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 unidirectional or bidirectional 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 (PFDs), 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 postrotational bursting shared several striking similarities with postrotational "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.