Abstract

Prior experience accelerates acquisition of novel, related information through processes like assimilation into mental schemas, but the underlying neuronal mechanisms are poorly understood. We investigated the roles that prior experience and hippocampal CA3 N-Methyl-D-aspartate receptor (NMDAR)-dependent synaptic plasticity play in CA1 place cell sequence encoding and learning during novel spatial experiences. We found that specific representations of de novo experiences on linear environments were formed on a framework of pre configured network activity expressed in the preceding sleep and were rapidly, flexibly adjusted via NMDAR-dependent activity. This prior experience accelerated encoding of subsequent experiences on contiguous or isolated novel tracks, significantly decreasing their NMDAR-dependence. Similarly, de novo learning of an alternation task was facilitated by CA3 NMDARs; this experience accelerated subsequent learning of related tasks, independent of CA3 NMDARs, consistent with a schema-based learning. These results reveal the existence of distinct neuronal encoding schemes which could explain why hippocampal dysfunction results in anterograde amnesia while sparing recollection of old, schema-based memories. DOI: http://dx.doi.org/10.7554/eLife.01326.001.

Highlights

  • An essential capacity of the brain is to form internal representations of the external world

  • Ensemble neuronal recordings were performed from the CA1 area of the hippocampus in control mice (CT) and CA3 N-Methyl-D-aspartate receptor (NMDAR) KO mice alternating between periods of sleep/rest in the sleep/rest box and periods of exploration of portions of walled linear and L-shaped tracks under three conditions of behavioral novelty (Figure 1A)

  • Our approach is to study the process of internal development of novel spatial representations as a dynamic whole by comparing and correlating the activity of ensembles of neurons during the sleep/ rest period prior to first time exploration of a linear track with the one during the exploration, and both of these activities with the one during the post-Run sleep/rest session, in naïve and experienced animals, in the presence and absence of CA3 NMDARs

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Summary

Introduction

An essential capacity of the brain is to form internal representations of the external world. Sequences of place cells with partially overlapping fields fire with compressed temporal delays that correspond to the Euclidian distance between the location of their place field peaks (Muller et al, 1996; Dragoi and Buzsaki, 2006) This phenomenon, known as sequence compression (Skaggs et al, 1996; Dragoi and Buzsaki, 2006) is thought to be an animal model of the internal representation of an external space by the place cell assemblies in the CA1 area of the rodent hippocampus (Skaggs et al, 1996; Dragoi et al, 2003; Dragoi and Buzsaki, 2006; O’Keefe and Nadel, 1978).

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