Is there a pilot in the brain? Contribution of the self-positioning system to spatial navigation

Bruno Poucet,Bruno Truchet,Vincent Hok,Franck Chaillan,Francesca Sargolini,Etienne Save

doi:10.3389/fnbeh.2015.00292

Abstract

Since the discovery of place cells, the hippocampus is thought to be the neural substrate of a cognitive map. The later discovery of head direction cells, grid cells and border cells, as well as of cells with more complex spatial signals, has led to the idea that there is a brain system devoted to providing the animal with the information required to achieve efficient navigation. Current questioning is focused on how these signals are integrated in the brain. In this review, we focus on the issue of how self-localization is performed in the hippocampal place cell map. To do so, we first shortly review the sensory information used by place cells and then explain how this sensory information can lead to two coding modes, respectively based on external landmarks (allothetic information) and self-motion cues (idiothetic information). We hypothesize that these two modes can be used concomitantly with the rat shifting from one mode to the other during its spatial displacements. We then speculate that sequential reactivation of place cells could participate in the resetting of self-localization under specific circumstances and in learning a new environment. Finally, we provide some predictions aimed at testing specific aspects of the proposed ideas.

Highlights

The 2014 Nobel Prize for Physiology or Medicine was awarded to John O’Keefe, Edvard Moser and May-Britt Moser for their discovery of the ‘‘inner GPS’’ in the brain
We focus on a single issue about hippocampal place cells
This raises the possibility that the parietal cortex is involved in the processing of proximal object landmarks, and may contribute to provide a stable local reference frame to place cells by using the objects as an anchor system to reset self-localization based on motion cues

Summary

INTRODUCTION

The 2014 Nobel Prize for Physiology or Medicine was awarded to John O’Keefe, Edvard Moser and May-Britt Moser for their discovery of the ‘‘inner GPS’’ in the brain. This raises the possibility that the parietal cortex is involved in the processing of proximal object landmarks (see Save and Poucet, 2000b), and may contribute to provide a stable local reference frame to place cells by using the objects as an anchor system to reset self-localization based on motion cues In this interpretation, parietal-damaged rats would be unable to use selfmotion cues to maintain place field stability in absence of objects and would rather rely on uncontrolled background information. As expected, place fields in rats with entorhinal damage are unstable compared to controls when landmarks are removed, there is no trend for them to align with static uncontrolled background cues In other words, their new angular position is randomly anchored in space as if, in addition to a difficulty in using self-motion cues, there was an additional loss of directional information provided by the distal environment. The rat hippocampus was shown to generate brief sequential activations of place cells that predicted the immediate future path taken by the rat to its spatial goal

A Possible Role for High-Frequency Oscillations in Self-Localization

CONCLUSION