Abstract

Spatial encoding in the hippocampus is based on a range of different input sources. To generate spatial representations, reliable sensory cues from the external environment are integrated with idiothetic cues, derived from self-movement, that enable path integration and directional perception. In this study, we examined to what extent idiothetic cues significantly contribute to spatial representations and navigation: we recorded place cells while rodents navigated towards two visually identical chambers in 180° orientation via two different paths in darkness and in the absence of reliable auditory or olfactory cues. Our goal was to generate a conflict between local visual and direction-specific information, and then to assess which strategy was prioritized in different learning phases. We observed that, in the absence of distal cues, place fields are initially controlled by local visual cues that override idiothetic cues, but that with multiple exposures to the paradigm, spaced at intervals of days, idiothetic cues become increasingly implemented in generating an accurate spatial representation. Taken together, these data support that, in the absence of distal cues, local visual cues are prioritized in the generation of context-specific spatial representations through place cells, whereby idiothetic cues are deemed unreliable. With cumulative exposures to the environments, the animal learns to attend to subtle idiothetic cues to resolve the conflict between visual and direction-specific information.

Highlights

  • Place cells in the hippocampus are an important part of the neuronal substrates for spatial navigation and spatial memory (O’Keefe and Nadel, 1978)

  • The firing characteristics of the place cells were segregated according to paradigm-naïve, paradigm-familiar and illuminated sessions (Figure 4)

  • When a corridor barrier was removed and the animal could access both chambers by commuting between the environments, using their trajectory to help them discriminate the two environments, place fields did not remap, indicating that idiothetic cues were subordinate to the local visual cues

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Summary

Introduction

Place cells in the hippocampus are an important part of the neuronal substrates for spatial navigation and spatial memory (O’Keefe and Nadel, 1978) They exhibit high-frequency discharges when animals traverse a specific location within an environment. Tanila (Tanila, 1999) recorded hippocampal place cells mainly from the CA3 subfield, during navigation within two visually identical boxes that were illuminated from above by four incandescent lights and were connected door-todoor in the same orientation. He showed that distinct spatial representations occur in both boxes despite their ostensible visual similarities. In these two latter studies, distal (extra-environmental) cues were not available, this suggests that the relative reliance of the animals on local visual and idiothetic cues strongly impacts on their perception and spatial representations of visually similar environments

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