Amphioxus neuroanatomy is important not just in its own right but also for the insights it provides regarding the evolutionary origin and basic organization of the vertebrate nervous system. This review summarizes the overall layout of the central nervous system (CNS), peripheral nerves, and nerve plexuses in amphioxus, and what is currently known of their histology and cell types, with special attention to new information on the anterior nerve cord. The intercalated region (IR) is of special functional and evolutionary interest. It extends caudally to the end of somite 4, traditionally considered the limit of the brain-like region of the amphioxus CNS, and is notable for the presence of a number of migrated cell groups. Unlike most other neurons in the cord, these migrated cells detach from the ventricular lumen and move into the adjacent neuropile, much as developing neurons do in vertebrates. The larval nervous system is also considered, as there is a wealth of new data on the organization and cell types of the anterior nerve cord in young larvae, based on detailed electron microscopical analyses and nerve tracing studies, and an emerging consensus regarding how this region relates to the vertebrate brain. Much less is known about the intervening period of the life history, i.e., the period between the young larva and the adult, but a great deal of neural development must occur during this time to generate a fully mature nervous system. It is especially interesting that the vertebrate counterparts of at least some postembryonic events of amphioxus neurogenesis occur, in vertebrates, in the embryo. The implication is that the whole of the postembryonic phase of neural development in amphioxus needs to be considered when making phylogenetic comparisons. Yet this is a period about which almost nothing is known. Considering this, plus the number of new molecular and immunocytochemical techniques now available to researchers, there is no shortage of worthwhile research topics using amphioxus, of whatever stage, as a subject.

Amphioxus has an assortment of cells and organs for sensing light and mechanical stimuli. Vertebrate counterparts of these structures are not always apparent, and a strong case can be made for homology in only a few instances. For example, amphioxus has anatomically simple but plausible homologs of both the pineal and paired eyes of vertebrates. Placodal and neural crest derivatives are, however, more problematic: the evidence for an olfactory system in amphioxus is only circumstantial and, despite the variety of secondary sensory cell types that occur on the body surface in amphioxus, none are obvious homologs of vertebrate taste buds, neuromasts or acoustic hair cells. A useful perspective can nevertheless be gained by examining differences in amphioxus and vertebrate development, specifically how each specifies and positions sensory precursors, controls their proliferation, and deploys them through the body. The much larger size of vertebrate embryos and the need to cope developmentally with increased scale and cell numbers may account for some key vertebrate innovations, including placodes and neural crest. The presence or absence of specific structural adaptations, like the latter, is therefore less useful for judging homology between amphioxus and vertebrates than shared features of specific cell types. It is also clear that the duration of embryogenesis in vertebrates has been significantly extended in comparison with ancestral chordates so as to incorporate events that would originally have occurred during the post-embryonic growth period, including events of neurogenesis. Consequently, no scenario for the origin of vertebrates can be considered complete unless it deals explicitly with the whole of the life history and changes to it.

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.

Motile larvae figure prominently in a number of past scenarios for chordate and vertebrate origins, notably in the writings of Garstang, Berrill, and Romer. All three focus on the motile larva of a primitively sessile tunicate ancestor as a vertebrate progenitor; Garstang went further in deriving chordates themselves by neoteny from a yet more ancient larva of the dipleurula type. Yet the molecular evidence currently available shows convincingly that the part of the tunicate larva that persists to the adult expresses only a subset of the genes required to specify a complete bilaterian body axis, and essentially the same appears to be true of dipleurula larvae. Specifically, both are essentially heads without trunks. Hence, both are highly derived and as such are probably poor models for any real ancestor. A more convincing case can be made for a sequence of ancestral forms that throughout their evolution were active, motile organisms expressing a full complement of axial patterning genes. This implies a basal, ancestral form resembling modern enteropneusts, although a pelagic organism at a hemichordate level of complexity is also possible. A reassessment is thus required of the role played by adult and larval tunicates, and of larvae more generally, in chordate evolution. Tunicates need to be interpreted with caution, since the extreme degree of modification in the adult may have been accompanied by reductions to the larva. Dipleurula larvae may retain some ancestral features (e.g., of apical, oral, and anal organization), but are otherwise probably too specialized to be central players in chordate evolution. Garstang nevertheless remains a key figure in the history of evolutionary thought for his innovative ideas on the relation between ontogeny and phylogeny, and the way in which major innovations in morphology and body plan arise.

The rostral epithelium of a newly metamorphosed juvenile of Branchiostoma floridae was examined at the EM level to confirm previous reports on its sensory cells. The majority of the sensory cells are of three types: two type I variants, with simple collars of unbranched microvilli surrounding their cilia, and one kind of type II cell, with an extended collar of repeatedly branched microvilli. The two type I variants differ in the structure and arrangement of the microvilli, basal body and rootlet, and the length of the cilium. Both variants are probably primary sensory cells (i.e. each has its own axon), but the data supporting this conclusion are much better for one variant than for the other. Type II cells are secondary sensory cells, with synaptic terminals borne on short extensions of the cell body. The presence of degenerating type II cells suggests that they may be subject to a regular process of loss and renewal. The results do not resolve the evolutionary issue of how amphioxus sensory cells relate to the epithelial sensory and receptor cells of vertebrates. Being primary, the type I cells resemble the supposed ancestral type more closely than do type II cells. Type II cells may be chemosensory, however, and should not be ruled out a priori as possible homologues of either primary or secondary chemosensory cells in vertebrates.