes place over timescales of weeks and has been suggested to support time coding via ongoing modification of the hippocampal circuitry by newborn neurons. We are currently investigating to what extent variation in neurogenesis rates could explain the dynamics in the downstream CA1. A closely related issue is the role of the interactions between the absolute passage of time and the experience itself on the observed ensemble dynamics. Thus, we are also currently investigating the interaction between the time and experience in affecting the CA1 ensemble dynamics. We do that by examining changes in CA1 spatial representation after varying either the duration between imaging sessions, or the number of imaging sessions within a fixed time period. In this work we adopt a perspectives of hippocampal coding that are distinct from previous studies in the field: we not only examine the stability of a few cells’ place fields over multiple days but also track ensembles of > 1,000 neurons, over multiple weeks, and in the context of long-term memory.

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