Spatial orientation and navigation rely on the acquisition of several types of sensory information. This information is then transformed into a neural code for space in the hippocampal formation through the activity of place cells, grid cells and head-direction cells. These spatial representations, in turn, are thought to guide long-range navigation. But how the representations encoded by these different cell types are integrated in the brain to form a neural 'map and compass' is largely unknown. Here, we discuss this problem in the context of spatial navigation by bats and rats. We review the experimental findings and theoretical models that provide insight into the mechanisms that link sensory systems to spatial representations and to large-scale natural navigation.
Graphical AbstractHighlights d Bat hippocampal neurons do not exhibit rodent-like theta oscillations d Non-rhythmic synchronization and phase precession exist in bat place cells d Demonstration of nonoscillatory phase coding in a mammalian brain circuit d Synchrony and phase coding, but not oscillations, are conserved across bats and rodents
Hippocampal place cells encode the animal's spatial position. However, it is unknown how different long-range sensory systems affect spatial representations. Here we alternated usage of vision and echolocation in Egyptian fruit bats while recording from single neurons in hippocampal areas CA1 and subiculum. Bats flew back and forth along a linear flight track, employing echolocation in darkness or vision in light. Hippocampal representations remapped between vision and echolocation via two kinds of remapping: subiculum neurons turned on or off, while CA1 neurons shifted their place fields. Interneurons also exhibited strong remapping. Finally, hippocampal place fields were sharper under vision than echolocation, matching the superior sensory resolution of vision over echolocation. Simulating several theoretical models of place-cells suggested that combining sensory information and path integration best explains the experimental sharpening data. In summary, here we show sensory-based global remapping in a mammal, suggesting that the hippocampus does not contain an abstract spatial map but rather a 'cognitive atlas', with multiple maps for different sensory modalities.
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