Vestibular Adaptation: How Models Can Affect Data Interpretations

Abstract

Vestibular adaptation can be induced optically or by chemical or physical injury to the vestibular apparatus or the brain stem. In searching for the sites or mechanisms of vestibular adaptation, neurophysiologists often rely on comparing central resting (background) activities and central modulations (sensitivity) during vestibular stimulation, before and after motor learning or vestibular compensation. It is assumed that adapted central sites must exhibit modulation changes that parallel vestibulo-ocular reflex changes. Using model simulations and analysis, we will show that such presumptions may be misleading. First, using a simple schematic of interconnected cells or nuclei, one can show that modulation depth and background “tone” can be modified (or fixed) independently, using weightings on direct or indirect afferent projections. That is, if synaptic weights along all stimulus pathways are altered, one may fix or strongly modify central premotor characteristics in a manner apparently unrelated to global reflex changes. In the vestibulo-ocular reflex, the dominant premotor pathways contain position-vestibular-pause cells and eye-head-velocity cells (which are behaviorally similar to floccular-target neurons). Several experiments have reported negligible changes in the velocity sensitivity of position-vestibular-pause cells, despite large gain changes in the vestibulo-ocular reflex induced by training with visual-vestibular conflict. On the other hand, the modulation changes on floccular-target neurons (position-vestibular-pause) can be much larger than the changes in reflex gain. Using a bilateral vestibulo-ocular reflex model, we show that overall increases or decreases in reflex gain can be expressed (even overexpressed) in one particular subgroup of premotor neurons. Nevertheless, such observations are theoretically compatible with synaptic changes on all primary projections in a widely interconnected central network. Hence, stable neural responses during reflex adaptation are not sufficient to exclude a potential site of sensory-motor adaptation. Similarly, modified neural responses (as in cerebellum) need not necessarily imply a direct role in supporting the adapted state. Model predictions should help to design additional experimental protocols, to test hypotheses, and to refine diagnostic measures of recovery after vestibular lesions.