A Developmental Switch in Place Cell Accuracy Coincides with Grid Cell Maturation

Laurenz Muessig,Jonas Hauser,Thomas Joseph Wills,Francesca Cacucci

doi:10.1016/j.neuron.2015.05.011

Abstract

SummaryPlace cell firing relies on information about self-motion and the external environment, which may be conveyed by grid and border cells, respectively. Here, we investigate the possible contributions of these cell types to place cell firing, taking advantage of a developmental time window during which stable border cell, but not grid cell, inputs are available. We find that before weaning, the place cell representation of space is denser, more stable, and more accurate close to environmental boundaries. Boundary-responsive neurons such as border cells may, therefore, contribute to stable and accurate place fields in pre-weanling rats. By contrast, place cells become equally stable and accurate throughout the environment after weaning and in adulthood. This developmental switch in place cell accuracy coincides with the emergence of the grid cell network in the entorhinal cortex, raising the possibility that grid cells contribute to stable place fields when an organism is far from environmental boundaries.

Highlights

Place cells are pyramidal cells in the CA1 and CA3 fields of the hippocampus that fire only when an animal visits selective regions of the environment (‘‘place fields’’)
Place cell firing relies on information about selfmotion and the external environment, which may be conveyed by grid and border cells, respectively
We investigate the possible contributions of these cell types to place cell firing, taking advantage of a developmental time window during which stable border cell, but not grid cell, inputs are available

Summary

Introduction

Place cells are pyramidal cells in the CA1 and CA3 fields of the hippocampus that fire only when an animal visits selective regions of the environment (‘‘place fields’’). Place cell firing is thought to integrate inputs from several other types of spatially tuned neurons (Zhang et al, 2013) These include border cells (Solstad et al, 2008), which fire close to the boundaries of an environment, and grid cells (Hafting et al, 2005), which fire in a regular, hexagonally symmetric series of locations across the whole environment; both are found in the medial entorhinal cortex (mEC). More recent evidence has shown that place fields can exist in the absence of regular grid cell firing both during post-natal development (Langston et al, 2010; Wills et al, 2010) and in adulthood (Koenig et al, 2011). This leaves open the question of the exact contribution of grid cell input to place cell firing

Results

Discussion

Conclusion