Multiple maps and multiple reference frames in the hippocampal representation of space

Abstract

Populations of simultaneously recorded hippocampal place cells were studied in three tasks that required shuttling between a variably placed box and a reward location predicted by fixed or variably located landmarks. Groups of place cells fired at fixed locations relative to the behaviorally relevant landmarks or to the absolute spatial framework of the environment. The initial segment of the journeys was represented by a sequence of cells that fired at fixed distances with respect to the landmark of origin, behind the animal, irrespective of where that landmark was located. The final segments of the journeys were represented by cells that fired at fixed locations relative to the landmark of destination. We propose that on the initial parts of the journey, the spatial coordinate represented by each cell was updated predominantly by path integration. When approaching the landmark of destination, the coordinates were updated and corrected by visual landmarks (or other sensory cues). The intermediate zone was characterized by a transition from the reference frame of the origin to the reference frame of the destination. Small distortion of the environment led to a smooth, continuous transition, while a large distortion led to abrupt transitions. These observations suggest that in the hippocampus, place can be represented in multiple spatial reference frames established by behaviorally relevant landmarks. Further experiments showed that these landmarks, or their sensory properties, are not represented explicitly by place cells, because cells did not maintain their landmark-related firing in a similar task, performed in a different environment.