Time course of sensory substitution for gravity sensing in visual vertical orientation perception following complete vestibular loss

Abstract

Loss of vestibular function causes severe acute symptoms of dizziness and disorientation, yet the brain can adapt and regain near to normal locomotor and orientation function through sensory substitution. Animal studies quantifying functional recovery have yet been limited to reflexive eye movements. Here we studied the interplay between vestibular and proprioceptive graviception in macaque monkeys trained in an earth-vertical visual orientation (subjective visual vertical) task, and measured the time course of sensory substitution for gravity perception following complete bilateral vestibular loss. Graviceptive gain, defined as the ratio of perceived versus actual tilt angle, decreased to 20% immediately following labyrinthectomy, and recovered to nearly pre-lesion levels with a time constant of approximately 3 weeks of post-surgery testing. We conclude that proprioception accounts for up to 20% of gravity sensing in normal animals, and is re-weighted to substitute completely perceptual graviception after vestibular loss. We show that these results can be accounted for by an optimal sensory fusion model.

Significance statement Verticality perception is based on gravity sensing by the vestibular organs in the inner ear and by trunk proprioceptors. Here we measured the contribution of vestibular and proprioceptive signals to verticality perception in macaque monkeys before and following complete vestibular lesion. We found that proprioception contributes to 20% of gravity sensing in healthy animals. Following vestibular loss, gravity sensing recovers to baseline levels in weeks, and is affected by how often the animals performed the task. Comparison with previous experimental and modeling studies indicate that our results likely generalize to gravity sensing in humans, at least at small (<30°) tilt angles.