Control of anterodorsal thalamic head direction cells by environmental boundaries: comparison with conflicting distal landmarks.

Experiments were conducted to determine whether environmental boundaries exert preferential control over the tuning of head direction (HD) cells. In each experiment, HD cells were recorded in the rat anterodorsal thalamus while they foraged for randomly scattered food in trapezoid- and rectangle-shaped environments. After an initial recording session, each environment was rotated 90°, and changes in the preferred firing directions of HD cells were monitored. Rats were disoriented before each test session to prevent the use of self-movement cues to maintain orientation from one session to the next. In Experiment 1, we demonstrate that HD cell tuning consistently shifted in register with the trapezoid shaped enclosure, but was more variable in the rectangle shaped environment. In Experiments 2 and 3, we show that the strong control by the trapezoid persists in the presence of one clearly visible distal landmark, but not when three or more distal landmarks, including view of the recording room, are present. Together, the results indicate that distinct environmental boundaries exert strong stimulus control over HD cell orientation. However, this geometric control can be overridden with a sufficient number of salient distal landmarks. These results stand in contrast to the view that information from geometric cues usually takes precedence over information from landmark cues.