Cross references:140706 - 2037 Win7 from XP
This 29 page paper raised a number of issues I'd like to come back to. Below is a brief, initial survey:
The most recent reviews on amphioxus
are by Ruppert (1997), for the general anatomy of the
animal as a whole, and Nieuwenhuys (1998), for the nervous
of de Quatrefages (Fig. 3), putative mechanosensory
organs consisting of primary sensory cells enclosed in a capsule
The epithelia that line the buccal and atrial cavities, as
well as the organs embedded within them, are also supplied
with an extensive set of neural plexuses collectively known
as the atrial nervous system. Though the system is more or
less continuous, it is usually subdivided on the basis of the
organs it innervates; i.e., there are buccal, velar, gonadal, parietal,
pterygeal, pharyngeal, and endostylar subdivisions,
and so on (Bone 1961).
The connection to the nerve cord via nerves 1–7
(1–8 according to Dogiel 1903; Kutchin 1913) is highly
asymmetrical. Nerves 3 and 4 on the left side are exceptional
in having contralateral branches that connect with the inner
buccal plexus on the right side. In addition, a subsidiary
branch from the contralateral branch of the left nerve 4 connects
to the right side of the velar plexus, while its left side
connects to nerve 5 by means of a caudal branch from that
nerve. This is all a consequence of the fact that the larval
mouth develops initially on the left side and is innervated
entirely by nerves emerging from the left side of the nerve
cord (Lacalli et al. 1999). The initial connections are then
retained during subsequent development, so the nerves are
dragged along as the mouth is repositioned.
Solitary receptors are widely distributed over the entire
epidermis but are most common in the region of the rostrum,
buccal cirri, and tail (Dogiel 1903; Franz 1923; Bone 1960b;
Stokes and Holland 1995a; Holland and Yu 2002). They
form small clusters in some instances (Sinnesknospen, Franz
1923; Schulte and Riehl 1977), especially along the buccal
cirri. The most common receptor cell types are referred to
by convention as types I and II (Schulte and Riehl 1977;
Bone and Best 1978).
Type I cells are primary sensory neurons
with an apical circlet of microvilli, a single cilium, and
a basal neurite. There are several subtypes, but all are probably
mechanosensors (Baatrup 1981; Lacalli and Hou 1999).
Their axons project to the CNS via the dorsal nerves; once
there, they travel along the cord in two fiber tracts, dorsal
and subdorsal in the terminology of Holland and Yu (2002),
which may correspond to the somatosensory and viscerosensory
tracts of Bone (1960a; see Fig. 4). The central axons
of type I cells reach considerable lengths, so an axon entering
the CNS via the first nerve can typically project caudally
to mid-spinal levels, at least in larvae (Holland and Yu
Little is known about the neurotransmitters released
by peripheral neurons, but there is evidence that at least
some type I cells are GABAergic (Anadón et al. 1998).
Anadón, R., Adrio, F., and Rodríguez-Moldes, I. 1998.
Distribution of GABA immunoreactivity in the central and peripheral nervous
system of amphioxus (Branchiostoma lanceolatum Pallas).
J. Comp. Neurol. 410: 293–307. Copied to: Amphioxus Neurotransmitters .
Ruiz, M.S., and Anadón, R. 1991b.
The fine structure of lamellate cells in the brain of amphioxus (Branchiostoma lanceolatum, Cephalochordata).
Cell Tissue Res. 263: 597–600.
Copied to: Lamellar Body = Pineal Eye .
Ruiz, M.S., and Anadón, R. 1991c.
Some considerations on the fine structure of rhabdomeric photoreceptors in the amphioxus, Branchiostoma lanceolatum (Cephalochordata).
J. Hirnforsch. 32: 159–164.
Link to Frontal Eye .
Type II receptors (Fig. 4) are secondary sensory cells with
synaptic terminals borne on short basal processes, usually
three per cell (Stokes and Holland 1995a; Lacalli and Hou
1999). Apically, they have a modified nonmotile cilium surrounded
by a collar of branched microvilli. This extensive
elaboration of the apical surface suggests a chemoreceptive
function, but essentially nothing is known for certain about
chemoreception in amphioxus, either in terms of structures
or physiology (Lacalli 2004).
The synaptic zones in each segment consist of two distinct
domains, the ventral and dorsal synaptic compartments
(Figs. 3, 4). Both utilize acetylcholine as a transmitter (Flood
Flood, P.R. 1974.
Histochemistry of cholinesterase in amphioxus (Branchiostoma lanceolatum, Pallas).
J. Comp. Neurol. 157: 407–438. Copied to: Amphioxus Neurotransmitters .
The ventral synaptic compartments are where the
deep, anaerobic, fast muscle cells receive their innervation.
The presynaptic motoneurons involved belong to a class of
cells that Bone (1960a) called somatomotor (SM) cells; they
may therefore also be called ventral compartment motoneurons.
They are found in the ventral parts of the grey matter
and have a tendency to cluster opposite the synaptic
contact zones, and each has a broad apical process connecting
it to the ventricular cavity. Some have internal vacuoles,
and this character, together with size and positional differences,
has been used to define several subtypes (Bone 1960a;
only one such type, the SM1 cell, is shown in Fig. 4). The
axons of the SM cells project laterally into the bundle of
somatomotor fibers adjacent to the synaptic zone of the ventral
The dorsal compartment is where the superficial, aerobic,
slow muscle cells of the myomeres receive their innervation.
The DC motoneurons are known from larvae (Lacalli and
Kelly 1999; Lacalli 2002a) but have not yet been identified
with certainty in adults. From the larval data, however, it
seems that the whole of the DC innervation along the nerve
cord may derive from motoneurons located in the anterior
cord at the level of somites 2–6 (see below). This is approximately
equivalent to the zone fated to become the IR of the
anterior cord, which extends from myotomes 2 to 4.
Thus, there are serially
(but not segmentally) repeated neurochordal synaptic
contacts at the base of the nerve cord. These are thought to
be cholinergic (Flood 1970), but their source within the
nerve cord has not been identified.
GABA, neuropeptide Y, and several other neuropeptides
have been detected in various cells loosely classified as
interneurons (Uemura et al. 1994; Anadón et al. 1998; Castro
et al. 2003)
Castro, A., Manso, M.J., and Anadón, R. 2003.
Distribution of neuropeptide Y immunoreactivity in the central and peripheral
nervous systems of amphioxus (Branchiostoma lanceolatum Pallas).
J. Comp. Neurol. 461: 350–361. Copied to: Amphioxus Neurotransmitters .
Second, a novel class of interneurons, Anadón’s cells,
has been identified in the vicinity of the ventral expansion
of the central canal (Anadón et al. 1998; see Fig. 5).
These are very small GABAergic cells interspersed between
the cell bodies of SM and VM neurons (cf. Figs. 4, 5).
Anadón et al. (1998) have suggested
that they might be comparable to the inhibitory Renshaw
cells of vertebrates.
Whether by light microscopy (e.g., Edinger 1906; Franz
1923; Ekhart et al. 2003) or EM (Meves 1973), it is difficult
to discern much about the neuronal and glial cells of the anterior
vesicle, since most cells are small and rather densely
stained and have few visible distinguishing features. Franz
(1923, 1927) therefore concluded that the entire anterior vesicle
consisted only of glial cells. However, GABAergic
(Anadón et al. 1998) and serotoninergic neurons (Moret et
al. 2004) have since been identified in this region in adult
Moret, F., Guilland, J.-C., Coudouel, S., Rochette, L., and Vernier, P. 2004.
Distribution of tyrosine hydroxylase, dopamine and serotonin
in the central nervous system of amphioxus: implications
for the evolution of catecholamine systems in vertebrates.
J. Comp. Neurol. 468: 135–150.
Copied to: Amphioxus Neurotransmitters .
Then, just ventral to
the Joseph cells and surrounding the dorsal expansion of the
central canal, there are bilateral, longitudinal bands of neurons
immunoreactive for urotensin and FMRFamide (Uemura
et al. 1994), GABA (Anadón et al. 1998), neuropeptide Y
(Castro et al. 2003), and catecholamines (the catecholaminergic
population I of Moret et al. (2004)).
Firstly, the more posterior alm cells (slightly
rostral to the junction of myomeres 1 and 2; black squares in
Fig. 6) seem to correspond to the anterolateral serotoninergic
cells of Holland and Holland (1993) that were also observed
by Moret et al. (2004). Slightly more anterior (black circles
in Fig. 6) is another group of immunocytochemically identifiable
cells within the alm group. This is the catecholaminergic
population II of Moret et al. (2004). There is some
uncertainty about the exact positions of these two cell
groups, however. Moret et al. (2004) place them adjacent to
the rostral half of the second myomere. In an independent
immunocytochemical study, H. Wicht (unpublished data) localized
them more anteriorly, adjacent to myomere 1 and
thus within the confines of the alm group (see Fig. 6). Wicht’s
study did confirm, however, that both the catecholaminergic
population II and the anterolateral sertoninergic neurons
have long descending projections to the spinal cord. In retrograde
tracing experiments, Fritzsch (1996) found pairs of labelled
cells in late larvae that may correspond to the
anterolateral serotoninergic cells, even though he did not
specify their exact position, but Ekhart et al. (2003), in a
similar study in adults, did not find such cells. Assuming the
latter result is a false negative, the cells and projections appear
to be real; it is only their exact axial position that is a
matter of some uncertainty.
Serotonin-containing neurons are absent in this region
(Moret et al. 2004), but a relatively large number of
GABAergic and peptidergic cells (Uemura et al. 1994;
Anadón et al. 1998; Castro et al. 2003) do occur. In addition,
there are four relatively large catecholaminergic cells (population
III of Moret et al. 2004) with translumenal processes
in the vicinity of the roots of the fifth dorsal nerves.
Uemura, H., Tezuka., Y., Hasegawa, C., and Kobayashi, H. 1994.
Immunohistochemical investigation of neuropeptides in the central
nervous system of the amphioxus, Branchiostoma belcheri.
Cell Tissue Res. 277: 279–287.
Despite the usefulness of the infundibular cells as anatomical
markers, there is no obvious transition in terms of
neuronal cell type at this point. Instead, cells of essentially
anterior character are found from the preinfundibular region
to the beginning of the PMC. "Anterior" here refers to cells
with irregular basal neurites that form repeated varicosities
containing mixed vesicle types and few, if any, synapses.
These are features that are generally associated with slow
transmission, often involving neuropeptides (Burns and Augustine
1995). Beginning in the PMC, most of the neurons
have well-defined axons and separate dendritic structures, either
arbors or spines (both occur), and synaptic junctions,
often with clear vesicles, predominate. This implies fast
transmission and aminergic or amino acid transmitters,
which is perhaps logical for neurons directly involved in the
locomotory control circuits.
The LPN3s are thus the best candidates for neurons exerting
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 escape
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 pathway
seems to be mainly under the control of the PPN2s
mentioned above, a class of preinfundibular projection neurons
that make repeated junctional contacts with the axons
of the DC motoneurons.
There are a number of specialized cell groupings at the
anterior end of the adult nerve cord that are not present in
early larvae, including various types of migrated cells described
above from the adult IR. Judging from the time that
the anterolateral serotoninergic cells first appear (Holland
and Holland 1993), these cell groupings probably develop in
the late larval phase or during metamorphosis. Despite the
proliferative activity this entails, the anteriormost region
fails to thicken as much as the rest of the cord, so the CV
progressively disappears as an externally recognizable zone.
Of the late-developing cell groups, the dorsal (population I)
dopamine-containing cells reported by Moret et al. (2004)
are especially noteworthy. These are as dorsal and anterior
as one can get in the nerve cord, which is precisely where a
telencephalic homolog would be predicted to form if
amphioxus had one. For this and other reasons, Lacalli (2004)
suggested that the population I cells may represent a primitive
version of the olfactory bulb.
CotA AmphAuth NrvSysStrDevEv