Abstract

Effective spatial navigation is enabled by reliable reference cues that derive from sensory information from the external environment, as well as from internal sources such as the vestibular system. The integration of information from these sources enables dead reckoning in the form of path integration. Navigation in the dark is associated with the accumulation of errors in terms of perception of allocentric position and this may relate to error accumulation in path integration. We assessed this by recording from place cells in the dark under circumstances where spatial sensory cues were suppressed. Spatial information content, spatial coherence, place field size, and peak and infield firing rates decreased whereas sparsity increased following exploration in the dark compared to the light. Nonetheless it was observed that place field stability in darkness was sustained by border information in a subset of place cells. To examine the impact of encountering the environment’s border on navigation, we analyzed the trajectory and spiking data gathered during navigation in the dark. Our data suggest that although error accumulation in path integration drives place field drift in darkness, under circumstances where border contact is possible, this information is integrated to enable retention of spatial representations.

Highlights

  • In the hippocampal formation, four neuronal populations enable the encoding of spatial representations

  • Place cells are found in the CA1 region of the hippocampus (O’Keefe and Dostrovsky, 1971) and fire when an animal finds itself in a specific location of an environment

  • Fifty-one well-isolated place cells were recorded in the CA1 region of the hippocampus from four rats, following the sequence of light (S1), dark (S2), and light again (S3)

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Summary

Introduction

In the hippocampal formation, four neuronal populations enable the encoding of spatial representations. Grid cells occurring in the medial entorhinal cortex exhibit firing fields that define a triangular array representing the entire perceived environment (Hafting et al, 2005). All of these spatially selective firing patterns derive from external information in the form of stable sensory cues (Muller and Kubie, 1987; Save et al, 2000; Zhang and Manahan-Vaughan, 2013) and from internal information such as self-motion generated path integration (McNaughton et al, 1989; Quirk et al, 1990)

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