The Brain Compass: A Perspective on How Self-Motion Updates the Head Direction Cell Attractor

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. Laurens and Angelaki present a quantitative model of how multisensory self-motion signals update the firing rate of head direction cells to maintain a sense of orientation in light or darkness, during active or passive motion, and during three-dimensional movements.