Ensemble Place Codes in Hippocampus: CA1, CA3, and Dentate Gyrus Place Cells Have Multiple Place Fields in Large Environments

Eunhye Park,André A Fenton,Dino Dvorak,Clayton T Dickson

doi:10.1371/journal.pone.0022349

Eunhye Park, André A Fenton + Show 2 more

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https://doi.org/10.1371/journal.pone.0022349

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Abstract

Previously we reported that the hippocampus place code must be an ensemble code because place cells in the CA1 region of hippocampus have multiple place fields in a more natural, larger-than-standard enclosure with stairs that permitted movements in 3-D. Here, we further investigated the nature of hippocampal place codes by characterizing the spatial firing properties of place cells in the CA1, CA3, and dentate gyrus (DG) hippocampal subdivisions as rats foraged in a standard 76-cm cylinder as well as a larger-than-standard box (1.8 m×1.4 m) that did not have stairs or any internal structure to permit movements in 3-D. The rats were trained to forage continuously for 1 hour using computer-controlled food delivery. We confirmed that most place cells have single place fields in the standard cylinder and that the positional firing pattern remapped between the cylinder and the large enclosure. Importantly, place cells in the CA1, CA3 and DG areas all characteristically had multiple place fields that were irregularly spaced, as we had reported previously for CA1. We conclude that multiple place fields are a fundamental characteristic of hippocampal place cells that simplifies to a single field in sufficiently small spaces. An ensemble place code is compatible with these observations, which contradict any dedicated coding scheme.

Highlights

The discharge of the principal cells in hippocampus subregions CA1, CA3, and dentate gyrus (DG) all have the remarkable property of location-specificity, which has motivated their intense study in the effort to understand how space and memories are represented in the mammalian brain [1,2,3,4,5]
Summary The main finding is that CA1, CA3, and DG place cells all characteristically discharged in multiple, irregularly-arranged place fields in the large box the spatial discharge pattern of the vast majority of these cells simplified to a single place field in the 5.6 times smaller cylinder (Fig. 3)
This replicated our prior report that the fundamental spatial firing pattern of CA1 place cells is to express multiple place fields

Summary

Introduction

The discharge of the principal cells in hippocampus subregions CA1, CA3, and dentate gyrus (DG) all have the remarkable property of location-specificity, which has motivated their intense study in the effort to understand how space and memories are represented in the mammalian brain [1,2,3,4,5]. The spatial discharge properties of these ‘place cells’ have been well characterized in standard laboratory environments, which typically have a maximum linear dimension less than 1 m In such environments, most place cells discharge action potentials in a single location called the cell’s place field. The CA1 place code is fundamentally similar in small and large environments, but appeared to differ in the two environments because the available space for characterizing place cell discharge was limited in the small environment This view is consistent with the observation that both place cells in the dentate gyrus [2,3] and grid cells in the entorhinal cortex have multiple firing fields [7,8] even in standard small environments. CA3 place cells tended to have a single place field, and the size of the field expanded with the ventral location of the cell

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