AMER. ZOOL., 33:424-433 (1993)
Neural Crest: Contributions to the Development of the
Vertebrate Head1
A N N C. GRAVESON
Department of Biology, Dalhousie University, Halifax, Nova Scotia B3H 4J1, Canada
SYNOPSIS. The neural crest is a major source of mesenchyme in the head,
but not the body, of the vertebrate embryo. For some of these mesenchymal derivatives, the differences between the normal fates of cranial
and trunk neural crest cells are not necessarily due to differences in the
potentials of the cells for the various derivatives, but reflect a lack of
interaction with appropriate inductive tissues. Chondrogenic potential,
however, is restricted to those axial levels which normally give rise to
cartilage. This chondrogenic subpopulation is not homogeneous; even
prior to neural crest cell migration, cells from different axial levels display
differences in migratory and morphogenetic abilities. While the events
which give rise to these segregations have never been examined, some
models have been proposed for the establishment of the neural crest itself.
within the neural folds are neural crest cells;
neural folds also contain presumptive brain
and epidermal cells (Brun, 1984, 1985).
Furthermore, neural crest cells can also arise
outside the neural folds, both from the neural plate and from adjacent ectoderm (Brun,
1981, 1985; Lumsden, 1988). In the head,
this adjacent ectoderm is placodal, and will
give rise to the sense organs, and some of
the cranial ganglia. Placodal ectoderm is
considered to be distinct from the neural
crest, despite some similarities in behaviour
and derivatives, and is discussed by Webb
and Nolan (1993).
ii) Neural crest cells do not remain in the
neural tube. At some stage, usually after,
but in some species before, neural tube closure, they begin an extensive migration along
specific pathways to their ultimate destinations. They do not emigrate at the same
time from all axial levels of the neurepithelium; migration usually begins at the
mesencephalic level, and progresses both
anteriorly and posteriorly from this point.
In those mammals which have been studied, however, neural crest emergence does
not follow this axial sequence (Morriss-Kay
and Tan, 1987).
iii) Finally, neural crest cells differentiate
1
From the Symposium on Development and Evoa wide variety of cell types, among
into
lution of the Vertebrate Head presented at the Annual
Meeting of the American Society of Zoologists, 27-30 which are pigment cells, with the exception
of those of the pigmented retina (which are
December 1991, at Atlanta, Georgia.
INTRODUCTION
In this review, I will discuss only briefly
the basic roles and functions of neural crest,
and direct the reader to the more detailed
accounts of Weston (1970), LeDouarin
(1982), and Hall and Horstadius (1988). This
paper deals with various aspects of, and
assumptions about, the mesenchymal
derivatives of these cells, which not only
play a major role in the development of the
vertebrate head, but whose production is
often considered a characteristic of head,
but not trunk, neural crest.
Despite its broad role in vertebrate development, there is no simple definition of the
neural crest. The only satisfactory definitions are functional: where the cells arise,
how they behave, and their ultimate fates.
Thus, the neural crest consists of those cells
which have combinations of the following
characteristics, none of which alone is sufficient to define the neural crest:
i) The cells are initially found in the neural folds, at the boundary between the neural
plate (neurectoderm) and the non-neural
(epidermal) ectoderm. However, not all cells
424
425
NEURAL CREST
formed by the neural plate), and the elements of the peripheral nervous system,
except for some cranial ganglia, which are
derived from ectodermal placodes. Pigment
and neuronal cells can and do arise from all
axial levels of neural folds, both cranial
(adjacent to the presumptive brain) and
trunk (adjacent to the presumptive spinal
cord). Figure 1 depicts the locations of these
axial levels in an amphibian neurula, as well
as the system of coordinates which will be
used to describe the axial levels of cranial
neural folds.
Neural crest cells also give rise to a large
number of mesenchymal derivatives,
including cartilage, bone, odontoblasts of
the teeth, and connective tissues. These
derivatives tend to be considered as a separate class, because all can also be derived
from mesoderm, except the odontoblasts,
and because their production is generally
considered to be the domain of cranial, but
not trunk, neural crest. However, it must be
noted that while this is generally true, the
production of mesenchymal cells is not
exclusive to the cranial neural crest. For
example, in amphibians, the mesenchyme
of the dorsal fin is derived from trunk neural
crest (Hall and Horstadius, 1988).
Detailed fate maps for the neural crest are
available for both amphibians and birds,
where labelled cells from different axial levels were followed to the individual skeletal
elements. Extirpations of segments of neu-.
ral folds from lamprey and teleost embryos
have also been performed to identify the
neural crest-derived skeletal elements, as
well as the axial levels from which they arise.
The results are remarkably similar in all
species studied to date (Hall and Horstadius, 1988). The entire visceral skeleton,
except for the second basibranchial, is neural crest-derived. Portions of the neurocranium are also neural crest-derived. The
only differences among the classes appear
to be in some elements which are mainly of
mesodermal origin. For example, while the
otic capsule appears to be entirely of mesodermal origin in amphibians, there is a neural
crest cell contribution in birds. Conversely,
the avian parachordal and basal plate cartilages are entirely derived from mesoderm,
although there is a nonessential neural crest
30°
150°
FIG. 1. System of coordinates used to describe the
axial levels of amphibian cranial neural folds, shown
here on a mid-neurula stage axolotl embryo. Cranial
neural folds are found at levels 0°-150°, while trunk
neural folds are at all levels posterior to 150°. Adapted
from Chibon (1966).
contribution in amphibians (in the absence
of neural crest cells, these elements will
develop normally; Chibon, 1966). Finally,
these labelling and extirpation studies have
also demonstrated similar regionalisations
of the skeletogenic neural crest; rostral skeletal elements originate from rostral levels,
caudal elements from more caudal levels.
Unfortunately, we do not yet have a detailed
fate map for the mammalian neural crest,
although current information tends to suggest that it is similar to other vertebrates;
cranial neural crest cells have skeletogenic
potential, and their migratory pathways not
only lead them to the visceral arches, but
the relationship between their rostro-caudal
origin and the various arches is similar to
that seen in the other classes (Morriss-Kay
and Tan, 1987).
FATE VERSUS POTENTIAL: CARTILAGE
Because of their extensive migration,
neural crest cells have ample opportunity to
contact and interact with a large number of
cells, tissues, and extracellular matrices. In
426
A. C. GRAVESON
fact, these interactions are essential for the
proper differentiation of skeletal tissues in
all species studied to date. However, the
inductive tissue is not always the same. In
amphibians, chondrogenesis from neural
crest cells always requires an inductive
interaction with pharyngeal endoderm. In
some species, such as the axolotl (Ambystoma mexicanum; Graveson and Armstrong, 1987) and Triturus alpestris (Epperlein and Lehmann, 1975), this is sufficient,
but in others there are additional requirements, such as dorsal mesoderm for Pleurodeles waltl (Corsin, 1975), or stomodeal
ectoderm for Ambystoma
maculatum
(Wilde, 1955). For the chick, the inductive
tissue is ectoderm. It is not known if these
different tissues are producing the same or
different signals, but cranial neural crest from
lampreys can be induced to chondrify using
amphibian head epithelia as the inductor
(Newth, 1956).
Pharyngeal endoderm is the only inductor required for chondrogenesis of the neural crest in the axolotl (Graveson and Armstrong, 1987). We have shown that all the
endoderm of the head is equally inductive,
but that neither trunk endoderm nor notochord (which is the inductor for somitic
chondrogenesis) has any inductive capacity.
Given that chondrogenesis requires contact with endoderm, and that inductive ability is found exclusively in the head, it is
possible that the trunk neural crest does not
form cartilage because it never comes into
contact with the inductive endoderm under
normal circumstances. Therefore, while the
trunk neural crest is not fated to form cartilage, the question arises as to whether it
has the potential to do so. This question has
been asked before, but the potential of the
neural crest has usually been tested by transplanting trunk neural crest into the head.
There is a basic assumption underlying this
approach: that the transplanted trunk neural crest cells are thereby exposed to all of
the inductive influences that head neural
crest cells normally encounter. However, this
assumption has now been shown to be
untrue.
For example, in the axolotl, after the presumptive chondrocytes of the branchial
arches leave the neural tube, they initially
migrate between the ectoderm and the
mesoderm (Fig. 2A, B), then move into the
branchial arches, surrounding the mesodermal core (Fig. 2C), and finally contact the
pharyngeal endoderm while continuing their
ventral migration (Fig. 2D) (Stone, 1922).
However, when trunk neural folds are
transplanted to cranial levels, the trunk neural crest cells do not follow the cranial
migration pathways (Fig. 3). In fact, there
appears to be very little migration, except
for a few pigment cells (Fig. 3B). Therefore,
transplanting trunk neural crest cells to the
appropriate cranial level will not necessarily
test their potential for chondrogenesis; the
cells cannot follow head migration pathways and thus cannot contact the inductive
endoderm, at least in the axolotl.
Since the chondrogenic potential of trunk
neural crest cells could not be tested using
heterotopic transplantations, its potential
was directly tested by placing it in intimate
contact with inductive endoderm in explant
culture. Under these conditions, >90% of
cultures containing cranial neural crest form
cartilage (Graveson and Armstrong, 1987).
Explants containing trunk neural crest never
formed cartilage. Trunk neural crest therefore does not have chondrogenic potential,
fortuitously confirming the conclusions
based on transplantation experiments (Chibon, 1966; Hall and Horstadius, 1988).
The anterior-most neural folds, known as
the transverse fold in amphibians (0°-30°;
Fig. 1), is also normally non-skeletogenic.
Indeed, it is often considered not to contain
neural crest cells at all, but to only form part
of the forebrain. Again, the lack of chondrogenesis may be due to a lack of potential
or to a lack of interaction with an inductive
tissue, a problem that remains unresolved.
Although we have never had cartilage
develop from cultures of transverse fold and
inductive endoderm in the axolotl, cartilage
has been reported to develop in explant cultures from another urodele, Pleurodeles waltl
(Cassin and Capuron, 1979), and two anurans {Xenopus laevis; Seufert and Hall, 1990;
and Discoglossus pictus; Cusimano-Carollo,
1972). This may reflect species differences
or some other factors, such as differences in
the tissues used, or different culture conditions.
NEURAL CREST
427
_^^to^J
FIG. 2. Normal migration patterns of cranial neural crest in A. mexicanum. A cranial neural fold (80°-15O°;
Fig. 1) was homotopically transplanted from a wild-type to an albino neurula. The neural crest cells can be
visualized through the pigmentless ectoderm of the host. See text for details, m: mandibular; h: hyoid; b: branchial.
Bar = 1 mm. Adapted from Graveson (1990).
between 30° and 70°, and the mandibular
teeth from those between 70° and 100°. The
fate map for odontoblasts therefore comprises the levels from 30° to 100°, which is
much less than that for the chondrogenic
levels, which extend from 30° to 150°. Based
FATE VERSUS POTENTIAL:
on the results of his transplantations of
TEETH AND FIN MESENCHYME
labelled posterior cranial and trunk neural
It is important to note, however, that the folds to normally odontogenic levels, Chinormal fate of cells is not always a reflection bon (1966) concluded that the neural crest
of their potential. One case in point is that cells from these levels did not have odonof another derivative of the cranial neural togenic potential, although 1 of his 30 trunk
crest, the odontoblasts, which produce the transplantations did give rise to labelled
dentine of the teeth. Chibon (1966), in map- odontoblasts.
ping the cartilaginous neural crest elements
Like chondrogenesis, tooth formation is
in Pleurodeles waltl, also mapped the origin also the result of a series of tissue interacof the teeth using heterotopic transplants. tions. Although the parameters of the inducHe showed that the odontoblasts are derived tion^) are not completely known in
from the same axial levels of neural folds amphibians, we have developed an explant
as the skeletal elements which support them. culture system which produces teeth in the
The palatine teeth arise from the folds majority of cases, when cranial neural crest
Thus, it appears that, for the axolotl at
least, the only neural crest which has chondrogenic potential is that which normally
contributes to the skeleton (30°-150°). In
this case, potential equals prospective fate.
428
A. C. GRAVESON
FIG. 3. Lack of migration of trunk neural crest following transplantation to cranial levels. A trunk neural fold
from a wild-type neurula was transplanted to levels 80°-l 50° (Fig. 1) of an albino neurula. The embryos in A
and B were at the same stages as those in Figure 2A and C, respectively. Bar = 1 mm. Adapted from Graveson
(1990).
429
NEURAL CREST
from 30°-100° is included. Using this system, we are testing the odontogenic potential of neural crest cells from different axial
levels. Although we only have preliminary
results at this time, it appears that odontogenic potential is much more extensive
than previously suspected. In fact, the
odontogenic potential of the neural crest
appears to extend even further posteriorly
than the chondrogenic potential. While cultures containing inductive endoderm and
cranial neural crest from known chondrogenic levels develop both cartilage and teeth,
there is a short segment immediately posterior to 150° from which teeth develop, but
cartilage does not (Graveson, M. M. Smith,
and Hall, in preparation). Lumsden (1988)
has reported similar results with cultures of
mouse trunk neural crest cells and inductive
epithelia, in which both teeth and bone are
formed. There is, therefore, a long segment
of neural crest whose odontogenic potential
is not normally realized due to an apparent
lack of interaction with the appropriate
inductive tissues; fate does not equal potential for the odontogenic neural crest.
This is also true for a number of other
neural crest derivatives. The dorsal fin of
amphibians is the result of an interaction
between trunk neural crest and the overlying epidermal ectoderm. Amphibians do not
have a fin on the head, but this is not because
of differences in the potential of cranial and
trunk neural crest, but because head ectoderm cannot participate in dorsal fin formation (Woerdeman, 1946). Similarly, in
the chick, where only cranial neural crest
normally forms mesenchymal derivatives,
it has been shown that early trunk neural
crest can form dermis and connective
(though not skeletal) tissue, given the right
conditions (Nakamura and Ayer-LeLievre,
1982).
These studies demonstrate that when the
potentials rather than fates of the neural crest
cells are considered, there does not appear
to be an absolute distinction between cranial and trunk, with the possible exception
of the chondrogenic subpopulation (Fig. 4).
The localization of derivatives depends not
only on the potential of these cells, but also
on the presence of the inductive tissues
required to elicit this potential.
F«TE
UTEITIU
FIG. 4. Comparison of axial levels of neural crest cells
which normally produce specific mesenchymal derivatives (left) with the axial levels of neural crest which
have the capacity to form them (right), in the axolotl.
The horizontal line delineates the cranial and trunk
levels of neural folds (150°). F: dorsal fin mesenchyme;
O: odontoblasts; C: chondrocytes.
REGIONALISATION OF THE
CRANIAL NEURAL CREST
The results of heterotopic transplantations, while not necessarily useful for testing
potential, clearly demonstrate that cells with
the same potential are not identical (see also
Langille, 1993). There appears to be a
regionalisation within the cranial neural crest
which is present prior to the onset of cell
migration. Posterior cranial neural crest did
not participate in tooth formation when
transplanted to anterior cranial levels
although the cells have odontogenic potential and were placed at axial levels whose
migration routes normally lead to inductive
tissues. Therefore, these cells must differ at
least in their ability to follow different
migration pathways. Similarly, branchial
arch crest cells will not form any skeletal
elements when transplanted to the level of
the anterior trabecular crest (Chibon, 1966).
Differences in the ability to follow migration cues are not the only differences present, however. Horstadius described 3 distinct levels of chondrogenic neural crest,
based on heterotopic transplantations in the
axolotl: trabecular (30°-70°), mandibular
(70°-100°), and branchial (100°-150°) (Hall
and Horstadius, 1988). The trabecular neural crest cannot form any of the visceral
arches, while visceral arch crest cannot form
trabeculae. This may be the result of differ-
430
A. C. GRAVESON
ences in migratory abilities, as described
previously. Finally, the mandibular and
branchial arch levels also appear to be distinct, although not because of migratory differences. Heterotopically transplanted neural crest cells will follow the appropriate
route for the new level, and will differentiate
into "arch" elements, but the elements
formed are not completely normal. The cartilages derived from branchial levels always
fuse with the basibranchials, even when they
are at mandibular levels. Conversely, the
elements derived from mandibular levels
never fuse with the basibranchials when
placed at branchial levels; they remain free.
The cells from a particular level do not
appear to have a fixed fate, but rather, seem
to have a limited range of possible morphological fates, with the ultimate element
produced being influenced by the local environment. In the chick, there appears to be
an early regionalisation of neural crest cells
destined to form the visceral arch elements,
while they are still in the neural folds. Heterotopically transplanted neural crest cells
apparently follow the normal migratory
route for the new axial level, and differentiate into the appropriate tissue, but the type
of element which is formed is not necessarily appropriate for either the new or the
original location; neural crest from levels
destined to form frontonasal structures gave
rise to mandibular elements when transplanted to the hyoid level, after migrating
to the hyoid arch (Noden, 1988). The possibility that neural crest cells may possess a
range of morphological fates is borne out
by Chibon's (1966) observations of regulation following neural crest extirpation in
Pleurodeles waltl; bilateral removal of segments less than 30° resulted in complete regulation, leading to normal skeletogenesis.
The replacement cells must have been
derived from flanking segments of neural
crest cells; if the missing cells were replaced
by new neural crest cells, regulation would
also be possible for longer extirpations,
which was not the case.
In summary, there are three ways in which
chondrogenic neural crest can be shown to
be segregated. Each of these successively
subdivides the cells into smaller subpopulations. The first is the restriction of chon-
drogenic potential to only those axial levels
which are normally chondrogenic. The second is the restriction of migratory abilities,
and the third is the restriction of morphogenetic potential.
This regionalisation within the cranial
neural crest stands in stark contrast to the
results of similar studies of heterotopic
transplantations within amphibian (Chibon, 1966) and chick (LeDouarin, 1982)
trunk neural crest, where the neural crest
cells apparently migrate and differentiate
completely in accordance with their new
locations.
NEURAL CREST FORMATION
Thus far, I have concentrated on the
chondrogenic neural crest, since it is a strictly
cranial derivative (with respect to both its
fate and potential), plays a major role in the
development of the vertebrate head, and is
an extremely well-studied system.
We have yet to determine how potential
becomes restricted to cranial levels. Do all
neural crest cells initially have chondrogenic ability which is subsequently lost from
trunk cells? Or are all neural crest cells initially non-chondrogenic with those in the
head subsequently acquiring this potential?
As a final possibility, perhaps cranial and
trunk neural crest are truly distinct, arising
via different processes. These questions have
never been addressed. This is not surprising,
since the processes responsible for neural
crest formation per se are not known. This
question, at least, has been addressed, but
there is no definitive answer.
It is generally believed that neural crest
formation is associated with neural induction, when the chordamesoderm (the future
notochord and adjacent mesoderm) induces
the overlying ectoderm to neuralise and
acquire anterior/posterior regionalisation
properties. Neural crest would arise either
as a direct result of neural induction, or as
the result of a process immediately subsequent to it. Several models have been proposed (Fig. 5), each of which is supported
by different experimental evidence. Since
most of the experimental evidence was
obtained using the axolotl, species differences cannot account for the differences in
the models.
431
NEURAL CREST
In one model, proposed by Raven and Direct
Kloos (1945, 1946; Fig. 5A), neural crest is
formed because of differences in the inducA "
ing tissues. The inductive field of chordamesoderm is presumed to be rather broad,
and there are quantitative differences in the
putative signal between the medial and lateral portions of the chordamesoderm. The
response of the ectoderm depends on the
quantity of signal; high signal levels give rise
to mid-neural plate, and low to neural crest.
In another model (Nieuwkoop et al, 1985;
B Albers, 1987; Nieuwkoop, 1985; Fig. 5B),
neural crest is formed because of differences
in the responding tissues. The inductive
chordamesoderm consists mainly or solely
of presumptive notochord, which induces
only the ectoderm directly overlying it (the
mid-neural plate). After this initial step,
neural induction proceeds homiogeneti- Subsequent
cally; neuralised ectoderm induces adjacent
ectodermal cells to neuralise, and the signals
are then propagated through the ectoderm
itself. With time, the competence of the
ectoderm to respond to the induction fades.
Neural crest is the result of a weakened
response, caused by the loss of competence.
In the indirect models (Fig. 5C, D), neural
crest formation is believed to be the result
of interactions between the products of neural induction. In other words, the neural
crest is formed at the junction between neuT
r
ral and non-neural ectoderm because these
tissues are apposed. Moury and Jacobson's
(1990) model (Fig. 5C) requires only the
presence of ectoderm next to neurectoderm, FIG. 5. Models for neural crest formation. A and B:
crest formation as a direct result of neural inducbut Rollhauser-ter-Horst (1977a, b, 1979) neural
tion; C and D: neural crest formation as a result of
believes that neural crest formation requires interactions occurring subsequent to neural induction.
the presence of additional, unidentified, tis- See text for details.
sue^) (Fig. 5D).
However, the question of anterior/pos- affects some, but not all, neural crest cells,
terior regionalisation of the neural crest is including the chondrogenic subpopulation
not addressed by any of these models. One (Graveson and Armstrong, 1990, in prepof the major stumbling blocks has been that aration). The mutant gene affects the ectothe number of steps involved has not been derm; chordamesoderm, whatever its role,
determined, possibly because specification is apparently normal (Graveson and Armand regionalisation of the neural crest (if strong, in preparation). We suspect that an
there is more than a single step involved) early segregation event is affected. Neural
occur in rapid succession. However, we think crest cells are established, and appear to be
that we may have a useful model for study- properly regionalised with respect to their
ing this (these) process(es), in the form of a migratory ability along specific pathways at
developmental mutant of the axolotl. This specific axial levels, but these apparently
mutation, aptly named premature death (p), normal neural crest cells appear to be inca-
TV
432
A. C. GRAVESON
pable of normal differentiation. Particularly
exciting is our recent finding that the lateralline placodes, which arise in the head ectoderm immediately adjacent to the neural
folds, are also affected by the p gene (Graveson, S. C. Smith, and Hall, in preparation).
This strongly suggests the presence of a
developmental (and possibly evolutionary)
link, which has long been suspected, between
the neural crest and ectodermal placodes.
Graveson, A. C. and J. B. Armstrong. 1987. Differentiation of cartilage from cranial neural crest in
the axolotl (Ambystoma mexicanum). Differentiation 35:16-20.
Graveson, A. C. and J. B. Armstrong. 1990. The
premature death (p) mutation ofAmbystoma mexicanum affects a subpopulation of neural crest cells.
Differentiation 45:71-75.
Hall, B. K. and S. Horstadius. 1988. The neural crest.
Oxford University Press, London.
Langille, R. M. 1993. Formation of the vertebrate
face. Amer. Zool. 33:462-471.
LeDouarin, N. M. 1982. The neural crest. Cambridge
University Press, Cambridge.
ACKNOWLEDGMENTS
Lumsden, A. G. S. 1988. Spatial organization of the
This work was supported by operating
epithelium and the role of neural crest cells in the
initiation of the mammalian tooth germ. In P. V.
grants to J. B. Armstrong and B. K. Hall
Thorogood and C. Tickle (eds.), Craniofacial
from the Natural Science and Engineering
development, Development, Vol. 103 (suppl.), pp.
Council of Canada. I thank B. K. Hall and
155-169. The Company of Biologists Ltd., CamS. C. Smith for their valuable comments
bridge.
and discussions.
Morriss-Kay, G. and S.-S. Tan. 1987. Mapping cranial neural crest cell migration pathways in mammalian embryos. Trends Genet. 3:257-261.
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