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Emergence of preconfigured and plastic time-compressed sequences in early postnatal development

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Science  11 Jan 2019:
Vol. 363, Issue 6423, pp. 168-173
DOI: 10.1126/science.aav0502

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Memory capabilities develop with age

During memory formation, time-compressed neuronal sequences underlie consolidation as well as encoding of novel information. Such memory traces are largely contributed by a selection of preconfigured neuronal patterns. However, when and how these preconfigured patterns first emerge in the hippocampus is unknown. Farooq and Dragoi identified an age-dependent development of network preconfiguration into trajectory-like sequences. This preconfiguration was expressed spontaneously during sleep and emerged from the assembly of persistent, location-depicting ensembles, largely controlled by intrinsic developmental programs. Thus, the compressed binding of adjacent locations into spatial trajectories during navigation and their experience-dependent replay emerge in coordination from spontaneous preconfigured sequences.

Science, this issue p. 168

Abstract

When and how hippocampal neuronal ensembles first organize to support encoding and consolidation of memory episodes, a critical cognitive function of the brain, are unknown. We recorded electrophysiological activity from large ensembles of hippocampal neurons starting on the first day after eye opening as naïve rats navigated linear environments and slept. We found a gradual age-dependent, navigational experience–independent assembly of preconfigured trajectory-like sequences from persistent, location-depicting ensembles during postnatal week 3. Adult-like compressed binding of adjacent locations into trajectories during navigation and their navigational experience–dependent replay during sleep emerged in concert from spontaneous preconfigured sequences only during early postnatal week 4. Our findings reveal ethologically relevant distinct phases in the development of hippocampal preconfigured and experience-dependent sequential patterns thought to be important for episodic memory formation.

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