A sense of space in postrhinal cortex

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.