Experimental determination of the primary trigeminal projections in lampreys

Abstract

The trigeminal complex of lampreys, like that of anamniotic gnathostomes, consists of profundus and 'mandibulo 'mandibulomaxillary' branchesa, s. The profundus branch possesses a distinct ganglion (supraorbital ganglion) separate from the ganglion (suboptical ganglion) of the 'mandibulomaxillary' brancheslL However, both ganglia send their processes into the medulla as a single trigeminal sensory root (Figs. 1A, 2A). The lamprey trigeminal complex differs from that of other anamniotes in that the anterior lateral line and facial ganglia are not closely associated with the trigeminal ganglia but are located beneath and within the optic capsule a,12. This separation clearly simplifies experimental analysis of the trigeminal projections, as the trigeminal ganglia can be lesioned or the sensory roots transected without damaging facial or lateralis inputs. Earlier studies claim that scattered lateral line receptors on the dorsal surface of the head are innervated by the trigeminal nerve~, ~. This condition has not been reported for any other vertebrate and has been interpreted as supporting the hypothesis that a lateralis component existed ancestrally in each branchiomeric cranial nerve. It is also claimed that the trigeminal nerve in lampreys projects directly to the cerebellum, the octavolateralis area and the funicular nucleus (presumed precursor of the dorsal column nuclei4,6). This trigeminal projection pattern has been interpreted as supporting the claim that the dorsal column nuclei, octavolaterlis area and cerebellum arose from a single somatic sensory column, and that lampreys essentially retain that primitive condition 6. Finally, a distinct mesencephalic trigeminal nucleus has not been identified in lampreys and is assumed to have arisen with the evolution of jawed vertebrates. These claims are of considerable importance regarding the evolution of the trigeminal system and were the impetus for the present study. The trigeminal ganglia in 5 transformed specimens (11-16 cm in length) of Ichthyomyzon unicuspis were unilaterally destroyed by transection or heat cauterization of the ganglia under MS222 anesthesia. The animals survived 3, 5, 7 and 12 days at 23 °C before they were reanesthetized, the brains dissected from the neurocranium and emersed in 107o formalin. The brains were embedded in 25~ gelatin and processed by the Wiitanen procedure 14 for demonstrating degenerating axons and their terminals. All the survival times were adequate to reveal degenerating trigeminal