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The Journal of Neuroscience, October 1, 2003, 23(26):8827-8835

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Behavioral/Systems/Cognitive
Heterogeneous Modulation of Place Cell Firing by Changes in Context

Michael I. Anderson and Kathryn J. Jeffery

Department of Psychology, University College London, London, WC1H OAP, United Kingdom

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.

Key words: hippocampus; single-unit; place cells; context; remapping; spatial representation

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Received May 12, 2003; revised July 17, 2003; accepted July 22, 2003.

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