Paper - The fifth aortic arch of mammalian embryos; the nature of the last pharyngeal evagination
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Reagan F. The fifth aortic arch of mammalian embryos; the nature of the last pharyngeal evagination. (1912) Amer. J Anat. 12(4): 493-505.
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The Fifth Aortic Arch of Mammalian Embryos; the Nature of the Last Pharyngeal Evagination
Frank Reagan
Contribution Number 121 from the Zoological Laboratory of Indiana University
Sixteen Figures
Part 1
The question of the existence of six aortic arches in mammalian embryos has recently received much attention. In the minds of some, perhaps, it is definitely and satisfactorily settled; yet the known facts and the conclusions drawn from them are diverse and conflicting. For this reason, anything further to be added may be of interest.
The significance of the question is well understood. A demonstration of six arches would serve to bring into line the branchial
circulation of mammals with that of the lower vertebrates, and
to strengthen the belief in the similarity of ontogenies in related
groups. By Lehmann and Locy the view has been advanced,
that, upon a demonstration of the same number of arches in all
air-breathing groups depends the comparability of the arches
giving rise to the pulmonary arteries. This view seems altogether unnecessary since, if it be granted that mammals have
only five pairs of arches, all doubt of comparability should fall
on the more transitory and questionable vessels. To deny the
similarity of the pulmonic arches because of a variable number of
arches anterior to them, is as illogical as to doubt the identity
of the systemic arches because of the fact that different numbers of arches may exist posterior to them. Because of the constancy of their characteristics, the identity of the pulmonic arches of all air-breathing vertebrates is well established.
All workers are agreed that the transitory vessel representing a new arch is to be looked for between the fourth and pulmonic arches.
Although the results of previous observers have been rather
exhaustively discussed, mention may profitably be made of points
which have direct bearing on the present work.
The first evidence in favor of the predicted existence of a new
arch in mammals, was adduced by Zimmermann ('89), when he
found in a 7 ram. human embryo, a small vessel arising from and
re-entering the posterior side of the fourth arch. He also
described a complete and typical fifth arch in an eleven day rabbit. The arch arose from the ventral aorta and emptied into the
aortic root, not far from the dorsal lumen of the pulmonic arch.
Tandler ('02) found, in a rat embryo, a broad connection
between the fourth and pulmonic arches, parallel to the dorsal
aorta; he identified it as a fifth arch, despite the fact that it was
without connection with either aorta, and that there was no
corresponding pharyngeal pouch. In two human embryos he
found vessels connecting the ventral aortae with dorsal portions
of the pulmonic arches.
Lehmann ('05) has figured a complete arch for the pig, and has described it as follows:
A short distance from its union with the truncus arteriosus the fourth arch increases greatly in width and there is given off from its posterior side near the middle of the arch, a smaller, but perfectly distinct vessel which, bending slightly downwards, follows along the course of the fourth arch and joins the dorsal aorta immediately beneath it. Just ventral to its union with the aortic root there passes back from the rudimentary vessel, a branch which joins the sixth arch immediately ventral to its union with the dorsal aorta.
From this description we are to interpret the portion of the
vessel joining the aorta as the distal portion of the arch proper, and
the vessel to the pulmonic as a branch of it. These indeed would be
conditions requisite to a typical arch; but Locy's interpretation of
the same vessel is not in accord with the above view when he describes it as "passing dorsad and caudad to unite with the pulmonic
arch near the union of the latter with the aortic root." He
also states that "it is connected with the aortic root by an independent branch." This conclusion he bases on the results of
previous observers and upon the other figures of Lehmann, but
from her fig. 10, it must be admitted that there is as much and
perhaps more ground for Lehmann's interpretation, because the
blind spurs on the aortic root in that figure are more prominent
than those on the pulmonic vessel.
Lewis ('06) having investigated the conditions in the rabbit
and the pig, maintained that the vascular irregularities, blind
spurs, and anastomosing sinuses near the bases of the fourth and
pulmonic arches furnish no evidence that a typical arch exists
between them. His figures afford strong evidence to support
this view. He regards the attempts to demonstrate a fifth arch
as "morphological speculations of extreme interest" but adds
his belief that "the general recognition of a new arch in mammals
seems to be due to those considerations which led Boas to predict it rather than those which come from the study of mammalian embryos themselves."
In mole embryos of 4.7, 5, 5.5, and 6 mm., Soulie and Bonne
('08) found a number of complete vessels arising from both the
truncus anteriosus and the fourth arch. Their 5.5 mm. embryo is
of interest becaue of a more typical fifth vessel. This vessel is
described as "entierement distinct et isole" from the fourth and
sixth arches. Its origin from the aortic bulb is given as 30ai
above the ventral lumen of the fourth arch in a plane vertical to it.
(From this description the ventral aorta is considered as extending dorsally and laterally to the point of origin of the fifth arch and
including the common trunk of the fourth and fifth arches.) On
leaving the bulbus it turns outwards, curves, and apphes itself
against the external face of the fifth pouch, embracing the latter iii
its concavity. On leaving the fifth visceral arch it turns freely to
unite with the aortic root, about 80^ from the lumen of the pulmonic arch. Their 6 mm. embryo 'C shows remarkably distinct
fifth visceral arches. They maintain themselves to have demon-
strated perfect fifth aortic arches (regarding those connected with
the pulmonic as typical), but admit that the work of other observers may profitably be annexed to their own.
In a dicephalous lamb, three or four weeks after its birth, a
vessel suggesting a fifth arch was found by Bishop ('08). It
was seen as a slender sinus, connecting the two component aortic
trunks. Since the more stable arches, as such, had either degenerated or become greatly modified, and since the vessel had no
connection with either aortic root, it affords rather uncertain evidence of a fifth arch.
In cat embryos, Coulter ('09) found spurs and sinuses which he
suggests as rudiments of a fifth vessel, but in no case did he find
a complete arch.
If we are to be so exacting as to demand of this new arch, those
qualifications and characteristics common to other arches with
which we attempt to prove the vessel homologous, it will be
seen that the only typical fifth arches yet demonstrated, are
those of the eleven day rabbit of Zimmermann, and of the 5.5
mm. mole of Soulie and Bonne. These are described as typical
in that they were said to connect the aortae and occupied distinct
visceral arches. But the description of the vessel in the Zim-
mermann embryo was unaccompanied by figures; furthermore,
the existence of the vessel in the rabbit has been doubted by Lewis
(assent to Lewis's view has been given by Coulter) . Also, from the
description of the 5.5 mm. mole of Soulie and Bonne, the ventral
aorta is considered as extending to a point 30^ vertically above
the lumen of the fourth arch, so that the common trunk of the
fourth and fifth arches must have been interpreted as ventral
aorta. This interpretation is allowable, yet an arch arising more
ventrally would be more typical. From their reconstruction
'A,' the dorsal portions of the fifth vessel and the pulmonic arch
seem sufficiently intimate to justify their being regarded as entering
the dorsal aorta in common. The supposition is in harmony with
the view of Coulter in which he, reviewing the results of Soulie
and Bonne, stated that their fifth arches emptied "in every case
into the dorsal aorta in common with the pulmonic arch." At
any rate, this intimacy renders the arch less typical. From the
foregoing consideration, a demonstration of an arch more typical
than those just mentioned seems desirable, even though it be
granted with Soulie and Bonne that they may have successfully
demonstrated their " phylogenetic souvenir."
Since the extreme irregularities back of the systemic arch render
the existence of a typical fifth" arch more doubtful, the follow-
ing question naturally suggests itself: do such irregularities occur
in connection with the other arches; if so to what extent; and is
a tendency towards bi-lateral duplication of irregularities more
strongly displayed in the region of the new vessel than elsewhere?
In order to determine these points and to throw as much light
as possible on the probable nature of this fifth vessel and its associated pharyngeal parts, a study was made of one hundred and fifty
pig embryos, between stages of eighteen somites and 15 mm.
Most of the embryos studied were between and including the
stages of 8.5 and 9.5 mm.
In embryos smaller than 6 mm., marked irregularities were
rare. The first, second and third arches often showed blunt
protuberances and rough walls. These seemed more common
on each arch at the height of its development.
In an embryo of 6.5 mm., a vessel of about one third the calibre
of the fourth arch (fig. 15) was found springing from the middle
of the anterior side of that arch, and returning to it near its dorsal
lumen. This smaller vessel is a trifle similar to that of the human
embryo of Zimmermann, except that it is found on the anterior
face of the fourth arch. The conditions in fig. 15 would indicate
that the vessel described by Zimmermann was merely a division
of the fourth arch.
At the stage of 7 mm., short spurs were occasionally present
near the ventral end of the fourth arch, projecting caudally.
Short projections were common on all portions of the posterior
face of the fourth arch. Stages of 8 mm. showed shghtly more
irregularities in the region of the fifth vessel than in the preceding
stage. In a few 8.5 mm. embryos, slender dorsal connections between the fourth and puhnonic arches were observed. Projecting into the dorsal aorta and sometimes piercing it, 'islands' of mesoderm were often found. There was a sUght tendency
towards a duplication of these conditions on opposite sides.
- I am much indebted to Professors C. H. Eigenmann and F. Payne for direction
and helpful criticism of the work undertaken. Acknowledgment of indebtedness is also due Professor Frank R. Lillie for permission to consult the embryological collection of the University of Chicago, and Professor C. H. Spurgeon of Drury College, for the use of his excellent private collection. Besides the embryos of these collections, those of the embryological cabinet of Indiana University, a number of series of my own preparation, many student preparations were also examined.
An 8.6 mm. pig (measured after having been killed in Zenker's fluid and dehj^drated), number 78. S of the C. H. Spurgeon collection, is of unusual interest because of the remarkably well developed fifth arch. The vessel exists typically on the right side without dorsal connection with either of the neighboring arches. ^
Figs. 6 and 7 are from wax reconstructions of the branchial circulation
of the embryo. They were made by the method of Born. The cavities
of the arches are represented as solid. The entodern of the pharynx
and the ectodern of a portion of the body wall are represented as such.
In maintaining perspective, some parts of the model may appear to
have been drawn out of proportion, but apparent discrepancies will be
accounted for by a comparison of figures. In fig. 7, for instance, the
intimacy of the fifth vessel with the ventral aorta would seem exaggerated, since it is impossible to show the extent of the ventral aorta in
a lateral view. On the other hand, fig. 6 hardly does justice to this
intimacy since the ventral diverticulum of the third pharyngeal pouch
conceals the point of diversion of the third and fourth arches. The origin
of the fifth arch, however, is definitely located when the sections (figs.
1 to 5) are consulted.
Fifteen microns lateral to the plane containing the point of
diversion of the third and fourth arches, the most median and
ventral indication of the fifth vessel is seen as a low ridge- (fig. 5)
on the ventro-caudal surface of the ventral aorta. ^ The ridge
increases in size and follows for a very short distance the course
of the ventral aorta laterally and dorsally. Continuous with this ridge the fifth vessel has its origin. It curves freely in a
latero-dorsal and at the same time, caudal direction (fig. 7),
passing between the glandule thyroidienne and the 'prepulmonic
caecum.'* From this point, the fifth vessel curves rather abruptly
towards the median line. Just ventral to its union with the aortic
root, the vessel increases greatly in size; this increase is more
prominent on the posterior surface (figs. 1 and 7). Opposite
this prominence^ is a slight outbulging on the anterior face of the
pulmonic arch. The mesenchyme is continuous between the
two vessels (fig. 1). The dorsal lumen of the fifth vessel is situated about midway between the systemic and pulmonic arches,
(figs. 1 and 7).
- After the completion of the reconstruction another small island of mesoderm was found in this ridge, but is not shown in Fig. 6.
- The common trunk of the fourth and fifth arches lateral to the diversion of the
third and fourth arches may still be considered as ventral aorta for the following reasons: (1) the distance is only 15 microns; (2) for the same reason that the common trunk of the third and fourth arches isalways regarded as ventral aorta; (3) greater intimacy of the arches is allowable at their points of origin than at their places of termination since they must all arise from a common centre, necessitating the existence of common trunks. But in no instances do the more stable arches normally enter the dorsal aorta by common trunks.
The left side of the same embryo (fig. 10) has only the rudiments
of a fifth arch. The vessel seems to have lost its original and
most ventral connection, and has formed a second one higher up
on the fourth arch. The portion between this and the original
connection has partly degenerated. There are dorsal connec-
tions with the adjoining arches somewhat similar to those in fig.
8. (In both instances the pulmonic connection is the smaller.)
These dorsal branches have persisted and probably represent the
connecting sinus found by Tandler in the rat. I have found
dorsal connections between the fourth and pulmonic arches in
about thirty-five instances in which the dorsal connection varies
from a very slender to a broad connection where the fourth and
pulmonic arches apparently come in contact (fig. 14). The very
slender connections seldom have direct connection with the dorsal
aorta.
- For the significance of this term, see part 2.
- On the postero-dorsal surface of the systemic arch is also a small prominence of about the same size. These probably indicate the beginning of branches of the fifth arch.
The 9 mm. sagittal series Number 1299 of the University of
Chicago collection is of much interest because of a complete fifth
vessel (fig. 8). Twenty microns lateral to the plane of diversion
of the third and fourth arches, there is seen on the ventro-caudal
surface of the ventral aorta (somewhat similar in position to the
vessel on the right side of the preceding embryo) a prominent ridge. After coursing dorsally and laterally 30m from its most
median indication, this ridge abruptly gives off, continuous with
its extremity a fifth vessel which, after a very short ventro-caudal
course makes a right angle turn in a dorso-caudal direction, curving at the same time laterally. After passing between the much
attenuated glandule thyroidienne and the broad 'pre-pulmonic
caecum, the vessel curves in a dorso-median direction and joins
the dorsal aorta not far from the dorsal lumen of the fourth arch.
But just before uniting with the dorsal aorta, the fifth vessel
gives off two branches neither of which has so great a diameter
as that of the fifth vessel at this point. The smaller of these two
branches passes in a caudal direction and joins the pulmonic
arch near its dorsal lumen. The larger branch lies practically
opposite the branch just described; it passes anteriorly to join
the systemic arch just ventral to the union of that vessel with the
aortic root.
The conditions of this embryo are suggestive of those seen in
Lehmann's fig. 12. Their points in common are: that in each
case the fifth arch has a branch communicating with the pulmonic
arch; these communications leave (or perhaps enter) the fifth
arch at about the same angle; the anterior portion of each pulmonic connection is relatively small, while the posterior portion
of each is large and flaring. The last fact may be suggested as
indicating the connection to have originated from the pulmonic
arch. My figure differs from that of Lehmann, in that the fifth
vessel of my fig. 8 is more intimately connected with the ventral
aorta; the portion entering the aortic root is much larger than
the pulmonic branch. These conditions indicate that Lehmann
was correct in interpreting the pulmonic connection in her fig.
12 as a branch of the fifth arch. My fig. 9 is made from a reconstruction of a 9 mm. embryo. The rudiment of the fifth vessel
has a systemic connection, but is in no way connected with the
pulmonic arch. These conditions also point to the correctness
of Lehmann's conclusions.
Stages later than 9 mm. exhibit irregularities in abundance,
but they gradually become less typical. In a 10 mm. embryo,
a pulmonic arch was seen as a Y-shaped vessel. A long finger-like projection extended down behind it from the dorsal aorta. Blunt protuberances were found similarly located in three instances.
Figs. 11, 12 and 13 show irregularities slightly suggestive of a
fifth arch, but they are situated so far dorsally and laterally that
they need not be considered seriously. Also, they form such
straight and direct communications, lacking the curvature
found in the typical arches, that I consider it mere conjecture to
suggest their having significance. Granting with Locy that
irregularities such as these serve to demonstrate the extreme
variability of the supposed vessel, it must be admitted that these,
and those to which he had reference cannot at the same time prove
a typical existence for the new arch.
On the grounds of majority it has been held that a perfect
fifth arch has, for its distal termination, the dorsal extremity of
the pulmonic arch. It was this consideration that led Locy to
oppose the view of Lehmann (above stated and confirmed).
But it is evident that, in the pig at least, the fifth arch connects
the two aortae and lies between successive pharyngeal evaginations; hence it conforms to the requisites of a typical arch. It
may be that conditions other than these represent the highest
degree of development attained to by certain forms, but such
forms can not be said to exhibit it in a theoretically typical manner. On the other hand, it is only to be expected that the vessel
in question generally be found in an a-typical condition and very
exceptionally perfect. Therefore an occasional constancy in
atypical conditions should not be allowed to dominate our conception of a theoretically perfect arch.
The relatively late appearance of the supposed fifth arch is another point which believers in that vessel have seen fit to neglect. This point receives consideration in Part 2.
Part 2
The double pharyngeal out-pocketing found back of the sys- temic arch is not well understood. At present there are three views concerning its significance: (1) that the double outpocket- ing represents the fourth pharyngeal pouch with its dorsal and ventral diverticula (Fox, Tandler, Coulter); (2) that the dorsal and ventral parts of the outpocketing represent the fourth and fifth pouches respectively (Greil, Zimmermann) ; (3) that the ven- tral portion represents the postbranchial body of lower verte- brates (Mauer, Verdun). From these considerations the ventral portion of the double outpocketing has been designated by the following terms: (1) ventral diverticulum of the fourth evagina- tion; (2) fifth branchial pouch or ultimo-branchial body; (3) post-branchial body. Since no one of these terms is sufficiently general to cover all the views presented, the term 'pre-pulmonic caecum' might be suggested. This term is applicable to the ventral division of the out-pocketing, whatever may be its signif- icance. The further usefulness of the term is shown later.
This much, however, is definitely settled: the dorsal portion
of the double pouch is the anlage of the 'glandule thyroidienne' of Prenant, while the 'pre-pulmonic caecum' becomes the rudimentary lateral thyroid.
According to Verdun the development of the last pharyngeal
evagination (or evaginations) is as follows: the pre-pulmonic
caecum is first given off as a latero-ventral diverticulum, posterior
and mesial to the third pouch. Near the dorsal extremity of the
caecum, and slightly anterior to it the glandule thyroidienne"
is given off immediately from the pharynx as an independent
diverticulum. Both push out laterally, drawing with them the
wall of the pharynx lying between their bases. Thus they acquire
secondarily a common pharyngeal orifice. Their formation differs
in this last respect from that of the pouches anterior.
Fox ('08) in describing the posterior evagination of a 6.5 mm. pig,
gave the location of the ' dorsal portion of the fourth pouch' as posterior
and dorsal; he gave the 'ventral portion' as anterior and ventral. This
may have been due to his considering directions with reference to the
general contour of the embryo, and not with reference to the direction
of the pharynx where the evagination joins it.
In the rabbit and the pig the glandule thyroidienne is generally considered anterior to the pre-pulmonic caecum.
The posterior evagination in the cat is figured by Coulter as
having dorsal and ventral portions, the dorgal portion having become constricted into anterior and posterior divisions. The anterior division is more directly continuous with the ventral portion,
and is labeled the dorsal diverticulum of the fourth pouch. The
posterior division is represented as the fifth pouch. If the entire
dorsal portion of the evagination be considered anterior, as in
other forms, the fifth pouch of the cat would be morphologically
anterior to the ventral diverticulum of the fourth pouch. If as
stated by Verdun (and as I have observed in a limited study
of the development of the evagination in the pig) the earliest
indication of the Y-shaped pouch is its ventral portion, Coulter
erred when he labeled the most caudal pharyngeal prominence of
his 4.5 mm. cat as 'pouches 4-5.'
The 'glandule thyroidienne,' like the pouches anterior to it,
comes in contact with the ectodern, differing radically in this
respect from the prepulmonic caecum. Occasionally I have found
it constricted into dorsal and ventral portions. In one instance
(fig. 16) which is very unusual, the glandule thyroidienne is
divided into dorsal and ventral portions, each of which has direct
connection with the exterior through the pre-cervical sinus.
Between the small diverging tubes thus formed, is the mesodermal
connection presumably between the fourth and fifth visceral
arches. The plane passing through the pre-pulmonic caecum
is shown slightly above (posterior to) that of the glandule thyroidienne. The occasional division of the glandule thyroidienne
into dorsal and ventral portions is suggestive of its representing
an independent pouch.
Attention may profitably be called to the chronological relations of the portions of the double evagination to the associated
aortic arches, since these relations have hitherto remained unnoticed. The 'glandule thyroidienne' and the 'fifth' arch,
despite their anterior position, appear respectively later than the
pre-pulmonic caecum and the pulmonic arch. (The same conditions are found in birds.)
The dorsal portion of the V-shaped evagiiiation would appear,
then, to correspond to the transient fifth vessel, and to have lost
its double nature proportionately to the degeneration of the fifth
arch. The tendency towards a distinctness of division of the
'glandule thyroidienne' from the pre-pulmonic caecum closely
parallels the tendency towards the development of a perfect
'fifth' arch.
The pre-pulmonic caecum, therefore, is branchial in nature to
the extent to which the pulmonic vessel is a true aortic arch;
what this extent is, must be determined by a more thorough
study than has yet been given to the question. Both seem to
have been greatly modified, if they have ever resembled closely
the parts anterior which have generally been considered their
homologs.
From the foregoing considerations two views are possible:
- that the new arches so far exploited are merely irregularities which happened to be suggestive of a fifth arch but have no significance; and that the Y-shaped evagination is simply a fourth pouch
- that the fifth arch occasionally exists and the intimately related pharyngeal evagination represents more than a fourth pouch.
There is much to favor the latter alternative,
Conclusions
- The vascular irregularities are more or less common throughout the branchial circulation and may in any part show a slight tendency towards bi-lateral duplication.
- Even though this tendency is far more pronounced in the region of the supposed fifth arch, the irregularities here should be considered very reservedly, since in most instances they are merely an expression of the tendency towards anastomosis, common to vessels in close juxtaposition.
- A fifth vessel, very closely approximating a theoretically perfect aortic arch can be demonstrated for the pig; it may be with or without connecting branches from either the systemic or the pulmonic arch or from both.
- If a 'fifth' arch actually exists, appearing after the pulmonic arches are formed the latter vessels must he regarded as differing, to a certain extent, from the vessels anterior to them; and to this extent the branchial nature of the pre-pulmonic caecum has become modified.
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