The vestibulo-ocular reflex (VOR) is subject to long-term adaptive changes that minimize retinal image slip and keep eye movement equal to and opposite head movement. As a step toward identifying the site of neural changes, we have used a transient vestibular stimulus to study the dynamic response properties of the vestibular signals carried by the modifiable pathways. In normal monkeys, "rapid changes in head velocity" (30 degrees/sec in 50 msec) evoke a VOR that has a slight overshoot and reaches a steady-state gain (eye velocity divided by head velocity) of 1.0. Adaptation to magnifying spectacles causes changes in both the steady-state gain and the degree of overshoot in the eye velocity of the VOR. When the steady-state gain is decreased, the transient overshoot increases, so that peak eye velocity is twice steady-state. When the steady-state gain is increased, the overshoot decreases, so that peak eye velocity is nearly equal to steady-state. The discharge of vestibular primary afferents suggests an explanation for the inverse relationship between the transient overshoot and the steady-state gain of the VOR. In normal monkeys, 73 afferents showed a range of transient responses during rapid changes in head velocity. The afferents with the most regular spontaneous discharge had little overshoot in firing rate. Afferents with less regular discharge had large overshoots in firing; the peak change in firing was 2-6 X the steady-state change. We suggest that the large overshoot in eye velocity when VOR gain is low represents the contribution of vestibular signals from afferents with large transient responses.(ABSTRACT TRUNCATED AT 250 WORDS)