The PMC contains the anteriormost motoneurons in the cord and a number of large premotor interneurons. These cell types occur elsewhere in the cord, but not in such a large cluster. The important cells, from an organizational standpoint, are three pairs of large paired neurons (LPNs). These are extensively innervated by sensory inputs, both directly by primary sensory cells in the periphery and by synapses from the anteriormost RB cells (= B cells of Bone 1959, aRB cells in Fig. 8). The third pair, the LPN3s, are the most important and are cross-innervated in a bilaterally symmetrical fashion, an indication that they may be mutually inhibitory and hence capable of pacemaker function (Lacalli 1996; Lacalli and Kelly 2003b). Their output is to ventral compartment (VC, or fast) motoneurons via synapses and to DC (slow) motoneurons via an unusual class of intercellular junctions (juxtareticular junctions; see Lacalli 2002a). 

Fig. 8.

(A) Side view of the head of an amphioxus larva showing the position of the nerve cord (nc) in relation to the notochord (shaded). The head is highly asymmetric, with the mouth (heavy outline) on the left side and the pharyngeal (gill) slits (lighter out- lines) on the right.

(B) Oblique dorsal view of the anterior nerve cord showing its main landmarks and selected cells. Asterisks indi- cate the third pair of large paired neurons (LPN3s), which are putative locomotory pacemaker neurons. Landmarks include the frontal eye (fe), infundibular organ (io), lamellar body (lb), and primary motor center (PMC); the zone of neuromuscular junctions is shaded. This view extends to just beyond the boundary between somites 1 and 2, roughly the extent of the cerebral vesicle as anatomically de- fined and coextensive with the zone of Otx expression. The io marks the junction between the anterior and posterior parts of the cere- bral vesicle. The two regions differ in the shape of the central canal and the direction in which most cilia project into it. Other abbreviations and their corresponding terms are listed in Appendix A. See text for further details. Modified from Lacalli (1996).

The LPN3s are thus the best candidates for neurons exert- ing a direct controlling influence over both fast and slow swimming, which appear to have a similar neuromuscular basis in amphioxus and vertebrates (Bone 1989). Fast or es- cape swimming occurs in response to sensory inputs, which are a massive and redundant input to the VC system. The VC system also receives synaptic input from fibers in the postinfundibular neuropile and may be subject to additional paracrine input as well, via fibers passing through the neuropile, all of which provides an opportunity to modulate the response to sensory stimuli. In contrast, the slow system, which drives vertical migration, is almost devoid of synaptic input. Besides its link via junctions to the LPN3s, this path- way seems to be mainly under the control of the PPN2s mentioned above, a class of preinfundibular projection neu- rons that make repeated junctional contacts with the axons of the DC motoneurons. What this means in functional terms is not clear, but the circuitry (Fig. 9) suggests a switching device of some kind. Perhaps the escape response is sup- pressed during migration, which might itself be under circa- dian control. To assess such proposals, however, much more information is needed on the nature of the various types of preinfundibular neurons than is currently available. 

Fig. 9.

Schematic diagram of the main locomotory control cir-cuits in the anterior cord in young amphioxus larvae. The LPN3s (third pair of large paired neurons) are central control neurons that probably act as pacemakers. They receive external sensory inputs via several pathways and communicate with the two classes of motoneurons (DCm and VCm) by synapses or junctions as shown. There is extensive additional synaptic input (not shown) to the VC (fast) system, but almost none to the DC (slow) sys- tem except for junctions with a single class of preinfundibular neurons (type 2 preinfundibular projection neurons, PPN2s) and, more caudally (not shown), input from the dorsal ocelli. The function of the ipsilateral projection neurons (IPNs) is not clear, but they appear to provide some kind of link between the two systems. The postinfundibular (= tegmental) neuropile is a para- crine center, and the specific interactions among its components are not clear from the morphological data. Modified from Lacalli (2002a)

VC motoneurons in larvae resemble the somatic moto- neurons (SM cells) reported from the adult in overall mor- phology (cf. Lacalli and Kelly 1999; Bone 1959, 1960a). They are distributed rather irregularly in the anterior cord, with roughly equal numbers on each of the two sides, but there is no sign of bilateral pairing. They receive synapses on dendritic spines of varying length, located all along the axon, which confirms the supposition that the thin collaterals reported from adult motoneurons (Bone 1960a; Castro et al. 2004) are dendrites. It is useful to note that as the cord grows, and its neuropile expands, early dendrites would have to lengthen to maintain their original connections. Spines in the adult cord will thus be longer than those in the larval cord, and the longest spines are the earliest, and presumably most important, functional connections. Since the longest spines in the larva are postsynaptic to LPNs, this interpreta- tion supports the central role proposed for these cells in ini- tiating swimming.

It is not known whether the larval motoneurons persist through to the adult stage or whether the larval cells are replaced at some point in development. Lacalli (2000) has ar- gued for the former, based on the measured lengths of the motoneuron apices. These are axially elongated by an amount that roughly matches the axial expansion of the somites during development. 

DC motoneurons differ from VC motoneurons in being restricted to the anterior part of the cord, specifically somites 2–6. This restriction was first inferred from EM data, which showed that while axons project both rostrally and caudally from the last two members of the series, located in somites 4 and 5, none travel forward from more caudal segments (Lacalli and Kelly 1999). Confirming this, the amphioxus homolog of the estrogen-related receptor gene (ERR) selectively marks the same cells, revealing six pairs in the anterior somites and none more caudally (Bardet et al. 2005). Various molecular data support the idea of a segmen- tal or otherwise periodic repeat in the arrangement of cell types in the cord at the level of somites 2–7 (Jackman and Kimmel 2002; Mazet and Shimeld 2002), which is essen- tially the amphioxus homolog of the hindbrain. The DC motoneurons evidently form a compressed series, with more than one pair per segment. The true nature of patterning in this part of the anterior cord is still, therefore, not clear. It may be that some cell types show a strictly repeating seg- mental pattern, while others are more loosely controlled, or there may be several quasi-segmental patterns superimposed over one another. See Shimeld and Holland (2005) for further discussion.

In contrast to the detailed information now published on the microanatomy of the anterior cord, nothing comparable is yet available for more caudal regions. Swimming behavior changes as the larva grows, from a phased side-to-side bend- ing of the whole body in very young stages to what looks like a propagated wave of contractions (Stokes 1997). The latter implies a locomotory signal propagated from segment to segment, more like the situation in vertebrates. One inter- pretation is that the pacemaker circuits identified in the ante- rior cord of young larvae are involved in initiating locomotory contractions, but these are probably propagated through the more caudal segments by a series of local pace- makers. Regardless of details, it seems clear that the control circuits described from the anterior cord of young larvae cannot account fully for the complexity and dynamics of be- havior in older larvae."