Neural correlates of sensory substitution in vestibular pathways following complete vestibular loss

Sensory substitution is the term typically used in reference to sensory prosthetic devices designed to replace input from one defective modality with input from another modality. Such devices allow an alternative encoding of sensory information that is no longer directly provided by the defective modality in a purposeful and goal-directed manner. The behavioral recovery that follows complete vestibular loss is impressive and has long been thought to take advantage of a natural form of sensory substitution in which head motion information is no longer provided by vestibular inputs, but instead by extravestibular inputs such as proprioceptive and motor efference copy signals. Here we examined the neuronal correlates of this behavioral recovery after complete vestibular loss in alert behaving monkeys (Macaca mulatta). We show for the first time that extravestibular inputs substitute for the vestibular inputs to stabilize gaze at the level of single neurons in the vestibulo-ocular reflex premotor circuitry. The summed weighting of neck proprioceptive and efference copy information was sufficient to explain simultaneously observed behavioral improvements in gaze stability. Furthermore, by altering correspondence between intended and actual head movement we revealed a fourfold increase in the weight of neck motor efference copy signals consistent with the enhanced behavioral recovery observed when head movements are voluntary versus unexpected. Thus, together our results provide direct evidence that the substitution by extravestibular inputs in vestibular pathways provides a neural correlate for the improvements in gaze stability that are observed following the total loss of vestibular inputs.