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The evolution and development of the dens of the mammalian axis.

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The Evolution and Development of the
Dens of the Mammalian Axis
Department of Anatomy, College of Physicians and Surgeons,
Columbia University, N e w Yorlz, N e w Yorlz 10032
Certain members of the extinct reptilian group from which mammals
evolved possessed both a dens and a n atlas body. Available paleontologic evidence
supports the conclusion that the dens evolved as an addition to the atlas body. Therefore, the dens is not homologous with the atlas body as is generally claimed on the
basis of supposed developmental evidence. The atlas body is large in the most primitive of living mammaIs, the monotremes, which also possess a dens of typicaI mammalian proportions. In metatherian and most eutherian mammals, both a dens and
an atlas body remnant of variable size are present. The development of the dens in
the Virginia opossum, Didelphis marsupialis, confirms the fact that the dens arises
from, but does not replace, the a t h body anlage. The dens evolved as a functional
replacement of the atlanto-axial articular processes which were lost when the mammalian atlanto-axial joint became specialized for rotational movement.
The dens of the mammalian axis is a
bony, peg-like process which projects
craniad into the atlas ring. The dens is
present in all living members of all orders
of mammals except Cetacea (whales,
dolphins). The loss of the dens in most
modern cetaceans is secondary, for it is
clearly present in fossil representatives of
this order which lived during early Tertiary
times (Kellogg, ’36). A few modern
cetaceans possess a vestigial dens.
The origin of the dens, both developmentally and phylogenetically, is often expressed in terms of homology with the
atlas body of primitive tetrapods. Textbooks of human anatomy usually state
simply that the dens represents “...the
displaced body of the atlas..
.the lost body of
and Peterson, ’66) or
the atlas. , (Lockhart et al., ’65). Other
texts imply or explicitly state that embryologic evidence establishes that the dens is
the homologue of the atlas body (e.g., Sisson and Grossman, ’53; Young, ’57; Romer,
’62; Crouch, ’65). The concept of an atlas
body-dens homology is one of the oldest in
comparative anatomy. Cuvier (1835) probably first expressed the general idea, but
he merely employed the tern “analogue”
(not homology). It is doubtful whether
Cuvier recognized the concept of homology
as later proposed by Owen, for homology
in its strictest sense implies evolutionary
continuity and Cuvier did not believe in
ANAT. REC., 164: 173-184.
“. .
evolution. Rathke’s (1839) statement, that
“Der Korper des Atlas aber verschmilzt mit
dem Epistropheus, und macht dann den
Processus odontoideus desselben ans,”
is perhaps the first positive statement of
the equivalency of the dens and atlas body.
This statement was made specscally with
regard to the axis of a snake (Coluber
natrix), and the mammalian condition was
not discussed; but it is obvious that to
Rathke, at least, the term odontoid process
could signify the atlas body of reptiles as
well as the dens of mammals (from which
it presumably derived its name). Whether
intentional or not, these terms were already synonymous. Bergmann (1845) subsequently compared the atlas and axis in
mammals, reptiles and birds, and was
probably the first to make an unequivocal
claim that the so-called 0s odontoideum of
mammals represents the atlas body of
lower tetrapods. The concept was fully
accepted and promulgated by Owen (1854),
Robin (1864) and other anatomists who
subsequently undertook a comparative
study of the atlas-axis complex.
Firsthand information on the development of the dens is limited. Such studies
as are available do not necessarily support the supposed strict homology between
the dens and atlas centrum. Macalister’s
(1894) findings are typical; he states that
Received Dec. 2, ’68. Accepted Jan. 21. ’69.
the cartilaginous dens forms from the
“perichondral body’’ of the atlas, i.e., from
material in a position expected of an atlas
body. But there is no statement that the
dens is the homologue of the atlas body.
Superficially, at least, the developmental
processes of the mammalian dens and the
reptilian atlas centrum are sufficiently
similar as to suggest strict homology. Both
are developed through sclerotomic resegmentation of the first and second cervical
sclerotomes and by addition of material
from a “pro-atlantal” sclerotomite. During
sclerotomic resegmentation in amniotes,
the caudal sclerotomite of the fist cervical
sclerotome combines with the cranial
sclerotomite of the second cervical sclerotome, thus forming the anlage of the
atlantal arches and body. The cranial
sclerotomite of the first cervical sclerotome
does not combine with another (caudal)
sclerotomite, but it left alone, so to speak,
to follow a variety of developmental
courses. In mammals, one such course
was thought by early workers to lead to
the formation of the anterior chondrification center of the dens (Goodrich, ’30;
Cave, ’38). The contribution of this socalled “pro-atlantal” sclerotomite in forming the tip of the dens has since been
confirmed in several mammals (Dawes,
’30; Sensenig, ’43), including man (Sensenig, ’57). In reptiles, the anterior half
of the atlas body is also formed by a “proatlantal” sclerotomite, i.e., the cranial half
of the first cervical sclerotome (Hayek,
’24). The dorsal half of this ‘‘pro-atlantal”
sclerotomite is almost certainly the anlage
of the proatlas ossicle in those reptiles
which retain this primitive feature. In
mammals a proatlas does not develop; instead, the arch anlage of the “pro-atlantal”
sclerotomite (as opposed to the body
anlage which comprises the tip of the
dens) enters into the formation of the
cranial edge of the atlas ring (cf. Sensenig,
Despite the apparent simple developmental history of the dens, opinions are
diverse as to the composition of the dens
in terms of the separate parts of the primitive atlas. For example, Romer (’62)
states that the dens also includes the intercentrum of the atlas, while Lessertisseur
and Saban (’67)admit the additional pos-
sibility that the axial intercentrum may
be completely lost. Miller et al. (’64) claim
.is morphologthat in the dog the dens
ically the caudal part of the body of the
atlas,. ,”, implying thereby that a cranial
part is not accounted for or is lost. The
paradox of the developmental evidence to
date is that although it seems to justify a
dens-atlas body homology, it does not precisely delineate the composition of the
dens or the morphological division between
the axis body and atlas body. Furthermore,
the developmental evidence is clearly insufficient as a guide to the phylogenetic
history of the dens which yields a more
precise account of its characteristic shape
and relations.
The present study attempts to summarize and to correlate the developmental,
evolutionary and functional aspects of this
important mammalian structure. The critical question is whether the dens, at any
time from its initial differentiation through
its completed development (both in the
embryological and evolutionary sense),
can be regarded as homologous with the
atlas body of reptiles and other primitive
tetrapods. Separate development of the
dens could possibly be construed as evidence for its homology with the primitive
atlas body. Conversely, its development as
a process arising from a post-dens oss&
cation would support the hypothesis that
the dens arises as an addition to the atlas
body, and is not homologous with it.
“. .
Fossil skeletal material pertaining to the
evolution of the dens among cynodont
therapsids (advanced mammal-like reptiles
from which mammals probably evolved)
was studied with the aid of a dissecting
microscope. This material includes : Thrinaxodon Ziorhinus, British Museum of Natural History nos. R. 511, R. 511a, and
3731; Galesaurus planiceps, University
Museum of Zoology (Cambridge, England)
no. R. 2721; and two specimens referred
to as Diademodon sp., D.M.S. Watson Collection nos. R. 204 and R. 205 (housed in
the University Museum of Zoology, Cambridge, England). Skeletal material pertaining to the development of the dens
among representatives of the orders of
modern mammals was studied by gross ex-
amination; this material is cited below by
museum number with the following abbreviations : AMNH, American Museum of
Natural History; YPMOC,Osteological Collection of Peabody Museum, Yale University.
The early development of the dens in
the opossum, Didelphis marsupialis, was
studied by light microscopic examination
of sagittal sections through the atlas and
axis of a 20 day and 25 day post partum
pouch young. Sections of the 20 day old
individual were bormwed from the Wistar
Institute Collection, Serial Catalogue No.
17683. The atlas and axis of the 25 day
old individual were serially sectioned at
7 CI and stained with hematoxylin and triosin. The skeleton of a second 25 day old
individual was stained with alizarin red S
and studied intact after the soft tissues
had been cleared.
and thus the vertebral arch halves are
capable of movement on the atlas body. In
addition, a pair of proatlas ossicles link
each atlas arch half with the occiput (pa,
fig. IB).
The structural evolution of the dens is
clarified by first reviewing the paleontological evidence. In pelycosaurs the basic
plan of the atlas-axis complex, as noted
above, is essentially reptilian. The atlas
body is comparable in size to other cervical
bodies, although its anteroposterior length
is shortened. Vertebral bodies in pelycosaurs are amphicoelous, i.e., possess a
deep, funnel-shaped concavity or fossa at
each end (Romer and Price, ’40). The
apex of each funnel-shaped fossa is directed toward the center of the body. The
apices of each pair of fossae communicate
by a small foramen through the middle of
the vertebral body. Thus each body enOBSERVATIONS
closes an hour glass shaped space which
In adult mammals the atlas-axis com- is open at either end. In embryonic
plex usually consists of only two bones - modern reptiles, the vertebral body enthe atlas and axis vertebrae. In living closes a similar “space” which is occupied
reptiles the atlas-axis complex may con- by the notochord. The embryonic cartilage
sist of as many as eight separate bones. is first laid down around the notochord
That the reptilian condition is phyloge- near the middle of the developing body;
netically antecedent to the mammalian ar- subsequent enlargement of notochord is
rangement is demonstrated by the fossil therefore restricted at this point, but is alremains of some of the reptilian ancestors lowed to continue towards either end.
of mammals, i.e., pelycosaurs (Romer and Thus in late embryonic stages the notoPrice, ’40). In pelycosaurs and in rela- chord is constricted intravertebrally and
tively generalized living reptiles, there are expanded intervertebrally. The differential
two bodies for each vertebral segment. growth of the notochord is recorded in the
The anterior of the two bodies is wedge- shape of the space within each vertebral
shaped and is smaller than the other; it is body. The initial site of pericordal choncommonly referred to as the intercentrum drification becomes the foramen; subseor hypocentrum (ic, fig. 1B). The second quent chondrification around the notobody lies posteriorly and is spool-shaped; chord which is increasing in diameter reit is usually referred to as the centrum or sults in the two funnel-shaped fossae
pleurocentrum and is homologous with within the body. Among modern reptiles,
the body of the mammalian vertebra. In the amphicoelous type of vertebral body
the following discussion, the anterior of (with a communicating foramen) persists
the two bodies will be referred to as the into adult life only in geckos, Sphmodon,
intercentrum, while the posterior will be and in the trunk vertebrae of turtles; tissue
designated (following common anatomical derived from the degenerated notochord,
usage) as the body or corpus. In addition often fibrous, occupies the fossae and the
to an intercentrum and body, the atlas of center of the intervertebral discs (Romer,
reptiles typically has an incomplete verte- ’56). In the folIowing discussion, the funbral arch. The two halves of the arch do nel-shaped fossae of amphiocoelous vertenot synostose sagittally above the vertebral brae will be referred to as notochordal
canal. Moreover, the articulation of each fossae as a reminder of both the developpedicle with the atlas body is diarthrodial, mental process and the enveloped tissues.
On the anterior aspect of the atlas body
in pelycosaurs, the notochordal fossa is
shallower and smaller in diameter than
in other centra (nf, fig. 1C). Moreover,
instead of occurring in the center of the
anterior aspect, it is located slightly above
center. This fossa is apposed by a similarly
structured fossa on the occipital condyle
(nf, fig. 1A). The eccentric position and
reduced size of the anterior notochordal
fossa is the most salient modification of
the atlas body which is otherwise typically
reptilian. A dens is certainly not present
at this phylogenetic stage. The next stage
in atlas-axis evolution is found among
cynodont therapsids, a group of advanced
mammal-like reptiles from which mammals probably arose ( c f . Crompton and
Jenkins, '68). In cynodonts all the separate elements of the pelycosaur atlas-axis
are retained (fig. lE), but with several
modifications. Among the most significant
of these is the loss of all vestiges of the
primitive notochordal fossa on the anterior aspect of the atlas body. In place of
the fossa, and slightly above it, occurs a
small protuberance which may be interpreted as an incipient dens, or odontoid
process (d, fig. 1F). If this interpretation
is correct, namely, that a dens can occur
as part of an atlas body of primitive, large
size, then the dens should not be considered homologous with the atlas body.
The identification of the small atlantal
protuberance of cynodonts as a dens would
certainly be questionable were there no
other corroborative evidence. However,
two independent lines of evidence support
the contention that the cynodont atlantal
protuberance is indeed a dens. The fkst
of these concerns the evolution of mammalian apical ligament which unites the
apex of the dens to the basioccipital bone.
Developmentally, this ligament is derived
from a notochordal remnant present at the
atlanto-occipital level (Hecker, '23; Goodrich, '30: fig. 61; Gadow, '33). The developmental fate of this section of the
embryonic notochord is therefore quite different from that between other vertebrae
where it contributes to the nucleus pulposus (Williams, ' 0 8 ) . In terms of special
relationships, the apical ligament is a
notochordal remnant situated dorsal to
other notochordal remnants represented by
each nucleus pulposus. In primitive fossil
reptiles, the notochordal remnant between
the first cervical vertebral body and the
occipital condyle was not situated dorsal
to all other notochordal remnants. Instead, the position of the notochordal fossae on the cranial aspect of the first cervical body and on the caudal aspect of the
occipital condyle is evidence that the notochordal remnant was in direct line with
those following ( c f .Romer, ' 5 6 ) . Both the
nucleus pulposus of mammals and the
inferred notochordal remnant of certain
primitive fossil and living reptiles occupy
a centric position relative to the vertebral
bodies, i.e., along a craniocaudal axis
through the centers of the bodies. The
mammalian apical ligament, however, represents a notochordal remnant that is eccentric in position, for in the adult mammal the apical ligament lies dorsal to a
cl,cz, corpus or body of first and second cervical
d, dens or odontoid process
fca, cranial articular facets of the axis
icl, icz, intercentrum of first and second cervical
j, joint between bodies of first and second cervi-
cal vertebrae
nf, notochordal fossa
oc, occipital condyle or condyles
pa, proatlas ossicle
Val, Val, vertebral arch of the first and second
cervical vertebrae
Fig. 1 Occipital condyle and atlas-axis evolution from pelycosaurs to mammals. Left
hand column: occipital views of the skulls of A, a; pelycosaur, Dimetrodon; D, a cynodont,
Cynognuthus; G, a monotreme, Omithorhynchus; L, a metatherian, Didelphis. Center column: left lateral views of atlas-axis components in B, a pelycosaur, Ophiacodon; E,
a cynodont, Galesaurus; H, axis of a tritylodont, Oligokyphus; I, axis of Omithorhynchus;
M, axis of Didelphis. Right hand column: anterior views of atlas body in C, Ophiucodon; F,
Galesaurus; dorsal view of axis body in J, Okligokyphus; K, Omithorhynchus; N, Didelphis.
Figures not to scale. A,B,C, after Romer and Price, '40; D, after Brofi and Schriider, '34;
H, J, after Kuhne, '56.
Pelycosaur stage
Cynodont stage
Tritylodont- monotreme stage
M e t a therian-eutherian stage
Figure 1
craniocaudal axis through the vertebral
bodies. The evolution of the apical ligament involves a dorsal displacement of the
atlanto-occipital notochordal remnant relative to all other remnants (i.e., the nuclei
puZposi) which retain their primitive, centric position.
The dorsal displacement of the atlantooccipital notochord segment was already
under way in pelycosaurs. The eccentric
positions of the notochordal fossae of the
occipital condyle and cranial aspect of the
atlas body (fig. 1A,C) in pelycosaurs certainly attest to this displacement. Moreover, the reduced size of the atlanto-occipital notochordal fossae relative to postatlantal fossae is evidence that the associated notochordal remnant was at least
smaller and perhaps altered in structure
and function. In cynodonts, the loss of
atlanto-occipital notochordal fossae r e p
resents the culmination of the pelycosaurian trend toward the size reduction of
these fossae. With the loss of the fossae,
what became of the notochordal remnant?
The well known developmental origin of
the mammalian apical ligament is proof
enough that the atlanto-occipital section of
the embryonic notochord was never lost.
In cynodonts, the dorsomedian protuberance on the cranial aspect of the atlantal
body is situated in a position which might
be expected of a notochordal fossa in an
advanced pelycosaur. Thus, the protuberance may be reasonably interpreted to have
been associated with the persistent atlantooccipital notochordal remnant. Likewise
the atlanto-occipital notochordal remnant
of the adult cynodont, no longer confined
within the notochordal fossae, must have
been different structurally and functionally
from other notochordal remnants which
retained their primitive relationship to
amphicoelous vertebrae. The protuberance
in cynodonts probably records the presence
of a ligament. Whether ligamentous or
not, the notochordal remnant in cynodonts
became associated with a convexity rather
than a concavity. In this sense the protuberance of cynodonts may represent an
incipient dens.
A second line of evidence supporting the
above interpretation is derived from other
fossil and recent forms representing structurally more advanced stages in the evolu-
tion of the dens. A fossil form of particular interest is Oligokyphus, a tritylodont.
The tritylodonts were a n advanced group
of mammal-like reptiles, although they
were not mammalian ancestors themselves. Kuhne ( ’ 5 6 ) has shown that
Oligokyphus possessed an atlas centrum
of large, primitive size (fig. lH,J); the
bodies of the atlas and axis vertebrae were
synostosed (fig. 1J). But in place of the
slight protuberance of cynodonts is a dens
of typically mammalian proportions, ie.,
a bony, peg-like projection (d, fig. lH,J).
In all other respects the bodies of this tritylodont’s axis and atlas vertebrae are similar to those in cynodonts. The only significant difference is the extension of the
cynodont protuberance into a “mammalian” dens. Since, on evidence of cranial
osteology, the tritylodonts are thought to
have been derived from cynodonts (Kuhne,
’ 5 6 ) , it is difficult to oppose the conclusion
that the cynodont protuberance is the precursor of the dens.
The fossil record of the earliest (it-.,
Triassic) mammals is represented mostly
by teeth and jaws; to date, no atlas-axis
components have been recovered. It is
probable, however, that the morphology of
the dens of earliest mammals was similar
to that in Mtylodonts. The evidence for
such a conclusion is based on the morphological similarity between the tritylodont
axis and the axis characteristic of the most
primitive mammals surviving today, the
monotremes. The order Monotremata includes both the platypus (Omithorhynchus
anatinus) and the spiny anteaters or
echidnas (various species of the genera
Tachyglossus and Zagbssus). In the platypus, for example, the dens is of typical
mammalian size and proportions (d, fig.
11). But between the dens and the axis
body (cz, fig. 11) is a bulbous ossification
(cl, fig. 11) which bears the articular
facets for the atlas. In position, shape and
relations, this ossification is extremely
similar to both the cynodont and the tritylodont atlas centrum. Moreover, it is
joined to the axis body along a distinct
joint (j, fig. 11,K) as in cynodonts and
tritylodonts. The conclusion is unavoidable that this ossification is the atlas body,
and that the dens is merely a process aris-
ing from it. Therefore, the two cannot be
The joint between the synostosed atlantal and axial bodies of pre-mammals and
monotremes delineates the boundaries of
originally separate but articulating ossifications. If the dens of advanced mammals,
i.e., marsupials and eutherians, represents
the only vestige of the atlas centrum in
these groups (as is generally claimed),
then a joint might be expected to occur at
the base of the dens. Such a joint would
represent the plane of synostosis of the
first two cervical vertebral bodies. In fact,
however, a joint is never found transecting
the base of the dens. In representative
genera of all living families of marsupials,
a joint transversely divides the ‘‘body” of
the axis in a plane posterior to the cranial
articular facets. In a few genera, the
joint transects the dorsolateral corners
of the facets (j, fig. 1M,N) but elsewhere
lies entirely posterior to them. The position of the joint posterior to the cranial
articular facets of the axis signifies that
the atlas ring retains its original primitive
articular relationship. In pelycosaurs and
cynodonts, the separate atlas arches and
intercentrum articulated with the atlas
body. Among modern mammals, the atlas
arches and intercentrum synostose to form
a bony ring which is the atlas; yet in
monotremes and marsupials, the atlas
ring still articulates with the primitive
atlas body, i.e., on facets lying anterior
to the transverse joint of the axis.
The axes of eutherian mammals are
morphologically rather variable between
orders and even between families. Yet
even in the most specialized forms, the
transverse joint of the axis does not occur
across the base of the dens. There is invariably a sizable osseous body caudal to
the dens and cranial to the transverse joint
which represents the atlas body- although much diminished in size and completely altered in form from that in cynodonts and monotremes (cl, fig. 2). The
tendency to reduce the atlas body is accompanied by a displacement of part of
cranial articular facets onto the actual
body of the axis. Thus, in some eutherians, the transverse joint bisects the cranial facets (fig. 2B). In other groups, the
greater part of the facets are borne by
the axis (fig. 2C). But even in the most
highly modified forms, such as man
(fig. 2F), the dens alone is not the sole
vestige of the atlas body. Even in those
mammals in which the cranial articular
facets are formed entirely from axis elements, a post-dens ossification - the
vestige of the original atlas body is retained.
The development of the dens in the
opossum, Didelphis marsupialis, may now
be evaluated in light of the paleontological
and comparative morphological evidence
which supports the conclusion that the
dens arises as an extension of the primitive atlas body. The earliest section available is from a pouch young 20 days post
partum (fig. 3). At this stage the completely cartilaginous dens is characterized
by two zones of hypertrophied chondrocytes. The dens is recognizable as a bulbous excrescence on the anterior of the
two zones. From the apex of the developing dens runs a connective tissue strand
which later forms the apical ligament.
There is no indication at this stage that
the dens develops as a structure independent of the cartilaginous anlage of the atlas
The second stage is from a pouch young
of about 25 days post partum (fig. 4). The
ossifying axis body is clearly set off from
that of C3 and from an anterior ossification (representing the atlas body) by the
developing intervertebral discs. The dens
is still cartilaginous, and is developing in
conjunction with a large center of ossification interpreted as serially homologous
with the other ossifying bodies. Parasagittal sections show that the dens is the apex
of a broad-based, triangular mass of cells,
of which the ossification center noted above
forms the largest part.
The third and fourth stages are represented by skeletal preparations of pouch
young estimated to be 50 and 70 days post
partum. In the 50 day old specimen (fig.
5A), the axis consists of four unfused
ossifications: the two vertebral arch
halves, the axis body, and the atlas body
with the dens. The atlas body is a triangular ossicle, the blunt apex of which is directly anteriorly. The differentiation of the
dens as a peg-like, bony structure has just
begun. In the 70 day old specimen (fig.
f ca
Fig. 2 Dorsal view of the axis in various juvenile mammals to show the position of the transverse
joint ( j ) . A an echidna (Tachyglossus aculeatus), YPMOC 1961. B, dog (Canis familiaris), six
months old, YPMOC 2600. C, pig (Sus s c f o f a ) ,YPMOC 1580. D, an armadillo, (Dasyps nouemcinctus), YPMOC 2333. E, 12 day old colt (Equus caballus), YPMOC 198. F, man (Homo sapiens),
AMNH 99-8594, approximately seven years old. Not to scale. Abbreviations as in figure 1.
SB), the vertebral arches have nearly
completed synostosis. The axis is not yet
synostosed to the vertebral arches nor to
the atlas body ossicle. The dens appears
as a process arising from the atlas body
ossicle of which it is small part.
The fifth and last stage is represented
by an osteological preparation of a young
adult opossum estimated to be six months
old (fig. 5C). In this specimen the dens
is but a small process arising from the
atlas body. The atlas body ossification, as
in other marsupials, forms the anterior
third of the axis body, and includes the
cranial articular facets. The joint between
the atlas body ossification and the axis
body is clearly visible.
The developmental history of the opossum dens demonstrates that the dens alone
cannot be considered the homologue of
the primitive atlas body, as is so often
implied or stated. It is indisputable that
the dens originates in conjunction with an
embryonic structure, the so-called atlas
body ossicle, which is homologous in position with the atlas body anlage of primitive tetrapods. The dens as a distinct process is most appropriately regarded as
Only a few authors have recognized the
relevance of the transverse joint of the
axis in delineating the axial and atlantal
bodies. W. H. Flower (1885) reported that
.if the axis [of a mammal] is examined
a year or two after birth, its body appears
to be composed of two parts, one placed in
front of the other, the fmt including the
odontoid process [dens] and the anterior
part of the body, the second all the remainder of the body." Flower drew no fur-
". .
Fig. 3 Sagittal section through the atlas and axis bodies of opossum (Didelphis marsupialis) pouch young 20 days post partum (Wistar Institute Ser. cat. No. 17683). x 35.
The two adjacent zones of hypertrophied chondrocytes represent the axis body (C2) and the
atlas body ((21). The developing dens is indicated ( d ) . Below and to the right of the dens
is a section through the atlas intercentrum which will form the ventral part of the atlas ring.
Fig. 4 Sagittal section through the atlas and axis bodies of opossum (Didelphis marsupialis) pouch young 25 days post partum. x 40. The two adjacent zones of ossification
represent the axis body ( C , ) and the atlas body (C,). The cartilaginous extension to the
right from the atlas body represents the developing dens ( d ) . Below the dens is a section
through the atlantal intercentrum which will form the ventral part of the atlas ring.
Fig. 5 The development of ossification in the
axis of the opossum, Didelphis marsupialis, to
demonstrate that the dens ( d ) arises in conjunction with the ossicle representing the primitive
atlas body (cI). Left column, lateral views; right
column, dorsal views. A, pouch young opossum,
YPMOC 5502, estimated to be 50 days post parturn; approximately x 3.25. B, pouch young opossum, YPMOC 5331, estimated to be 70 days post
partum; approximately X 3.25. C, young adult
opossum, YPMOC 243; approximately x 1.2.
ther conclusions from this observation,
except to propose that the posterior extremity of the odontoid ossification represents the “usual disk-like epiphyses of the
vertebral bodies.” Gadow (’33) objected
to these observations on the ground that
Flower “. . .looked upon the odontoid as
part of the axis centrum instead of a
centrum in its own right.. .”. In fact,
Flower did not reject the homology of the
odontoid and atlas body, but implied, although somewhat indirectly, that more
than just the odontoid process was homologous to the atlas body. Subsequently,
Rueger ( ’ 3 8 ) examined the axial joint patterns in a variety of mammals. He observed that in all cases at least part if not
all of the cranial articular facets of the
axis arose from the atlas body. But even
with this evidence in hand, he did not
challenge the concept of the atlas bodydens homology. More recently, Brocher
(’55) repeated Rueger’s observation that
“. . .Strenggenommen bildet der urspriingliche Wirbelkorper des Atlas nicht nur den
spateren Processus odontoideus, sondern
auch einen Teil des Epistropheuskorpers.”
The failure to exploit this evidence fully,
and to reveal the actual relationship of the
dens and atlas body, may be attributed to
a dependence on developmental evidence
The function of the dens will now be
briefly discussed with reference to its evolutionary origin. Rockwell et al. (’38) and
Slijper (’46) have shown that the mechanics of cervical vertebrae are analogous to
a loaded beam supported at one end only.
In quadrupedal animals, the bodies may be
regarded as compression-resisting members, and the vertebral arches, their processes and associated ligaments as tensionresisting members. In the evolutionary
lineage leading to mammals, the first two
cervical vertebrae became specialized to
permit an increased amount of cranial
mobility. Movement at the atlanto-axial
joint is virtually restricted to rotation of
the atlas (and cranium) on the axis. In
order to achieve atlanto-axial rotation, the
articular processes joining the atlas and
axis must be lost altogether because their
contact would only serve to prevent rotation. However, loss of the atlanto-axial
articular processes also entails loss of a
principal tension-resisting mechanism at
this joint. The weight of the head, which
tends to flex the cervical series, would be
the factor inducing a disproportionate
amount of stress at the atlanto-axial joint
relative to other cervical joints. The dens
and its associated ligaments in effect substitute for the lost atlanto-axial articular
processes. These structures do not inhibit
rotation because they reinforce the joint
along its axis of rotation. This arrangement prevents the atlas (and head) from
flexing on the axis, or, in other words,
acts as a tension-resisting mechanism (and
is probably less flexible than that of other
cervical articular joints).
In pelycosaurs the presence of well developed atlanto-axial articular processes
prohibited rotation at the atlanto-axial
joint. In cynodonts, however, the cranial
articular processes of the axis are vestigial
and the caudal process of the atlas are altogether lost. Atlanto-axial rotation was
clearly possible. The vestigial cranial articular processes on the axis probably represent the attachment of some ligamentous
or other connective tissue strand which
only incompletely sustained the tensional
forces generated by the weight of the head.
The remainder of the tensional forces were
undoubtedly accommodated by the incipient dens and its associated ligaments.
Many authors state that the dens acts as
an “axis” or pivot about which the atlas
rotates. While this analogy is convenient
in describing the movement involved, it
carries a misleading functional connotation. The atlas can and does rotate on the
axis in cases where the dens is congenitally
absent or separate from the axis. In reported cases of congenital absence of the
dens in man (cf. Fullenlove, ’54, and other
authors cited by him), the anomaly gave
no symptoms until, through accident or
during the course of normal exercise, more
than usual stress was brought to bear on
the head and neck. Subluxation of the
atlas, sometimes accompanied by neurological symptoms, was the common result.
Werne (‘57) reported similar cases in which
“insufficiency” of the transverse ligament
also permitted atlas dislocation. The normal function of such an atlanto-axial joint
in the absence of injury may be attributed
to the fact that the function of the dens
and transverse ligament is to reinforce
against flexing stresses. The vertical posture and shortness of the human neck
tends to minimize these stresses, and therefore the dens defect is manifest only when
such stresses are increased. In quadrupedal mammals, and especially in those that
employ powerful movements of head and
neck in feeding and other activities, the
selective disadvantages of a congenitally
absent or separated dens must be great.
I have been greatly aided by advice and
constructive criticism from Dr. E. S . Crelin
of the Department of Anatomy, Yale Uni-
versity School of Medicine, and by technical assistance from Mr. E. V. Newton.
Professor A. W. Crompton of Yale University generously provided facilities for the
completion of this study, and provided
helpful guidance in my study of cynodont
therapsids. I am grateful to Dr. F. R. Parrington, F.R.S., for the loan of fossil specimens from the University Museum of
Zoology, Cambridge, and to Dr. A. J.
Charig for the loan of specimens from the
British Museum of Natural History. I also
thank Dr. H. Shapiro of the American
Museum of Natural History for permitting
me to study certain human skeletal material in the Department of Anthropology.
I profited from discussions with Dr. Robert
Shapiro, M.D., during the early stages of
this study. I am grateful to Mr. R. J.
Demarest for preparing figure 1. Part of
this study was extracted from a doctoral
dissertation submitted to the Graduate
School, Yale University.
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