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Experiments on the aortic arches in the chick.

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Barvard Medical. School, Boston, Massachusetts
Since the early days of comparative anatomy and embryology it has been recognized that the arrangement of the
adult aortic arches varies in the different types of vertebrates. Rathke’s well-known diagrams, imperfect as they
are now known to be, show that in the lower forms both
right and left fourth aortic arches remain permanently, in
birds the right arch alone forms the connection with the
dorsal aorta, while in mammals the left member of the pair
is the permanent aortic vessel. Further details should, however, be noted. I n the lizard group the two fourth arches
arise from the two more or less completely separated ventricles, the right arch from the left ventricle and the left
arch from the right ventricle in company with the pulmonary
vessels. I n mammals the right fourth arch is not obliterated,
as might be inferred from the usual inaccurate comparison
of the vessels in mammals and birds, but remains as the
proximal segment of the right subclavian artery, reduced t o
a branch of its former mate. I n birds the left aortic arch is
actually ‘lost,’ as it becomes obliterated and ultimately disappears. This change is made possible by the development
of the secondary subclavian arteries in birds, vessels growing
out from the ventral portion of the third aortic arches,
and tapping and finally replacing the original subclavian
arteries, which arise from the dorsal aortae. There is thus
no necessity for either fourth arch to remain as part of a
37, NO. 3
subclavian artery. The left pulmonary arch persists in mammals, in part as a segment of the corresponding pulmonary
artery, in part as the ductus arteriosus, whereas the dorsal
segment of the right vessel is early obliterated. I n birds
and in most reptiles both arches function as ductus, though
in the snake, Eutaenia, the left arch alone remains, in spite
of the fact that the single pulmonary artery is developed
on the right.
The causes leading to these differences in the aortic-arch
system, which in all forms is originally one of approximate
symmetry, were not sought for by the earlier embryologists.
A+, present, however, we are less satisfied to record such
facts as ‘avian’ or ‘mammalian’ characteristics, inexplicable
and probably predetermined. We desire at least to delve
deeper into the immediate causes, though perhaps these may
still rest on facts which we cannot yet explain. With this in
view, I have tried, during the last few years, to change the
conditions in developing chicks so that the relations of the
aortic vessels might be more like those in developing mammals or reptiles, hoping thereby t o produce birds with the
characteristically mammalian left fourth aortic arch, or the
paired aortic arches of lower forms. I was chiefly concerned
with only one of the probably numerous factors wherein the
three classes differ, namely, the extent of the torsion entailed
by the shape and position of the heart.
While these experiments were going on, Congdon and
Wang( 1) published their paper on “The mechanical processes concerned in the formation of the differing types of
aortic arches of the chick and the pig and the divergent early
development of their pulmonary arches.” Their findings
have been of help in the study of my models, but I cannot
agree with some of their conclusions as to the normal loss of
the left fourth arch, though fully confirming their opinion
that this is mainly the result of mechanical forces. The differences in our points of view will be referred to later.
The present approach to the problem was suggested by the
study of chick no. 1944 of the Harvard Embryological Collec-
tion, labeled ‘5 days,’ but from the thick arterial coats and
the advanced development of some of the organs probably
several hours older. This abnormal embryo, as seen in the
Fig. 1 Model of the cavities of the aortic arches of chick embryo, H. E. C.
no. 1944, abnormal, about five days. The aortic and pulmonary valves are indicated as depressions. From the aortic trunk arise the right and left third arches
and the right fourth arch; from the pulmonary trunk, t h e left fourth arch and
both pulmonary arches. Small pulmonary arteries grow down from t h e latter,
Model made b y Miss M. F. Lewis.
model (fig. I),has all three pairs of arches-a third, a fourth,
and a pulmonary on each side. The left fourth arch is as
large a vessel as the right fourth. At this age normally t,he
left arch should be much smaller than the right, if not entirely obliterated. More striking is the fact that this left
fourth arch arises from the right ventricle, in company with
the pulmonary arches. I n this respect the arches of this
chick resemble those of reptiles ; venous blood would in part
pass through the fourth arch to the dorsal aorta.
111 sceking a clue t o this anomaly, I noticed that the coeliac
artery in no. 1944 is a median vessel, arising from the ventral
wall of Ihe aorta at the proper level. The avian coeliac artery normally at this age springs from the right dorsolateral
surface of the aorta. As I have already pointed out in a
former paper(2), this condition seems to be the result of
asymmetrically placed nerves which approach the artery
from one side only, surround its root, and pull it from its
originally ventral position. The asymmetry of the nerves is
in turn due t o the sinistral rotation of the bird’s head during
the second and third days of incubation. This chick was
prcsumably symmetrical at the critical stage for the coeliac
artery-a condition which would have been attained by the
rotation of its head in the reverse direction, dextrally, so
that the right eye rested on the yolk. As was explained in
the earlier paper, this position places the heart underneath
the foregut, aiid moves caudally the area of torsion, so that
in the heart region the chick body is symmetrical, though
lying on its side. Such chicks are not infrequently seen in thc
forty-eight-hour stage, though they usually turn over before
the nerves have grown out to encircle the coeliac artery. It
seemed possible that this same abnormal symmetry might
also be responsible for the reptilian type of aortic arches in
the embryo in question, and that the same experiments by
which the coeliac arteries were formerly retained in their
original midventral position might also influence the development of the aortic arches. It may be said at once that
chicks in which the artery is median do not necessarily retain
the left fourth arch; the two anomalies do not necessarily
accompany each other as in chick no. 1944. But among the
experimental embryos three were found with this arch intact,
and these throw much light on the mechanical forces at work
in its normal obliteration.
The obliteration of the left fourth arch in chicks takes
place normally during the sixth day, but the mere knowledge
of the hours of incibation should not be relied on in cases
where the operation might cause a retardation of the usual
growth processes. Better guides to the developmental age
of such embryos are the thickness of the coats of the arteries,
the presence of well-defined aortic and pulmonary valves in
the heart, and the nearly complete separation of the ventricles. The secondary subclavian arteries, arising ventrally
from the third arches and tapping the original vessels from
the dorsal aortae, should also be present at this age. I n maki n s this new connection the secondary subclavian arteries
seem t o join, o r spring as laterally running branches from,
the base of the ventral aortae just before the obliteration of
the latter, though this is not the usual description. These
facts were used as measures of age, and a few embryos in
which the left fourth arch was present, but which were without secondary subclavian arteries, heavy arterial coats and
well-defined T-alves were considered as merely retarded, in
spite of their known age, and therefore discarded as not
necessarily showing their permanent relations.
A model of the arches of a normal chick embryo of four
days three hours, H. E. C. no. 1943, before the obliteration
of the left fourth arch, is shown in figure 2. The branches
arising from the third arches are the remains of the ventral
aortae, with no subclavian connection; the walls of all the
vessels are thin and the common aortic trunk is as yet imperfectly separated into its aortic and pulmonary componeiits.
The third and fourth pairs of arches are fairly symmetrical,
in that the vessels all pass directly t o their respective sides,
though the left fourth arch is of much smaller caliber than
the right. The left arch also appears as a branch of the aortic
trunk, coming off at nearly a right angle, while the right arch
continues’the direction of the trunk. Perhaps this fact alone
might be enough t o cause the smaller vessel’s ultimate obliteration, but further changes leading more directly to this
end soon make their appearance. These can be readily no-
ticed by comparison of this model with that of an embryo of
six days, chick no. 15 of my series (fig. 3). I n this older
Fig. 2 Aortic arches of chick embryo, H. E. C. no. 1943, four days three
hours. All three pairs of arches are present; the left fourth arch arises from
the left wall of the trunk and is smaller than the right. Aortic and pulmonary
valves are barely indicated. Model made by Miss J a n e t Williamson.
embryo the left fourth arch arises from the ventral side of
the trunk, the right arch from the dorsal side. The same is
trine to a lesser degree for the third pair. I n other words,
the aortic. portion of the common trunk has rotated nearly
90". Another indication of this rotation can be seen in the
relative positions of the valves in the two models. In the
younger embryo the aortic valve lies to the right of the pulmonary valve, a line connecting them being thus almost in
the frontal plane; in the older embryo a similar line would
Fig. 3 Aortic arches of chick embryo, no. 15 of operated series, six days
four hours. Electrode on left 9th somite a t forty-eight hours' incubation. Right
third arch normal, left third arch ends by continuing laterally as the secondary
subclavian artery. Remnant of dorsal portion of this arch runs upward in front
of dorsal aorta (carotid). Both fourth arches present, but the left turns cephalad
only. Both pulmonary arches normal.
be nearly sagittal, as the valves lie in a dorsoventral relation.
The whole common trunk, as well as the aortic portion,
undergoes the rotation. These changes are characteristic of
normal embryos during the sixth day.
The normal torsion of the common aortic trunk of the heart
was recognized by Boas and accepted by Langer and many
other authors, including Congdon and Wang. It has been
denied by Greil, in his study of the ridges which cause the
separation of the bulbus into aortic and pulmonary channels ;
he regarded the development as indicating a spiral ridge
growth in a straight tube instead of considering both tube
and ridges spirally twisted. Many others have taken this
vicm, both as regards the heart of lower forms and in the
case of mammals. Whatever the reason f o r its presence, the
direction of the spiral, as shown by the ridges and later by
the separated aortic and pulmonary trunks, is dextral o r
clockwise, following from the ventricles t o the arches, with
the course of the blood.
The heitrt of the chick shows curves and twists that remind
one of the coils taken by a rubber tube. By imitating with a
tube the changing shapes taken by the developing chick heart,
one can demonstrate that in the tube an actual torsion inevitably results from these shapes. The facts recorded in
this paper seem t o indicate that the same is true of the living
chick heart.
I n the young chick embryo of about thirty hours’ incubation
the heart is a straight tube of two layers, endothelium loosely
coated by epicardium, fixed at one end by the vitelline veins
and at the other by the ventral aortae, but suspended between these points in the coelom or pericardial cavity by a
short dorsal mesocardium, connecting the heart with the ventral wall of the foregut. With continued development, the
heart grows faster than the structures bounding the pericardial cavity, and to accommodate itself t o the relatively
constricted space it must curve or bend. Normally, it bends
t o the right, being restricted ventrally by the underlying yolk.
The mesocardium ruptures with the consequent stretching,
and the bent tube lies free in the cavity, suspended only by
its two fixed ends. As the heart becomes relatively longer
in comparison with the cavity, a deeper and deeper curve
results. The process may be imitated by bringing together
the two ends of a rubber tube, holding them, however, always
in the same position that they take when the tube is stretched
out straight, as is shown in figure 4, A. This imitates correctly the entrance of the vitelline veins caudally and the
exit of the ventral aorta cranially.
Further growth in length of the tube in this position may
result in the lengthening of the loop, which would cause a
Fig. 4 Diagrams of rubber tube held rigidly by clamps a t each end; showing
development of dextral spiral as the tube is forced into shapes simulating those
of the developing chick heart. Lateral and sagittal views. A , a, sagittal bend;
B , b, transverse U-form; C, c, sagittal loop form.
great extension ventrally ( o r to the right, since the bend
normally takes this direction). But this is an unstable condition, maintained only by holding the two ends rigidly as
they are brought nearer together. The slightest rotation of
either end converts the vertical or sagittal bend, A , into a
transverse bend like that in B (fig. 4), giving a U-shaped
figure, b, in sagittal view. If the ‘venous’ end, which we
may suppose t o lie a t the left of the diagrams, is rotated
slightly clockwise, or the ‘aortic’ end counterclockwise, the
transverse part of the tube (the bottom of the U ) will run
from left t o right, following the supposed course of the blood
stream. Reversing the rotation reverses the U-figure. The
‘heart’ now occupies less room craniocaudally ; in other words,
it has been able to grow relatively larger in its confined
space, though extending farther to right and left. The necessary dextral rotation in birds may be given by the normal
habit of development. As pointed out by Patten(3) and
others, the position of the chick heart in relation to the rotation of the head brings it about that at a certain period of
growth the aortic end is fixed by the arches in the plane of
the head, and thus viewed from the right side on opening the
shell, while the venous end is still in the original plane of
the body, the t;wo veins extending right and left. Under these
circumstances, the aortic end of the heart is rotated 90” counterclockwise in reference to the venous end, and the bent tube
would assume the transverse U form, the aortic limb lying
nearer to the shell. But the deeply bent form is so unstable
that the slightest rotation is sufficient t o supply the necessary
impulse, and the same form is taken by the mammalian heart
in the absence of marked head rotation.
If the rubber tube has been marked to indicate the right
and left sides when it is held straight o r stretched, it will be
noticed that in the transverse U form the sides have been
displaced. At the bottom of the U the right side of the tube
now points caudally; the left side, cranially. Moreover, if
the ends of the tube have been held in their original craniocaudal positions while making the figure, they will tend to
rotate in the fingers. Released, the 'aortic' end will rotate
in a counterclockwise direction (always reckoning as though
following the course of the blood stream). I f the 'venous'
end is released, it will rotate in the opposite direction, clockwise. Obviously, the mere forcing of the tube into this shape
has caused it to assume a dextral spiral twist, masked by
the accompanying bends, bnt still readily traceable by following the right and left sides of the tube and recognizable by
the force necessary to hold the ends.
If the two ends of the tube in the transverse U form be
brought still nearer together (or if the tube grow still longer
between fixed ends), the U form changes to a closed loop
(fig. 4, C) ; if the bottom of the U ran from left t o right. the
'aortic' limb will cross to the right of the 'venous' limb.
This, which is the next step in the growth of the chick heart,
is not apparently accomplished in mammalian hearts, a s they
remain in the transverse U form. The loop form again occupies less space laterally. This fact is utilized by the chick,
f o r at this time the heart is expanding in the right extraembryonic coelom, a cavity compressed between the yolk and
the vitelline membrane which are t o left and right, respectively, of the rotated head and upper body of the chick of
sixty- t o seventy hours.
The extent t o which the tube tends to unwind when released from the loop form (C) seems t o be slightly greater
than in the case of the transverse TJ form. The 'aortic' end
of the U will rotate between 90" and 180", depending on the
elasticity of the rubber, while the same end of the loop will
rotate sometimes as much as 360". This is the true total
amount, as can be seen by slipping off one turn of tape or
ribbon from a spool, without turning the spool or altering the
position of either hand; a complete spiral of 360" results
when the tape is pulled straight.
The figures formed by the rubber tube follow sufficiently
closely the actual shape of the chick heart, as shown by Dnval,
Patten, and many others. Of course, the heart is not a rubber
tube. WIth its gradual growth into the loop form, its irregu-
lar expansions and thickenings, one might perhaps expect the
spiral to have been lost or at least greatly masked. To test
whether there is any tendency t o unwind in the living heart,
I cut across the aortic trunk of normal chick embryos of three
t o four days’ incubation. The embryos were removed from
the yolk and placed in warm Loeke’s solution, the body wall
removed, and the aortic trunk completely severed. The heart
continued beating, but only as f a r as the cut. Later, the beat
could be revived by stimulation of the atrium, but not of the
The immediate and most noticeable result of the operation
was the change of direction of the two cut ends. They immediately turned ventrally and cranially, respectively (fig.
5 , a, b ) , as though the tube were under considerable restraint.
This is due t o the final curve of the aortic trunk, where it
turns dorsally in these older hearts to join the aortic arches
( a ) . Under the binocular microscope, the severed ends were
also seen to rotate slightly in opposite directions. Subsequent
study of the sections showed that the rotation was in no case
more than 60” in all. The heart tissues had for the most part
adjusted themselves to the spiral form, but even in the living.
heart at this age one can demonstrate a slight tendency to
unwind the dextral spiral twist.
4 characteristic often noted in bird embryos is the elongation of the aortic arches as the heart ‘descends.’ Whereas in
man and other mammals at about 10 mm. the arches are
short, closely embracing the dense tissue surrounding the
trachea and oesophagus, in the chick of comparable age they
are long and apparently drawn downward caudally and ventrally. The descent finally lodges the ventral ends of the
fourth pair of arches within the limits of the pericardial cavity, which surrounds for a short distance the common wall
of trnncus and arches. The difference between the chick and
the pig in this respect can be seen by comparing the photomicrographs (figs. 6, a and b ) , which show the individual
arches of the chick drawn within the pericardial cavity, but
the union of the two fourth arches of the pig in the pretra-
cheal tissue. As pointed out by Congdon and Wang, the
arches in the chick lie in loose mesenchyma, far in front of
the tracheal condensation, and may therefore be considered
capable of being moved readily if force is applied. These
Fig. 5 Lateral view of chick heart of one hundred hours’ incubation, t o show
result of severing the aortic trunk. The two cut ends twist slightly in the direction shown by the arrows (b).
authors suppose the two fourth aortic arches to have been
thus moved, the left cranially, the right caudally, by the rotation of the aortic bulb, and give this change in position of
the left arch, which brings it .in contact with the body wall,
as a cause for its obliteration bj7 pressure. The ability of
the aortic trunk to cause the movement of the arches through
the looser mesenchyma is strongly suggested by the relative
positions of the arches already alluded to in figure 6.
If the aortic end of the spirally twisted tube is anchored
closely to the dense peritracheal mesenchyma by short arches,
the rotation will be limited to the tube itself. If, on the other
hand, the tube is split into its arch components while still in
Fig. 6 Photograph of transverse sections through ventral
aortic arches in man (a) and chick ( b ) . I n the chick the arches
a common mass within the pericardial cavity, between the atria.
left fourth arch can be seen as a small mass between the right
the left pulmonary arch. I n man the fourth arches join close
cranial to the pericardial cavity.
end of fourth
are included in
The obliterated
third arch and
t o the trachea,
a movable position, as would occur with lengthened arches,
the ventral ends of which are lodged in the pericardial cavity,
a part of the spiral rotation would be transferred t o the
arches. This is illustrated by the diagrams in figure 7 . The
first figure, ‘a,’ represents the relations found in mammals
o r in young chick embryos (compare fig. a), the second, ‘b,’
gives the picture of older chicks (compare fig. 3 ) . I n the
latter the root of the left fourth arch arises from the ventral
wall of the aortic trunk, that of the right arch from the dorsal
wall, the whole tube having rotated counterclockwise nearly
go", which, as we have seen, is the tendency of this end of
the loop-shaped tube. The final curve of the aortic end of
the loop now- includes the roots of the fourth arches, and the
left arch, being on the convex border of the curve, is still
further stretched downward. The third pair of arches show
less of the rotation, as the influence is diminished distally.
Fig. 7 Diagram to show the relations of the third and fourth pairs of aortic
arches to the pericardial cavity in mammalian ( a ) and chick embryos (71).
mammals the arches are entirely within the pretracheal tissue; in the chick the
ventral ends have been pulled down into the cavity, where they are subjected to
the spiral rotation of t h e aortic trunk.
Such a change in the course of the arches gives a distinct
advantage t o the right fourth arch, which now runs practically straight to the dorsal aorta, continuing almost exactly
the direction of the common trunk. The left fourth arch, on
the other hand, now- leaves the aortic trunk at a sharp angle,
running at first almost ventrally, and makes an abrupt curve
before passing dorsally t o the dorsal aorta. An embryonic
vessel with such an acute angle at its origin and such a torT H E ANATO&LIICII~RECORD, VOL.
37, NO. 3
tuous course is doomed to obliteration at its weakest part
when i n competition with other and more favorably placed
channels. Usually the weakest spot is at about the middle
of the arch. Congdon and Wang think that the vessel is here
compressed between the third and pulmonary arches and the
wall of the neck, where the latter is sharply incurved a t the
cervical sinus. I n my studies it seems rather that the arch,
as it is drawn down and stretched by the rotation at its ventral end, is bent against the upper edge of the pericardial
cavity. I n one of my embryos the obliteration took place
near the dorsal aorta. It seems that the site of the obliteration is merely incidental.
Rven before the descent of the heart and consequent rotation of the left fourth arch toward the front, this vessel, as
has already been noted in the normal chick of four days three
hours, no. 1943, is somewhat at a disadvantage from the fact
that the aortic trunk is placed to the right of the pulmonary
trunk and to the right of the median line (compare fig. 2). The
longer common aortic trunk of the bird’s heart, combined
with the loop form as opposed t o the transverse U form of
mammals, results in a more median and axial direction of
the avian trunk as contrasted with the obliquely right-to-left
direction well known in mammals. This difference was noted
by Lillie in his “Development of the chick,” where, on page
348, he states that “ A gradual rotation of the ventricular division on its antero-posterior axis accompanies its posterior
displacement; and this takes place in such a way that the
bulbus is transferred t o the mid-ventral line, where it lies
between the auricles.’’ The subsequent splitting of the bulbus places the aortic portion to the left of the median line.
I n the younger chicks studied the left fourth arch often has a
much thinner coat than the other arches, though still widely
open, probably showing that the volume of blood passing
through it is less than in the others.
The developmental history of the loss of the avian fourth
aortic arch can, then, be summarized as follows: Originally
practically symmetrical with its opposite neighbor, it first
becomes lengthened and unfavorably placed by the movement of the aortic trunk to the right, and then is pulled just
within the pericardial cavity by the descent of the heart. In
this position it is subjected t o the tendency toward counterclockwise rotation which is characteristic of this end of the
heart tube, and is carried to the ventral surface of the trunk,
entailing an acute angle and a sharp bend. In this condition,
the already weakened vessel cannot survive and is obliterated
at some point.
To prevent the loss of the fourth arch it would apparently
suffice to reduce the spiral heart twist; this has been accomplished in one case. But also the arch may remain patent,
even though tortuous, if for any reason it is necessary as an
important channel.
It was evident from my former experiments designed to
result in the retention of the median origin of the coeliac
artery that simple inversion of the chick’s head at from forty
to sixty hours was not sufficient to insure the desired change
in the heart spiral. Symmetry was obtained in the coeliac
region by this dextral rotation of the head; but the rotation
extended caudally beyond the heart region, so that, the whole
heart being turned over, the spiral within the heart was not
affected. Besides, the difficulty of keeping the head in this
inverted position for a sufficiently long time to be sure of
the results seemed insuperable. It was hoped that some of
the crooked embryos obtained by the use of the electrode on
one side might be so twisted that the aortic end and the
venous end of the heart might lie in different planes. In my
series, also, an occasional embryo appeared with more or
less of the ventral body wall missing-not an infrequent result of any operation involving the early cutting of the fetal
membranes. I n these cases the heart may be displaced, by
the pressure of the incomplete wall, as it protrudes through
the opening.
The first embryo in which the left fourth arch remained
present after the age at which it should have become obliterated is no. 15 of the series. The arches, dorsal aortae, and
heart valves are shown in figure 3. This and the other models
represent casts of the cavities of the vessels; the thickness
of the vessel walls are not indicated. I n this case they are
sufficientlythick to make it reasonably certain that no further
obliteration would have taken place. The embryo, at fortyeight hours ’ incubation, was subjected to electric cauterization at the left 9th somite and allowed to incubate f o r a
further period of more than four days. It was then removed
while still alive, fixed, and sectioned. Both pulmonary and
both fourth aortic arches are present and of about the same
size. The right third arch is normal and gives rise t o a
normal secondary subclavian artery. A s this arch approaches the right dorsal aorta, it turns sharply cranially
and runs for a long distance parallel to, and in front of, the
aorta, which it joins high up in the neck. This is normal and
is an indication of the rapid growth of the neck in the chick;
for in the younger normal chick shown in figure 2 the segment of dorsal aorta between the fourth and third arches is
very short.
The left third arch is interrupted. The ventral end arises
normally and takes a normal course, but ends abruptly by
turning laterally as the left secondary subclavian artery,
which curves over the fourth arch to pass laterally at a lower
level than that taken by the right vessel. The dorsal end of
the arch begins blindly, runs with a wavy course toward the
left dorsal aorta, and turns abruptly t o run cranially parallel
to this vessel, which it joins at a considerably higher level.
If there was any flow of blood in this part of the third arch
it must have come from the dorsal aorta, with a reversal of
the normal direction.
The left fourth arch has been subjected to the usual lengthening and torsion, as can be seen by the downward trend of
its ventral end and by the position of the heart valves, which
lie in the normal almost sagittal plane. The arch arises from
the ventral or ventrolateral surface of the aortic trunk,
sweeps ventrally, laterally, and then dorsally and cranially
to the left dorsal aorta. The course is thus the same as that
described as normal, yet this arch shows no sign of the normal obliteration. At the dorsal end it is contiiiued as the
dorsal aorta to the head, f o r the left dorsal aorta is lost
between the fourth and pulmoiiary arches. The blood passing through this arch could not have reached the body, and
the arch -therefore does not resemble the mammalian left
fourth arch in its connections. Rather should it be COMpared with a carotid arch, the third, sending arterial blood t o
the head.
The question arises as to the probable cause of this loss of
the left third arch and the retention of the left fourth. At
the forty-eight-hour stage the 9th somite is at about the level
of the most caudal of the three aortic arches, which then are
the first, second, and third. It is difficult, if not impossible,
t o judge, at the time of operation, of the extent of injury done
by the electrode. It is possible that this left third arch was
injured at the time of operation and that the fourth was called
upon t o supply the blood to the left side qf the head. Similar
instances of the unusual retention of a vessel normallv obliterated t o take the place of the one normally present are
common among the anomalies. The obliteration of the left
third arch could not iii this case have followed immediately
on the operation, however. Had it done so, there would have
been no opportunity for the growth of the secondary subclavian artery. Also it is probable that at that time the
second arch, still present at forty-eight hours, would have
been called on to take the place of the injured third. The
history may be reconstructed somewhat as follows : the cauterp caused a destruction of tissues just caudal to the third
arch, resulting in the formation of scar tissue, which, after
the normal loss of the first and second arches and after the
growth of the secondary subclavian vessel, finally involved
the midportion of the left third arch. Perhaps the arch was
drawn do~lrninto the region of the scar by the descent of the
heart. The fact that the dorsal, apparently unused, portion
of this arch is still unabsorbed points t o a recent obliteration.
Under these circumstances, the left fourth arch received all
the blood passing to the left side of the head. The greater
current in this direction molded the angle of entrance of
this arch into the dorsal aorta, and caused the obliteration
of the aorta between the fourth and the pulmonary arches,
the remains of the connection showing as short points on each
of these vessels.
This left fourth arch, therefore, is not like that found in
either mammals or reptiles, in that it is not connected with
the descending aorta. It is probably a substitute for the missing third arch, and in adult life would have been mistaken
f o r it, except for the unusual origin of the left subclavian
artery. The case brings out clearly, however, the fact that
the crooked course of the fourth arch is not of itself sufficient
to cause its obliteration ; as a well-used channel it will remain
and develop thick walls, but with a lessening of its current it
will succumb to even a slight secondary agent for obliteration.
There is nothing inherent in the avian fourth arch which is
bound to cause its degeneration.
The next model t o be described is that of the great vessels of
chick no. 39 of this series (fig. 8). I n this embryo at the
forty-hour stage the electrode was applied to the right side
of the spinal cord at the level of the 9th and 10th somites.
The resalt was a much-twisted embryo, as shown by the curve
of the notochord, which has been included in the model. The
coeliac artery remained ventral, since the sympathetic nerves
of the right side were retarded. The right abdominal wall
was missing, and by the protrusion of the liver the heart was
pushed far t o the left. The large vessels had thick coats and
were presumably in their permanent condition.
If the rubber tube in the closed-loop form (fig. 4, C) is
rotated t o the left on the axis of its two fixed ends, the effect
is to unwind slightly the spiral twist in the ‘aortic’ end. This
result is noticeable in the model; the pulmonary heart valves
are now located to the left of, and dorsal to, the aortic valves,
as in the younger normal embryo (fig. 2), instead of being
ventrolateral to them as in normal embryos of six days or
in chick no. 15 (fig. 3 ) . That this is not caused by mere
retardation of development is shown by the complete separation of the aortic and pulmonary trunks. The aortic trunk
is also less spirally twisted than usual, though the left fourth
arch still arises from the ventral border of the lateral surface. The arch takes almost the usual sharp curve before
running dorsally to the aorta; it is still patent, though nar-
Fig. 8 Aortic arches of chick no. 39, operated. Notochord indicated to show
curve of embryo. Partially untwisted since pnlmonary valves lie t o the left of
aortic. Both fourth arches present, but continuing mostly to head. L e f t secondary subclavian artery not present.
row at the usual point of obliteration, where it bends over the
upper edge of the pericardial cavity. It does not seem to be
crowded by the other two left arches, however. On the ot,her
hand, the left pulmonary arch, though sharply bent around
the pericardial edge, shows no sign of becoming obliterated.
There are grounds for doubt as t o whether the left fourth
arch in this case would have remained open and functional,
bemuse slightly less tortuous than usual, or whether it would
later have succumbed. Of more significance, perhaps, is the
relation of the two fourth arches to the dorsal aortae. Normally, at this age most of the blood from the fourth arches
passes caudally, the head being mostly supplied by the third
pair. The dorsal aortae cranial t o the fourth arches are
usually smaller than the third pair of arches which run up
parallel to them, while the segments of the dorsal aortae
between the fourth and the pulmonary pairs are considerably
larger. Tn the model of chick no. 39 these latter segments
are unusually long, crooked, and slender ; in the sections they
lack the thick coat found on the rest of the aorta. It is obvious that most of the blood from the fourth pair of arches
passed toward the head in this embryo. The caudal part of
the body must have been chiefly supplied by the pulmonary
arches through the two ductus arteriosi.
This abnormal distribution of the blood stream is probably
due to some unusual lengthening of the aortic segments between the fourth and the pulmonary arches caused by the
curvature of this embryo. Yet both fourth arches, in these
operated embryos, seem to be peculiarly subject to change of
their normal dorsal connections. I n chick no. 15 the left
fourth arch was continued only t o the head, and in the embryo
next to be described the right fourth arch is similarly connected. Neither of these two embryos is especially crooked
in this region of the body. Whether, in chick no. 39, the fact
that the left fourth arch poured blood toward the head as
well as toward the body, thus possibly necessitating a flow
greater than usual, had any influence in prolonging its usefulness is problematical. It is not the only vessel to the head
on this side, as was the case in chick no. 15, for the left third
arch is also present.
I n the two embryos just, described the left fourth arch has
been preserved, in one case permanently and in the other
perhaps only temporarily, in spite of the disadvantage of its
normal course. Only slightly, in the latter example, has the
cause of this disadvantageous course been removed. They
give little proof, then, that the cause as we have imagined it
from our comparisons of the heart t o a rubber tube is the
correct one. The next embryo to be described seems to me
to supply the necessary proof.
Embryo no. 10'26 was subjected to a very slight operation.
The egg was opened at thirty hours' incubation; the vitelline
membrniie was cut over the heart and slit well forward beyond the head. The amnion had not yet begun t o form, and
the head, then straight and with no indication of the spiral
twist, rose immediately above the surrounding edges of the
cut membrane, showing the compression normally exerted by
the latter. After the closure of the shell, the egg was further
incubated for five and one-quarter days. When removed. it
was therefore of six and one-half days' total incubation. The
chick was alive and apparently normal, except that a part of
the body wall was lacking. This defect is not infrequently
found after any operation involving the injury of the amnion,
which plays so large a part in the normal closure of the body
wall. I n this case the lifting of the head at the critical moment may have retarded its engulfment by the cranial amniotic fold and thus delayed the amnion in covering the body.
Whatever the reason, the heart protruded freely, one portion, later found to be the left ventricle, touching the beak,
another projecting caudally. The neck was bent t o the left,
but the back was straight and the limbs symmetrical. Study
of the sections shows that the coeliac artery arises from the
ventrolateral surface of the dorsal aorta. The heart is almost
completely inverted, left for right. The right ventricle lies
to the left of the left ventricle, the left atrium ventral and
caudal to the right atrium. The aortic valves within the
trunk are almost directly cranial t o the pulmonary valvesa reversal of the normal condition (fig. 9). The inversion of
the ventricles has caused a dextral rotation of the proximal
o r venous end of the common aortic trunk of about 180": thus
unwinding the normal dextral spiral, which, as we have seen,
results in the normal crookedness of the left fourth arch.
This arch now persists as a straight vessel, with thick coat
and slightly larger than its mate on the right side. Without
the normal dextral spiral within the common trunk, the left
fourth arch, even though arising within the pericardial area,
Fig. 9 Aortic arches of chick no. 10’26, operated. Aortic trunk entirely
untwisted, right ventricle t o the left of the right, atrioventricular openings, indicated by dotted lines, in sagittal plane. The aortic and pulmonary trunks are
parallel, incompletely divided in one place, and in craniocaudal relation. The
right third and fourth arches turn toward head. The left third and pulmonary
arches are absent, the left fourth arch sends out a pulmonary artery.
and being earlier at a slight disadvantage from its position,
as shown in the younger embryo (fig. a ) , remains as a functional channel coming, as in the case of mammals, from the
left ventricle.
I n this chick this arch shows, however, some important
modifications which call for explanation. Dorsally, it connects with the dorsal aorta which extends both cranially and
caudally. Ventrally, it gives off as a branch the left pulmonary artery. I n the absence of the left third arch and the
left pulmonary arch, this vessel takes over the duties of supplying blood to the head and to the lungs, as well as to the
On the right side the three arches are present; the third
gives off a normal secondary subclavian artery; the pulmonary arch, a normal branch to the right lung. The right
fourth arch is normal in that it has taken over some of the
ventral aorta, thus carrying the third arch along with it on a
short common trunk (compare figs. 3 and 8 ) ; but is abnormal dorsally in that it turns cranially with the dorsal
aorta. The segment of dorsal aorta between the right fourth
and right pulmonary arches has completely degenerated, so
that the fourth arch cannot perform its normal function of
sending blood to the embryonic body. This fourth arch has
become a segment of the carotid artery, no longer serving
as the definitive aorta. There is a striking analogy between
this arrangement and that found in mammals, where, in the
presence of a definitive left fourth arch, the right member of
the pair is utilized as a segment of the subclavian artery.
The single left vessel must be considered a fourth arch; it
arises from the aortic portion of the common trunk in connection with the right fourth and third arches, and conveys
blood to the descending dorsal aorta. Though it also sends
blood to the cranial part of the dorsal aorta, it is obviously
not the third arch, since it does not give off a left secondary
subclavian artery ; the primary subclavian artery still arises
from the dorsal aorta at a lower level on this side. A tiny
brmch running up the front of the neck may represent a persistent ventral aorta, not present on the opposite side. Perhaps this replaces the missing third arch as a ventral carotid
vessel. Ventrally, the present arch is practically straight,
with no sign of the normal curved course at its origin from
the truncus. The resemblance to the mammalian arrangement is very close, in that this left fourth arch is the only
vessel which can convey arterial blood t o the descending
aorta, since the right fourth arch turns cranially. On the
other hand, it resembles a pulmonary arch in having a branch
to the left lung.
The explanation of the anomalous origin of the pulmonary
artery is given, I think, in one of my earlier papers, on the
development of the aortic arches(4). I n the rabbit, as was
then demonstrated, the ventral aortae extend caudally from
the conns or truncus as a plexus of small vessels on each side
in front of the foregut. This takes place after the aortic
trunk has assumed the final curve, already mentioned,
whereby it points dorsally instead of cranially as in the
beginning. Dorsolateral branches from each plexus meet
sprouts from the dorsal aortae t o form successively the third,
fourth, and pulmonary arches, as well as the evanescent fifth
arches. Thus, before the completion of the pulmonary arch,
each fourth arch is provided with a ventral plexiform branch
running caudally. This branch becomes the pulmonary artery, and connects with a plexus in front of the lung bud
derived, as was pointed out by Huntington(5), from lower
branches of the dorsal aorta. I n the chick, also, this small
caudal branch frbm the ventral end of each fourth arch can
be seen running toward the lung bud. I n the Harvard Embryological Collection it is present in chicks nos. 2071, 2072,
and 3073, from two days eighteen hours to two days twentytwo hours; in none of these embryos has the pulmonary arch
formed, though in the last-mentioned the fifth arch, connecting dorsally with the fourth, is present on one side. If for
any reason the sprouts from this small branch should not
reach those from the dorsal aorta, the pulmonary arch would
not be completed, and the pulmonary artery would remain a
branch of the fourth arch. Distance alone might be responsible f o r this condition. I f , at about seventy hours, the
caudal surface of the common aortic trunk, bearing the fourth
pair of arches, were moved to the right, as would result from
a dextral rotation of this end of the heart, the caudally directed plexus might be carried far enough away from the left
dorsal aorta to prevent the normal connection, with consequent absence of the dorsal portion of the left pulmonary
arch. Dextral rotation of the lower end of a tube will either
unwind a dextral spiral already present, or, if the spiral is
resistant, will impart a dextral rotation to the other end. In
the case of chick no. 10’26 such a dextral rotation has, as we
have seen, been imparted to the proximal end of the common trunk, which might be transmitted to the distal end.
It remains to see whether the sequence of events as we
have outlined them in this case is compatible with what we
know of the embryo. Freeing the head of young straight
embryos from the vitelline membrane does not prevent the
iiormal development of the head bends and the spiral turn.
As seen through the window in the shell, this embryo appeared normal in contour at fifty hours and again at sixty
hours. It seems probable that the heart was until then normally twisted. After about sixky hours the embryo sinks into
the diminishing yolk, offering only its back for inspection,
so that the heart can no longer be seen. Within the next few
hours the body wall should be completed. I n this case the
wall, perhaps because delayed, formed behind the heart, leaving part of it ontside. The hole in the body wall is bounded
caudally by the diaphragm, below which is the liver. Growth
of the liver would thus push forward, or cranially, the part
of the heart resting on the diaphragm.
,4t seventy hours the chick heart is in the form of a closed
loop (fig. 4, C). I f with the rubber tube in that position the
caudal curve of the loop is pressed forward, the loop unwinds. The dextral spiral of the ‘aortic’ end is counteracted,
or, if the normal spiral is considered as already fixed, the
distal end is further rotated dextrally. The fixed or resistant
nature of the spiral trunk at this age is shown by the slowness of its response after being severed. It seems probable,
then, that the pressure of the body wall was in this case the
factor in both the abnormalities, the rotation of the distal end
of the trunk causing the absence of the left pulmonary arch,
later followed by the unwinding of the spiral in the somewhat resistant trunk.
As a result of the anomalies in this case, a curious condition exists, comparable with that found in chick no. 39. Because of the loss of the dorsal aorta between the right fourth
and pulmonary arches, the body receives blood only from
the right pulmonary arch and the left fourth arch, both of
which also carry blood to the lungs. Moreover, the left lung
would have received arterial blood from the left ventricle.
I n chick no. 39 the blood to the body comes mostly from the
two pulmonary arches from the right ventricle. It is doubtful whether either condition would permit of life after
The normal loss of the left fourth aortic arch in the chick is
due, at least chiefly, to mechanical forces. As contrasted with
the condition found in mammals, the ‘descent’ of the heart is
accompanied by an elongation of the arches, so that the ventral ends of the pulmonary and fourth pairs come to lie within
the pericardial cavity. I n this position they are free to respond to the tendency of the common aortic trunk to a counterclockwise rotation, which is imposed upon it by the dextral
spiral twist resulting from the loop form of the chick heart.
The dextral spiral can be demonstrated as a necessary result
of the loop form by the manipulations of a rubber tube, and
can be detected by severing the aortic trunk in the living
heart. The spiral in the chick is imparted to the arches, and
the left fourth arch is rotated to the ventral surface of the
trunk. The resultant stretching of the arch and the sharp
bend at its origin place this vessel at a distinct disadvantage,
especially since the right fourth arch has been correspondingly rotated to the caudal surface of the trunk, in direct line
with the axis of the blood stream. The weakened vessel succumbs to some secondary influence, usually, apparently, the
pressure of the upper edge of the pericardial cavity, but per-
haps to pressure against the deep cervical sinus, as suggested
by Congdon and Wang.
I n spite of its disadvantageous course, the left fourth arch
has been found to persist when the left third arch was discontinuous, thus assuming a carotid function. I n another
instance, in which the disadvantageous origin of this arch was
only partly corrected by the rotation of the whole heart to the
left, both the left third and lsft fourth arches were present,
both serving as carotids to the head. I n this case the right
fourth arch also turned cranially, instead of joining the descending aorta.
In one chick embryo the dextral spiral twist of the aortic
trunk was completely counteracted by the inversion of the
ventricles. The right ventricle was turned over to the left
side of the heart, and vice versa. The aortic division of the
trunk is straight and cranial to the straight pulmonary division; the usual spiral arrangement is lacking. Under these
circumsiances, the left fourth arch is the definitive aortic
arch; the right fourth arch becomes a branch, leading t o the
dorsal carotid artery. T i these respects the arrangement is
comparable with that found in mammals. On the other hand,
this embryo shows an entire absence of the left third and left
pulmonary arches.
It seems, then, that the chief cause of the difference in the
arrangement of the aortic arches in birds and mammals can
be traced to a greater ‘descent’ of the heart in the former.
I n comparing chick embryos of about five days with pig o r
rabbit embryos of comparable age, one can readily appreciate
that the whole upper region of the body is longer and more
slender in the birds. The distance between limb bud and cwvical sinus is proportionately greater, the neck and thorax
more slender and tapering. The abdomen is much less prominent, and perhaps it is the relatively small development of the
large abdominal organs, the liver and the wolffian bodies, at
this age which is responsible for the difference in form by
allowing the heart more room caudally. Later, the body becomes more compact, the elongated neck remaining as the
chief avian feature. Of the reasons f o r the differences in the
relative growth of organs in different types of embryos we
kcow as yet practically nothing. The comparative study of
embryonic metabolism has not been attempted, but it seems
probable that this might give a n answer to some of the questions which a r e not yet solved.
Given the proposition that the heart does move further
caudally i n the chick, the resulting fate of the originally practically symmetrical aortic arches seems purely a matter of
mechanics, involving the expected action of the coiled heart
on vessels which have been drawn into a position where they
are free to respond.
AND WAXG 1926 Am. Jour. Anat., vol. 37, pp. 499-520.
J. L. 1926 Anat. Rec., vol. 33, pp. 299-310.
B. M. 1922 Am. Jour. Anat., vol. 30, pp. 373-397.
.J. L. 1012 Am. Jour. Anat., vol. 13, pp. 111-128.
G . S. 1919 ilnat. Rer., vol. 17, pp. 165-201.
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