Behavioral correlates of the distributed coding of spatial context

Abstract

Hippocampal place cells respond heterogeneously to elemental changes of a compound spatial context, suggesting that they form a distributed code of context, whereby context information is shared across a population of neurons. The question arises as to what this distributed code might be useful for. The present study explored two possibilities: one, that it allows contexts with common elements to be disambiguated, and the other, that it allows a given context to be associated with more than one outcome. We used two naturalistic measures of context processing in rats, rearing and thigmotaxis (boundary-hugging), to explore how rats responded to contextual novelty and to relate this to the behavior of place cells. In experiment 1, rats showed dishabituation of rearing to a novel reconfiguration of familiar context elements, suggesting that they perceived the reconfiguration as novel, a behavior that parallels that of place cells in a similar situation. In experiment 2, rats were trained in a place preference task on an open-field arena. A change in the arena context triggered renewed thigmotaxis, and yet navigation continued unimpaired, indicating simultaneous representation of both the altered contextual and constant spatial cues. Place cells similarly exhibited a dual population of responses, consistent with the hypothesis that their activity underlies spatial behavior. Together, these experiments suggest that heterogeneous context encoding (or "partial remapping") by place cells may function to allow the flexible assignment of associations to contexts, a faculty that could be useful in episodic memory encoding.