Neck motoneurons usually receive disynaptic excitation and inhibition from individual semicircular canal nerves. However, in motoneurons of some neck muscles, trisynaptic inhibition is evoked by stimulation of the contralateral vertical canal nerves. The present study was performed to analyze this pathway and the location and properties of the last-order interneurons responsible for mediating this trisynaptic inhibition from the contralateral vertical canal nerves to neck motoneurons in anesthetized cats. 2. Bipolar stimulating electrodes were implanted on the contralateral anterior (ACN), lateral (LCN), and posterior canal nerve (PCN), and postsynaptic potentials (PSPs) evoked by electrical stimulation of individual canal nerves were intracellularly recorded from motoneurons of the obliquus capitis inferior (OCI), longus capitis (LC), and rectus capitis posterior (RCP) muscles. Stimulation of the contralateral ACN evoked trisynaptic inhibitory PSPs (IPSPs) in OCI and LC motoneurons and disynaptic excitatory PSPs (EPSPs) in RCP motoneurons. Stimulation of the contralateral PCN evoked di- and trisynaptic IPSPs in OCI and RCP motoneurons and disynaptic EPSPs in LC motoneurons. Stimulation of the contralateral LCN evoked disynaptic EPSPs in all of the motoneurons examined. 3. To determine the pathway that mediates these trisynaptic IPSPs from the vertical canal nerves to neck motoneurons, a lesion was made in the lower medulla, and the patterns of PSPs evoked by stimulation of the three contralateral canal nerves were compared before and after the lesion. Interruption of the ipsilateral medial longitudinal fascicle (MLF) abolished all disynaptic EPSPs and IPSPs from the three contralateral canal nerves in OCI, LC, and RCP motoneurons. In contrast, trisynaptic IPSPs evoked by stimulation of the contralateral ACN or PCN remained unaffected by sectioning the MLFs bilaterally. Sectioning of the contralateral lateral vestibulospinal tract (LVST) eliminated the trisynaptic IPSPs in OCI and LC motoneurons evoked by contralateral ACN stimulation and trisynaptic IPSPs in OCI and RCP motoneurons evoked by contralateral PCN stimulation but did not affect disynaptic EPSPs and IPSPs. 4. Stimulation of the contralateral LVST in the lower medulla after sectioning the bilateral MLFs evoked disynaptic IPSPs in OCI, LC, and RCP motoneurons. Because the LVST only projects ipsilaterally, this finding indicates that the last-order interneurons that mediate the trisynaptic inhibition through the LVST are most likely commissural neurons located in the spinal cord. 5. To determine the locations of last-order commissural neurons terminating on OCI motoneurons, wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP) was injected into the OCI muscle nerve at C1.(ABSTRACT TRUNCATED AT 400 WORDS)
