Maintenance of rat head direction cell firing during locomotion in the vertical plane

Previous studies have identified a subset of neurons in the rat anterodorsal thalamus (ADN) that encode head direction (HD) in absolute space and may be involved in navigation. These HD cells discharge selectively when the rat points its head in a specific direction (the preferred firing direction) in the horizontal plane. HD cells are typically recorded during free movement about a single horizontal surface. The current experiment examined how HD cell firing was influenced by 1) locomotion in the vertical plane and 2) locomotion on two different horizontal surfaces separated in height. Rats were trained in a cylindrical enclosure containing a single polarizing cue card attached to the cylinder wall, covering approximately 100 degrees of arc. The enclosure contained two horizontal surfaces: the cylinder floor and an annulus around the cylinder top 76 cm above the floor. A 90 degrees vertical mesh ladder that could be affixed at any angular position on the cylinder wall allowed the rats to locomote back and forth between the two horizontal surfaces. Rats were trained to retrieve food pellets on the cylinder floor as well as climb the mesh ladder to retrieve food pellets on the annulus. HD cell activity was monitored as the rat traversed the horizontal and vertical surfaces of the apparatus. When the angular position of the mesh corresponded to the cell's preferred firing direction, the HD cells maintained their peak discharge rate as the rat climbed up the mesh, but did not fire when the rat climbed down the mesh. In contrast, when the mesh was positioned 180 degrees opposite the preferred firing direction, HD cells did not fire when the rat climbed up the mesh, but exhibited maximal firing when the rat climbed down the mesh. When the mesh was placed 90 or 270 degrees from the preferred firing direction, HD cells exhibited background firing rates during climbing up or down the mesh. While preferred firing directions were maintained between the two horizontal surfaces, peak firing rate increased significantly (approximately 30%) on the annulus as compared with the cylinder floor. These data demonstrate that HD cells continue to discharge in the vertical plane if the vertical locomotion began with the rat's orientation corresponding to the preferred firing direction. One model consistent with these data are that HD cells define the horizontal reference frame as the animal's plane of locomotion. Further, we propose that HD cell firing, as viewed within a three-dimensional coordinate system, can be characterized as the surface of a hemitorus.