Active and passive movement are encoded equally by head direction cells in the anterodorsal thalamus

The head direction (HD) system is composed of cells that represent the direction in which the animal's head is facing. Each HD cell responds optimally when the head is pointing in a particular, or preferred, direction. Although vestibular system input is necessary to generate the directional signal, motor/proprioceptive inputs can also influence HD cell responses. Previous studies comparing active and passive movement have reported significant suppression of the HD signal during passive restraint. However, in each of these studies there was considerable variability across cells, and the animal's head was never completely fixed. To address these issues, we developed a passive restraint system that more fully prevented head and body movement. HD cell responses in the anterodorsal thalamus (ADN) were evaluated during active and passive movement with this new system. Contrary to previous reports, HD cell responses were not affected by passive restraint. Both head-fixed and hand-held restraint failed to produce significant inhibition of the active HD cell response. Furthermore, direction-specific firing was maintained regardless of 1) the animal's previous experience with restraint, 2) whether it was tested in the light or dark, or 3) the position of the animal relative to the axis of rotation. The maintenance of a stable directional signal without appropriate motor, proprioceptive, or visual input indicates that vestibular input is necessary and sufficient for the generation of the HD signal. Motor and proprioceptive influences may therefore be important for the control of the preferred firing direction of HD cells, but not the generation of the signal itself.