The sensations of sound and motion generated by the inner ear are controlled by the brain through extensive centripetal innervation originating within the brainstem. In the semicircular canals, brainstem efferent neurons make synaptic contacts with mechano-sensory hair cells and with the dendrites of afferent neurons. Here, we examine the relative contributions of efferent action on hair cells and afferents. Experiments were performed in-vivo in the oyster toadfish, Opsanus tau. The efferent system was activated via electrical pulses to the brainstem, and sensory responses to motion stimuli were quantified by simultaneous voltage recording from afferents and intracellular current and/or voltage-clamp recordings from hair cells. Results showed synaptic inputs to both afferents and hair cells leading to relatively long latency intracellular signaling responses: excitatory in afferents and inhibitory in hair cells. Generally, the net effect of efferent action was an increase in afferent background discharge and a simultaneous decrease in gain to angular motion stimuli. Inhibition of hair cells was likely the result of a ligand-gated opening of a major basolateral conductance. The reversal potential of the efferent-evoked current was just below the hair cell resting potential thus resulting in a small hyperpolarization. The onset latency averaged ~90ms and latency to peak response was 150-400ms. Hair cell inhibition often outlasted afferent excitation and in some cases latched hair cells in the "off" condition for over a second following cessation of stimulus. These features endow the animal with a powerful means to adjust the sensitivity and dynamic range of motion sensation.