Research Article

A sense of space in postrhinal cortex

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Science  12 Jul 2019:
Vol. 365, Issue 6449, eaax4192
DOI: 10.1126/science.aax4192

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From local space to higher-order maps

Successful movement depends on an accurate sense of one's location within a particular environment. Neuroscientists distinguish self-centered and world-centered navigation and have been searching for a brain region where all ingredients of navigation come together. As rats foraged in an open field, LaChance et al. recorded activity from single neurons in an area called the postrhinal cortex. The authors found a population of cells that transform an animal's immediate sensory perception of its environment into a spatial map. This map is markedly different from the high-level representations observed in hippocampal place cells or entorhinal grid cells, but it is very flexible and is likely to provide the necessary building blocks for creating higher-level representations.

Science, this issue p. eaax4192

Structured Abstract

INTRODUCTION

Navigation and spatial learning depend upon a topographic representation of local space, which is defined with respect to the world (allocentric) and as opposed to the observer (egocentric). Spatial processing in the rodent brain has been primarily explored through recordings of neurons thought to encode elements of an allocentric spatial map, such as place cells in the hippocampus and grid cells in the medial entorhinal cortex (MEC). Such a map, however, must be constructed from sensory information that is initially coded egocentrically. Theoretical models have suggested mechanisms by which egocentric information can be transformed into an allocentric spatial reference frame, though the precise neural mechanisms underlying this integration are not well understood.

RATIONALE

A potential locus for the integration of egocentric and allocentric spatial information in the rat brain is the postrhinal cortex (POR). The POR is the rodent homolog of the human parahippocampal cortex, which is thought to be involved in topographic spatial learning and processing of local spatial cues. The POR is also extensively connected with brain areas thought to be involved in both egocentric and allocentric spatial processing. It has been suggested that cells encoding the egocentric bearing and distance of the geometric center of the local environment, as well as the animal’s allocentric head direction, could provide a readout of allocentric self-position. Such a signal could drive navigational behavior and support the high-level spatial maps exemplified by entorhinal grid cells and hippocampal place cells.

RESULTS

We recorded from 338 single neurons in POR (11 rats) as animals freely foraged for sugar pellets in a 1.2-m square arena. Thirty-nine percent of the cells encoded the egocentric bearing of the center of the arena (“center-bearing”). The tuning preferences of center-bearing cells were consistent across space and time. Seventeen percent of POR cells showed tuning to the animal’s distance from the center of the arena (“center-distance”), with both positive and negative linear responses to center-distance observed. Thirty-eight percent of POR cells were tuned to the rat’s head direction in an allocentric reference frame. Many POR cells were conjunctively tuned, with 51% of the cells encoding one of the three spatial variables showing conjunctive tuning to at least one other variable. The egocentric neuron types identified in POR were largely absent in neighboring MEC and parasubiculum, areas implicated in allocentric spatial processing. Unlike neurons in these areas, POR neurons rarely showed modulation of their spike trains by theta rhythm (5 to 11 Hz). Spiking properties of POR cells were sufficient to decode an animal’s allocentric position. All three spatial cell types continued processing elements of space in the presence of objects and in the dark. Decreasing the size of the arena did not affect the tuning slopes of center-distance cells. Rotation of the arena led to a corresponding shift in the preferred firing directions of head direction cells without altering the tuning of egocentric center-tuned cells.

CONCLUSION

Our results reveal a population code for allocentric space in POR that is more strongly tuned to the spatial layout of a local scene than to the contents of that scene. The cells supporting this code signal the instantaneous egocentric bearing and distance of the geometric center of the local environment, as well as allocentric head direction. Center-distance cells respond linearly to absolute distance from the environment center, whereas each center-bearing cell shows preferential firing to a single egocentric bearing of the apparatus center that remains constant across environmental manipulations. Responses of these cells are tied to local cues and maintain their tuning properties in darkness. Egocentric encoding of the local environment’s geometric center, as opposed to the encoding of its boundaries or to discrete physical cues within that environment, could allow for the use of a common spatial reference frame across environments with disparate geometries. POR projects strongly to MEC, where grid cells are found. The egocentric and allocentric correlates identified in POR might help to create or support that spatial metric. POR also projects to lateral entorhinal cortex, where egocentric correlates and object signals have been reported. The functional cell types investigated in POR may provide a foundation for spatial processing in both entorhinal subdivisions. Representations from each area can then be routed to the hippocampus and efficiently integrated for high-level spatial processing and encoding of episodic memory.

Spatial coding in postrhinal cortex.

Neurons in the rat postrhinal cortex encode the egocentric bearing and distance of the geometric center of the local environment during free foraging, as well as the animal’s head direction in allocentric coordinates. Combining these firing correlates reveals a code for representing two-dimensional allocentric space that could serve as a spatial template for the neuronal activity in the downstream entorhinal cortex and hippocampus.

Abstract

A topographic representation of local space is critical for navigation and spatial memory. In humans, topographic spatial learning relies upon the parahippocampal cortex, damage to which renders patients unable to navigate their surroundings or develop new spatial representations. Stable spatial signals have not yet been observed in its rat homolog, the postrhinal cortex. We recorded from single neurons in the rat postrhinal cortex whose firing reflects an animal’s egocentric relationship to the geometric center of the local environment, as well as the animal’s head direction in an allocentric reference frame. Combining these firing correlates revealed a population code for a stable topographic map of local space. This may form the basis for higher-order spatial maps such as those seen in the hippocampus and entorhinal cortex.

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