The cortical connections of two vestibular fields [parieto-insular vestibular cortex (PIVC) and area 3aV] were studied in the squirrel monkey (Saimiri sciureus) by means of retrograde tracer techniques. Small iontophoretic or pressure injections of horseradish peroxidase (HRP), wheat-germ-HRP, Nuclear Yellow, and Fast Blue were administered to the cytoarchitectonic areas Ri (PIVC), 3aV, the parieto-temporal association area T3, the granular insula (Ig), and the rostral part of area 7 (7ant). The injection sites were physiologically characterized by means of microelectrode recordings and vestibular, optokinetic, or somatosensory stimulation: Area Ri is the region of the parieto-insular vestibular cortex (PIVC) as defined in macaques. The neck-trunk region of area 3a (area 3aV) also contains many neurons responding to stimulation of semicircular canal receptors. Some neurons of area T3 bordering on the PIVC also receive vestibular signals, but most neurons in area T3 responded preferentially to large-field optokinetic stimulation and not to vestibular stimulation. In none of the areas mentioned were responses to otolith stimulation found. The PIVC receives inputs from frontal and parietal cortical areas, especially areas 8a, 6, 3a, 3aV, 2, and 7ant. Area T3 receives signals from the insular and retroinsular cortex, various parts of area 7, visual areas of the parieto-occipital and parieto-temporal regions (area 19) and from a sector of the upper bank of the temporal sulcus (STS-area). The cortical afferents to area 3aV stem from areas 24, 4, 6, 7ant, from other parts of the primary somatosensory cortex, the secondary somatosensory cortex (SII), the retroinsular cortex (Ri), and the granular insula (Ig). In the border region of the areas 2 and 7ant, labelled neurons appeared after injections into both the PIVC and the area 3aV. This region is presumably the homologue to the vestibular area 2v of the macaque brain. In all regions cells within the contralateral cortex were less frequently labelled than cells in the homologous structures of the ipsilateral hemisphere. The cortical system for processing vestibular information about head-in-space movement consists mainly of the reciprocally interconnected areas PIVC and 3aV, and most likely of border regions of area 2 and 7ant. This "inner cortical vestibular circuit" also receives signals from two other cortical sensory systems, the somatosensory-proprioceptive system mediated by the primary somatosensory cortex and the visual movement system (optokinetic or visual flow signals). These visual movement signals reach PIVC via area 19 and area T3.(ABSTRACT TRUNCATED AT 400 WORDS)