Independence of landmark and self-motion-guided navigation: a different role for grid cells

Abstract

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.

Keywords: entorhinal cortex; grid cells; navigation; place cells.

Figure 1.

Block diagram summarizing the proposed organization for a two-state model of navigation. The basic notion is that information flow in the navigational system depends on whether the animal is using landmark (as in the light) or self-motion (as in the dark) signals to select its path through space. The short arrows from the Map to the Path stand for the neural machinery required to transform the hippocampal encoding into locomotion. The long arrows from the path stand for changes in sensory information brought about when the path is taken; in the light, this means changes in landmark configuration caused by movement; in the dark it means vestibular and odometry signals that can be used to estimate movement. In the light, the essential information flow to the hippocampus is via ventral MEC place-like cells; in the dark it is via the dorsal MEC grid cell strip. Depending on the state, the navigational loop including the map and the actual path does not depend on network elements linked by black lines. The arrow from the map to the grid cell strip signifies: (a) that hippocampal inactivation reduces the net excitatory drive on grid cells [51], (b) that grid cell fields stay in register with place cell firing fields during the topological distortion induced by small cue conflicts. The bidirectional arrows between the grid cell strip and ventral MEC indicate the possibility of interaction between the landmark and self-motion subsystems. Although a comprehensive review of temporal lobe neuroanatomy [86,87] cites no direct connections between the two portions of MEC, they might be linked via the intermediate zone. dMEC, dorsal medial entorhinal cortex; vMEC, ventral medial entorhinal cortex. (Online version in colour.)