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 behavior. Experiments have shown that the semicircular canals provide a necessary component for generating this head direction (HD) signal. Most studies on HD cells have explored how they respond in two-dimensional environments within the horizontal plane. However, many animals live and locomote in a three-dimensional world. My talk will review the studies on how HD cells discharge when the animal is in a vertical plane or inverted on a ceiling. We have 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 behavioral studies have found that rats were capable of accurately performing a navigational task when inverted, but only when the task was simple and started from one or two entry points. When they were started from novel locations, their performances fell to chance. 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. One major component that is different when animals are inverted is the nature of the otolith signal, which is responsible for monitoring linear acceleration of the head as well as static head tilt. To examine the role the otolith signal plays in HD cell responses we recorded cells in otoconia-deficient tilted mice. We found that although HD cells could be identified in these mice, the percentage of HD cells was significantly less, and their firing properties and responses to landmark manipulations were not as robust compared to controls. Taken together, these findings indicate that the otolith organs contribute an important role to HD cell discharge.