How does the 3D neural compass work in the mouse brain?

Angelaki, Dora E., Julia Ng, Amada M. Abrego, Henry X. Cham, J. D. Dickman, and Jean Laurens. “A gravity-based three-dimensional compass in the mouse brain.” bioRxiv (2019): 570382.

Summary
“Head direction cells in the mammalian limbic system are thought to function as an allocentric neuronal compass. Although traditional views hold that the compass of ground-dwelling species is planar, we show that head-direction cells in the rodent thalamus, retrosplenial cortex and cingulum fiber bundle are tuned to conjunctive combinations of azimuth, pitch or roll, similarly to presubicular cells in flying bats. Pitch and roll orientation tuning is ubiquitous, anchored to gravity, and independent of visual landmarks. When head tilts, azimuth tuning is affixed to the head-horizontal plane, but also uses gravity to remain anchored to the terrestrial allocentric world. These findings suggest that gravity defines all three degrees of freedom of the allocentric orientation compass, and only the azimuth component can flexibly remap to local cues in different environments. Collectively, these results demonstrate that a three-dimensional, gravity-based, neural compass is likely a ubiquitous property of mammalian species, including ground-dwelling animals.”

 

Laurens, Jean, and Dora E. Angelaki. “The brain compass: a perspective on how self-motion updates the head direction cell attractor.” Neuron 97, no. 2 (2018): 275-289.

Summary

“Head direction cells form an internal compass signaling head azimuth orientation even without visual landmarks. This property is generated by a neuronal ring attractor that is updated using rotation velocity cues. The properties and origin of this velocity drive remain, however, unknown. We propose a quantitative framework whereby this drive represents a multisensory self-motion estimate computed through an internal model that uses sensory prediction errors of vestibular, visual, and somatosensory cues to improve on-line motor drive. We show how restraint-dependent strength of recurrent connections within the attractor can explain differences in head direction cell firing between free foraging and restrained passive rotation. We also summarize recent findings on how gravity influences azimuth coding, indicating that the velocity drive is not purely egocentric. Finally, we show that the internal compass may be three-dimensional and hypothesize that the additional vertical degrees of freedom use global allocentric gravity cues. “

 

Further references:

Shinder, Michael E., and Jeffrey S. Taube. “Three-dimensional tuning of head direction cells in rats.” Journal of neurophysiology 121, no. 1 (2018): 4-37.

Laurens, Jean, and Dora E. Angelaki. “A Model-Based Reassessment of the Three-Dimensional Tuning of Head Direction Cells in Rats.” Journal of neurophysiology (2019).

Page, Hector JI, Jonathan J. Wilson, and Kate J. Jeffery. “A dual-axis rotation rule for updating the head direction cell reference frame during movement in three dimensions.” Journal of neurophysiology 119, no. 1 (2017): 192-208.