Advantage was taken of differences in the electrical excitability of vestibular-nerve fibers to characterize the afferent input to the canal- related vestibulo-ocular reflex. Large anodal (inhibitory) currents, when delivered to both ears, result in a selective, reversible ablation of irregular afferents. Their background discharge and responses to head rotations are temporarily abolished. The same currents have less effect on the background discharge and no effect on the rotational sensitivity of regular afferents. Eye movements were evoked by head rotations in alert monkeys. The ablating currents did not alter the ocular responses to sinusoidal head rotations in yaw or pitch planes. Responses to rapid changes in head velocity were similarly unaffected. It is concluded that irregular afferents do not make a net contribution to the reflex. Slow-phase eye movements evoked by unilateral galvanic currents are consistent with this conclusion. The results are incorporated into a systems model of the reflex. There are three conclusions from the model: (1) the signal to motoneurons consists of the sum of three components related, respectively, to head velocity, eye position, and filtered eye velocity; (2) regular afferents provide the best match to the dynamic requirements of the reflex; and (3) the central pathways responsible for all three signal components receive regular inputs.