Single- and multiple-unit recordings were made from nerve cells located in the different nuclei of the brainstem vestibular nuclear complex (VNC) of anaesthetized squirrel monkeys (Saimiri sciureus) by conventional stereotaxic techniques. After neurons responding to semicircular canal stimulation in a yaw, roll, or pitch direction or to otholith stimulation were identified, small amounts of retrograde tracer substances were deposited at the recording sites. Up to three different tracers were administered to different parts of the VNC in the same animal (Fast Blue, HRP-WGA, and Rhodamine-dextranes). After adequate survival times, the animals were sacrificed. Following histological processing, the cortical grey matter was screened systematically for cells labelled with the retrograde tracers (fluorescence microscopy or light microscopy for HRP processing). Labelled nerve cells which clearly project to the VNC directly were found predominantly in the cytoarchitectonic layer 5 of seven different cortical areas: 1) The parieto-insular vestibular cortex PIVC, which in squirrel monkeys consists mainly of the medial area Ri and parts of the anterior area Ig; 2) area 7ant, which presumably corresponds to the macaque area 2v; 3) area 3aV, a vestibular field of area 3a; 4) the temporal area T3 bordering on area Ri; 5) the premotor area 6a; and 6, 7) the areas 6c and 23c of the anterior cingulate cortex. The PIVC, area 7ant, and area 3aV form the "inner cortical vestibular circuit" (Guldin et al.: J. Comp. Neurol. 326:375-401, '92), while the other cortical areas mentioned also have direct projections to the structures of the inner cortical vestibular circuit. It is speculated that the direct projections of the cortical vestibular structures to the brainstem vestibular nuclei regulate the vestibulo-ocular, the vestibulo-spinal, and the optokinetic reflexes mediated through the VNC, thus preventing counteractions of these reflexes during voluntary, goal-directed head movements or locomotion.