Heterogeneous Modulation of Place Cell Firing by Changes in Context

TLDR

Hippocampal place cells exhibit spatially localized firing that can be modulated by geometric and nongeometric cues, such as colors, odors, and behaviors, and understanding how contextual information influences hippocampal activity is crucial for theories that the hippocampus constructs spatial context representations. The study aimed to investigate how contextual cues modulate place cell activity and to propose a model of contextual remapping in which geometric inputs are selectively activated by subsets of contextual stimuli. Place cells were recorded in rats foraging in compound contexts combining black or white color with lemon or vanilla odor, and a model was proposed in which geometric inputs are selectively activated by subsets of contextual stimuli. Some place cells responded to color or odor alone, most responded to combinations of both, revealing heterogeneous contextual input into the hippocampus and indicating that the full context representation requires population‑level activity.

Abstract

Hippocampal place cells show spatially localized activity that can be modulated by both geometric information (e.g., the distances and directions of features in the environment) and nongeometric information (e.g., colors, odors, and possibly behaviors). Nongeometric information may allow the discrimination of different spatial contexts. Understanding how nongeometric (or contextual) information affects hippocampal activity is important in light of proposals that the hippocampus may play a role in constructing a representation of spatial context. We investigated the contextual modulation of place cell activity by recording hippocampal place cells while rats foraged in compound contexts comprising black or white color paired with lemon or vanilla odor. Some cells responded to the color or odor changes alone, but most responded to varying combinations of both. Thus, we demonstrate, for the first time, that there is a heterogeneous input by contextual inputs into the hippocampus. We propose a model of contextual remapping of place cells in which the geometric inputs are selectively activated by subsets of contextual stimuli. Because it appears that different place cells are affected by different subsets of contextual stimuli, the representation of the entire context would require activity at the population level, supporting a role for the hippocampus in constructing a representation of spatial context.