On the absence or presence of 3D tuned head direction cells in rats: a review and rebuttal.

A major question in the field of spatial cognition is how animals represent three-dimensional (3D) space. Different results have been obtained across various species and may depend on whether the species inhabits a 3D environment or is terrestrial (land dwelling). The head direction (HD) cell system is an attractive candidate to study in terms of 3D representations. HD cells fire as a function of the animal's directional heading in the horizontal plane, independent of the animal's location and on-going behavior. Another issue concerns whether HD cells are tuned in 3D space or tuned to the 2D horizontal plane. Shinder and Taube (Shinder ME, Taube JS. J Neurophysiol 121: 4-37, 2019) addressed this issue by manipulating a rat's orientation in 3D space while monitoring responses from classic HD cells in the rat anterodorsal thalamus. They reported that HD cells did not display conjunctive firing with pitch or roll orientations. Direction-specific firing was primarily derived from horizontal semicircular canal information and that the gravity vector played an important role in influencing the cell's firing rate and its preferred firing direction. Laurens and Angelaki (Laurens J, Angelaki DE. J Neurophysiol 122: 1274-1287, 2019) challenged this view by performing a mathematical analysis on the Shinder and Taube data and concluded that they would not have seen 3D tuning based on their experimental approach. We provide a historical review of these issues followed by a summary of the experiments, which includes additional analyses. We then define what it means for a HD cell to be tuned in 3D and finish by rebutting the reanalyses performed by Laurens and Angelaki.