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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.

The ventral octavolateral area of lampreys contains three nuclei: the anterior, intermediate and posterior octavomotor nuclei, formed of large neurons that are contacted by thick primary vestibular fibres. We used horseradish peroxidase (HRP) or fluorescein-dextran-amine (FDA) labelling to study the projections of the anterior octavomotor nucleus (AON) in the larval sea lamprey, Petromyzon marinus. The tracers were injected either in the AON, the oculomotor nucleus or the rostralmost spinal cord. HRP injection in the AON labelled thick axons that coursed to the basal mesencephalic tegmentum, where most decussate and project to the oculomotor nucleus and the third Müller cell. Electron microscopy confirmed that AON axons contact with the contralateral third Müller cell and with oculomotor neurons. Some AON axons run in the mesencephalic tegmentum and the ventral diencephalon. An AON axon was observed to run close to the axon of the contralateral third Müller cell, establishing what appeared to be en passant contacts. HRP injection in the AON also revealed commissural fibres projecting to the contralateral octavolateral area. HRP or FDA injections in the oculomotor nucleus labelled both large and small neurons of the AON, mostly contralateral to the injection site, as well as of cells in the intermediate octavomotor nucleus, mainly ipsilateral. HRP injection in the AON or in the rostral spinal cord did not reveal any projections from the AON to the spinal cord. Our results indicate that the pattern of octavo-oculomotor connections in the lamprey is different from that observed in other vertebrates.

The medullary and spinal connections of the trigeminal nerve of larval sea lampreys Petromyzon marinus were studied by anterograde and retrograde HRP transport after application into the orbit. Three components were found, all of them ipsilateral: 1) The motor nucleus was undivided in the larva, and its neurons possessed a rich dendritic tree. The single motor root was well separated from the sensory root. 2) The descending root was laterally located, and its fibers ran compactly to spinal levels. 3) Most medullary and many rostral spinal dorsal cells were labeled. Dorsal cells, which were mostly multipolar, had numerous mutual contacts. Some dorsal cell processes contacted the fourth ventricle. The name "primary medullary and spinal nucleus of the trigeminal nerve" (PMSV) is proposed for these dorsal cells. Medullary dorsal cells were not labeled by applying HRP at the level of spinal nerves, but application to the vagus nerve did label some. The possible relationship of this nucleus with the mesencephalic trigeminal nucleus of jawed vertebrates is discussed.