1. Neurons activated by stimulation of the horizontal and/or vertical vestibular semicircular canals were recorded in the parietoinsular vestibular cortex in four awake Java monkeys (Macaca fascicularis) and three squirrel monkeys (Saimiri sciureus). Steady tilt in darkness or during illumination of a vertically striped cylinder or of the normal laboratory surroundings did not lead to a significant change in PIVC neuron activity. Thus vestibular input to this cortical region seems to be restricted to signals originating in the semicircular canal receptors. 2. Vestibular stimulation in the three main experimental planes (roll, yaw, and pitch) and in planes in between provided clear evidence that optimum activation can be found in planes that do not coincide with the planes of the semicircular canals but are distributed over all possible spatial planes through the head. 3. Definite evidence of clustering in subdivisions of PIVC of neurons responding to the same optimum rotation plane was obtained in squirrel monkeys and is also suggested to exist in PIVC of Java monkeys. 4. Nearly all neurons responding to vestibular stimulation were also activated by visual large-field movement (optokinetic stimulation). Responses to optokinetic stimuli were always at optimum when the direction of the movement pattern corresponded to the optimum vestibular plane. Two classes of visual-vestibular interaction were found: Synergistic neurons were those PIVC cells with the strongest response to visual movement stimulation in the opposite direction to that leading to a maximum response to vestibular stimulation. Antagonistic neurons had a response maximum when the visual stimulus was moved in the direction of optimum vestibular stimulation. 5. Most PIVC neurons responded to stimulation of the deep mechanoreceptors in the neck region. This input from the neck receptors was tested quantitatively only in the horizontal plane (trunk rotation with the head fixed in space or head rotation with the trunk fixed in space). It interacted with vestibular signals at the PIVC neurons either in an antagonistic or a synergistic manner, the latter meaning activation during rotation of the head in the same direction as that leading to activation induced by semicircular canal stimulation. 6. In addition to the direction-specific vestibular, visual, and neck receptor inputs, a rather complex somatosensory input to PIVC neurons exists, including responses to stimulation of mechanoreceptors of the skin, the muscles, and the joint receptors of legs and arms. Total body vibration also led to activation of some of the neurons.(ABSTRACT TRUNCATED AT 400 WORDS)