Landmarks in the Anterior Central Nervous System of Amphioxus Larvae

Abstract

The anterior end of the dorsal nerve cord of amphioxus is described at the 3-4 gill slit stage based on serial transmission electron microscopy and three-dimensional reconstruction, with special attention to structures that are potential landmarks for comparing amphioxus with other chordates. The larval nerve cord is divisible, at approximately the level of the first somite, into a short anterior region, the cerebral vesicle (c.v.), and an extended posterior region that is thought to include homologues of the vertebrate hindbrain and spinal cord. The c.v., in turn, has an anterior part with a tubular neural canal and a posterior part with a keyhole-shaped neural canal similar to that found in the rest of the cord. The junction between these two parts of the c.v. is marked by a cluster of infundibular cells. The anterior c.v., whose cells have cilia that point anteriorly, includes (i) a structure we call the frontal eye, consisting of a pigment spot and transverse rows of putative receptor and nerve cells, and (ii) several small ventral commissures bridging the major nerve tracts that run ventrolaterally along either side of the nerve cord. The posterior c.v., in contrast, contains cells whose cilia point posteriorly, and includes (i) the beginnings of the floorplate, which continues posteriorly through the rest of the nerve cord, (ii) the dorsal lamellar body, made up of cells with cilia that expand into flattened lamellae, and (iii) a large ventral commissure that incorporates fibres arising from cells of the lamellar body. Where probable homologues of c.v. structures can be identified in vertebrate brain, they are found in the diencephalon, which suggests the c.v. and the vertebrate diencephalon are, to a degree, homologous. On structural evidence, the frontal eye and the lamellar body are both ciliary photoreceptors, contrasting with the microvillar ocelli (organs of Hesse) distributed along most of the rest of the nerve cord. In young larvae the lamellar body is large and conspicuous. We suggest it functions as a high sensitivity, non-directional photoreceptor. The frontal eye is smaller, but organizationally more complex. We suggest it functions as a low sensitivity directional photoreceptor. The frontal eye is potentially of considerable interest from an evolutionary standpoint. Two issues are discussed: (i) that it is sufficiently similar in structure and organization to the paired eyes of vertebrates to indicate homology; and (ii) that its position at the extreme anterior end of the cord, together with structural and histochemical evidence, suggests it may derive from the apical organ, an evolutionarily ancient structure marking the embryonic anterior pole in diverse invertebrate phyla, whose homologue in chordates has hitherto not been identified.