A model-based reassessment of the three-dimensional tuning of head direction cells in rats

In a recent study, Shinder and Taube (Shinder ME, Taube JS. J Neurophysiol 121: 4-37, 2019) concluded that head direction cells in the anterior thalamus of rats are tuned to one-dimensional (1D, yaw-only) motion, in contrast to recent findings in bats, mice, and rats. Here we reinterpret the author's experimental results using model comparison and demonstrate that, contrary to their conclusions, experimental data actually supports the dual-axis rule (lson JJ, Jeffery KJ. JNeurophysiol 119: 192-208, 2018) and tilted azimuth model (Laurens J, Angelaki DE. Neuron 97: 275-289, 2018), where head direction cells use gravity to integrate 3D rotation signals about all cardinal axes of the head. We further show that the Shinder and Taube study is inconclusive regarding the presence of vertical orientation tuning; i.e., whether head direction cells encode 3D orientation in the horizontal and vertical planes conjunctively. Using model simulations, we demonstrate that, even if 3D tuning existed, the experimental protocol and data analyses used by Shinder and Taube would not have revealed it. We conclude that the actual experimental data of Shinder and Taube are compatible with the 3D properties of head direction cells discovered by other groups, yet incorrect conclusions were reached because of incomplete and qualitative analyses.NEW & NOTEWORTHY We conducted a model-based analysis previously published data where rat head direction cells were recorded during three-dimensional motion (Shinder ME, Taube JS. J Neurophysiol 121: 4-37, 2019). We found that these data corroborate previous models ("dual-axis rule," Page HJI, Wilson JJ, Jeffery KJ. J Neurophysiol 119: 192-208, 2018; and "tilted azimuth model," Laurens J, Angelaki DE. Neuron 97: 275-289, 2018) where head direction cells integrate rotations along all three head axes to encode head orientation in a gravity-anchored reference frame.