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The origin of the vertebral and external carotid arteries in birds.

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Department of A n a t o m y , Harvard Medzcol
Since, iip to the present time, iiivestigatioii of certain cephalic arteries of bird embryos has been restricted to familiar
carinate species, it has seemed desirable to present aii account of the development of these blood vessels i n such a 5
widely divergent species a s Struthio-a
procedure oiily recently made possible through the acquisition of a graded
series of ostrich embryos collected by Prof. E. A. Boydeii,
under whose direction this work has been conducted.]
The series coiisists of twelve embryos ranging from 7 to
18 mm., tlie fonr oldest of whicli (the 12-, 13.5-,I&, and 18-mm.
stages) a r e so evenly spaced as to show, when reconstructed,
a more detailed picture of this stage of development than has
yet been recorded f o r any other avian species. The most
striking feature of this period, as in other birds, is the shifting of arterial trunks in response to the elongation of the
neck, by virtue of which tlie terminal branches acquire more
direct coniiections with the main blood stream. Three sets of
arteries a r e especially involved in this process, each of whicli
will be described i n turn, namely, the dorsal segmental, the
subclavian, a i d the external carotid arteries. The chaiiges
* This series 11:~salready h e n utilized t o compare the development of the cloaca
in ostrich eiiibryos with siwh other birds as the pheasant, duck, chick, and tern
(Boyden, ’ 2 2 ) . The present paper represents a portioii of a more elaborate
study, undertaken by thc writer i n conjunction with Doctor Boyden, which has
for it,s object a detailed comparison of the fire-day chick with the corresponding
stage of the ostrich.
T H E .\.\iA’I’Oitl~CdT~ RLCOIW. 3’01..
4UGUST, 1 9 2 6
:33, NO. 4
which the subclavian vessels undergo are remarkably like
those to be found in flying birds, but the development of the
other two groups presents striking modifications not yet reported in any other amniote. Another conspicuous difference
consists in the precocious atrophy of the left aortic arch,
which has completely lost connection with the ventral aorta
by the 12-mm. stage, so that its absence is to be noted in all
reconstructions shown in this paper.2
A t the time when the left fourth aortic arch of the ostrich
becomes detached from the ventral aorta, the dorsal segmental arf eries consist of a continuous series of vessels, the
first of which, the hypoglossus artery, is associated with the
third or last occipital nerve root (Occ., fig. 3 ) . Already the
simple metameric arrangement of earlier stages is undergoing
modification, as indicated by the consolidation of adjacent
segmental arteries into several groups following the downw a r d displacement of their aortic ends (nos. 4-5, 6-8,
and 10-13 of this particular embryo). By the 16-mm.
stage (fig. 4) the relative shifting of aorta and spinal cord
1x1s become so pronounced that the bifurcation of the aorta
now lies a t the level of the fourteenth slpinal segment instead
of opposite the seventh, a s in the 12-mm. stage. Accompany111 chick embryos the left fourth aortic arch becomes detached froin the
vmtral aorta shortly after the sixth day, being present and patent at five days
and twenty-thrce hours (15 nim., H. E. C. 2074), but existing only as a detached
iemnant a t six days and two hours (16 inm., 15. E. C. 1950). I n most other bird
riiibryos in tlic Harlard Collection a similar condition exists, the arch still being
picsrnt, though smaller, at 12.2 mm. (pheasant, 2217), and 13.5 min. (duck,
3 2 0 0 ) . T n thi, wries of ostrich embryos i t becomes detached between the 10.6-mm.
and 32-mm. stages (H. E. C. 2211, 2242), the discrepaiicy between the ostrich
and these other species being greater than a t first appears wheii we consider
that tlic iiirul~ationperiod of the ostrich (forty-two days) is twice that of the
<.hick. The only apparent exception t o this generalization (among available
is the common tern, in which the fourth left arch loses connection a t
10.2 nim. But since the tissues and organs of the 12-mm. ostrich are much less
differentiated than those of the 10.2-mm. term, one may still sag that the left
arch of tlic ostrich is interrupted relatively much earlier than in the tern or 111
a n y of the other flying birds inentioncd above.
ing this extraordinary shift in position and probably as a
result of it, a peripheral chain of anastomoses develops between adjacent segmental arteries, by means of which the
distal portions of the whole series receive their chief supply
of blood through the first spinal segmental artery (8-1,
fig. 4).
Subsequently, the primary stems of all the other segmentals,
as f a r back as the subclavian (no. 20), will become attenuated
and atrophy (fig. 5).
This chain of anastomoses is the forerunner of the cervical
vertebral artery. Its exact mode of origin seems not to be
clearly understood in any species of birds hitherto studied.
I n the ostrich the critical period lies between the 12- and
13.5-mm. stages. I n the former embryo (fig. 3) the vertebral
artery is not present, but in the latter (fig. 1) it consists of a
longitudinal anastomosis connecting the first four spinal segmental arteries. I n the 16-mm. stage (fig. 4) it extends continuously to the fourteenth (with one interruption). It can
thus be said in the ostrich to originate at the anterior end of
the segmental series and extend progressively and rapidly
In ostrich embryos the order of events in its formation
seems t o be as follows. The first premonition of a change
is the enlargement and peripheral dilation of the first spinal
artery (i3-1, fig. 3). Why this artery should be larger than
the hypoglossus artery or the second spinal is an obscure
point. I n the youngest ostrich embryo of the collection (a
7-mm. stage), the first spinal is larger even then than the two
hypoglossus arteries in front of it or the spinal segmentals
immediately below it.3 This advantage, however secured,
seems to be held, f o r , as the succeeding segmentals beginning with the second successively drop out (figs. 1 and
4),the first artery actually increases in diameter. The same
is true in the rabbit (Hochstetter, '90, pl. 21, fig. 2) and in
Its relation t o the anterior spinal artery (the continuation of the basilar)
cannot be a factor, because the hypoglossus artery of the 7-min. stage is also coniieeted with it, and we know in the human that both arteries are equally nrell
developed a t thc 4.9-mm. stage (Ingalls, '07).
man (Elm, ' O i ) , although in these mammals the first segmental, as the root of the cervical vertebral artery, is eventually replaced by the seventh. The second and third steps,
repeated serially from the first to the twentieth segments, are,
i*espectively, the sinus-like enlargement of the upper end of
each spinal segmental and the appearance of a loiigitudinal
anastomosis connecting these adjacent sinuses. Evidence for
the precedence of sinus formation over that of anastomosis
is provided by the 13.5-mm. stage (fig. 1 ), in ~ h i c hthe swellings appear on the fifth and sixth segmentals before there is
any indication of longitudinal connection. The fourth step is
the atrophy of the aortic ends of the second l o iiineteeiith
segmentals following the diversion of tlie blood stream along
the new vertebral artery. In the 13.5-mm. embryo (fig. 1)
only the second has atrophied; by the 16-mm. stage (fig. 4)
the third and fourth segmentals have gone, and liy the 18-mm.
stage (fig. 5) all in front of the subclaviaii (excepting the
first) have dropped out. Rut this is not all. Whereas in
mammals, the first segmental artery drops out, leaving the
subclavian as the permaiieiit source of the vertebral artery,
i n the ostrich the first segmental retains its I-& as the priiieipal feeder of the peripheral portion of the cervical segmental
vessels. Finally, as the neck elongates and carries this artery
farther away from its aortic supply, it acquires a secondary
coiiiiectioii with the dorsal carotid (y, fig. 5 ) ; as a consequence
of which its primary root ( " ) begins to atrophy. Although
oiir series contains no older embryos, it is presumed that this
iiew origin represents the permanent position of this artery.
In flying birds the development of the verteliral arteries
I-epreseiits a highly specialized modification of the simple
plan found hi the ostrich. I n spite of the excelleiit work of
Twining ('06) and Krassnig ( '13), the history of the vertebral
artery in chick embryos is incomplete. We have been obliged
t o make several recoiistructioiis to fill the gap and recoiicile
the two accounts. One of these (fig. 2 ) shows the first change
iii the primitive pattern of the dorsal segmental arteriesthe coiisolidatioii of the first five (sometimes six) spinal seg-
Fig. 1 Graphic reconstruction of a 1 3 5 r n t i i . ostrich embryo, showing the
early stages in the formation of the vertebral artery (8-1) and the shifting of
the dorsal external carotid from the top of the third aortic arch (D') along
the course of the dorsal carotid artery t o a secondary position (D*).
Fig. 2 Graphic reconstruction of the corresponding stage of a 10-mm. chick
embryo. *, Arteria cerviris communis. (For other legends, see abbreviations
opposite plate 1.)
mentals into a common stem which Doctor Boyden has named
the arteria cervicis communis. It evidently represents a further development of that consolidation which appears in the
12-mm. stage of the ostrich (fig.3).4 Twining shows several
stages in its development, without, however, naming it or
recognizing its relation to the first six cervical segmentals.
His drawings further imply that this common cervical vessel
persists and gives origin to the vertebral artery of the adult,
to which Krassnig correctly takes exception. Rut Krassnig
fails to show at what level the new origin appears and this
we have determined (see below).
The first step in the formation of the vertebral artery of
the chick may therefore be described a s the consolidation of
the first five or six segmental arteries into one system, which
originates from the dorsal aorta (in the region of the aortic
arches) by a single stem representing the persistence of any
of the first few primary segmental arteries.
The second step is the formation of a longitudinal anastomosis at the ventrolateral border of the spinal cord, coiinecting up the sinus-like enlargemeii ts of each segmental artery.
-4s in the ostrich, so i n the chick, sinus formation (fig. 2)
precedes anastomosis ; we find no adequate explanation of
this in the mechanics of circulation. It may he noted, how’ q’he pnsition
of this coiniiton stein o n the dorsal .aorta is soniewhat variable.
I n Doctor Boyden’s account ( ’ 1 6 ) he shows two photographs of injected e n -
hryos, i n one of whirh (fig. 29, 11-mm. embryo) the common cervical trunk arise$
from that part of the dorsal aorta ronnecting the third and fourth aortic arches.
In the other (fig. 28, 13.5-iniii. embryo), this connecting portion has dropped
out, leaTing the eoninion cervical with its six segmentals attached t o the dorsal
carotid. I n fisure 2 of this paper it is attached to t h a t portion of the dorsal
aorta connecting thc, fourth and pulmonary arches. When this drops out the
cervical 111 this embryo will acrordingly be left, attached t o the descending
aorta. Probablp this is atypwal. The explanation of this variability map be
Pound in figures 1 and 2 of Twining’s account, from which one m a y infer that
the coninion ceriieal mag arise from any of several spinal segmentals whosi~
aortic ends pwsist a f t e r longitudinal anastomoses have united the peripheral
portions of the first five or six segnieiitals into one system. In one chick r m b r j o
of five days and fiftren hours--al>out the time when the roininon cervical drops
out--the third and fourth srgincntals were found arising separately from the
dorsal carotid and n o trace of‘ the coninion rrrvical exlsted.
ever, that these dilatations occur between somites and at the
level of the secondary sympathetic chain. Nor is it known
why a longitudinal anastomosis develops at all, since this
precedes the dropping out of the primary segmental stems.
Where the anastomoses first appear in chicks is also open to
debate. On the basis of the large size of the midcervical portion of the vertebral artery, Rrassiiig infers that anastomosis
first takes place in that region and then spreads in either
direction (p. 598), thus bringing this into harmony with such
other processes in this region as the fusion of the lateral
dorsal aortae and the closure of the medullary groove. But
in a reconstruction of a slightly older embryo than the one
shown in figure 2 (H. E. C. 1951, 5 days, 13 mm.) the first
three segmentals are connected and then no other until the
seventh, from which point the vertebral artery continues until
the fifteenth. It would thus appear that in the chick different
portions of this artery may arise independently and not in
serial order.
The third step is the dropping out of the primary stems
which connect the vertebral parts of the segmentals with the
aorta. I n the chick embryo just referred to (13 mm.), the
first two segmentals have gone. By the 15-mm. stage (H. E.
C. 1945) all segmentals in front of the subclavian (no. 16)
have dropped out, including the communis. A t this stage the
pattern of the vertebral artery is the same as the permanent
one found in mammals. It is instructive to note that the
atrophy of the segmentals occurs during that period wheii
the caudalward migration of the bifurcation of the aorta is
most pronounced; in the interval between five and five and
one-half days it moves back from the level of the seventh
t o the fourteenth spinal nerve. I n the next day and a half
it moves only four segments, and then four more in an equal
period of time, so that by eight days twenty hours (25 mm.)
it has reached the twenty-second vertebra.
The fourth step is the formation of a connection between
the extreme anterior end of the vertebral artery and the
dorsal aorta through the occipital branch of the dorsal ex-
teriial carotid artery. This takes place in the chick immediately after the 15-mm. stage (five days fifteen hours).
Haff erl ( ’21 a ) describes a similar vessel in the plover.
The fifth step consists in the acquisition of a n additional
origin of 1,he vertebral artery from the lower portion of thc
dorsal carotid, intermediate between the one just described
and the subclavian origin. As pointed out by Rrassiiig, this
appears i n embryos of about 13-mm. head length. 111 the
I-Iarvard series it first appears i n an embryo of 15-mm. head
length (H. E. C. 1965, eight days, twenty hours, twenty-five
mm.). Its position is of more importance, our reconstructions showing that this new vessel connects with the vertebral
artery at the level of the eighth spinal nerve. Consequently,
it could not, under any circ~mstances,represent a persistence
of the arteria cervicis communis, a s implied by Twining.
Therefore, at the stage just described, the vertebral artery
taps the dorsal aorta or its cephalic derivatives in three
places : in the occipital region (through the occipital artery),
in the middle cervical region (at the level of the eighth verteb r a ) , and in the subclavian region (through the sixteenth segmental artery). That the first two of these persist in the
adalt may be inferred from Twining’s figures. The fate of
the third is unknown to the writer. I n concluding this section
of the paper, it may be pointed out that the striking feature
in the development of the vertebral arlery is the simplicity
of this artery in the ostrich a s compared with its complicated
development in flying birds.
Subclavian arteriez
The developmeiit of the arteries to the wing in the ostrich
presents no substantial difference from the development of
the same arteries in the chick. The primary subclaviaii (i.e.,
the one corresponding to the adult vessel in mammals) develops froin the dorsal aorta in conjunctjon with the twentieth
segmental artery (sixteenth iii the chick, a s determined by
Royden, ’16) ; but shortly after the 16-mm. stage a coniiection
(”, fig. 4) is formed with a branch from the ventral part of
the third aortic arch (not yet developed at 16 mm.). After
this secondary origin becomes established (ScZ.-2, fig. 5) part
of the blood supply of the wing is diverted from the twentieth
segmental artery of the aorta ( f 7 d - I ) and reaches the wing
by way of the third aortic arch. There seems no reason t o
doubt that the primary connection with the aorta will drop
out in older stages and that the definitive subclavian, as in
the chicli (Sabin, 'Ori), will become a branch of the innominate
Since the work of Twining, it has been known that the external carotid artery in chick embryos develops first as a
ventral vessel springing from the base of the third aortic
arch and that, secondarily, its terminal branches are talieii
over by a new trunk arising from the dorsal carotid artery.5
But in the early development of the external carotid iii the
ostrich some new and striking facts have been observed which
add t o the significance of these changes in bird embryos.
In the series of ostrich embryos just described the dorsal
external carotid artery is first recognizable in the 12-mm.
stage (D-I, fig. 3) as an unbranched vessel springing from
the medial side of the dorsal carotid just anterior to the juiiction of the latter with the third aortic arch. It runs cranially
along the ventromedial side of the dorsal carotid, and near
its termination bends abruptly down around and for a short
distance along the side of the pharynx. Tn other birds where
'Hochstetter ('04) seems t o have been the first t o suggest the probability of
such a process in birds on the basis of his studies on reptiles, and he described
the peripheral connection of the two external carotid arteries in the crocodile
embryos which he studied-although
in the crocodile the proximal p a r t of the
ventral external carotid does not disappear. Twining, in the chick, and Hafferl
( '21 a ) , in the plover, proved t h a t Hochstetter's suggestion was correct and that
a n anastomosis between the ventral and dorsal external carotids takes place, while
the proximal portion of the ventral vessel drops out. According to Shindo ( '14)
the same process occurs in the turtle, but not in the lizards, as Hafferl ('21 h) has
caonfirmed in the gecko. In lizards no dorsal external carotid artery develops
and the stapedial and ventral external carotid arteries a r e distributed t o the
regions which in the rest of the Sauropsida would be supplied by the dorsal
cxternal carotid.
its origin is known, it has been said to originate on the dorsal
carotid near the site of the upper end of the second aortic
arch, in the immediate vicinity of the stapedial artery
(Hafferl, '21a). To this region (0-2) its position in the
ostrich is almost immediately shifted by a series of anastomoses between it and the dorsal carotid lying just above it
(13.5-mm. embryo, fig. 1). The rapidity with which this shift
occurs raises the question as to whether a similar primary
origin may not have been overlooked in other species.
Kecoiistructions of a five-day chick show that, indeed,
this is the case. I n the embryo shown in figure 2 this artery
arises from near the junction of the third aortic arch and the
dorsal aorta as in the ostrich, and its origin is rapidly shifting (as in fig. 1) to a position near the stapedial artery. The
significance of this finding lies in the fact that it makes pos
sible for the first time, as Doctor Boytlen has pointed out,
B direct homology between the dorsal exteriial carotid of a
warm-blooded amniote and that of fishes.
When one first considers the origin of the external carotid
arteries in warm-blooded vertebrates, two disconcerting questions at once arise. How does it happen that the external
carotid of mammals develops from that portion of the aorticarch systern which is afferent to the gill arches and which in
gill-hearing forms contains venous blood? Secondly, hov7
can a ventral origin be reconciled at all with the fact that
in the lowest vertebrates (i.e., most of the fishes) the external
arteries of the head arise from the dorsal aorta (and, incidentally, from an anterior portion of that) ?
The first difficulty is perhaps more apparent than real,
sirice it has been shown that in such gill-bearing forms as
the Dipnoi and Anura (forms in which the external carotids
are homologous with those of mammals) the apparently ventral external carotid really originates f tom a down-growing
portion of a dorsal artery-the efferent branch of the third
aortic arch-which in turn quite probably reestablishes preexisting afferent chaiiiiels once continuons with the ventral
The situation presented by the second question, however,
offers a very real problem in comparative embryology. According to the conclusions reached by Allis, there are two
kinds of external carotid arteries found in vertebrates, it
being “sometimes a dorsal and sometimes a ventral artery.”
Which is the more primitive is difficult to say, since both
appear in fishes ; in Protopterus (Parker, ’SS), Lacertilia,
amphibians, and mammals it is usually ventral, but in most
other fishes and reptiles and in birds the persistent artery is
the dorsal one. The matter is further complicated by the
fact that in reptiles (excepting Lacertilia) and birds both
kinds are present in the embryo, the upper one in most cases
superseding the lower after taking over its distal portion
by anastomosis.
Since the dorsal vessel in birds is the most important one,
the question at issue, then, is the homology of this dorsal
artery. It cannot be directly derived from the dorsal external
carotid of elasmobranchs and teleosts, because that arises
from the dorsal aorta between the first and second aortic
arches (8llis, ’08). But Spencer (’92) and Kellicot (’05)
have also shown that in Neoceratodus Forsteri-a lungfish in
which the dorsal artery is the more prominent, although the
ventral is present-the dorsal artery originates from the top
of the third arch after the dropping out of the dorsal aorta
between the second and third arches. This is the very position in which we have found the origin of the dorsal external
carotid artery in the ostrich and chick. I n commenting on
this vessel in Ceratodus, Allis says: “If it is not an artery
wholly different from that in any other fish, it must be at least
a serial homologue t o the artery in elasmobranchs, ganoids
and teleosts.” Considering the phylogenetic position of the
lungfish, at the transition between water and air-breathing
forms, and the reduction i n the number of aortic arches that
accompanies this transition, it is not strange that the dorsal
external carotid should have moved back to the third arch
and thereby have become the prototype of that artery in
birds which supplies the outer tissues of the head.
A ciompai~isoiiis made between the relatively simple development of the vertebral arteries of the ostrich and the
highly specialized mode of origin of these vessels iii flying
In addition, a new origin has been discovered f o r the extemal carotid artery in both chick axid ostrich embryosfieom the top of tho third aortic arch, its later positioii tiear
the stapedial, hitherto considered its primary origin, being
merely a secondary modification. 011 the basis of these 11em7
facts, it is pointed out that this vessel may be homologoi~s
for the
with the posterior carotid artery of Ceratodas-thus
first time liiilting, through the luiigfish, the exteriial carotid
artery of birds and fishes.
New details in the development of t h e vertebral artery are
lilmvisp set forth, the most striking features being the formation of sinus-like enlargements on i,he dorsal segmental
vessels a s a p~*elirninarp
step iii the formatjoii of a loiigitiidinal cliaiii of anastomoses, and, second, the persistence of
the first spinal segmental artery in the ostrich as the principal
aortic stem of t h p vertebral artery.
ALLIS, E.: P., JR. 1908 The pseudobranehisl and carotid arteiies in the gnathostome fishes. Zoolog. Jahrb., Bd. 27, S. 103.
ROYDEN,14. A. 1916 An anatomical study of the 1 3 mm. chick, etc. Thesis
deposited in H a r r a r d College Library.
__ 1922 The early development of t h e cloaca i n ostrith cnihrgos, w i t h
special reference t o the reduction of the caudal intrstine. Anat. Itec.
vol. 24, p. 211
ELZC, C. 1907 Beschreil>ung eines menschlichen Embryo, etc. Anat. I-Iefte,
Ed. 35, S. 409.
A. 1921 a Zur Entwickeluiigsgeschiclite der Kopfarterien lieiiii
I<iebitz (Vanellus cristatus). Anat. Hefte, Bd. 59, S. 521.
1821 h Zur Eiitwjckelungsgesehichte der Iiopfgefasse der Gecko
(Platydactylus annularis). Anat. Hefte, Bd. 59, S. 1.
L’E‘I’TCR, F. 1890 Ueber die Elitwicklung dcr A . vertebralis h i i n Kaniii
clien, rtc. Morph. Jahrh., Ed. 16, S. 572.
1904 Die Entwickelung des Elutgefksssystems. HanPlbuch tler rei glcich. 11. experiment. Eiitwirklungslehre der Wirbcltiere, herausgeg.
von Oscar Hertwig.
S. W. 790‘3 Hcsehrejbung pines incnschiichen Embryo von 4.9 mm.
Sreh. f . mihr. Anat., Bd. i0, S. 506.
W. E. 1905 The derelopment of the vascular and respiratory s t s terns of Ceratodus. Meni. N. Y . Acad. Sciences, 1-01. 2, part 4, p. 131.
k‘r~4ssNIG, M. 1913 Von der Arteria vertebralis thoracica der Saugcr und
Vdgel. Anat. Refte, Bd. 49, S. 523.
T. J. 1886 On the blood vessels of Mustelus antaretieus, ctc. Phil.
Trans. Roy. Soc., London.
SABIN,C. G. 1905 The origin of the subclavian artery i n the chick. Anat.
Ane., Bd. 26, S. 3li.
SIIINDO,T. 1914 Zur vergleicliende iinatomie d e r arteriellen Kopfgefasse cler
Reptilien. Anat. Heftc, Bd. 51, S. 267.
HI’EN(EK, W. l3. 1892 Contributions t o our knowleclgc of Ccratodus, part I,
Macleay Memorial Volume.
T X I S I N G C;.
, IS. 1906 The einbr~oiiir history of the carotid arteries in the
chick. Anat. A m . , Rd. 29, S. 650.
Gra~tliie rcconstruetions showing successive stages in the development of t,Iw
vertebral, suhclavian, and external carotid arteries of the ostrich. Text figurc 1
should be interpolated between figures 3 and 4 t o complete the series.
3 12-mm. ostrich embryo (Struthio australis ( ? ) , 1%.E. C. 2242.
4 16-mni. ostrich embryo, 1%.E. C. 2244.
3 18-mm. ostrich embryo, €1. E. C. 2245.
Alw., primary inferior alveolar artery
Has., basilar artery
Ceph.Szn., cephalic sinus
D', primary dorsal external carotid artery
ll', secondary dorsal external carotid
Ling., lingual artery
Ow., third root of hypoglossal nerve
Pzdni., pulmonary artcry
Scl., subclavian artery
Scl', primary subclavian artery
Sc12, secondary subclavian artery
S - I , first spinal dorsal segmental arter?
St., stapedial artery
77, ventral external carotid artery
Tog., vagws nerve
The numbcrs, 3, i, 10, 13, 20, drsignate the respectjve spinal nerves.
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carotid, bird, arteries, vertebrate, origin, external
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