Head direction cell firing properties and behavioural performance in 3-D space

Previous studies have identified a population of neurons in the rat brain that discharge as a function of the animal's directional heading in the horizontal plane, independent of their location and on-going behaviour. Most studies on head direction (HD) cells have explored how they respond in two-dimensional environments within the horizontal plane. Many animals, however, live and locomote in a three-dimensional world. This paper reviews how HD cells respond when the animal locomotes on a vertical surface or inverted on a ceiling. We found that HD cells fire in a normal, direction-dependent manner when the rat is in the vertical plane, but not when the animal is inverted. Recent behavioural studies reported that rats are capable of accurately performing a navigational task when inverted, but only when the task was simple and started from not more than one or two entry points. Probe trials found that they did not have a flexible, map-like representation of space when inverted. The loss of the directional signal when the animal is in an inverted orientation may account for the absence of the map-like representation. Taken together, these findings indicate that a normal otolith signal contributes an important role to HD cell discharge.