Place Cell Networks in Pre-weanling Rats Show Associative Memory Properties from the Onset of Exploratory Behavior.

L Muessig,F Cacucci,J Hauser,T J Wills

doi:10.1093/cercor/bhw174

L Muessig, F Cacucci + Show 2 more

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https://doi.org/10.1093/cercor/bhw174

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Abstract

Place cells are hippocampal pyramidal cells that are active when an animal visits a restricted area of the environment, and collectively their activity constitutes a neural representation of space. Place cell populations in the adult rat hippocampus display fundamental properties consistent with an associative memory network: the ability to 1) generate new and distinct spatial firing patterns when encountering novel spatial contexts or changes in sensory input (“remapping”) and 2) reinstate previously stored firing patterns when encountering a familiar context, including on the basis of an incomplete/degraded set of sensory cues (“pattern completion”). To date, it is unknown when these spatial memory responses emerge during brain development. Here, we show that, from the age of first exploration (postnatal day 16) onwards, place cell populations already exhibit these key features: they generate new representations upon exposure to a novel context and can reactivate familiar representations on the basis of an incomplete set of sensory cues. These results demonstrate that, as early as exploratory behaviors emerge, and despite the absence of an adult-like grid cell network, the developing hippocampus processes incoming sensory information as an associative memory network.

Highlights

The hippocampus has an essential role in the encoding of longterm memories, including spatial (Morris et al 1982) and episodic memories (Scoville and Milner 1957)
Place cells undergo global remapping at all ages: place fields shift to new positions or cease firing, while others, which were silent before, become active
Comparing baseline levels of stability (Fig. 1B,C) and rate overlap (RO) (Fig. 1D,E) in the familiar environment with those across familiar and novel environments, we found that the hippocampus generates orthogonal place codes for the two environments throughout development, as both spatial correlation” (SC) and RO measures approach chance levels for familiar-novel comparison at all ages (Fig. 1B–E; SC, F1,496 = 533.6, P < 0.001; RO, F1,535 = 130.4, P < 0.001; see Supplementary Table 4 for full statistical analysis)

Summary

Introduction

The hippocampus has an essential role in the encoding of longterm memories, including spatial (Morris et al 1982) and episodic memories (Scoville and Milner 1957) It contains “place cells”, neurons that fire only when an animal visits a restricted area of the environment (the “place field”). Pattern completion refers to the recall of a complete memory or neural representation following the presentation of a partial or degraded stimulus, allowing content addressable memory and accurate recall in the face of noisy input (Gardner-Medwin 1976; Hopfield 1982; McNaughton and Morris 1987; Treves and Rolls 1994; McClelland et al 1995) Another key characteristic of an efficient associative memory network is pattern separation: the decorrelation of similar sensory inputs reaching the network, such as to minimize the overlap between their neural representations.

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