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.

Development of vestibular afferent projections into the hindbrain and their central targets

“…In the frog, similar excitatory and inhibitory canal neurons of the medial and descending vestibular nuclei seem to derive from r5 to r6, while ipsilateral projecting neurons appear to be restricted to parts of r6 [91]. Only contralateral projecting vestibulo-ocular neurons have been reported in lampreys [35,49] suggesting that the ipsilateral projecting group that relates horizontal canal information [6,24,91] is either very small in lampreys or does not exist.…”

“…Overall, the wiring of the vestibular-ocular and vestibular-spinal projections seems to be extraordinarily conserved among vertebrates. However, some additional new tracts may have formed in jawed vertebrates and elasmobranches may have a reduction of second order projections owing to the simpler wiring diagram of vestibulo-ocular interactions [29,45,49].…”

The stepwise development of the lamprey visual system and its evolutionary implications

“…In addition, by inhibiting both horizontal and vertical excitatory burst neurons (EBNs), pontine omnipause neurons (OPNs) coordinate the horizontal and vertical saccades (Sparks, ). A difference in the innervation pattern of the extra‐ocular muscles between the gnathostomes and lampreys may also lead to changes in the microcircuitry of the gaze centres, although the internuclear connections between neurons associated with abducens motoneurons and the oculomotor medial rectus subnucleus, as well as other internuclear connections in larval lampreys are similar to those in the gnathostomes (González et al, ). In mammals, the medial and lateral rectus muscles contract for horizontal saccades and are innervated by the oculomotor and abducens nerves, respectively, whereas vertical saccades depend on the superior and inferior rectus muscles, which are innervated only by the oculomotor nerve (Sparks, ).…”

Development and Functional Organization of the Cranial Nerves in Lampreys

“…E,F; Fritzsch et al, ; Pombal et al, ); therefore, the putative presence of a direct vestibular input into trochlear and abducens motoneurons would shorten the reflex arc in these animals from three to two neurons (Fritzsch, ). Even so, a number of internuclear neurons between the abducens and the oculomotor complex were identified in larval lampreys (González et al, ; Meléndez‐Ferro et al, ), including oculomotor interneurons projecting to the abducens ventral rectus motor subnucleus (and probably also to the abducens lateral rectus motor subnucleus), lateral abducens interneurons projecting to the oculomotor medial rectus motor subnucleus, and periventricular abducens interneurons, which likely project to the oculomotor dorsal rectus and rostral oblique motor subnuclei.…”