The primary afferent pathway of extraocular muscle proprioception in the pigeon

Recent physiological experiments in our laboratory suggest that extraocular muscle proprioceptive signals are involved in oculomotor control in the pigeon [e.g., Knox and Donaldson (1993) Proc. R. Soc. Lond. B 253, 77-82]; the present results provide information about the primary afferent pathway involved in these actions. In other physiological experiments [Hayman et al. (1993) Proc. R. Soc. Lond. B 254, 115-122] we have shown that extraocular muscle afferent signals modify vestibularly driven neck reflexes in the pigeon; the present results suggest an anatomical substrate for these effects. The localization of the cell bodies and of the central terminations of afferent fibres from the extraocular muscles of the pigeon was examined using transport of horseradish peroxidase. The results showed that primary afferent cell somata subserving extraocular muscle proprioception are located within the ipsilateral trigeminal ganglion. The presence of heavily labelled brainstem neurons reported in a previous study [Eden et al. (1982) Brain Res. 237, 15-21] was confirmed; however, these cells were shown to be accessory abducens motoneurons innervating the quadratus muscle, and presumably the pyramidalis muscle also, and not proprioceptive afferent somata as had been suggested. The central projections of extraocular muscle afferent neurons were found consistently in a restricted area of the external cuneate nucleus. This is in contrast to findings in a number of mammals in which the terminal label has been seen to cluster in portions of the spinal trigeminal nucleus. The presence of a lateral trigeminal tract in the pigeon, through which the afferent axons course, which terminates exclusively in the ventral portion of the external cuneate nucleus may explain this finding.