Recent interest in the neural bases of spatial navigation stems from the discovery
of neuronal populations with strong, specific spatial signals. The regular firing
field arrays of medial entorhinal grid cells suggest that they may provide place cells
with distance information extracted from the animal's self-motion, a notion we critically
review by citing new contrary evidence. Next, we question the idea that grid cells
provide a rigid distance metric. We also discuss evidence that normal navigation is
possible using only landmarks, without self-motion signals. We then propose a model
that supposes that information flow in the navigational system changes between light
and dark conditions. We assume that the true map-like representation is hippocampal
and argue that grid cells have a crucial navigational role only in the dark. In this
view, their activity in the light is predominantly shaped by landmarks rather than
self-motion information, and so follows place cell activity; in the dark, their activity
is determined by self-motion cues and controls place cell activity. A corollary is
that place cell activity in the light depends on non-grid cells in ventral medial
entorhinal cortex. We conclude that analysing navigational system changes between
landmark and no-landmark conditions will reveal key functional properties.
