Distal landmarks and hippocampal place cells: Effects of relative translation versus rotation

Abstract

Hippocampal neurons are selectively active when a rat occupies restricted locations in an environment. These place cells derive their specificity from a multitude of sources, including idiothetic cues and sensory input derived from both distal and local landmarks. Most experiments have attempted to dissociate the relative strengths and roles played by these sources by rotating one set against the other. Few studies have addressed the effects of relative translation of the local cue set versus salient distal landmarks. To address this question, ensembles of place cells were recorded as a rectangular or circular track was moved to different locations in a room with controlled visual landmarks. Place cells primarily maintained their firing fields relative to the track (i.e., occupying new locations relative to the distal landmarks), even though the track could occupy completely nonoverlapping regions of the room. When the distal landmarks were rotated around the circular track, however, the place fields rotated with the landmarks, demonstrating that the cues were perceptible to the rat. These results suggest that, under these conditions, the spatial tuning of place cells may derive from an interaction between local and idiothetic cues, which define the precise firing locations of the cells and the relationships between them, and distal landmarks, which set the orientation of the ensemble representation relative to the external environment. © 2003 Wiley-Liss, Inc.