The Neural Correlates of Spatial Disorientation in Head Direction Cells.

While the brain has evolved robust mechanisms to counter spatial disorientation, their neural underpinnings remain unknown. To explore these underpinnings, we monitored the activity of anterodorsal thalamic head-direction (HD) cells in rats while they underwent uni- or bi-directional rotation at different speeds and under different conditions (light vs. dark, freely-moving vs. head-fixed). Under conditions that promoted disorientation HD cells did not become quiescent but continued to fire, although their firing was no longer direction-specific. Peak firing rates, burst frequency, and directionality all decreased linearly with rotation speed, consistent with previous experiments where rats were inverted or climbed walls/ceilings in zero-gravity. However, access to visual landmarks spared the stability of preferred firing directions, indicating that visual landmarks provide a stabilizing signal to the HD system while vestibular input likely maintains direction-specific firing. In addition, we found evidence that the HD system underestimated angular velocity at the beginning of head-fixed rotations, consistent with the finding that humans often underestimate rotations. When head-fixed rotations in the dark were terminated HD cells fired in bursts that matched the frequency of rotation. This post-rotational bursting shared several striking similarities with post-rotational "nystagmus" in the vestibulo-ocular system, consistent with the interpretation that the HD system receives input from a vestibular velocity storage mechanism that works to reduce spatial disorientation following rotation. Thus, the brain overcomes spatial disorientation through multisensory integration of different motor-sensory inputs. Significance statement Head direction (HD) cells are neurons in the brain that underlie spatial orientation, but little is known about how these cells function during disorientation. To investigate this, we monitored HD cell responses in rats as they were rotated under a variety of conditions. We found that their activity fitted predictions from an attractor network model. We also found that visual and vestibular inputs differentially support stability and directionality respectively. Lastly, we found evidence that HD cells may share a network associated with stabilizing gaze and velocity storage. Together, these findings add a missing piece to the HD system puzzle, help us understand the neural mechanisms of reorientation and will improve computational models of HD cells in the future.