The morphology of single medial vestibulospinal tract (MVST) axons was investigated by iontophoretic injection of horseradish peroxidase into single axons at the upper cervical cord in pentobarbital-anesthetized cats. MVST axons were identified by their monosynaptic responses to stimulation of the vestibular nerve and their direct responses to stimulation of the medial longitudinal fusciculus (MLF). Reconstructions of the axonal trajectory were made from 22 uncrossed and 19 crossed MVST axons at C1-C4. MVST axons ran in the ventral funiculus and gave rise to multiple axon collaterals to the upper cervical gray matter at different segments. These axons could be traced over the distance of 2.5-15.3 mm. Within these lengths, up to 9 axon collaterals were identified per axon (mean +/- s.d., 3.3 +/- 2.0, n = 41). Axon collaterals ramified in the gray matter several times and spread in a delta-like manner in both the transverse and horizontal planes. There were usually gaps free from terminal arborizations between adjacent axon collaterals, since the rostrocaudal extension of individual axon collaterals (mean = 820 microns) was very much limited in contrast to wide intercollateral intervals (mean = 1,510 microns). Axon terminals were distributed mainly in laminae IX, VIII, and VII, and sometimes in laminae VI-IV. Most abundant terminals were observed in lamina IX, including the ventromedial (VM), the spinal accessory (SA) nuclei and the nucleus dorsomedial to the VM nucleus (DM nucleus). A majority of individual axon collaterals provided some terminal branches to at least one of the above three motor nuclei. Axon collaterals projecting to laminae VIII-VI without terminals in the motor nuclei were rarely observed. Individual MVST axons had a preferential terminal distribution in each motor nucleus, but all three motor nuclei were covered by axon terminals of an ensemble of all MVST axons, indicating that all neck muscles innervated by these three motor nuclei are influenced by vestibular inputs through MVST axons. Most collaterals from a single axon produced circumscribed terminal arborizations in one or two common areas in the transverse plane (mainly in lamina IX) that were in line with one another in the longitudinal axis of the cord. This longitudinal arrangement of discontinuous terminal arborizations in lamina IX from a single axon may correspond to a continuous sagittal column of motoneurons for a particular muscle.(ABSTRACT TRUNCATED AT 400 WORDS)