Internuclear neurons of the ocular motor system of the larval sea lamprey.

Abstract

The internuclear neurons of the ocular motor system of lampreys are characterized here for the first time. Horseradish peroxidase (HRP), fluorescein-, or Texas red-(TRDA) coupled dextran-amine applied into the oculomotor nucleus of larval lamprey (Petromyzon marinus) retrogradely labeled two populations of contralateral abducens interneurons, one lateral and the other periventricular. Tracer application to the abducens nucleus anterogradely labeled thick contralateral fibers that specifically contact the medial rectus motor subnucleus by means of large boutons. Local application of TRDA to this subnucleus allowed identification of the lateral abducens interneurons as the origin of this projection. Electron microscopy of the medial rectus motor subnucleus showed large boutons bearing round synaptic vesicles that contact on the perikarya, as well as small boutons with pleomorphic vesicles. This lateral rectus (abducens) -- medial rectus (oculomotor) internuclear projection of lampreys appears to be similar to those involved in the coordination of horizontal eye movements in mammals. The periventricular abducens interneurons projected bilaterally to other oculomotor subnuclei. Tracer application to the abducens nucleus labeled a group of small interneurons in the ipsilateral dorsal rectus motor subnucleus. Anterograde labeling indicates that oculomotor interneurons project ipsilaterally to the ventral rectus abducens subnucleus, thus, corresponding to oculomotor interneurons found in mammals and frogs. The interneurons of the dorsal rectus and ventral rectus motor subnuclei are probably involved in the control of conjugate vertical eye movements. The present results strongly suggest that the internuclear coordination of conjugate eye movements appeared in the earliest vertebrates. The homologies of extraocular muscles of lampreys and gnathostomes were reexamined.