Spinalized toadfish were held in a lucite chamber and perfused through the mouth with running seawater. Primary vestibular afferents and vestibular efferent axons and somas were studied with glass microelectrodes. Vestibular semicircular canal afferent and efferent axons were visually identified and penetrated with glass microelectrodes. Afferents responded to pulses of injected current with trains of action potentials, whereas efferents responded with only a single spike. This differential response to injected current served to further distinguish these two classes of nerve fibers that share the same canal nerve for part of their course. When current pulses were injected into efferent somadendritic recording sites, cells responded with trains of action potentials similar to those seen in other central nervous system neurons. Semicircular canal afferents were spontaneously active and occupied the same spectrum of regularity as vestibular afferents recorded in other species. Behavioral arousal evoked by lightly touching the fish on the snout or over the eye resembled spontaneous arousal observed in the field and consisted of eye withdrawal, fin erection, and attempted swimming. Efferent vestibular neurons were spontaneously active and increased their frequency of discharge when the fish was behaviorally aroused. Most efferents were briskly activated by behavioral arousal, but the time constant of the decay of their responses was variable ranging from 100 to 600 ms. Not only touch, but multimodal stimuli were capable of increasing the level of spontaneous activity of efferent vestibular neurons. The shortest latency to behavioral activation was 160 ms. Vestibular primary afferents also manifested increase in neuronal activity with behavioral activation. Irregularly discharging afferents were much more responsive than regularly discharging afferents. One rare case of transient inhibition in a regularly discharging afferent is illustrated. Severing the efferent vestibular nerve blocked behavioral activation in vestibular primary afferents. Electrical stimulation of the efferent vestibular nerve produced excitatory postsynaptic potentials (EPSPs) at latencies within the monosynaptic range in vestibular primary afferents. These monosynaptic EPSPs could produce action potentials in primary afferents or could sum with subthreshold depolarizations produced by current passed through the microelectrode to initiate impulses.(ABSTRACT TRUNCATED AT 400 WORDS)