Flexible use of proximal objects and distal cues by hippocampal place cells

Abstract

The purpose of the present experiment was to examine how distal cues and proximal objects interact to control firing fields. In a previous study, Shapiro et al. (1997) Hippocampus 7:624-642, suggested that hippocampal place cell firing is controlled by distal cues and proximal floor inserts in a flexible and hierarchical fashion. Control exerted by the combined set of cues prevailed over control by distal cues, which itself prevailed over control by proximal cues. Here, we examined the generality of this hierarchy in the use of cues. Place cells were recorded as rats performed a pellet chasing task on a platform containing three proximal objects, surrounded by a curtain where three visual stimuli were hung. A double rotation of distal and proximal cue sets producing a 180 degrees mismatch revealed noncoherent responses of place cells. Most fields were controlled by the configuration of proximal and distal cues (i.e., remapped). Less often, fields were controlled by specific cues with a majority being controlled by proximal cues, thus suggesting that response hierarchy is modulated by the environment. We finally examined the effect of removing one set of cues after the double rotation session. Half of the fields were controlled by the remaining cues while the other half remapped, thus suggesting a competition between pattern completion and pattern separation processes. Furthermore, cells that were controlled by the remaining cues were mainly those that had remapped in the double rotation session. Our results are compatible with the idea that the flexibility of the place cell system results from an interaction between the sensory properties of individual cell and the attractor networks properties of the whole place cell population.