Talk:Paper - The early embryology of the auditory ossicles in man: Difference between revisions

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TH F. F..-\Rl.Y I~'.MBRY()l.()GY OF THE AUl)lT()RY OSSICLES
The Early Embryology Of The Auditory Ossicles In Man: Illustrated In Atlas Series
IN MAN‘


Illustrated in Atlas Series"-’
Jerome R. Hanson, M.S., Barry J. Anson, Ph.D. (Med. Sc.)
and Theodore H. Bast, Ph.D.*


_IF.R()l\-IF. R. H.-\'.\'SOT\', M.S., BARRY J. AN'SOI\', l’h.D. (Med. Sc.)
INTECEDENT phases of an_ otological investigation, carried out at
and THEODORF. H. BAST, l’h.D.3
Northwestern University and the University of Wisconsin de: ut with developmental stages in which the otic capsule,


AI\"I‘lC(‘l*Il)l*II\"l‘ phases of an oto-
the auditory ossicles and the related
logical invest igation, carried out at
.\'orthwestern I'ni\'ersity and the Uni-
versity of Wisconsin dealt with develop-
mental stages in which the otic capsule,
the auditory ossit [es and the related
branchial arches were well formed in
branchial arches were well formed in
cartilage.‘ .As a recent supplement
cartilage.t As a recent supplement
 
to these more general discussions, three
to these more general discussions, three
articles have offered detailed information
articles have offered detailed information
on the morphogenesis of the otic capsule,
on the morphogenesis of the otic capsule,
the stapes and the incus (with atlas ar-
the stapes and the incus (with atlas arrangement of figures). A fourth article,
rangement of figt11'es)."’ A fourth article,
comparably concerned with the malleus,
comparably concerned with the malleus,
is in preparation.
is in preparation.


It now remains to report upon the de-
It now remains to report upon the de
 
'From the Department of Anatomy of the University
‘From the l)epartment of Anatomy of the L'ni\'ersity
of Wisconsin and the Department of Anatomy of Northwestern University Medical School (Contribution No. 640
of Wis:-onsin and the Department of Anatomy of North-
western l'ni\'ersity Medical School (Contribution No. 640
from the latter department).
from the latter department).


A stlld_\' carried out with the continuing support of
A study carried out with the continuing support of
the (‘entral Bureau of Research of the American Otologicnl
the Central Pica of Research of the American Otological
.\'ociet_\' and of the _\'ational Institutes of Health of the
Society and of the National Institutes of Health of the
l'nite<l States Public Health .\'er\'iee (Grant No. B. 2237).
United States Publie Health Service (Grant No. B. 2237).
The cost of engravings was met by the use of the NIH
The cost of engravings was met by the use of the NIH
grant.
grant.


Based upon a thesis presented by Jerome R. Hanson
Based upon a thesis presented by Jerome R. Hanson
for the degree of Master of Science at the University of
for the degree of Master of Science at the U niversity of
\\'is-cousin: enlurgedas a collaborativeinvestigation. during
Wisconsin; enlarged as a collaborative investigation, during
his service as Project-Assistmit on the above-named grant.
his service as Project-Assistant on the above-named grant.


The drawings were executed by Miss Jean l\Ie.(‘onnell.
The drawings were executed by Miss Jean McConnell.
The plmtomierographs were taken by .Mr. Homer Montague. labelled by Miss Rosamond Howland.
The photomicrographs were taken by Mr. Homer Montague, labelled by Miss Rosamond Howland.


The authors are indebted to Dr. Hhafilt F. Ricliany who
The authors are indebted to Dr, Shafik F. Richany who
provided valuable assistance during the initial phase of
provided valuable assistance during the initial phase of
the in\'estii.'ation.
the investigation.
 
Received for publication September 18, 1959.
 
*The illustrations were prepared from the following
series in the G. L. Streeter ( ‘ollection, Carnegie Laboratory,
Baltimore, Kr sries 617; Figs. 3 and 4, 6517;


Rec:-i\'td for publication Septetnber I8. l!):')9.
59;


'-‘The illustrations w.-rt prepared from the following
series in the ( P. |.. Hticeter ('ollection. ('arneizie Laboratory.
Baltimore, Figs. 1 and ‘.2. series 6317; Figs. 3 and 4. 6517:
Fig. .3. .';.')‘.l; Fig. ti. 652-1; Figs. 8 and ‘J. 1430; and from the
T. H. Bast ('ollection. I'ni\‘crsit_\' of Wisconsin. Fig. 7.
series 180; l"i«1s. 10 and 11. 10; Fig. 12. 174; l"igs. 13. H.
15 and lti. 138 Fig. 17. 168; Fig. 18. 29; Fig. 19. B 124:
Fig. 20:1. I-"I; Fig. 30b, 2!l.\; Fig. 20c. H2: Fig. 2(!d. ‘JR.


.\Iagnification~i. reeonstruetions: Fig. 1. X 32; Figs.
 
3, 7., ti and 7. X 20; Figs. N and 10. X 18; Fig. 12. X 16.
Fig. 13. X 21).


.\I:lL'llllit‘:tiil)ll.'-3. 5rhutontierographsz Fig. 2. X 120;
Fig. 5, Fig. 6, 6524; Figs. 8 and 9, 4430: and from the
Figs. 4 and ‘J, N 13!); Figs. 11. H and 1.3. X 81; Fig. 16.
D; H. Bast Collection, University of Wisconsin, Fig. 7,
X 25: Fig. 17 X  Figs. 18 and 19, X 33; Figs. ‘_’0a and
series 180; ligs. 10 and 11, 10; Fig. 12, 174; Figs. 13, 14,
20 In. X 20; Fig. 20¢-, X 13; Fig. 20d. X 12.
15 and e ir fig. 17, 168; Fig. 18 : Fig. 19. B 124;
Vig. 20a, 13; Fig. 20b, 294; ( : Fig. 20d, 98.


“lleeeaseal January 23. ltlfiil.


‘I’:-rtinent articles already have been cited in an earlier
issue of this journal (vol. 32. 19.38, pp. 157-172).


"Alison. Ii. J. and ll-ust. '1'. H.: llevelopment of the (Mir
 
(‘apsule o. the Human Hair. Quart. Bull. l\'orthwe~itern
I'ni\'ersit,\' .\Iedit'al School. 32:]-'37-17L’. 19:38.


.~\nson. I5. J. and Bast. T. lI.: l)e\'elopment of the Slaves
of the Human Ear. Quart. Hull. Northwestern l'ni\'ersit_\‘
.\I(-dieal .\'('ltm)I. 332 -I-I--'19. ]95‘.I_


.\nson. ii. .I. aml Mast. 'l'.lI.: l)e\'4-lopment of the Int-us
 
of the Human liar. Quart. Bull. .\lorthwestern l'ni\'crsity
ml-Ilieal School, 33: 110-119. l!l.')9.
 
 
Magnific an reconstructions: Fig. Dex 32; Figs.
3, 5, 6 and 7 X 20; Figs. 8 and 10, X 18; Fig. 12, X 16,
Fi ‘ig. 13, X 2
 
Magnifie =m fie ea eens Vig. 2, X 120;
Figs. 4 and 9, X 69; Figs. 14 and 15, X 81; Fig. 16.
X 25; Fig. 17x 5, i gs. is a 19, X 33; Figs. 20a and
20 b, X 20; Fig. 20e, X 13 20d, X 12.
 
 
‘Deceased January 1
 
‘Pertinent articles already have been cited in an earlier
issue of this journal (vol. 32, 1958, pp. 157-172).
 
‘Anson, B. J. and Bast, T. H.: Development of the Otic
Capsule o. the Human Ear. Quart. Bull. Northwestern
University Medical School, 32:157-172, 1958.
 
Anson, B. J. and Bast, T. H.: Development of the Stapes
of the Human Ear. Quart. Bull. Northwestern University
Medical School, 33: 44-59, 1959.
 
Anson, B. J. and Bast, T.H.: Development of the Tneus
of the Human Bar. Quart. Bull. Northwestern University
medical School, 33: 110-119, 1959.


358
358


velopmental steps, taken before the stage
Developmental steps, taken before the stage
of 28-mm., in which localized portions of
of 28-mm., in which localized portions of
the mesenchyma in the branchial region
the mesenchyma in the branchial region
suddenly become distinguishable from
suddenly become distinguishable from
the tissues of which they are primordially
the tissues of which they are primordially
a part and, at the same time. assume an
a part and, at the same time, assume an
appearance and a position predictive of
appearance and a position predictive of
their adult form and topography.
their adult form and topography.
Line 102: Line 116:
stage, beginning with specimens in which
stage, beginning with specimens in which
the future ossicles and the related
the future ossicles and the related
branchial arches have not reached pre-
branchial arches have not reached pre‘artilaginous constituency. In the past,
cartilaginous constituency. In the past,
investigators attempted to explain the
investigators attempted to explain the
origin of the ossi:-les without benefit of
origin of the ossicles without benefit of
early embryos. In such studies. limited
surly embryos. In such studies, limited
as they were to the use of en1bt‘_vos in
as they were to the use of embryos in
which the branchial arches and their
which the branchial arches and_ their
derivatives were already ('ompos(‘d of
derivatives were already composed of
cartilage, conjecture inescapably took the
‘artilage, conjecture inescapably took the
place of fact in the attempt to account
place of fact in the attempt to account
for the genesis of the auditory ossicles
for the genesis of the auditory ossicles
in man.“
in man.®


Microscopic sections used alone are of
Microscopic sections used alone are of
Line 119: Line 132:
changing architecture of the branchial
changing architecture of the branchial
arches, but reconstructions provide the
arches, but reconstructions provide the
needed aid in determining what contribu-
needed aid in determining what contribution the mesenchymal condensations give
tion the mesenchymal condensations give
the developing structures.’ The following discussion will be based chiefly upon
the developing structures.7 The follow-
the use of such ‘‘models.”’
ing discussion will be based chiefly upon
the use of such “models.”


In the fifth week of fetal life the
In the fifth week of fetal life the
stapes is not yet a definiti\'e portion of a
stapes is not yet a definitive portion of a


"Reviews of the literature on ossicular development
‘Reviews of the literature on ossicular development
have been presented by Fraser (1882). (lradenigo (1887).
have been presented by Fraser (1882), Gradenigo (1887),
Dreyfuss (1893). (iaupp (1899). Broman (1899). Kingsley
Dreyfuss (1893), Gaupp (1899), Broman (1899), Kingsley
(1900). Fllelts (1905). Reagan (1917). van der Klanuw
(1900), Fuehs (1905), Reagan (1917), van der Klaauw
(1924). and (‘auldwell and Anson I19-I2). Translations of
(1924), and Cauldwell and Anson (1942). Translations of
the German literature prepared by .\Irs. Eyeke Strickland
the German literature prepared by Mrs. Eycke Strickland
have been used as guidance in this present study. A com-
have been used as guidance in this present study. A complete presentation of the literature on early embryology
plete presentation of the literature on early embr_\'o|og,\'
of the ossicles by Mrs. Strickland and the present authors
of the ossicles by Mrs. Strickland and the present authors
is in preparation.
1s Jn preparation,


'-As the authors have commented before. only by the
‘As the authors have commented before, only by the
use of reconstructions can the continuity of fluct.uatin;:
use of reconstructions ean the continuity of fluctuating
tissues and interrelationships of shifting structures be
tissues and interrelationships of shifting structures be


established to the conviction of the writer and be pictured
established to the conviction of the writer and be pictured
t.o the .“lIII\‘f:l('IlUl] of the reader.
to the satisfaction of the reader.
 
HANSON ET AL.—AUDITORY OSSICLES


blastemal lobe which is situated at the
blastemal lobe which is situated at the
proximal extremity of the hyoid (Rei-
proximal extremity of the hyoid (Reichert’s) bar (fig. 1). This lobe is grooved
chert’s) bar (fig. I). This lobe is grooved
by the facial nerve, which serves to
by the facial nerve. which serves to
divide it into a stapedial primordium and
divide it into a stapedial primordium and
the laterohyale, both of which temporarily
the laterohyale, both of which temporarily
retain h_\-oid continuity (fig. 2). In the
retain hyoid continuity (fig. 2). In the
Sl.t'i-mm. stage the division is more
9.6-mm. stage the division is more
definitely marked. The portion which
definitely marked. The portion which
connects the above-mentioned structures
connects the above-mentioned structures
is called the interhyale (fig. 3) ; it will give
is called the interhyale (fig. 3); it will give
rise to the stapedial tendon.
rise to the stapedial tendon.


In the earliest stages the two visceral
In the earliest stages the two visceral
bars are broadly connected by an inter-
bars are broadly connected by an interbranchial bridge of mesenchyme (figs.
branchial bridge of mesenchyme (figs.
1 and 3), the greater part of which is in
l :m(l 3). the greater part of which is in
the territory of the second arch as
the territory of the second arch as
indicated by its relationship to the
indicated by its relationship to the
pharyngeal g1'oo\'e (figs. 3 and -I). This
pharyngeal groove (figs. 3 and 4). This
blastemal mass is located between, and
blastemal mass is located between, and
continuous with. the middle segment of
continuous with, the middle segment of
the hyoid bar and the proximal portion
the hyoid bar and the proximal portion
of the mandibular (.\Ieckel’s) bar. This
of the mandibular (Meckel’s) bar. This
circumstance indicates that the man-
circumstance indicates that the manubrium of the malleus and long crus of
ubrium of the malleus and long crus of
the incusare mainly of second arch origin.
the incus are mainly of second arch origin.


In the 8-mm. specimen. which is more
In the 8-mm. specimen, which is more
advanced in ossicular development than
advanced in ossicular development than
the 9.1";-inm. stage. the interbranehial
the 9.6-mm. stage, the interbranchial
bridge is separating from the hyoid bar
bridge is separating from the hyoid bar
along a sulcns which transmits the
along a suleus which transmits the
chorda tympani (fig. .3). Separation is
chorda tympani (fig. 5). Separation is
complete in the 11.7-mm. stage. at which
complete in the 11.7-mm. stage, at which
time a secondary connection between
time a secondary connection between
the arches is formetl as the incus. now
the arches is formed as the incus, now
of distinguishable outline. comes to
of distinguishable outline, comes to
approximate the stapes (fig. Iii).
approximate the stapes (fig. 6).


l)uring the fifth week the stapedial
During the fifth week the stapedial
artery attains a central position in the
artery attains 2 central position in the
blastemal lobe. thereby seeming to aid
blastemal lobe, thereby seeming to aid
in the cot1\'eI'sion of the rounded mass
in the conversion of the rounded mass
into a ring-like structure with an obtur-
into a ring-like structure with an obturator foramen (figs. 5 to 9). Oceasionally
ator foramen (figs. 5 to 9). Occasionally
a ring fails to form, and an anomalous
a ring fails to form. and an anomalous
stapes is the result; the horseshoe-shaped
stapes is the result: the l1ol'sesl1(ie-sllapetl
stapes in a [4-mm. embryo is an example
stapes in a l-l-mm. embryo is an example
of this defect (fig. 7).
of this defect (fig. 7).


The malleus and ins-us in the l.3..")—nun.
The malleus and in¢us in the 15.5-mm.
embryo. although still precartilaginous.
embryo, although still precartilaginous,
become demarcated as the mannbrium
become demarcated as the manubrium
and long crus begin to assume char-
and long crus begin to assume characteristic form and as a groove appears
acteristic form and as a gl'o0\'t‘ appears
between the head of the malleus and
between the head of the malleus and
body of the incus (fig. 8). At this stage
body of the incus (fig. 8). At this stage
the ring-shaped stapes impinges upon the
the ring-shaped stapes impinges upon the
otic capsule. The laterohyale and short
otic capsule. The laterohyale and short crus of the incus end in loose adventitia
 
(fig. 9). In the 17-mm. embryo, both
35'!
the incus and malleus are clearly identifiable as chondrified structures. The
 
malleus temporarily remains in continuity with the mandibular (Meckel’s)
crus of the incus end in loose ad\'entitia
bar (fig. 10).
(fig. 9). In the 17-min. embryo. both
the incus and malleus are clearly iden-
tifiable as chondrified structures. The
malleus temporarily remains in contin-
uity with the mandibular (.\leckel’s)
bar (fig. 10).


The interhyale passes from the junc-
The interhyale passes from the junction of the stapes and incus to the hyoid
tion of the stapes and incus to the hyoid
bar (fig. 11) where the latter makes an
bar (fig. 11) where the latter makes an
acute angle to become the laterohyale
acute angle to become the laterohyale
(in contact with capsular tissue). The
(in contact with capsular tissue). The
primordium of the stapedial muscle is
primordium of the stapedial muscle is
identifiable in the 21-mm. stage (fig. 12)
identifiable in the 21-mm. stage (fig. 12)
as an outgrowth from the interhyale.
as an outgrowth from the interhyale,
located posterior to the angle of Reichert 's
located posterior to the angle of Reichert’s
cartilage and medial to the facial nerve
cartilage and medial to the facial nerve
(figs. 13 and H). The tendon of the
(figs. 13 and 14). The tendon of the
stapedial muscle is derived from the
stapedial muscle is derived from the
interhyale in the portion between the
interhyale in the portion between the
developing stapes and Reichert’s bar
developing stapes and Reichert’s bar
(figs. 15 and 1(3). The stapedial ring
(figs. 15 and 16). The stapedial ring
now fuses with the otic capsule. the
now fuses with the otic capsule, the
conjoined tissue thus becoming the
conjoined tissue thus becoming the
lamina stapedialis. The periphery of
lamina stapedialis. The periphery of
the lamina. through (litferentiation of its
the lamina, through differentiation of its
tissue. will become the annular ligament.
tissue. will become the annular ligament.
The zone of change is the site of the
The zone of change is the site of the
future vestibular fenestra (fig. 15>.
future vestibular fenestra (fig. 15).


('ontinuity between the interhyale
Continuity between the interhyale
(seemingly the primordium of the sta-
(seemingly the primordium of the stapedial muscle as well as the tendon) and
pedial muscle as well as the tendom and
the laterohyale is lost in the 40-mm fetus;
the laterohyale is lost in the ll)-mm fetus:
at this stage the constituent cells begin
at this stage the constituent cells begin
to assume the appearance of muscle
to assume the appearance of muscle
(fig. 17).
(fig. 17).


As the muscle (l(‘\‘elops and the incudo-
As the muscle develops and the incudostapedial joint is formed, the tendon
stapedial joint is formed. the tendon
usually gains an attachment to the neck
usually gains an attachment to the neck
stapes. Ilowever. the frequent partial
stapes. However, the frequent partial
insertion of the stapedial tendon into
insertion of the stapedial tendon into
the incus (figs. IS and 19) supports the
the incus (figs. 18 and 19) supports the
belief that the long crus of the incus. as
belief that the long crus of the incus, as
well as the stapes, is a deri\'ati\’e of the
well as the stapes, is a derivative of the
second arch.
second arch.


Both of the cartilaginous arches con-
Both of the cartilaginous arches contribute not only to the substance of the
tribute not only to the s-ubstance of the
auditory ossicles, but also to that of
atulitory ossicles, but also to that of
related structures in the head and neck.
related structures in the head and neck.‘
 
‘Bast. T. H., Anson, B. J. and Riechany, 8.
Development of the Second Branchial Arch
Cartilage), Facial Canal
 
Man. Qi Bull. Northwestern
School, 30 5-249, 1956.
 
Richany, F.. Bast, T. H. and Auson, B. J.: The
Development of the First Branchial Are in Man and
the Fate of Meckel's Cartilage. Quart. Bull. Northwestern
University Medica! Sehool, 30: 331-355, 1956.


‘Bast. T. H.. .\nson H. J. and lticluan). 5. Ii.‘ The
F.: The
l)e\'elopnn-nt of the .\'et-<-ml Iiranchial .\l‘I‘ll ltn-it-In-‘:‘l‘.~
Reichert's
(‘artila-_vel. Facial ('annl and .\~Isu<'l:th-cl .~‘tru«-turn-_a III
and Associated Structures in
.\lan. Quart. Hull. .\'«-rtlmeste-rn l'nm-vsit) .\lI'4i{l'{|i
Medieai
Fclltml, 30: ‘.’1§.’>-‘_’l‘J. l‘.l.'-ti.


l{iclu|Ir\. 5.  llast. T. ll. and .\nson. Ii. J ' The
 
l)e\'elopnn~ul of the Fi:-st l{!‘:|ln‘l|l.‘Il \rch ll| .\l;nn an-l
 
the |"ate of .\Ieekel's(':urtilaue. Quart. llull. Xorvlnu-~m-rtt
l'ni\'ersity .\lt-tlical Scluml. ::o: Ilfil-'2.';.':. l‘.t'.I‘».
300 QUARTERLY BULLE'1‘ll\', N.U.M.S.


While the inalleus is undergoing os-
While the malleus is undergoing ossification, the zone of continuity with
sification, the zone of continuity with
Meckel’s cartilage narrows rapidly (fig.
.\/Ieckel’s cartilage narrows rapidly (fig.
20a). This alteration in form is due to
20a). This alteration in form is due t.o
a retrograde change in the cartilage which
a retrograde change in the cartilage which
precedes differentiation of the tissue
precedes differentiation of the tissue
into that of the future anterior ligament
into that of the future anterior ligament
of the mallcus. As soon as bone is
of the malleus. As soon as bone is
formed in the head and neok of the
formed in the head and neok of the
mallcns the anterior process (an osseous
malleus the anterior process (an osseous
rod before bone-formation begins in the
rod before bone-formation begins in the
ossicle itself) fuses with the malleus
ossicle itself) fuses with the malleus
(fig. 20b). Distally the cartilage will be
(fig. 20b). Distally the cartilage will be
:ll)S()l'l)(’(l in the inaudible.
absorbed in the mandible.


l{eichert’s cartilage passes through an
Reichert’s cartilage passes through an
e\'en more dramatic series of changes in
even more dramatic series of changes in
attaining adulthood. At its proximal
attaining adulthood. At its proximal
e.\;tremit_v. that part of the cartilage which
extremity, that part of the cartilage which
is (lcrived from the laterohyale of the
is derived from the laterohyale of the


ea1'ly embryo forms :1 transito1'_v lateral
early embryo forms a transitory lateral
boundary for the developing facial canal
boundary for the developing facial canal
(fig. 200). By the 215-mm. stage, how-
(fig. 20c). By the 215-mm. stage, however, membrane bone is developing
ever, membrane bone is developing
internal to the cartilage—thus intervening between cartilage and nerve (and
internal to the -artilage-—thus interven-
stapedial muscle, derived from the interhyale). Concurrently, the otic capsule
ing between cartilage and nerve (and
stapedial muscle, derived from the inter-
hyale). Concurrently, the otic capsule
is ossifying. In early infancy, Reichert’s
is ossifying. In early infancy, Reichert’s
cartilage is merely a remnant within new
‘artilage is merely a remnant within new
bone, and the facial canal has acquired
bone, and the facial canal has acquired
new and permanent walls (fig. 20d).
new and permanent walls (fig. 20d).
I)istally the tissue of the original arch is
Distally the tissue of the original arch is
converted into the styloid process of the
converted into the styloid process of the
temporal bone, the stylohyoid ligament
temporal bone, the stylohyoid ligament
and the lesser cornu of the hyoid bone.
and the lesser cornu of the hyoid bone.


The 2'llustratz'0ns appear on the succeed-
The 2llustrations appear on the succeeding pages.
ing pages.
HANSON ET AL.—AUDITORY OSSICLES 361
I-IANSON FT AL.~—.-XUDITORY OSSICLES Cml


Embryo , 7mm.
Embryo, 7mm.


   
ae REICHERT’S CARTILAGE
 
Stapedial a yp». (branchial arch I)»
 


_ ‘3’-,__\ b msxcmsms CARTIIAGE
   
gtapedlal 5;’ l \ ( ranc1}1a1 archlt) ”%t1aPedm1
- ' H ’ astema
Faclal nerve iatemhyale
(Broman)


Chorda tympan v
_-- Stapedial
blastema
Laterohyale
(Broman )


MI-:CKEI.’S CARTILAGE / _ _
MECKEL’S CARTILAGE setae
(branchial arch I )
(branchial arch I)


   
   
    
    
    
    
   
   
   
   


b‘ Artery of branchial arch II
Stapedial a’
I
Facial nerve
laterohyale


/ ‘ I ‘3tapedia.‘l
‘Chorda tympani


Stapedial a.’ b15'5t"3ma
Posteroinferior view
\ Facial nerve


iaterohyale
SUPERIOR


‘Chorda tympani
\.. Facial nerve


SUPERIOR
=, ~Blastemal mass
for stapes


’"“Facia1 nerve
POSTERIOR
C‘ L'°t‘3"°hY51Q' “\~B1astema1 mass
for stapes
ANTERIOR POSTERIOR
I’ INFERIOR


Chorda tympani
   
 
 


Lateral View
C. Laterohyale~*


Fig. 1. In the embryo of .41/3 weeks (?'mm.) the precursor tissue for the mulitory 0s.\'tt‘lt‘.s' is n enm-
ANTERIOR 4
mon blastemal mass which is (listinynishable from the surroumflny mesenehyma only lu'l'IIItse of the
Chorda tympani INFERIOR
greater concentration of its ('()It-S‘l'lllI('Il! cells (compare fig. 3).


A lobe-like portion of this mass is located at the ertm-ial end of the seemul riseeral lmr (precursor
Fig. 1. In the embryo of 41/2 weeks (7mm.) the precursor tissue for the auditory ossicles is @ common blastemal mass which is distinguishable from the surrounding mesenchyma only because of the
of Re'ichert’s cartilage), where it is yroored by the facial nerve. Part of this mass is the prinmrtlium
greater concentration of its constituent cells (compare fig. 2).
Inf the stapes. However, it is still separate from the uyqregation of cells u'hieh will laeemne the ntie
capsule (the latter not included in the reconstruction). The stupetlial urtery ertemls from its snIII‘('t‘-
vessel to encroach upon the interiomerlial aspect of the l)l(1steIna ( f ('0. I (1); the (‘lll)l'(l(l t ym pan 1' lII'ltIl('lH‘.\'
from tI1e facial nerve to pass metlial to the first riseeral bar, the forerunner of J! eel.‘el's eurtiluye (fig. Ill).


A mesenchymal bridge of cells between the first and second I*ls('('I‘(ll lmrs (’.1‘l('Iuls f/‘um the proximal
A lobe-like portion of this mass is located at the cranial end of the second visceral bar (precursor
end ofthe mandibular bar (at I in fig. 1e) In a point on the hyoizl bar (at Il)just distal to the l)l(l.\'lt'IIl(tl
of Reichert’s cartilage), where it is grooved by the facial nerve. Part of this mass is the primordium
lobe of the stapes ( 1c). The prz'mor(l‘ia of the mulleus (tnrl lneus are not yet dist-inet .<.’rnrtures
of the stapes. However, it is still separate from the aggregation of cells which will become the otic
tl'itlIiIt this c0mlens(.ttion of cells (ehich will soon yire rise to them.
capsule (the latter not included in the reconstruction). The stapedial artery extends from its sourcevessel to encroach upon the interiomedial aspect of the blastema (fig. 1a); the chorda tympani branches
362 QUARTERLY BULLETIN, N.U.M.S.
from the facial nerve to pass medial to the first visceral bar, the forerunner of Meckel’s cartilage (fig. 1b).


     
A mesenchymal bridge of cells between the first and second visceral bars extends from the proxi mal
end of the mandibular bar (at I in fig. 1c) to a point on the hyoid bar (at IT) just distal to the blastemal
lobe of the stapes (fig. 1c). The primordia of the malleus and incus are not yet distinct structures
within this condensation of cells which will soon give rise to them.
362 QUARTERLY BULLETIN, N.U.MLS.


I \\ Pharynéeal
7mm. Glossopharyngeal


       
 


KI
Stapedial
, 4 .- ‘ roove I
artery


‘ - ,. _
(origin)


I « ~ - "' ‘$3
Ag: — Laterohyale


\}.,_Je.;'.-?_:fl1‘::‘.’¢. ~‘ . o ..
 
 


9'.‘ '%=.°3:'.5f°..C. \ ..ln. . -
4 Pharyngeal


I"i(/. J. .-l.\' is (‘tear/y (lmna/mtmtml in .s-m'tion,s, the rommon blastemal lobe is situated dorsal to the
> groove
_/irst phary/tyml yramw, ll‘/l(‘I'(’ it is indmtzltt by th0far"iaI )wr1'0 on its d0r.s'al(1t(’ral aspect. I t is through
the /n‘t'.s'('u('(' of the .s‘u[(‘I(.s' [I)‘(IIIlt('(‘(/ by the nerve that the followingforeraxt may be made: the metlial
amt laryor part of the tube will _r/tm» rise to the .s'I(l[)(’.s'.' the part lateral to the nerve will become the latera-
hyal('.' tho L'n.tm'(:m:rwrtiuy /mrtiun, u'h2'('/1 is still rcry broad, will b(I(/mm’ the inlorhyale. The 71.arrou'in_(/
of the intt-r/1yalr' amt .s-ubscquont .x'('])ar(lti(m of [hr stapotlial porlimt from the Iaterohyale is seemingly
-inflrtcnt-mt by (hr [)l'(‘.\'.\'IlI'(' of thr facial mrrro, as this ma.s-.- im-:'('a.s-e.x- at a more 1aup1'd rate than does
th.(* H(’)‘l‘(‘ 2't.x-1'1].


The p)‘('.s'(.'I1(‘(' of thv .s-tapmlial artvry zirlmtll/its part of tho q0m'raI blastema as the “stapes"; it is
 
still snl1'(l, not having yr‘! aw/uirml thcfarm of an annul(’t. 7'/mfI1tI()'(* p0.s'/ition. of th(' artery in the
('(’II[I'I' of tho ma.»-.s a,ppmr.x- to be ([110 to a f0Id~z'ng around the arty,-y as the blastema enlm-gcs, The
/II'()('('.\'.s' s('(’III.\‘ to bv one of ('ru'o[n/nnm/t of (ht! ar'cry by yrmrth of the ma.\-.:«- rather than one of ])erf0rat2'(m
I/I/‘ally/I ('/mI_.//atirm of the 1'o.s‘.s-('/.


.1! this .s-tayv tho blastoma may be .s-air/, for the _/irxt (mm, In ;u).s-.sc.s.s- a (list'iII_(/‘rlisllable boumlary.
I It th(- h‘7,,/,3-/uni. .-tayv thr» ti.x~.x-Ia‘ fit the ('0r/'('spaIuti-ng branchial arm is a .simpl(', tliflttsc I7I('S(’It(‘hynl('.
   
HANSO;\' ET .-\L.#AUI)ITORY OSSICLES M3


Embryo , 9. bmm.
f
rea
4 imae 3
4 a ag .


d.
avs : PP MeO a Gi
REICI-lIER'I"S CART ILAGE (II)


/  ,, Blastemal nmésczs:
aso,
PaO TT ae


~Stapes
   
‘:Ma11eus. , mcus


Latevohyale \
Fig. 2. As is clearly demonstrated in sections, the common blastemal lobe is situated dorsal to the
first pharyngeal groove, where it is indented by the facial nerve on its dorsolateral aspect. It is through
the presence of the sulcus produced by the nerve that the following forecast may be made: the medial
and larger part of the lobe will give rise to the stapes; the part lateral to the nerve will become the laterohyale; the interconnecting portion, which is still very broad, will become the interhyale. The narrowing
of the interhyale and subsequent separation of the stapedial portion from the laterohyale is seemingly
influenced by the pressure of the facial nerve, as this mass increases at a more rapid rate than does
the nerve itself.


 
The presence of the stapedial artery identifies part of the general blastema as the ‘‘stapes’’; it is
 
still solid, not having yet acquired the form of an annulet. The future position of the artery in the
 
center of the mass appears to be due to a folding around the artery as the blastema enlarges. The
   
process seems to be one of envelopment of the artery by growth of the mass rather than one of perforation
 
through elongation of the vessel,


Interhyale ~’ T
Al this stage the blastema may be said, for the first time, to possess a distinguishable boundary.
In the 6Yo-mm. stage the tissue in the corresponding branchial area is a simple, diffuse mesenchyme.
HANSON ET AL.—AUDITORY OSSICLES 363


\1:‘ac1a1 nerve
Embryo, 9.6mm.


 
   
   
   
   
 


t§r£r21joSuper'1or View a»
a.
REICHERT’S CARTILAGE (IL)
4 /
levee as / SMa Blastemal masses:
Interhyale-* stapes


MECKE/3L'S cA1mLAeE<I>l"‘
.-Malleus , incus
b. I
- .~S_Facial nerve
Anterosuperior view | wot


Triqeminal nerve
MECKEL’S CARTILAGE oy .


Trigeminal nerve
    
    
 
 
   
   
    
    


Facial nerve-
-Laterohyale
iaterohyaie


“lncus , malleus
.~Incus > malleus


I Postszromfczrior View ‘
I Spacek
Posteroinferior View


SUPERIOR
SUPERIOR


Triqczminal nerve
   
 
 
   
   
 
   
   
 
 


\
Blastema of stapes-_" 7
C. ANTERIOR


Pglastema of 1ateroh_\,u1c
I
 
Blastema of malleus, incus
PO ST ERIOR
\Fac1a1 nerve
 
Latgyal Vigw | Bleziétema of maueus , incus


| Lateral view
INFERIOR
INFERIOR


Fig. 3. In the embryo of 51/3 weeks (0.6 nun.) the branehial slrnetures have inereaserl greatly in
Fig. 3. In the embryo of 512 weeks (9.6 mm.) the branchial structures have increased greatly
size through hyperplasia of the znesenehynzal cells amt the outlines of the ossieutar prinmwlia hare
size through hyperplasia of the mesenchymal cells and the outlines of the ossicular primordia have
become more clearly defined.
become more clearly defined.


The second visceral bar projects farther tou'ar(t the otie labyrinth than /he first anrl has at its pro.ri-
The second visceral bar projects farther toward the otic labyrinth than the first and has at its proximal extremity the blastemal lobe with the primordium of the stapes. The facial nerve has grooved the
mal extremity the blasternal lobe with the ])I"tIlt()l‘(llltIIt of the stapes. 'I'he _,"aeial nerre has groom'Il the
lobe more deeply, the sulcus serving to mark off more distinctly the stapedial from the laterohyale
lobe more deeply, the su,lcns serving to mark ofl more ctistinetly the stapedial from the laterohyale
portion. The primordium of the stapes is still separated from the otic capsule (not shown) by a zone
portion. The primorzti um of the stapes is still separated from the otie capsule (not shown) by a zone
of cells which is less dense than the mesenchyme of either the stapes or the capsule. The general location
of cells which is less dense than the /nesenehyme of either the sttlpes or the capsule. The general location
of the stapes (lateral to the otic capsule and medial to the facial nerve) is one which persists throughout
of the stapes (lateral to the otie capsule and medial to the faeial nerve) is one I('h.ieh persists throughout
fetal life and into adulthood.
fetal life and into adulthood.


Although a stapedial artery is not yet centrally l0('(Il(‘(l within the blas/ema, an artery is fonml
Although a stapedial artery is not yet centrally located within the blastema, an artery is found
(not shown in the reconstruction) at the periphery of the lobe as it iras in the 1‘-nun. stage.
(not shown in the reconstruction) at the periphery of the lobe as it was in the 7-mm. stage.


The malleus and incus are not yet tlifferentiatett from the interhran.ehiat bridge of mesenehynu-
The malleus and incus are not yet differentiated from the interbranchial bridge of mesenchyme
which now broadly connects the two visceral bars aeross the first pharyngeal groore (jig. Jr at arrmr).
which now broadly connects the two visceral bars across the first pharyngeal groove (fig. de at arrow).
Since the groove is the boundary externally between the arehes (I am! I I ), rlmlble origin of the two
Since the groove is the boundary externally between the arches (I and II), double origin of the two
ossicles is thereby indicated.
ossicles is thereby indicated.


The chorda tympani, branching from the facial nerre, passes from the hyoltl arch (I I ). in_t'eri¢.-r
The chorda tympani, branching from the facial nerve, passes from the hyoid arch (IT), inferior
to the blastemal mass, into the mandibular arch ( I L It appears as if the nerve were playing an im-
to the blastemal mass, into the mandibular arch (1). It appears as if the nerve were playing an important role in the separation of the blastema from the second visceral har.
portant role in the separation of the blasterna from the serond I'isceral hm‘.
304 QU.-\R'I‘F.RLY BULI,F.TI‘.\', N.U.M.S.


(V
Blastema of laterohyale


 
POSTERIOR
 
b~Facial nerve
 


___4__-— Glosso—
/
Nf
364 QUARTERLY BULLETIN, N.U.MLS.


e a].
Second
visceral
ar


nerve
 


Second
Pharyngeal
vxsceral


bar
cavity _ _ ee


Triéernindl
nerve
 
I1€I"V€


Fig. 4. The first pharyngeal groove makes a deep impression on the lateral aspect of the blastemal
Fig. 4. The first pharyngeal groove makes a deep impression on the lateral aspect of the blastemal
mass zrhieh is established as the primary connection between the first and second visceral arches.
mass which is established as the primary connection between the first and second visceral arches.
The first visceral bar is located closer to the groove than is the second bar, meaning that the major portion.
The first visceral bar is located closer to the groove than is the second bar, meaning that the major portion.
of the cellular mass belongs to the second arch.
of the cellular mass belongs to the second arch.


Although no longitudinal grooves or diflerences in cellular density exist to distinguish the pri-
Although no longitudinal grooves or differences in cellular density exist to distinguish the primordium of the malleus from that of the incus, the relationships to adjacent structures and the course
mordium of the malleus from that of the incus, the relationships to adjacent structures and the course
of the chorda tympani (about to branch from the facial nerve) are indications that this mesenchymal
of the chorda tympani (about to branch from the facial nerve) are indications that this mesenchymal
mass is the source-tissue of both of these ossicles.
mass is the source-tissue of both of these ossicles.


.-is seen in neighboring sections, the chorda tympani, after branching from the facial nerve, passes
As seen in neighboring sections, the chorda tympani, after branching from the facial nerve, passes
medial to the pharyngeal groove and into the first visceral arch, where it joins the mandibular branch
medial to the pharyngeal groove and into the first visceral arch, where it joins the mandibular branch
of the trigeminal nerve. The pathway of this nerve from the lateral to the medial side of the blastema
of the trigeminal nerve. The pathway of this nerve from the lateral to the medial side of the blastema
serves to separate the primordium for the malleus and ineus from the second visceral bar. A large
serves to separate the primordium for the malleus and incus from the second visceral bar. A large
portion of this mass is located on the second arch side of the pharyngeal groove, suggesting that most of
portion of this mass is located on the second arch side of the pharyngeal groove, suggesting that most of
the primordial tissue which will develop into the manubriusm of the malleus and long crus of the incus
the primordial tissue which will develop into the manubrium of the malleus and long crus of the incus
comes from mesenehymal cells which are of second arch origin. This contradicts the usual belief
comes from mesenchymal cells which are of second arch origin. This contradicts the usual belief
that the malleus and incus are derived entirely from the first arch,
that the malleus and incus are derived entirely from the first arch.
H.-\.\'SO.\' ET AI..—AUI)lTORY OSSICLES St-5
HANSON ET AL.—AUDITORY OSSICLES
Embryo, 8 mm.
Embryo, 8mm.
d. RI£ICHER’I"S CARTILAGE
a. REICHERT’S CARTILAGE


, Hyoid arch
Hyoid arch


/ \
‘ \


   
 
   
   
   
   
 
Facial nerve
---- LL
Interhyale
~Blastema of
malleus and incus
MECKEL’S }
 
   
   


I
‘ é tympani, .
Int why 81 Q ll 1§‘ac1a1 nerve
he Mandibulay! A —
\\ J,
Anterosuperior view nerve, A E rideminal nerve


V "l '\ ‘blastema of
   


malleus and lncus


   
   


CAR’1‘ILAGB' ' tympani ~«
_Hyoid , b.


Mandibular ..\ V
Facial nerve-. vayeh
_ A nerve,/L Tnqemmal nerve
; A
Anterosupenor vlew
 
Facial nerve-. . ' Hyold ‘ '
   
 
     
 
 
   
 


      
      
    
    
    
    


Chorda tympam -
Chorda tympani


I
 
A
Ld,
 
Blastema for 2malleus and incus
 
   
 
 
 
Tyigemunal--- C.
nerve
SUPERIOR | Trigeminal
Mandibular nerve, TLSYVS
 
 
 
Lateral view
 
 
 
() POSTERIOR


Blastema for :1
ANTERIOR
malleus and incus
Malleus and incusy” “Interhyale


 
Ni
 


Triqemlna -—- C.
Laterohyale
nerve I
SUPERIOR ~ “ _IriQemina1
Mandibular nerve‘ nerve
‘ J POSTBRIOR


Anmuon ’Stap“3
4
Ivlalleus and incus :Int"“rhya1"’
Chorda .”
iaterohyale
Facial nerve
Facial nerve
Hyéid
 
tympani
Hyoid
INFERIOR
INFERIOR


Fig. 5. In the 8-mm. (5-week) embryo branchzfal devclagtnzent zs athvtrtcert over that of the -.'I.t2'-mm.
Fig. 5. In the 8-mm. (5-week) embryo branchial development is advanced over that of the‘9.6-mm.
stage in respect to the followirztg: deeper entry of the stapcdzal artery veto the .s't(Iped'tal aulage; _t:_1rth‘¢-r
stage in respect to the following: deeper entry of the stapedial artery into the stapedial anlage; further
separation of the laterohyale from the stapes by the faeml nerve; (l[IIIO.s't complete rupture of contuuuty
separation of the laterohyale from the stapes by the facial nerve; almost com plete rupture of continuity
of the intterbmnchial bridge adjacent to the second ms-coral bar (througlathe lIt.fl'lt(?7lC€ 0} the chnrda
of the interbranchial bridge adjacent to the second visceral bar (through the influence of the chorda
tympani). Ifhether the 8-mm. specilnen is adranccrl, 07‘ thc .’t.f>‘-nun. spcczlncrr ‘cs retarded zn I[¢'t‘('[0p-
tympani). Whether the 8-mm. specimen is advanced, or the 9.6-mm. specimen is retarded in development, cannot, of course, be determined.
ment, cannot, of course, be deternn'm-rt.
;‘m(. QU.~\R'l‘F.RI.Y BULl.F.'I‘I N, N.U.M.S.


Embryo , 11.7 mm.
365
366 QUARTERLY BULLETIN, N.U.MLS.


d. REICHERT '3 CAIIUILAGE
Embryo, 11.7 mm.


    
    
 
 


‘ I . ,Int<2vhya1e
a. REICHERT’S CARTILAGE
V’ ‘ /Laterohyalc
« a. Interhyale
> “Weta Sg
= 2: Wx, Laterohyale
- Stapes
-Incus
Malleus


— Stapczs
——_— e a
' {nous
xMa11euS


if/\ntc1»osu1)ic2.Jr1_oh1hr vLe_v\r I g
Anteroguperior vi¢w
MECKEUS CARTILAGE


Blqstema of hyoid cart11aQ<2
MECKEL’S CARTILAGE


b.
Blastema of hyoid cartilage
\ x /


 
   
   
   
   


Latevohyale
/
 
erg
Malleus


Postcaroinfczlrior View I
Posteroinferioy view .


lncus, shgnrt crus (related to capsule)
Incus, short crus (related to capsule )
POSTERIOR
< POSTERIOR


 
 
      
      
   
   
 
 


Ma11c:us\
Malleus,
SUPERIOR ‘ “
SUPERIOR ‘WS


Remnant of conmzctmon,
‘Remnant of connection,
arches I ,I[
arches I,Il


INFERIOR
INFERIOR


I Lateral viéw ;
I
| Lateral view
a


l"[r/_ (I. I)r’.~‘pi((' !Iwf(1('( (ha! [ha bran(:hi(1[ ol_¢'n1('n.’.s' )‘(‘III(liIl nuns-(’n.('/1.1/n1(1l, .s'em'ra( (l([I‘(lIl(‘(‘.\' have
Fig. 6. Despite the fact that the branchial elements remain mesenchymal, several advances have
I,”-,, ',,,m1pI;mp(w: (ho .‘).6‘-mm. .\'I(I_()('(lm1 the .s-pccznzm of I 1.? 221.211. ((2'_u'eo/vs), the latter here villustrated.
been made between the 9.6-mm. stage and the specimen of 11.7 mm. (6 weeks), the latter here illustrated.
'I'/ur .-lnpmlial (1I‘[(’7‘_I/ has (rI:a11.{/ml lhc .s-tap('rI*1'r1l anI_ag('.1nIn (L (mg Il‘llIl the formalzbn of an obturator
The stapedial artery has changed the sta pedial anlage into a ring with the formation of an obturator
fmwnmz (fig. 6(1); (ho inI.orl1_1/al(' has I‘(’_(]r('.\‘.s'('(I tn. _.s‘zz({, ozrmg [().[)I'('.s:.5‘ll7‘(.' pf llw fac1'al_ nerve,’ the
foramen. (fig. 6a); the interhyale has regressed in size, owing to pressure of the facial nerve; the
.\'I(I[)(‘(1I.(II m1.I(1.ge (mt? l(1I1‘roh_:/(1142 I)v(:q)n(* nmre (l('_.fI‘IlrI((’ p(1r!s of [has _sl1lI vn1z*n1b'rnm)u.s v'z.s'c:cr(1I l?ar,'
stapedial anlage and laterohyale become more definite parts of this still membranous visceral bar;
1}“, p,«i,,m,-y (:(m[iu,m'[_:/ b(’!u'(’('I1 (he m..s~cm'(zl b(1I'.s' z.s _Io.s't as a sepuratum of the uc.‘_crbrarz.cI1zal brulgo
the primary continuity between the visceral bars is lost as a separation of the interbranchial bridge
from the .s'e('.(n1.d vi.s('('2'al bar is (-mnplctcd through (ho 1/1_/I u('_n(-v of the chor(la_ Iynzpafrz (compare fig. 5);
from the second visceral bar is completed through the influence of the chorda tympani (compare fig. 5);
(L qrrmw in the III-(‘.S'(‘Il('}I._I/Hill] m(1.s'.s b('(11*v(»7{ (hr: (l{‘C}I(‘.S' (SUN x.‘0IlI”('Il 110118 11:1/)1 Ih(_' firs! 2'-z'st'e1'_(1I bar) has
‘a groove in the mesenchymal mass between the arches (still continuous with the first visceraltar) has
I[(‘l‘(’[0])(.’(I at riglzt angles to (he first bar, mznnlzng scparalzon of the vrmzordzum of the zncus from
developed at right angles to the first bar, initiating separation of the primordium of the incus from
that of tho maylleus (fig. (ic); 41 scconrlary contvinzz./il_11 b0Iu'cm the firs! two arches is established as the
that of the malleus (fig. 6c); a secondary continuity between the first two arches is established as the
unlugn of the incus np]n‘o.1‘1'7n(1!v.x- the .s-tapulitzl ring, (1 r(*1(IlI'0n.s'In'p zrhit-I1 .\'(‘I'I'('.\' in 27:19:/Iify the rapital
anlage of the incus approximates the stapedial ring, a relationship which serves to identify the capital
par! of (he przTnu'!1'mz s!upo.-.
part of the primitive stapes.
H.-\NSO=.\' ET AL.——AUDITORY OSSICLES 31»,
HANSON ET AL.—AUDITORY OSSICLES 367


Embryo , 14- mm.
Embryo, 14mm.


R1-:1CHERT’S CARTILAGE
a REICHERT’S CARTILAGE
 
; Hyoid blastema
d' Hyoid blastczma


    
    
Line 693: Line 741:
   
   
   
   
 
   
   
   


Stapes
[Anterosuperior view] ‘


[Ant.erosupev1or view!’ ,
MECKEL’S CARTILAGE


M13CKEL’s CARTILAGE
b.


b.
--Stapes


—‘Stapr2s
~~Incus, malleus


“1ncus,ma11euS


I
I


 
 
 
SUPERIOR
   
* Ma11s2US
«stapes


 
 
   
   
   
   


ANTERI OR POS
Posteroinferioy view
‘lnterhyale
h  II . CO1EI:§;I:1aOI;t Caamtrc has
I - II
I N FE RI OR


Fig. 7'. In. the embryo of 14 mm. (6%; -weeks), although general advancement in development is
SUPERIOR
I «Malleus
St
Incu eros
ANTERIOR POSTERIOR
¥ Interhyale
Remnant of
[Lateral view | a, a
INFERIOR
 
Fig. 7. In the embryo of 14 mm. (6% weeks), although general advancement in development is
evidenced, the stapes has not attained the form of a ring; it has been grooved by the artery, but has
evidenced, the stapes has not attained the form of a ring; it has been grooved by the artery, but has
assumed the form of a horseshoe. This observation would indicate a congenital origin for the exces-
assumed the form of a horseshoe. This observation would indicate a congenital origin for the excessively thinned and malformed ossicles frequently seen during endaural surgery.
sirely thinned and malformed ossir'les frequently seen (luring emlaural surgery.


The interbranchial bridge remains on the right side, but the continuity on the left side is broken:
The interbranchial bridge remains on the right side, but the continuity on the left side is broken;
only a remnant of this connection remains (fig. 7c). The interhyale is a rather prominent link
only a remnant of this connection remains (fig. 7c). The interhyale is a rather prominent link
between the stapes and the hyoid bar (fig. 7a). A groove has begun to separate the malleus from the
between the stapes and the hyoid bar (fig. 7a). A groove has begun to separate the malleus from the
incus, but the latter is not yet in contact with the stapes.
incus, but the latter is not yet in contact with the stapes.
.‘»!»8 QUARTF.RI.Y BULLETIN, N.U.M.S.
368 QUARTERLY BULLETIN, N.U.MLS.


Embryo, 15.5mm.
Embryo, 15.5mm.


a. .REICHER’I"S CARTIIIAGE
a. -REICHERT’S CARTILAGE
Hypid arch ,’
Hyoid arch }


   
     
 
 
!


I
laterohyalg


   
 


Laterohyqlz
Interhyale
» Stapes


 
|Anterosuperioy view


llptczrhyalz
‘ _ Stapes


_/’mt«21rosup<2v1'o1» V1<ZW I
MECKEL’S CARTILAGE


b.
to.


Interhyale -
   
   
 


SUDERI OR
Incus


   
   
   
   
 


-I\/lallcus
SUPERIOR
Cc: I Incus
-Malleus
POSTERIOR
POSTERIOR
\
ANTERIOR eas
.__ ~: I 7
lateral view] 1 PY ncrnyale
~ Latczrohyalcz
. \
Lateral vxew ’ 11 Inmyhyale
INFERIOR
INFERIOR
I"i_q. 5’. I N an. 4‘III’II‘_I/I) of 1.5.5 mm. (I11/3 lzw/rs) the annular .s-[(1 pox ron1(1iu.s in I-unflnuily u*i(h the
Fig. 8. In an embryo of 15.5 mm. (61 weeks) the annular stapes remains in continuity with the
/:_I/uirl hm‘ lhrmzglr I/In nmnbrtm.nu.x- I',II[(‘)‘/I]/(![(' as a ('()lIII‘(‘('[‘l..II.'(/ liulr. .-ll!/mug/1 r('du('mI SONI€Il’/N1! ‘in.
//I'i('/.'m‘.s'.\', I/:1‘ -I'n,lw'lI_I/«(Iv /ms 7'Iu'2'('II.s-ml in ('oIIulm' (l¢+n.\*[l_I/.
Only 4: .\‘/1'_(//I! I/n'('/.‘«'Iu'n.g in UN‘ /u/(ml hm‘ r(')n(11?ns I0 so/‘1'(' as u ronn'ml('r of its primary mrztinztily


will: //I(’ mumI2'l;ulm' lmrs, (hr I»I(1.s-(('m(1I IIl(I.\'.s‘ ii.»-(‘If I1(w1'n_(] rI1'fi}'rm1II'((I¢'(I inlo mcscn.c}1_1/mnl “m0dcls"
hyoid bar through the membranous interhyale as a connecting link. Although reduced somewhat in
of //I(’ IIHII/(’Il.\‘ mu! ’l'I1('Il.\’. ’I'Iu' pm-ilinn of HM’ c/mrda t1/mpaluf sorlws (0 remlor tI'isl‘in,gz12'sImble the
thickness, the interhyale has increased in cellular density.
prinumliul ];(II‘l.\' for [he nu1n.ub/"1'Iun of !/Io mallous and (he Iouq crus of [ho 'l'n(‘I1s,' they are not -yet
Ir/mlly .s-4'/mrrxlv, lm-(ruse lm).s-oI_1/ urr(m_r/(Id m('.s-cn.cl1_I/mt: brirl_(/('.x- the _(/(lp be./uwcn. the more densely
/nu-km] st/'u«:[ur('s. '1'/u’ bmly of tho 'zIn.(-us mu] the /mud of the m(tI[('u.s' are not lzzklologically scparaml,
bu! (1 rirvunIf('r¢'I1I'I7(Il .\‘Il[(‘Il.\' is iI:rl1'(:r1(I'z'r- of [/10 s17[(* of I/u*fu[ur(* 1'I1('mIunu1Il('0lur_jm'nl.


A .\'(’.(‘0)1(/(l)‘_I/ ('m1.!im1-I'l_I/ I)('((1'cm I/10 1'1'.s‘('('r(tI burs is m(11'-n!aITno¢l by [he iucmlostapetliul 1111-1701».
Only a slight thickening in the hyoid bar remains to serve as a reminder of its primary continuity
'I'/:(' IIl(’.S‘PI(.(‘/I]/lI((l[ (wlls of tlwir (mlu_(/on l;l(*ml in su('/I (1 n1a1nm' as [0 ub.s-1-urc (/10 mm'gin.s, u (.'2'rcu.m-
with the mandibular bars, the blastemal mass itself having differentiated into mesenchymal “models”
.\'/(lH('(’ 11'/rir/I .s-up/mI'!s (hr conrrpl (ha! (ho long crux of the 'l'I1(‘Il.\' and [he .s-lup('(I7'IIl ring (IeI.v*l0p from
of the malleus and incus. The position of the chorda tympani serves to render distinguishable the
a rmnmon. sourrv, mu/u'1_1/, I/Iw .\'(‘('IIII([ I'im'('/‘(II nrcll.
primordial parts for the manubrium of the malleus and the long crus of the incus; they are not yet
HANSON ET .-\L.——AUDITORY OSSICLES 369
wholly separate, because loosely arranged mesenchyma bridges the gap between the more densely
packed structures. The body of the incus and the head of the malleus are not histologically separated,
but a circumferential sulcus is indicative of the site of the future incudomalleolar joint.
 
A secondary continuity between the visceral bars is maintained by the incudostapedial union.
The mesenchymal cells of their anlagen blend in such a manner as to obscure the margins, a circumstance which supports the concept that the long crus of the incus and the stapedial ring develop from
a common source, namely, the second visceral arch.
HANSON ET AL.—AUDITORY OSSICLES 369


Anterior
Anterior
15-5 rnIn-- cardinal vein.
155 mm. cardinal vein
/


 
   
   
 
 


Auricle \\
Auricle.
(prirnordiuxn) ‘
(primordium)


. '. /. :~°‘:5‘\-
Laterohyale ~a
Otlc Ca sule


Fig. .9. The precartilage stage -is reached in the embryo of 15.5 mm. (7 weeks). However, only
Stapedial
the distal portion of the first and second visceral bars (n'e so adeanced; the pro.cirnal portions of both
bars and the prirnordia of the ossicles are still com posed of condensed mesench_I/me (more compact
than in the previous stage). The stapes is now definitely annular in form, with a distinct obturator
foramen whose margin is separated from the contained stapedial arterg by a less dense zone of Ines-
enchyme.


The crura of the stapes are round in cross—section. The stapes itself is annular. The medial part
nerve —— fe SAS Sa : — artery
seems to be imbedded in the precursor tissue (precartilage) of the developing otic capsule. It is as if
ps
this annular collection of cells, by pressing inward against the otie capsule, were causing capsular
cells to condense in the territory of the future lamina stapedialis ( which will contribute to the base of
the stapes and the annular ligament).


The facial nerve passes between the laterohyale and the stapedial ring just above the level of the
1 Eaed ti
interhyale. The laterohgale and the short crus of the ineus (that is, its Iuesenchymal forerunner) end
lygephetic
freely in loose mesenchymal tissue; they are not get in contact with the otic capsule. In the period
between this and the preceding stage the i nterh gale has undergone further decrease -in size.
370 QUARTERLY BULLETIN, '.\'.U.M.S.


"(wk (17mm.)
Otic capsule


3, Sxte of upper attachment of
Fig. 9. The precartilage stage is reached in the embryo of 15.5 mm. (7 weeks). However, only
the distal portion of the first and second visceral bars are so advanced; the proximal portions of both
bars and the primordia of the ossicles are still composed of condensed mesenchyme (more compact
than in the previous stage). The stapes is now definitely annular in form, with a distinct ebturator
foramen whose margin is separated from the contained stapedial artery by a less dense zone of mesenchyme. :


Re'1c;hert's cartilaqe (lat. hyale
The crura of the stapes are round in cross-section. The stapes itself is annular. The medial part
seems to be imbedded in the precursor tissue (precartilage) of the developing otic capsule. It is as if
this annular collection of cells, by pressing inward against the otic capsule, were causing capsular
cells to condense in the territory of the future lamina stapedialis (which will contribute to the base of
the stapes and the annular ligament).


1’ ~ mqlon) rt/S cartllaqe
The facial nerve passes between the laterohyale and the stapedial ring just above the level of the
interhyale. The laterohyale and the short crus of the incus (that is, its mesenchymal forerunner) end
freely in loose mesenchymal tissue; they are not yet in contact with the otic capsule. In the period
between this and the preceding stage the interhyale has undergone further decrease in size.
370 QUARTERLY BULLETIN, N.U.MLS.


   
Twk. (17mm.)


Rciche
a. Site of upper attachment of
Reichert’s cartilage (lat.hyale Reichert’s cartilage
Leper region ) ea


 
         
 
   
 
   
   
    
    
    
    


 
| 4 Primordium of
 
<~ stapedial muscle


stapedial muscle
e Gnterhyale
' (interhyale
region )
region )


Oslsificatxon center of mandible
Base ~”
of stapes


Mecke1’s cartil/aqrz . M‘ ‘H V '*' " ‘ L‘ L ~-Ossificatxon center (mandible)
Meckel’s cartilage ““a | Anterosuperior view |


Posterainierior View
Ossification center of mandible


thy. I I). I1’ _I/ the 1 7-mm. ()"-week) stage, the mandibular and hyoid bars have developed into cartilage
through the q/‘eater fraction. of their length, and hence may be properly termed Meckel’s and Reichert’s
 
carttlagcs. The prozrimal e.rtreImt_I/ of each. bar and the ossteles are still composed of precartilage;
>--Ossification center (mandible)
/IOII‘(‘l’(‘,I', the malleus and turns are more rtistinctty outlined ~— and less a part of the mesenchyma
 
Posteroinferior view
 
Fig. 10. By the 17-mm. (7-week) stage, the mandibular and hyoid bars have developed into cartilage
through the greater fraction of their length, and hence may be properly termed Meckel’s and Reichert’s
cartilages. The proximal extremity of each bar and the ossicles are still composed of precartilage;
however, the malleus and incus are more distinctly outlined — and less a part of the mesenchyma
from which they were derived.


from urhich they were deriI'ed.
The laterohyale and the short crus of the incus approximate and fuse to the under surface of the
developing capsule between the 15.5 and 17-mm. stages (fig. 10a, at reader's left). The secondary
nature of this continuity with the developing capsule means that the capsule makes no contribution
to these primordia.


The taterohg/ale and the short crus of the incus approximate and fuse to the under surface of the
Concurrently, ossification centers for the mandible appear as membrane bone, one on each half,
rleI'etop't'n_q capsule between. the 15.5 and 17-mm. stages (fig. 10a, at reader's left). The secondary
formed at the distal end of the mandibular arch,
nature of this c0ntin.I1,it_I/ with the (tevelomng capsule means that the capsule makes no contribution
HANSON ET AL.—AUDITORY OSSICLES 371
to these prz'numI2'a.


C'on.¢~urrentty, oss2'ficatt'on centers for the mandible appear as membrane bone, one on each half,
17 mm. REICHERT’S


_t'orrm-:1 at the distal end of the mandzbular arch.
t CARTILAGE
HANSON ET AL.—AUDlTORY OSSICLES 371


R1E11<c1HnERJr’s
(Branchial arch Il)
17 mm’ CARTIIILAGIE
filial


   
     
 
aS Interhyale
t
INCUS


(Branchial arch H)
Otic —4
Facial  «Va  ‘
nerve « T


Fig. 11. Although the interhyale has become considerably narrower in the embryo of 1?’ mm.
Fig. 11. Although the interhyale has become considerably narrower in the embryo of 17 mm.
(7 weeks), it still serves as a definitive connection between the visceral bar (Reichert's cartilage) and
(? weeks), it still serves as a definitive connection between the visceral bar (Reichert’s cartilage) and
the stapes. The second visceral bar may be regarded as bifurcating at its proximal extremity, the diver-
the stapes. The second visceral har may be regarded as bifurcating at its proximal extremity, the divergent parts continuing as the laterohyale and the interhyale, with the facial nerve passing over and
gent parts continuing as the laterohyale and the interhyale, with the facial nerve passing over and
between them. The laterohyale is now continuous with the capsule and the interhyale is (as it was
between. them. The laterohyale is now continuous with the capsule and the interhyale is (as it was
from the beginning) continuous with the stapes. The size, shape and relationships of the interhyale
from the beginning) continuous with the stapes. The size, shape and relationships of the interhyale
have changed markedly since its difierentiatioen from the blastemal lobe of the 7-mm. embryo; its mes-
have changed markedly since its differentiation from the blastemal lobe of the 7-mm. embryo; its mesenchymal composition has not yel been altered, despite the fact that it will soon assume the role of
cnchymal composition has not yet been altered, despite the fact that it will soon assume the ‘role of
tendon for the stapedial muscle.
tendon for the stapedial muscle.


The otic capsule, continuing its increase in size, shows transition from mesenehyme to preeartilage
The otic capsule, continuing its increase in size, shows transition from mesenchyme to precartilage
to cartilage. The stapedial impression into the capsular wall is thus increased by diflerential growth,
to cartilage. The stapedial impression into the capsular wall is thus increased by differential growth,
but the division between the annulus stapedialis and lamina stapedialis remains apparent. The
but the division between the annulus stapedialis and lamina stapedialis remains apparent. The
cells of the stapes, however, blend with those of the incus, there being no articulation as yet at the im-mlo-
cells of the stapes, however, blend with those of the incus, there being no articulation as yet at the incudostapedial junction.
stapedial junction.


A small stapedial artery (arrow) is seen medial to the stapedial ring; it can be traced through the
A small stapedial artery (arrow) is seen medial to the stapedial ring; it can be traced through the
obturator foramen to its source lateral to the ossicle.
obturator foramen. to its source lateral to the ossicle.
372
tr


 
QUARTERLY BULLETIN, N.U.M.S.


Embryo, 21mm.


QUARTERLY BULLETIN, N.U.M.S.
a. _Stapedial muscle
Embmyo, 21 mm.
6‘ /Stapedml muscle
- __Laterohya1e
Q, _  —Facia1 nerve L
l‘ \
lncus
Chorda tympani \ MGHQUS


ll/[\nLQ1‘OSUpC V101» vléw \
 


b Latcro\hya1c2 MECKEVS CART“-‘AGE 6tapeq1a1Lnusc1c


D
y Laterohyale


jg, H .
     
Maneus . \ H‘)/o’1d cartilage
   


’‘ \
p mee Facial nerve


/
 


r
u
..y, ‘
.1_


   
   
 
   
   
    
    
 
LPoSte1*omEer1or vxcw


SUPERIOR
Chorda tympani¥> J \ Malleus
C’ Malleus ’l.‘DCUS
érél  Choyda tylnpant :‘ Facial nerve.
ANTERIOR ; POSTEMOR
.. \ ‘Sta cs
11 / . \Stap<z§1a1mu5c1«2
Latcrohyalc


INFERIOR
Mandible


I"'i_t/. 1...’. I n the wnlnyo of .31 mm. (71/3 Il‘('(‘/Ls‘) the ()ss'i(‘l('.s' are almost entirely cart‘ilag'tn0us. The
[Anterosuperior vie
m(1mI'ihl(*, fornml -in nm)1ln'mu' bum’, is now I wo-thirds as long ax the br(m('h1'r1l arch wh'tch it will
ullimal('[_I/ r('pl(1(‘c.


A (‘omit’)/.s-(1I't0n of cells «lor.s-mrml'i(1l to tho _f(1(:‘£nl ncrrc can. be lI'(l(.'('ll u.pu‘ard to join with the inter-
YW
hyalv, u'}m'¢' the latter (toparts from Ifei(-lm'('.s- cartilage; the zmcrhyale, in turn, is connected with the
b Laterohyale MECKEL’S CARTILAGE ptapedial muscle
stapm at the point of its future arm-ulrltion. wit}: the stapes (cmnpare figs. 18 and 1.9). This con-
dcn.s-atitm. is apparently an outgrowth of me.s'(.'m'l1_I/Inal cells from the interhyale, hence, the primordimn
uf tho .s-tupmliul musclt’ (thv 'intr'rII_1/01¢» -it.s'('If tlemllopirzg into the temlmz. of the mus('le).
H.-\.\'SO.\' ET AL.—AUDITORY OSSlCI.F.S 373


2 8 mm.
wz
Tensor tympam


    
    
 
 
 


I"'i_(/. 1-)’. At a ppro.L'iIm1tel_I/ the J8-mm. stage the embr;/o ])Il.\'.\'('.s‘ ‘into the fetal phase of its 4leI'elop-
MA 1 ate . ‘ : I x
mental histo/'_z/. The ettrtilaginozts os.sieIe.s' hare beeome elearly pretlietiee “mo(lel.s-" of the mlult -S'lI‘ll('-
oe . ~® Hyoid cartilage |
lures, e1‘('t'])l for the retention of two embr_I/orrie feature.»-: the broad eonneetion between. the mull:-u.»
i \ i Mag
amt JIeekeI'.- 4-m'tila_(]e and .\'(’[)(II'(I((‘IH'.s'.\' of the (Interior ]))‘I)(‘(’.\'.\‘.
 
Stapedial  "  Otic
 
muscle - A
 
Qprirnordiuny)‘
 
    capsule


   
    
    
   
   
    
    
   
   
   
 
 
| Posteroinferior view


.4."  '
SUPERIOR


éu
Cc. a


.u g '.
Malleug Incus
‘Tateral view I Facial nerve
[ tateral_ view 4 Chorda tympani, 5 e
ANTERIOR POSTERIOR


: . Stapes
I 4 t at ape nial muscle
Laterohyale
Laterohyale


 
INFERIOR
 
 
Fig. 12. In the embryo of 21 mm. (72 weeks) the ossicles are almost entirely cartilaginous. The
mandible, formed in membrane bone, is now two-thirds as long as the branchial arch which it will
ultimately replace.


l"1'y. 14. By the ,3 -mm. .\'l(l_(](' (81/2 week), the ear(ilaginmt.»- “mo(Iel.s-" of the tI.\‘.\'it‘l(‘.s' I'('.\'eInl:le mlult
A condensation of cells dorsomedial to the facial nerve can be traced upward to join with the interhyale, where the latier departs from Reichert’s cartilage; the interhyale, in turn, is connected with the
.s-trueture.s,' formatiee .s-teps in (lerelopment hare been talcen amt prtmitire t;rr1neh1'al relation..-hip.»
stapes at the point of its future articulation with the stapes (compare figs. 18 and 19). This condensation is apparently an outgrowth of mesenchymal cells from the interhyale, hence, the primordium
have been lost - ~ the latter faet .s'ere-inq to em pt1a.-‘ize the importanee of xtmlying very young ('IIIl)I‘_I/(M.
of the stapedial muscle (the interhyale itself developing into the tendon of the muscle).
HANSON ET AL.—AUDITORY OSSICLES 373


The suleus zehieh will l)e(:ome thefaeial eanal is partially ('l().\‘('tl laterally by the laterohyale (pro.riIIml
28mm.
/)ort'ion of Re'iehert'.s‘ eartilage) where it fll-\‘(‘.s‘ with the otie eapsule. Thi.s- portion of the eartilagI'mm.-
‘Tensor tympam
har 'I'€lll(tl7t-\' an important parietal element up to the ;!.£-u'eel.' .s'IIl_(/e, when -it hegI'n.s- to l)(‘I‘0Ittt’ {neur-
porated in the lower part of the (le_/init2'1'e faeial eanal. El'(‘IIlIlIIll_l/ the entire luterohyale t;eenme.s-
()8-s"ifi(’rl amt loxex ‘its identity in the wall of the adult fueial eanal.


The primordium of the .S'l(l[)(‘(ll(Il mu.s-ele oeeupies a position in the .s-uleux u-hieh l)e('nIIte.\' the faeiul
eanal, lying medial to the nerve. The ea/cal is relatiI'ely small and the eontents are elosely ('()It_llIIt'll
   
therein. (see fig. 15 for the oppo.s-ite, or o.s-.s-iertlar e.1'tremitg of the .\'l(I[)(‘Il'l(ll musele).


The tympanie eaeity is e.rpaml1'n_(/, from the lateral end of the (1 u!litor_r/ tube, to imvule the prim itire
Fig. 13. At approximately the 28-mm. stage the embryo passes into the fetal phase of its developmental history. The cartilaginous ossicles have become clearly predictive ‘‘models” of the adult structures, except for the retention of two embryonic features: the broad connection between the malleus
mesenehymal tissue. The tympanie -mueous nzembrane will lure.»-t the 0.\'.\'l('l('.\' amt eorer the entire
and Meckel’s cartilage and separateness of the anterior process.
contents of the middle ear as the eaeity enlarges.


The ehorda tympani ln'anehe.s- from the fuel"! nerve below the laterohyale amt eou1'.x-es upzrarrl to
muscle —
pass betteeen the man uhrianz of the malleu.- am] the long eras of the ineu.s' teom1;m'e_tig. Id) and .ll:rre.
(primordium);
from into lllt mam!/itmlar areh.
4 Ql'.~\R'l‘F.Rl.Y Bl.'I.l.F,'l‘lT\', N.l'..\1.S.


Co chlea
Fig. 14. By the 28-mm. stage (8/2 week), the cartilaginous ‘“‘models”’ of the ossicles resemble adult
structures; formative steps in development have been taken and primitive branchial relationships
have been lost —- the latter fact serving to emphasize the importance of studying very young embryos.


 
The sulcus which will become the facial canal is partially closed laterally by the laterohyale (proximal
portion of Reichert’s cartilage) where it fuses with the otic capsule. This portion of the cartilaginous
bar remains an important parietal element up to the 24-week stage, when it begins to become incorporated in the lower part of the definitive facial canal. Eventually the entire laterohyale becomes
ossified and loses its identity in the wall of the adult facial canal.


Stap edial
The primordium of the stapedial muscle occupies a position in the sulcus which becomes the facial
.~ ten&on
canal, lying medial to the nerve. The canal is relatively small and the contents are closely confined
therein (see fig. 15 for the opposite, or ossicular extremity of the stapedial muscle).


T (inte rhyale)
The tympanic cavity is expanding, from the lateral end of the auditory tube, to invade the primitive
mesenchymal tissue. The tympanic mucous membrane will invest the ossicles and cover the entire
contents of the middle ear as the cavity enlarges.


I"i_(/. (:3. At a more cranial lerel than that .s-houvn in Fiqure 1.4, the 'iu,terh.t/ale (lemlou of the stapezlial
The chorda tympani branches from the facial nerve below the laterohyale and courses upward to
muxele) m.~'ert.~' into the head of th.e stapes (where the articulation. will later be formed). The course
pass between the manubrium of the malleus and the long crus of the incus (compare fig. 13) and therefrom into the mandibular arch.
of the .s-tapedial muscle can now be traced from -its source in the prim'iti1'e facial canal, to the angle in
374 QUARTERLY BULLETIN, N.U.M.S.
l.’eielIert'.s' cart,ila_(/e where the laterohyale be.giu.s',' then u pecan] and forward as the lateroh_I/ale, through
the loose meseu,ch_I/me of the mirlrlle ear; _/inally to an. iIiserti()u into the posterior aspect. of the heat] of
the stapes. At the stage here illustrated the primortlium of the .s-tapedial muscle aml its tendon are
still in approxiniation with Iteichertls cartilage.


The stapes is z'mp'ingtug on the cart1'lagiuou.s' otic capsule. This area of compact tissue ('_*) serl'e.s
to '1'/lelttif 1/ the developing lam,iu.a .s'l.ape(lia.lis at the site of the future I'e.stibulaI‘fcneslra (oval u'iml0u').
The ea psular t17.s-sue contril)utes to the base of the stapes and to the annular ligament, by which the stapes
will be held w27tl1m the capsule in later stages. The vestibular aspect and feuestral surface of the base
will retain this ea‘rtilaqin.ou.s' lam iua throughout the 'imli1'i(lual's lifetime, as u‘17ll, lil.'ezrI'.-e, the periphery


of the feuestrtl.
Fig. 15. Ata more cranial level than that shown in Figure 14, the interhyale (tendon of the stapedial
H.-\.\'SO'.\' ET AL. ~—.-\UDITORY OSSICl.F.S
muscle) inserts into the head of the stapes (where the articulation will later be formed). The course
of the stapedial muscle can now be traced from its source in the primitive facial canal, to the angle in
Reichert’s cartilage where the laterohyale begins; then upward and forward as the laterohyale, through
the loose mesenchyme of the middle ear; finally to an insertion into the posterior aspect of the head of
the stapes. At the stage here illustrated the primordium of the stapedial muscle and its tendon are
still in approximation with Reichert’s cartilage.


$4
The stapes is impinging on the cartilaginous otic capsule. This area of compact tissue (*) serves
‘Jo
to identify the developing lamina stapedialis at the site of the future vestibular fenestra (oval window).
The capsular tissue contributes to the base of the stapes and to the annular ligament, by which the stapes
will be held within the capsule in later stages. The vestibular aspect and fenestral surface of the base
will retain this cartilaginous lamina throughout the individual's lifetime, as will, likewise, the periphery
of the fenestra,
HANSON ET AL.—AUDITORY OSSICLES 37


FETUS, 81/2 WEEKS
way


Fetus, 8/2 WEEKS
 
   
   
   
    
    
   
    
    
O Dural venous
>...—-—;|--- Sinus
I
4
     
    
    
   
 
 
    
    
 
   
   
    
    


Meninéeal — » P°5.t°.r'i°r1
Dural venous
--—-4--— sinus


tissue ’.,,.»sern1:1lr‘cu ar
i
Can
Otic C2aP5ul°'  ,_.—‘-—Utri.cl.e
cartflage
C y  _.  _L Laterpl
‘lafclurn ‘*5 V1.3’.-' , :‘ 5ernic1r*cular‘
V2st1 u are ._ ; ‘-1. __ ___ duct


9}/’
Brain ~
Periofic tissue ; .‘


(future scala) J‘ l ‘
Meningeal _ Posterior
Cochlear d'L1Ct’;"
tissue _—semicircular
Auiitory tube '
can


— -'- Facial nerve
Otic capsule _——Utricle
cartilage e


Ectoclerrnal
at oo | Lateral
:3 plate for
. on rE BA: semicircular


Intern_a1 eXtQ1",n‘3l
Ge 3 < e ee a duct
Pteryéold —’ . acoustlc meatus
Periotic tissue ~~ i eet ——~ Facial nerve


muscle _ ._ I  .  .- . .
(future scala)
Ml1EClKlEIL°5/ 7  l 1 F l  . g “‘g;§f§§;°,,_§';§‘j5
Cochlear duct-#
Auditory tube +


CARIIIILAGIE » ’ ‘ ' - center)
— = plate for


(Branclnial \‘\
Internal extern
terydgoid — acoustic meatus
muscle
~-~~.Tympanic rin
MECKEL'S- \ Gas fae
CARTILAGE "ee center)
(Branchial ay’ Po


arch I )
arch L) cA


\\ Intecjument
Masa Mass eter


I \
Manclible Masseter
muscle
muscle
I"i_I/. I I-'. llllwr in1pm'tanl ('l1an_qr'.< l7(II‘(’ taken [)lm'(' in [he .38-Inm. _l'¢'lu.~'. Tilt’ 4-H/'lila_a¢ of flu’ nliv‘
(’(l]).\'Hl(' is tlworgrmizing armuul l/14' (‘IulI)l_l]IIIplI(Ill(' .\'[i(l('(‘.\‘ lo lporonzr pvrinlir li.~*.-m-. frnm Il‘lIl('lI ll/4
future I'c.s-lilml(n' aml fympaniv .s-ralar will be fornml. 'l'hi.~' [II‘I)l'(‘.\‘.\' has I"'”!lI'I'-'.~'wl nmrr I'(lI".'”!I
in the )'(’{]l0ll of the ('l)('lIl(’(7 lhan. i H the ('IIIlflll('Ill!lI' l'(’{]I‘()II. TIN’ .~'lII]u'Ill(Il I'IIIpI'¢-.-.-inn on tho mp.~'ulm'
wall, l)(’lIl‘(’(’.'! capsular arul tympani!‘ .s-I1l>4l1'I*i.sir)I¢.~‘. 'i4l('nli_Ii¢’.~‘ Ihc rl('I'¢'lnpin_(/ lamina .~'lapuliuli.- (4-u,.--
.-ular twnlrilmlimt of the base).
'l'h(' (I(l/lil0)‘_I/ lube is e.rlerulin_q -into (hr region of (In fulurr lllllllllt‘ our mwliul In (hr nirnutlr/‘irlrn
of H11’ III(Ill(’ll.\',‘ ils mm'0u.s- IIl(’lIIl)I‘lIl.'(’ (Pill (has ('.l'[)flI.'(l (I) h¢'('0m¢’ (ha! of (he l_I/mpllllil‘ ('m'il_I/.
JIo('kr*l's ¢'m‘lila_(]e mm‘ lim nmlial to (ho 0.s.~‘ifyin_(; mrzmliblc Irilh [ho (‘l0.s('l_.'/ u.s.~'m'ialwI nay.‘-.-«hr
IlIIl.s'('l(’ and lateral (.0 [he infernal [)l(')'i_(]oi(l mu.~*('1('. The ('m'lil(Igin(m.s hnr pu.-.-r.s- up Imrunl llu mull: u.~'.
u-ill: u‘hi¢'h. i.‘ is still broadly ('IHIIl('l'll‘(l (fig. 13).
The anlcrior promss (no! seer: (I! this lorel) aml l_I/I)I[)(1Ill(‘ rinq ma/cc llzwir _ti>'.~'l (1 p[u‘(II‘IIIu'( ul lln'.-
stage’ in llu’fo1'm of 0.\‘.s'iji('(1li0n ¢‘ml('r.s of mr°n1bram' born‘.
The (’('l0tl(’I'I)I(ll platefor (ho (’.l‘l('l’II!Il (uwuslic mcalus apprmu'h¢'.- the lalrml (I.\'p(‘('l of llw nmnuhrimu
of the mall¢*u.s', u‘lm'c it will um’! llw mm'(m.s- mmnbrmze of Me’ lympauit‘ ('(II‘ll[j aml flu’ inlarrrniny
l‘0IIll(’('llI‘(’ li.-.-Iu’ (4lm'im-cl frmn llw nu-.x-mu-l1_:/M111) In furln the lympm:.i(' IIl(’llll)I‘IlIlf'.
37!, QUARTERLY BULLETIN, N.U.M.S.


FETUS. 9WEEKS MIDDLE EAR
o Integument


40 l11l1f1- Tympanic cavity
Fig. 16. Other important changes have taken place in the 28-mm. fetus. The cartilage of the otic
{Auditory ossiclczs
capsule is deorganizing around the endolymphatic spaces to become periotic tissue, from which the
future vestibular and tympanic scalae will be formed. This process has progressed more rapidly
in the region of the cochlea than in the canalicular region. The stapedial impression on the capsular
wall, between capsular and tympanic subdivisions, identifies the developing lamina stapedialis (capsular contribution of the base).


The auditory tube is extending into the region of the future middle ear medial to the manubrium
of the malleus; its mucous membrane will thus expand to become that of the tympanic cavity.
Meckel’s cartilage now lies medial to the ossifying mandible with the closely associated masseter
muscle and lateral to the internal pterigoid muscle. The cartilaginous bar passes up toward the malleus,
with which it is still broadly connected (fig. 13).
The anterior process (not seen at this level) and tympanic ring make their first appearance at this
stage in the form of ossification centers of membrane bone.
The ectodermal plate for the external acoustic meatus approaches the lateral aspect of the manubrium
of the malleus, where it will meet the mucous membrane of the tympanic cavity and the intervening
connective tissue (derived from the mesenchyma) to form the tympanic membrane.
376 QUARTERLY BULLETIN, N.U.M.S.
FETUS, 9 WEEKS MIDDLE EAR
40 mm. Tympanic cavity
uditory ossicles
 
 
   
   
 


Chor1drocre\n1'urn—-—_—‘—‘/
Cranial cavi
 
Chondrocranium——==4 Grain excised)


EXTERNAL EAR
EXTERNAL EAR
“Auricle
be --Cartilage i


~ //’AUPiC1€
PD: caren (earaordicr)


.- ,/ /Cartila 2
 
 
   
 


. ' ///1VI<za’cus%pri1nor<iiurn)
Ne


INTERNAL EAR 3
Otic labyrintha==
Periotic labyrinth——
(future vestibule)
@xic capsule-~ RE LATED
STRUCTURES
~_~—--Condyle
~-~-Coronoid process


~. \ Dural /
RELATED fe
STRUCTURES "A “\


venous sinug
Meckel’s cartilage-* --~ 3 te lee ———— Palate
uditory tube ae NVA BC 77 ----- Body of mandible
nerynx (nasal) ---~ 5 ——-  ----- Nasal concha
o ;
/ if
Integumentum Nares Nasal septum (cartilage)


 
Fig. 17. In the fetus of 40 mm. (9 weeks) all structures which will become part of, or related to,
the ear of the adult, are present in a stale of recognizable incipiency.


.»_.
The cartilaginous otic capsule is a preosseous element of the chondrocranium; within it the reticular
tissue, which replaced precartilage, has in turn been resorbed to produce the intercommunicating
system of the perilymphatic (periotic) labyrinth. Lodged within this labyrinth is that of epithelia
ducts, the endolymphatic (otic) labyrinth.


INTERNAL EAR //_é_
The parts of the adult external ear are represented by the auricle (in which cartilage is already
developing) and by the primordial stalk of ectoderm which, upon rearrangement and disappearance
of cells, will become the external acoustic meatus.


Ohc 1r:\by1‘inth«€—/’—:'
In the middle ear the auditory ossicles are lodged in primitive mesenchymal tissue; they are still
wholly cartilaginous, and will remain so until the fetus has reached the 117-mm. stage, at which
time ossification appears first in the incus.


per-iotuc 1aLbyr1nt}1’ ;
The facial canal and the primordium of the stapedial muscle have changed little since the 28-mm.
stage, advancement being limited to separation of the stapedius from the source-structure, the laterohyale. Segregation is complete in the 43-mm. fetus, and conversion of the undifferentiated mesenchymal cells of the laterohyale into muscle tissue is under way.


(hltmu veshbule) /
In specimen of the same age, fibers from the facial nerve pass to the muscle blastema — an observation which led some investigators to conclude that innervation bu this nerve from the second arch spelled
Otic capsule/’
origin of the stapes from the same branchial source.
HANSON ET AL.—AUDITORY OSSICLES 377


 
Be ise, as r
edie of ™
pista: edial


 
 
   
   


* _ RE LATED
* 3
STRUCTURES
Vestibul
\:‘\——Condy1g
Fig. 18. In the 21-week stage the ossicles are still cartilaginous al the insertion of the tendon and
the incudostapedial joint is still mesenchymal. The ossification center in the slapes is advancing
toward the head, having already converted the crura and the tympanic part of the base into perichondral
bone.


‘ ‘~- Coronom process
The stapedial tendon is inserted into both the long crus of the incus and the head of the stapes (an
arrangement which was encountered in 30 of 198 series, fetal and adult).
378 QUARTERLY BULLETIN, N.U.M:S.


 
   
   
 
   
   
   
   
   
   


RELATED
Tendon of
STRUCTURES / '/
stapedial .
muscle.=


M k 1'5 C  / / Z ‘ I ‘ '‘ ‘‘‘—~——Pa1att2
 
ekfditoilyltgg: ////,’ \-' ‘ _ k » ———— ——Body ogntandible
   
pharynx. (ndfiem —/” /' . «- ““—'*" N<‘15<i1C01’1Cha
 
, _
/
[/1 fl I’/// ‘\
Intcguznentum Narwzé Nasal septun1(car't11aQe)


I"i{/. I 2. I u //I('f('lIl.\' of ,5!) mm. (fl :1'z'r'/rs) all -\'[I'IlI‘(I(I'(‘-N‘ u'lI1',r'/I will (m'umo pm‘! of, 0/‘ rc/4114-rl In,
 
.’/Iv rm‘ of [/10 mlu/I, are /m'.s'z'n( in u slulr of /'«:m_(/m'2(1l)I«' 'I.Il(‘I'/)l'(.'Il(']/.


'I'/In ('uI'Iil4I_r/1'/mus 011?‘ ('1:/;.s-rile is u [))'(’().\'.s'(‘0I(.\' (’[(‘lII('II( of [/l(' 1'/mmlrorrrmium; mil/Iii: [1 HM r('lir-ulrtr
 
I/.-wt‘, Irhir/I /'('pIm'('«I /n'('('tIr(i[u_r/(I, /ms in turn Imw 1'('.wrh('rl In pr0rlu('¢' I/11' (‘II/l‘I'(‘l)lIlIIIlIIl‘!'(‘Il/I'II{[
N‘!/.\'(l’IIl of Ila‘ pm‘/'/.1/m p/m./ir (pm'in[i<') /(I’)_I/I"l'Il(/I. Lmlqml wil/n'n (his [(1')]/I't-Ill/I ix ./lml uf('pi!/u'I1'u
1//u'(.~', /II!‘ rm/oI_I/m/;/IrI{1'(' (otir) (r1l)_I//‘/HI/I.


'I'/u’ /mrls nf /In’ mlull (‘.I‘(("I'Il(I[ mu‘ are I‘(‘[II'(’.\‘(’Il.[(’(I by [I'm uuri('I(- (in 11'/lit’/I ¢'m'(z'Iu_(/0 is /zlrcmly
membrane. 4
«/w'r'In/n'n,(/) uml by //I(’ priINm'4Ii.rIl slul/.‘ of ('rImI¢'rm u‘/I1'('/I, upon I‘('lIl'l‘(lIl{[(‘III(‘I(/ um! ([1.-WI/)[)(’(II'(lIl('(’
of I’('H.\', :ri// I;rm;m' (ln' ('.r(w'u.u( m-uu.s'!ir NIWI/Il.\‘.


I u I//r' m/«Ir//(' war //I(’ umIiIm']/ ns.s'1'('I('.s‘ (lI'(‘ Imly/ml in pI‘im[l1'1'(.' In('.w*Iu'II_I/III!!! I1'.\'.s'1(¢’.' UI¢'_I/ ll"(’ slill
te
u'/m/l_// rur(iluqiImu.x-, am] will ronmin so unlil (hr fetus Ims I'(‘II('/l(’(] [he 117'-mm. -\'IIl_(/I’, (It 1/‘/u'('h
limw n.\-.x~I'/it-I1(I'm1. II[I[I(‘(lI‘.\' _/ir.x'/ in (/10 1'm'u.x'.


'I'//w_l'm-iu/ (mm! um! I/11' /n'1'nmr(I1'm/1 Of I/:4‘ .s'((1pml[Iu' mIl.s‘('](' /mm’ (-I1(1n_(/ml lflllo .\'l'IlI‘(‘ HI!’ J8-mm.
 
.-/11.:/v, (Ir/a'r1nr'4'/mm! /:('/'n_(; I /In "(ml (4; .\‘(’[)(lI'(l[I.(II(, of (/10 .-[um'(liu.x‘ from (/10 .\'!)Il)'('(’-N/I'll/‘IIlI‘(’, l/'10 Iu(('r0-
I/_r/ulv. Sq//‘('_(/zllinn. ix (‘()III[)((’/(‘ in. [/l(' 4.3-mm. f('(u.s, and ('UI1.I'(')‘.\'i(m of (hr unr[I:[ft'r('n['irI(wl III(*.\‘('II-
('/I_I/IIHII r'('[l.s- of flu‘ [(1/(‘I'0/I]/.’l,(’ Dir/[0 Illll-\‘l‘[(‘ (i.s'.s‘Iu' is umlor (I'(I_I/.
 
I II .\‘/N'(‘I'III('I( of Nu» .wm1(' (l_(](’, _/ih(*1‘.s'fI‘tmI I/I('_fn('ial )l(’l‘l'(' [)(l.s'.s‘ In I/Io IIII(.\'('[(‘ I)/(I.s'(¢'nm ~— ma nb.s'('1'm1-
Hun u-/:{r-// /ml .s-mm’ in.I'('.<I{g(I(.(n‘.w In mm'lurl¢' I/ml 1',nIm'wI[1'rm. by [/1 ix n('r1'(' from NH.‘ sm-I)/ul Ill‘('/I xpollwl
m‘/g/in uf I//1' .\‘/ll/I(‘.\‘ from //H’ sumo I;mn.('I11'u.’ .s-uurr-('.
H.-XNSON F.T .-\I..——.-\UDlTORY OSSlCI.F.S 377


    
    
 
   
 


Cafitiiag I “T
iL
, \ ‘


' P2 r 1 chonclral :,  
Fig. 19. In the newborn the ossicles are, in all major features, adult elements of the human skeleton.
' b O  1'  (:,-7'.
The stapes, for example, retains a mere remnant of its fetal structure, namely marrow limited to the


_ ‘  _ M‘
interior of the cervical and capital parts and to the inner circumference of the base.
ca 5 1 u e . _
I"1'q. 18. In. the ,3]-r1'('('A' -\'[(I_lI(' I/Io n.x--[rle.»~ arr .~'lilI rurIilu_r;innu.»- u.’ I/u’ in.-pr/inn of ,/In’ I: L!/rm mul
the in(‘Iu[osII1p<'tIinI joint is .s-[ill lIl(‘.\'(‘Il('/I_I/III(l[. 'I'Iu- n.~'.s-.-'ji4-4Hirn/ (‘I'll/4'I' in [hr .-/u/u-.~' /.\' m/:~um'/nu
Iolmrd (ho hcml, /1uI'£ngu[rm(I_1/ ('l)II!‘('I‘/(‘/I (hv rruru mul llrr (_I/mull/iv purl of M4» /mxr in/n pu'i:-Im;ulru/
lmml.


The sltzpxv/2'(1l lwmlrm is 'L.Il-\‘(‘I'/(‘ll fulo Im//1 (hr lrmy ('ru.~' Hf Nu’ inru.- um’ ll/w /mul uf /In .\/rr_:u.\- mu
Evident likewise in this and many other postnatal specimens (including some to the age of 70 years)
(Irrun_(/enzwzl u‘/tit-/I uws on(-mm!(':'ml in -)’II 0 f 10.8’ .-u'ie~.\-, fvlnl mu.’ mlu//\.
is the occurrence of double insertion of the stapedial tendon. This. means that the early association
378 QUARTERLY BULLETIN, N.U.M.S.
with the incus (compare fig. 18) is not lost as the ossicles mature and as the incudostapedial joint


is formed.
 
 
 


Incufi -
These observations are interpreted to mean that the manubrium of the malleus and long crus of
[long proces


Tendon of ,
the incus, as well as the greater part of the stapes, are derived from the second branchial arch.
stapczdial
HANSON ET AL.—AUDITORY OSSICLES 379
muscle  A ’ i


.4‘ '
   
 


l"i,r/. HI. I n I/w m-whorn tlw U.s'.s'[('/(‘N are, in all majorf('atu.r('s, adult 0lonLmt.s- of the hmmm skeleton.
-Anterior
'I'/u» .\'{(l[I('.\', for (*.ram/:11», r('tm'n.<.' a nzvre renm.a.nt of its fetal .s-[rm'lur0, mmwly marrow limited (0 the
process of
'intrrior of the r'orI'-[ml mu] c-upilal ])(II‘l.\' am] to tho imwr ('[r('unzforen.('e of the base.
malleus


l£'I‘1'(I('/(I I z'Ir(':I"1'.~'o in (Iris mu! mam] 0!/wr po.s-(natal S])(’("iIII('II.S' (1'm'Imling sonic to the age of 70 _z/ears)
yf
is the 0(‘I'IlI'l‘(’II(‘(‘ of rIoul)I(' in.s-vrtftm of (/20 .s‘tapPd1'al tendon. 'I'InT.s-_mcr1n.s that the early association.
—- 1 f
will: I/u‘ I'II(‘I(.\' (mun/m/'(' _/if/. I8) is /to! lost as the n.5'.s'i(‘[:'.\' mature and ax the inczulostapedial joint
> itis. | 78 aul
is fIn'IIIml.


T/I('.w' nh.\-m‘1wIi(m.s- arr intvr/2/‘('14-rl to mean. that the mrmubrium of the mall('us and long (‘rim of
Fig. 20. In the fetus of 161 mm. (19 weeks) Meckel’s cartilage is beginning to undergo ossification
llw .-'m~u.\-I, (Ix uwll (Ix //l(' arm]:-r par! of the slit/ms, arr rIu"1'1'('rI from [hr .x'('('on4[ branrhial arch.
near the zone in which altered tissue will differentiate into that of the anterior ligament of the malleus
H.-\f\'SO.\' Ff!‘ .-\l.. .-\L'l)|TORY OSSlCl.F.S 3"!
(fig. 20a). Three weeks later, in the fetus of 190 mm. (22 weeks) the anterior process of the malleus
has become attached to the neck of the ossicle (fig. 20b, at arrows).


 
In the 215-mm. (24-week) stage, Reichert’s cartilage, continuous with the otic capsule, forms part
 
of the wall of the facial canal (fig. 20c). In early infancy, the cartilage (a derivative of the laterohyale) is a mere remnart (fig. 20d). Newly-formed membrane bone and expanding tympanic cavity


(at : in both figs. 20c and 20d) intervene between the contents of the canal and the residual, invested,
cartilage.


 
 
 


‘V '. _' /ryrnpanic c.‘1\v.'17c
_ ..’Ext..e.'T :1. acoustic X C V
 
' ‘rrgafiéatus -—”  2,4


I"1'g. .30. In [In-frills of Hi] mm. (1!) u‘:'z'A'.s') JIw-l.'('I'.x- rurlilugw is I».«;m’u::[/:_r/ In unr/rrgu u.\-.-v:'_/iv:/(inn
. #Tympanic cavit
near [ho zone in u‘/lirlz rlllorwl If.s-mu will 4Ii_[f('r.~n(irm' inln Hm! uf [hr uni:-riur /i_I/mm'u/ nf I/Ir mu//e rm
(fi!l- .3011). 'I'hro¢’ u'o('l.'.s' lu.’m‘, in .'Iu~f('lu.s- of I!!!) mm. (.3...) uwI.'.s'\ //u’ rmIrrim- /I/'n(‘(‘.x'.\' nf flu mu//ru.-
has ht-come (1[Im'huI to the n.u'Ix' of (low 0.»-.<;';-Io (jig. ..‘nh, ul urrm:-.-‘._


In the .31.’?-nzm. (3,;-Il‘¢'c!\') .\‘((I_(/t‘, lfm'<-Iu-rl‘.s- mrfilugr, 4-uniiuuuuw u-ill: //Ir ulir ('41/r.~’II’4', _/‘arms purl
ie
vfl./10 wall of lhcfrwittl (mm! (fig. Jllr). In curly inftuu-_I/, I/H’ rt:/'l"lug/r (41 ¢l¢'r[1'ulir:- of {hr /ulr:-u-
/l_I/(1[(') is (1 more rcnznm-I (fig. 301/). _\'m~[g-_,"nrnu'(I rm-mh/'um' ham and «gr/mruIin_q I1//n/xunir ruri/_/;
tat * in both _/i_([.\'. 3()(‘ am! 3011) l'II((‘I'l'('II(' bl‘(II'(‘(‘lI H10 ('m1lm.'.-.- nf /hr mnul unrl /hr r4-.-/rluuf. /III'e‘.~'/4'1/_
rnrl-ilage.

Latest revision as of 08:25, 25 December 2018

The Early Embryology Of The Auditory Ossicles In Man: Illustrated In Atlas Series

Jerome R. Hanson, M.S., Barry J. Anson, Ph.D. (Med. Sc.) and Theodore H. Bast, Ph.D.*

INTECEDENT phases of an_ otological investigation, carried out at Northwestern University and the University of Wisconsin de: ut with developmental stages in which the otic capsule,

the auditory ossicles and the related branchial arches were well formed in cartilage.t As a recent supplement

to these more general discussions, three articles have offered detailed information on the morphogenesis of the otic capsule, the stapes and the incus (with atlas arrangement of figures). A fourth article, comparably concerned with the malleus, is in preparation.

It now remains to report upon the de 'From the Department of Anatomy of the University of Wisconsin and the Department of Anatomy of Northwestern University Medical School (Contribution No. 640 from the latter department).

A study carried out with the continuing support of the Central Pica of Research of the American Otological Society and of the National Institutes of Health of the United States Publie Health Service (Grant No. B. 2237). The cost of engravings was met by the use of the NIH grant.

Based upon a thesis presented by Jerome R. Hanson for the degree of Master of Science at the U niversity of Wisconsin; enlarged as a collaborative investigation, during his service as Project-Assistant on the above-named grant.

The drawings were executed by Miss Jean McConnell. The photomicrographs were taken by Mr. Homer Montague, labelled by Miss Rosamond Howland.

The authors are indebted to Dr, Shafik F. Richany who provided valuable assistance during the initial phase of the investigation.

Received for publication September 18, 1959.

  • The illustrations were prepared from the following

series in the G. L. Streeter ( ‘ollection, Carnegie Laboratory, Baltimore, Kr sries 617; Figs. 3 and 4, 6517;

59;



Fig. 5, Fig. 6, 6524; Figs. 8 and 9, 4430: and from the D; H. Bast Collection, University of Wisconsin, Fig. 7, series 180; ligs. 10 and 11, 10; Fig. 12, 174; Figs. 13, 14, 15 and e ir fig. 17, 168; Fig. 18 : Fig. 19. B 124; Vig. 20a, 13; Fig. 20b, 294; ( : Fig. 20d, 98.








Magnific an reconstructions: Fig. Dex 32; Figs. 3, 5, 6 and 7 X 20; Figs. 8 and 10, X 18; Fig. 12, X 16, Fi ‘ig. 13, X 2

Magnifie =m fie ea eens Vig. 2, X 120; Figs. 4 and 9, X 69; Figs. 14 and 15, X 81; Fig. 16. X 25; Fig. 17x 5, i gs. is a 19, X 33; Figs. 20a and 20 b, X 20; Fig. 20e, X 13 20d, X 12.


‘Deceased January 1

‘Pertinent articles already have been cited in an earlier issue of this journal (vol. 32, 1958, pp. 157-172).

‘Anson, B. J. and Bast, T. H.: Development of the Otic Capsule o. the Human Ear. Quart. Bull. Northwestern University Medical School, 32:157-172, 1958.

Anson, B. J. and Bast, T. H.: Development of the Stapes of the Human Ear. Quart. Bull. Northwestern University Medical School, 33: 44-59, 1959.

Anson, B. J. and Bast, T.H.: Development of the Tneus of the Human Bar. Quart. Bull. Northwestern University medical School, 33: 110-119, 1959.

358

Developmental steps, taken before the stage of 28-mm., in which localized portions of the mesenchyma in the branchial region suddenly become distinguishable from the tissues of which they are primordially a part and, at the same time, assume an appearance and a position predictive of their adult form and topography.

In order to determine accurately the origin of the ossicles it is necessary to examine them prior to the aforementioned stage, beginning with specimens in which the future ossicles and the related branchial arches have not reached pre‘artilaginous constituency. In the past, investigators attempted to explain the origin of the ossicles without benefit of surly embryos. In such studies, limited as they were to the use of embryos in which the branchial arches and_ their derivatives were already composed of ‘artilage, conjecture inescapably took the place of fact in the attempt to account for the genesis of the auditory ossicles in man.®

Microscopic sections used alone are of limited value in following the rapidly changing architecture of the branchial arches, but reconstructions provide the needed aid in determining what contribution the mesenchymal condensations give the developing structures.’ The following discussion will be based chiefly upon the use of such ‘‘models.”’

In the fifth week of fetal life the stapes is not yet a definitive portion of a

‘Reviews of the literature on ossicular development have been presented by Fraser (1882), Gradenigo (1887), Dreyfuss (1893), Gaupp (1899), Broman (1899), Kingsley (1900), Fuehs (1905), Reagan (1917), van der Klaauw (1924), and Cauldwell and Anson (1942). Translations of the German literature prepared by Mrs. Eycke Strickland have been used as guidance in this present study. A complete presentation of the literature on early embryology of the ossicles by Mrs. Strickland and the present authors 1s Jn preparation,

‘As the authors have commented before, only by the use of reconstructions ean the continuity of fluctuating tissues and interrelationships of shifting structures be

established to the conviction of the writer and be pictured to the satisfaction of the reader. HANSON ET AL.—AUDITORY OSSICLES

blastemal lobe which is situated at the proximal extremity of the hyoid (Reichert’s) bar (fig. 1). This lobe is grooved by the facial nerve, which serves to divide it into a stapedial primordium and the laterohyale, both of which temporarily retain hyoid continuity (fig. 2). In the 9.6-mm. stage the division is more definitely marked. The portion which connects the above-mentioned structures is called the interhyale (fig. 3); it will give rise to the stapedial tendon.

In the earliest stages the two visceral bars are broadly connected by an interbranchial bridge of mesenchyme (figs. 1 and 3), the greater part of which is in the territory of the second arch as indicated by its relationship to the pharyngeal groove (figs. 3 and 4). This blastemal mass is located between, and continuous with, the middle segment of the hyoid bar and the proximal portion of the mandibular (Meckel’s) bar. This circumstance indicates that the manubrium of the malleus and long crus of the incusare mainly of second arch origin.

In the 8-mm. specimen, which is more advanced in ossicular development than the 9.6-mm. stage, the interbranchial bridge is separating from the hyoid bar along a suleus which transmits the chorda tympani (fig. 5). Separation is complete in the 11.7-mm. stage, at which time a secondary connection between the arches is formed as the incus, now of distinguishable outline, comes to approximate the stapes (fig. 6).

During the fifth week the stapedial artery attains 2 central position in the blastemal lobe, thereby seeming to aid in the conversion of the rounded mass into a ring-like structure with an obturator foramen (figs. 5 to 9). Oceasionally a ring fails to form, and an anomalous stapes is the result; the horseshoe-shaped stapes in a [4-mm. embryo is an example of this defect (fig. 7).

The malleus and in¢us in the 15.5-mm. embryo, although still precartilaginous, become demarcated as the manubrium and long crus begin to assume characteristic form and as a groove appears between the head of the malleus and body of the incus (fig. 8). At this stage the ring-shaped stapes impinges upon the otic capsule. The laterohyale and short crus of the incus end in loose adventitia (fig. 9). In the 17-mm. embryo, both the incus and malleus are clearly identifiable as chondrified structures. The malleus temporarily remains in continuity with the mandibular (Meckel’s) bar (fig. 10).

The interhyale passes from the junction of the stapes and incus to the hyoid bar (fig. 11) where the latter makes an acute angle to become the laterohyale (in contact with capsular tissue). The primordium of the stapedial muscle is identifiable in the 21-mm. stage (fig. 12) as an outgrowth from the interhyale, located posterior to the angle of Reichert’s cartilage and medial to the facial nerve (figs. 13 and 14). The tendon of the stapedial muscle is derived from the interhyale in the portion between the developing stapes and Reichert’s bar (figs. 15 and 16). The stapedial ring now fuses with the otic capsule, the conjoined tissue thus becoming the lamina stapedialis. The periphery of the lamina, through differentiation of its tissue. will become the annular ligament. The zone of change is the site of the future vestibular fenestra (fig. 15).

Continuity between the interhyale (seemingly the primordium of the stapedial muscle as well as the tendon) and the laterohyale is lost in the 40-mm fetus; at this stage the constituent cells begin to assume the appearance of muscle (fig. 17).

As the muscle develops and the incudostapedial joint is formed, the tendon usually gains an attachment to the neck stapes. However, the frequent partial insertion of the stapedial tendon into the incus (figs. 18 and 19) supports the belief that the long crus of the incus, as well as the stapes, is a derivative of the second arch.

Both of the cartilaginous arches contribute not only to the substance of the auditory ossicles, but also to that of related structures in the head and neck.

‘Bast. T. H., Anson, B. J. and Riechany, 8. Development of the Second Branchial Arch Cartilage), Facial Canal

Man. Qi Bull. Northwestern School, 30 5-249, 1956.

Richany, F.. Bast, T. H. and Auson, B. J.: The Development of the First Branchial Are in Man and the Fate of Meckel's Cartilage. Quart. Bull. Northwestern University Medica! Sehool, 30: 331-355, 1956.

F.: The Reichert's and Associated Structures in Medieai



While the malleus is undergoing ossification, the zone of continuity with Meckel’s cartilage narrows rapidly (fig. 20a). This alteration in form is due to a retrograde change in the cartilage which precedes differentiation of the tissue into that of the future anterior ligament of the malleus. As soon as bone is formed in the head and neok of the malleus the anterior process (an osseous rod before bone-formation begins in the ossicle itself) fuses with the malleus (fig. 20b). Distally the cartilage will be absorbed in the mandible.

Reichert’s cartilage passes through an even more dramatic series of changes in attaining adulthood. At its proximal extremity, that part of the cartilage which is derived from the laterohyale of the

early embryo forms a transitory lateral boundary for the developing facial canal (fig. 20c). By the 215-mm. stage, however, membrane bone is developing internal to the cartilage—thus intervening between cartilage and nerve (and stapedial muscle, derived from the interhyale). Concurrently, the otic capsule is ossifying. In early infancy, Reichert’s ‘artilage is merely a remnant within new bone, and the facial canal has acquired new and permanent walls (fig. 20d). Distally the tissue of the original arch is converted into the styloid process of the temporal bone, the stylohyoid ligament and the lesser cornu of the hyoid bone.

The 2llustrations appear on the succeeding pages. HANSON ET AL.—AUDITORY OSSICLES 361

Embryo, 7mm.

ae REICHERT’S CARTILAGE Stapedial a yp». (branchial arch I)»




_-- Stapedial blastema Laterohyale (Broman )

MECKEL’S CARTILAGE setae (branchial arch I)




Stapedial a’ Facial nerve laterohyale

‘Chorda tympani

Posteroinferior view

SUPERIOR

\.. Facial nerve

=, ~Blastemal mass for stapes

POSTERIOR



C. Laterohyale~*

ANTERIOR 4 Chorda tympani INFERIOR

Fig. 1. In the embryo of 41/2 weeks (7mm.) the precursor tissue for the auditory ossicles is @ common blastemal mass which is distinguishable from the surrounding mesenchyma only because of the greater concentration of its constituent cells (compare fig. 2).

A lobe-like portion of this mass is located at the cranial end of the second visceral bar (precursor of Reichert’s cartilage), where it is grooved by the facial nerve. Part of this mass is the primordium of the stapes. However, it is still separate from the aggregation of cells which will become the otic capsule (the latter not included in the reconstruction). The stapedial artery extends from its sourcevessel to encroach upon the interiomedial aspect of the blastema (fig. 1a); the chorda tympani branches from the facial nerve to pass medial to the first visceral bar, the forerunner of Meckel’s cartilage (fig. 1b).

A mesenchymal bridge of cells between the first and second visceral bars extends from the proxi mal end of the mandibular bar (at I in fig. 1c) to a point on the hyoid bar (at IT) just distal to the blastemal lobe of the stapes (fig. 1c). The primordia of the malleus and incus are not yet distinct structures within this condensation of cells which will soon give rise to them. 362 QUARTERLY BULLETIN, N.U.MLS.

7mm. Glossopharyngeal


Stapedial artery

(origin)

Ag: — Laterohyale




4 Pharyngeal

> groove




f rea 4 imae 3 4 a ag .

avs : PP MeO a Gi

aso, PaO TT ae


Fig. 2. As is clearly demonstrated in sections, the common blastemal lobe is situated dorsal to the first pharyngeal groove, where it is indented by the facial nerve on its dorsolateral aspect. It is through the presence of the sulcus produced by the nerve that the following forecast may be made: the medial and larger part of the lobe will give rise to the stapes; the part lateral to the nerve will become the laterohyale; the interconnecting portion, which is still very broad, will become the interhyale. The narrowing of the interhyale and subsequent separation of the stapedial portion from the laterohyale is seemingly influenced by the pressure of the facial nerve, as this mass increases at a more rapid rate than does the nerve itself.

The presence of the stapedial artery identifies part of the general blastema as the ‘‘stapes’’; it is still solid, not having yet acquired the form of an annulet. The future position of the artery in the center of the mass appears to be due to a folding around the artery as the blastema enlarges. The process seems to be one of envelopment of the artery by growth of the mass rather than one of perforation through elongation of the vessel,

Al this stage the blastema may be said, for the first time, to possess a distinguishable boundary. In the 6Yo-mm. stage the tissue in the corresponding branchial area is a simple, diffuse mesenchyme. HANSON ET AL.—AUDITORY OSSICLES 363

Embryo, 9.6mm.





a. REICHERT’S CARTILAGE (IL) 4 / levee as / SMa Blastemal masses: Interhyale-* stapes

.-Malleus , incus - .~S_Facial nerve Anterosuperior view | wot

MECKEL’S CARTILAGE oy .

Trigeminal nerve




-Laterohyale

.~Incus > malleus

I Spacek Posteroinferior View

SUPERIOR




Blastema of stapes-_" 7 C. ANTERIOR

I Blastema of malleus, incus

| Lateral view INFERIOR

Fig. 3. In the embryo of 512 weeks (9.6 mm.) the branchial structures have increased greatly size through hyperplasia of the mesenchymal cells and the outlines of the ossicular primordia have become more clearly defined.

The second visceral bar projects farther toward the otic labyrinth than the first and has at its proximal extremity the blastemal lobe with the primordium of the stapes. The facial nerve has grooved the lobe more deeply, the sulcus serving to mark off more distinctly the stapedial from the laterohyale portion. The primordium of the stapes is still separated from the otic capsule (not shown) by a zone of cells which is less dense than the mesenchyme of either the stapes or the capsule. The general location of the stapes (lateral to the otic capsule and medial to the facial nerve) is one which persists throughout fetal life and into adulthood.

Although a stapedial artery is not yet centrally located within the blastema, an artery is found (not shown in the reconstruction) at the periphery of the lobe as it was in the 7-mm. stage.

The malleus and incus are not yet differentiated from the interbranchial bridge of mesenchyme which now broadly connects the two visceral bars across the first pharyngeal groove (fig. de at arrow). Since the groove is the boundary externally between the arches (I and II), double origin of the two ossicles is thereby indicated.

The chorda tympani, branching from the facial nerve, passes from the hyoid arch (IT), inferior to the blastemal mass, into the mandibular arch (1). It appears as if the nerve were playing an important role in the separation of the blastema from the second visceral har.

Blastema of laterohyale

POSTERIOR b~Facial nerve

/ Nf 364 QUARTERLY BULLETIN, N.U.MLS.

Second visceral ar


Pharyngeal

cavity _ _ ee

nerve

Fig. 4. The first pharyngeal groove makes a deep impression on the lateral aspect of the blastemal mass which is established as the primary connection between the first and second visceral arches. The first visceral bar is located closer to the groove than is the second bar, meaning that the major portion. of the cellular mass belongs to the second arch.

Although no longitudinal grooves or differences in cellular density exist to distinguish the primordium of the malleus from that of the incus, the relationships to adjacent structures and the course of the chorda tympani (about to branch from the facial nerve) are indications that this mesenchymal mass is the source-tissue of both of these ossicles.

As seen in neighboring sections, the chorda tympani, after branching from the facial nerve, passes medial to the pharyngeal groove and into the first visceral arch, where it joins the mandibular branch of the trigeminal nerve. The pathway of this nerve from the lateral to the medial side of the blastema serves to separate the primordium for the malleus and incus from the second visceral bar. A large portion of this mass is located on the second arch side of the pharyngeal groove, suggesting that most of the primordial tissue which will develop into the manubrium of the malleus and long crus of the incus comes from mesenchymal cells which are of second arch origin. This contradicts the usual belief that the malleus and incus are derived entirely from the first arch. HANSON ET AL.—AUDITORY OSSICLES Embryo, 8mm. a. REICHERT’S CARTILAGE

Hyoid arch

‘ \




Facial nerve

LL

Interhyale

~Blastema of malleus and incus

MECKEL’S }



‘ é tympani, . he Mandibulay! A — Anterosuperior view nerve, A E rideminal nerve




_Hyoid , b.

Facial nerve-. vayeh

A








Chorda tympani


A Ld,

Blastema for 2malleus and incus





Tyigemunal--- C. nerve SUPERIOR | Trigeminal Mandibular nerve, TLSYVS



Lateral view



() POSTERIOR

ANTERIOR Malleus and incusy” “Interhyale

Ni

Laterohyale

4 Chorda .” Facial nerve

tympani Hyoid INFERIOR

Fig. 5. In the 8-mm. (5-week) embryo branchial development is advanced over that of the‘9.6-mm. stage in respect to the following: deeper entry of the stapedial artery into the stapedial anlage; further separation of the laterohyale from the stapes by the facial nerve; almost com plete rupture of continuity of the interbranchial bridge adjacent to the second visceral bar (through the influence of the chorda tympani). Whether the 8-mm. specimen is advanced, or the 9.6-mm. specimen is retarded in development, cannot, of course, be determined.

365 366 QUARTERLY BULLETIN, N.U.MLS.

Embryo, 11.7 mm.


a. REICHERT’S CARTILAGE « a. Interhyale > “Weta Sg = 2: Wx, Laterohyale - Stapes -Incus Malleus

——_— e a

Anteroguperior vi¢w

MECKEL’S CARTILAGE

Blastema of hyoid cartilage \ x /




/

erg Malleus

Posteroinferioy view .

Incus, short crus (related to capsule ) < POSTERIOR




Malleus, SUPERIOR ‘WS

‘Remnant of connection, arches I,Il

INFERIOR

I | Lateral view a

Fig. 6. Despite the fact that the branchial elements remain mesenchymal, several advances have been made between the 9.6-mm. stage and the specimen of 11.7 mm. (6 weeks), the latter here illustrated. The stapedial artery has changed the sta pedial anlage into a ring with the formation of an obturator foramen. (fig. 6a); the interhyale has regressed in size, owing to pressure of the facial nerve; the stapedial anlage and laterohyale become more definite parts of this still membranous visceral bar; the primary continuity between the visceral bars is lost as a separation of the interbranchial bridge from the second visceral bar is completed through the influence of the chorda tympani (compare fig. 5); ‘a groove in the mesenchymal mass between the arches (still continuous with the first visceraltar) has developed at right angles to the first bar, initiating separation of the primordium of the incus from that of the malleus (fig. 6c); a secondary continuity between the first two arches is established as the anlage of the incus approximates the stapedial ring, a relationship which serves to identify the capital part of the primitive stapes. HANSON ET AL.—AUDITORY OSSICLES 367

Embryo, 14mm.

a REICHERT’S CARTILAGE

Hyoid blastema





[Anterosuperior view] ‘

MECKEL’S CARTILAGE

b.

--Stapes

~~Incus, malleus


I






Posteroinferioy view

SUPERIOR I «Malleus St Incu eros ANTERIOR POSTERIOR ¥ Interhyale Remnant of [Lateral view | a, a INFERIOR

Fig. 7. In the embryo of 14 mm. (6% weeks), although general advancement in development is evidenced, the stapes has not attained the form of a ring; it has been grooved by the artery, but has assumed the form of a horseshoe. This observation would indicate a congenital origin for the excessively thinned and malformed ossicles frequently seen during endaural surgery.

The interbranchial bridge remains on the right side, but the continuity on the left side is broken; only a remnant of this connection remains (fig. 7c). The interhyale is a rather prominent link between the stapes and the hyoid bar (fig. 7a). A groove has begun to separate the malleus from the incus, but the latter is not yet in contact with the stapes. 368 QUARTERLY BULLETIN, N.U.MLS.

Embryo, 15.5mm.

a. -REICHERT’S CARTILAGE Hyoid arch }



!

laterohyalg


Interhyale » Stapes

|Anterosuperioy view


MECKEL’S CARTILAGE

to.

Interhyale -





SUPERIOR Cc: I Incus -Malleus POSTERIOR ANTERIOR eas lateral view] 1 PY ncrnyale INFERIOR Fig. 8. In an embryo of 15.5 mm. (61 weeks) the annular stapes remains in continuity with the

hyoid bar through the membranous interhyale as a connecting link. Although reduced somewhat in thickness, the interhyale has increased in cellular density.

Only a slight thickening in the hyoid bar remains to serve as a reminder of its primary continuity with the mandibular bars, the blastemal mass itself having differentiated into mesenchymal “models” of the malleus and incus. The position of the chorda tympani serves to render distinguishable the primordial parts for the manubrium of the malleus and the long crus of the incus; they are not yet wholly separate, because loosely arranged mesenchyma bridges the gap between the more densely packed structures. The body of the incus and the head of the malleus are not histologically separated, but a circumferential sulcus is indicative of the site of the future incudomalleolar joint.

A secondary continuity between the visceral bars is maintained by the incudostapedial union. The mesenchymal cells of their anlagen blend in such a manner as to obscure the margins, a circumstance which supports the concept that the long crus of the incus and the stapedial ring develop from a common source, namely, the second visceral arch. HANSON ET AL.—AUDITORY OSSICLES 369

Anterior 155 mm. cardinal vein /






Auricle. (primordium)

Laterohyale ~a

Stapedial

nerve —— fe SAS Sa : — artery ps

1 Eaed ti lygephetic

Otic capsule

Fig. 9. The precartilage stage is reached in the embryo of 15.5 mm. (7 weeks). However, only the distal portion of the first and second visceral bars are so advanced; the proximal portions of both bars and the primordia of the ossicles are still composed of condensed mesenchyme (more compact than in the previous stage). The stapes is now definitely annular in form, with a distinct ebturator foramen whose margin is separated from the contained stapedial artery by a less dense zone of mesenchyme. :

The crura of the stapes are round in cross-section. The stapes itself is annular. The medial part seems to be imbedded in the precursor tissue (precartilage) of the developing otic capsule. It is as if this annular collection of cells, by pressing inward against the otic capsule, were causing capsular cells to condense in the territory of the future lamina stapedialis (which will contribute to the base of the stapes and the annular ligament).

The facial nerve passes between the laterohyale and the stapedial ring just above the level of the interhyale. The laterohyale and the short crus of the incus (that is, its mesenchymal forerunner) end freely in loose mesenchymal tissue; they are not yet in contact with the otic capsule. In the period between this and the preceding stage the interhyale has undergone further decrease in size. 370 QUARTERLY BULLETIN, N.U.MLS.

Twk. (17mm.)

a. Site of upper attachment of Reichert’s cartilage (lat.hyale Reichert’s cartilage Leper region ) ea







| 4 Primordium of

<~ stapedial muscle

e Gnterhyale region )

Base ~” of stapes

Meckel’s cartilage ““a | Anterosuperior view |

Ossification center of mandible


>--Ossification center (mandible)

Posteroinferior view

Fig. 10. By the 17-mm. (7-week) stage, the mandibular and hyoid bars have developed into cartilage through the greater fraction of their length, and hence may be properly termed Meckel’s and Reichert’s cartilages. The proximal extremity of each bar and the ossicles are still composed of precartilage; however, the malleus and incus are more distinctly outlined — and less a part of the mesenchyma from which they were derived.

The laterohyale and the short crus of the incus approximate and fuse to the under surface of the developing capsule between the 15.5 and 17-mm. stages (fig. 10a, at reader's left). The secondary nature of this continuity with the developing capsule means that the capsule makes no contribution to these primordia.

Concurrently, ossification centers for the mandible appear as membrane bone, one on each half, formed at the distal end of the mandibular arch, HANSON ET AL.—AUDITORY OSSICLES 371

17 mm. REICHERT’S

t CARTILAGE

(Branchial arch Il) filial


aS Interhyale t INCUS

Otic —4

Fig. 11. Although the interhyale has become considerably narrower in the embryo of 17 mm. (? weeks), it still serves as a definitive connection between the visceral bar (Reichert’s cartilage) and the stapes. The second visceral har may be regarded as bifurcating at its proximal extremity, the divergent parts continuing as the laterohyale and the interhyale, with the facial nerve passing over and between them. The laterohyale is now continuous with the capsule and the interhyale is (as it was from the beginning) continuous with the stapes. The size, shape and relationships of the interhyale have changed markedly since its differentiation from the blastemal lobe of the 7-mm. embryo; its mesenchymal composition has not yel been altered, despite the fact that it will soon assume the role of tendon for the stapedial muscle.

The otic capsule, continuing its increase in size, shows transition from mesenchyme to precartilage to cartilage. The stapedial impression into the capsular wall is thus increased by differential growth, but the division between the annulus stapedialis and lamina stapedialis remains apparent. The cells of the stapes, however, blend with those of the incus, there being no articulation as yet at the incudostapedial junction.

A small stapedial artery (arrow) is seen medial to the stapedial ring; it can be traced through the obturator foramen. to its source lateral to the ossicle. tr

QUARTERLY BULLETIN, N.U.M.S.

Embryo, 21mm.

a. _Stapedial muscle




y Laterohyale



p mee Facial nerve


u




Chorda tympani¥> J \ Malleus

Mandible

[Anterosuperior vie

YW b Laterohyale MECKEL’S CARTILAGE ptapedial muscle

wz



MA 1 ate . ‘ : I x oe . ~® Hyoid cartilage | i \ i Mag





| Posteroinferior view

SUPERIOR

Cc. a

Malleug Incus ‘Tateral view I Facial nerve [ tateral_ view 4 Chorda tympani, 5 e ANTERIOR POSTERIOR

. Stapes

I 4 t at ape nial muscle Laterohyale

INFERIOR

Fig. 12. In the embryo of 21 mm. (72 weeks) the ossicles are almost entirely cartilaginous. The mandible, formed in membrane bone, is now two-thirds as long as the branchial arch which it will ultimately replace.

A condensation of cells dorsomedial to the facial nerve can be traced upward to join with the interhyale, where the latier departs from Reichert’s cartilage; the interhyale, in turn, is connected with the stapes at the point of its future articulation with the stapes (compare figs. 18 and 19). This condensation is apparently an outgrowth of mesenchymal cells from the interhyale, hence, the primordium of the stapedial muscle (the interhyale itself developing into the tendon of the muscle). HANSON ET AL.—AUDITORY OSSICLES 373

28mm. ‘Tensor tympam



Fig. 13. At approximately the 28-mm. stage the embryo passes into the fetal phase of its developmental history. The cartilaginous ossicles have become clearly predictive ‘‘models” of the adult structures, except for the retention of two embryonic features: the broad connection between the malleus and Meckel’s cartilage and separateness of the anterior process.

muscle — (primordium);

Fig. 14. By the 28-mm. stage (8/2 week), the cartilaginous ‘“‘models”’ of the ossicles resemble adult structures; formative steps in development have been taken and primitive branchial relationships have been lost —- the latter fact serving to emphasize the importance of studying very young embryos.

The sulcus which will become the facial canal is partially closed laterally by the laterohyale (proximal portion of Reichert’s cartilage) where it fuses with the otic capsule. This portion of the cartilaginous bar remains an important parietal element up to the 24-week stage, when it begins to become incorporated in the lower part of the definitive facial canal. Eventually the entire laterohyale becomes ossified and loses its identity in the wall of the adult facial canal.

The primordium of the stapedial muscle occupies a position in the sulcus which becomes the facial canal, lying medial to the nerve. The canal is relatively small and the contents are closely confined therein (see fig. 15 for the opposite, or ossicular extremity of the stapedial muscle).

The tympanic cavity is expanding, from the lateral end of the auditory tube, to invade the primitive mesenchymal tissue. The tympanic mucous membrane will invest the ossicles and cover the entire contents of the middle ear as the cavity enlarges.

The chorda tympani branches from the facial nerve below the laterohyale and courses upward to pass between the manubrium of the malleus and the long crus of the incus (compare fig. 13) and therefrom into the mandibular arch. 374 QUARTERLY BULLETIN, N.U.M.S.


Fig. 15. Ata more cranial level than that shown in Figure 14, the interhyale (tendon of the stapedial muscle) inserts into the head of the stapes (where the articulation will later be formed). The course of the stapedial muscle can now be traced from its source in the primitive facial canal, to the angle in Reichert’s cartilage where the laterohyale begins; then upward and forward as the laterohyale, through the loose mesenchyme of the middle ear; finally to an insertion into the posterior aspect of the head of the stapes. At the stage here illustrated the primordium of the stapedial muscle and its tendon are still in approximation with Reichert’s cartilage.

The stapes is impinging on the cartilaginous otic capsule. This area of compact tissue (*) serves to identify the developing lamina stapedialis at the site of the future vestibular fenestra (oval window). The capsular tissue contributes to the base of the stapes and to the annular ligament, by which the stapes will be held within the capsule in later stages. The vestibular aspect and fenestral surface of the base will retain this cartilaginous lamina throughout the individual's lifetime, as will, likewise, the periphery of the fenestra, HANSON ET AL.—AUDITORY OSSICLES 37

way

Fetus, 8/2 WEEKS








Dural venous --—-4--— sinus

i

Brain ~

Meningeal _ Posterior tissue _—semicircular can

Otic capsule _——Utricle cartilage e

at oo | Lateral . on rE BA: semicircular

Ge 3 < e ee a duct Periotic tissue ~~ i eet ——~ Facial nerve

(future scala) Cochlear duct-# Auditory tube +

— = plate for

Internal extern terydgoid — acoustic meatus muscle ~-~~.Tympanic rin MECKEL'S- \ Gas fae CARTILAGE "ee center) (Branchial ay’ Po

arch L) cA

Masa Mass eter

muscle

o Integument

Fig. 16. Other important changes have taken place in the 28-mm. fetus. The cartilage of the otic capsule is deorganizing around the endolymphatic spaces to become periotic tissue, from which the future vestibular and tympanic scalae will be formed. This process has progressed more rapidly in the region of the cochlea than in the canalicular region. The stapedial impression on the capsular wall, between capsular and tympanic subdivisions, identifies the developing lamina stapedialis (capsular contribution of the base).

The auditory tube is extending into the region of the future middle ear medial to the manubrium of the malleus; its mucous membrane will thus expand to become that of the tympanic cavity.

Meckel’s cartilage now lies medial to the ossifying mandible with the closely associated masseter muscle and lateral to the internal pterigoid muscle. The cartilaginous bar passes up toward the malleus, with which it is still broadly connected (fig. 13).

The anterior process (not seen at this level) and tympanic ring make their first appearance at this stage in the form of ossification centers of membrane bone.

The ectodermal plate for the external acoustic meatus approaches the lateral aspect of the manubrium of the malleus, where it will meet the mucous membrane of the tympanic cavity and the intervening connective tissue (derived from the mesenchyma) to form the tympanic membrane. 376 QUARTERLY BULLETIN, N.U.M.S.

FETUS, 9 WEEKS MIDDLE EAR 40 mm. Tympanic cavity uditory ossicles



Cranial cavi

Chondrocranium——==4 Grain excised)

EXTERNAL EAR “Auricle

be --Cartilage i

PD: caren (earaordicr)




Ne

INTERNAL EAR 3 Otic labyrintha== Periotic labyrinth—— (future vestibule) @xic capsule-~ RE LATED STRUCTURES ~_~—--Condyle ~-~-Coronoid process

RELATED fe STRUCTURES "A “\

Meckel’s cartilage-* --~ 3 te lee ———— Palate uditory tube ae NVA BC 77 ----- Body of mandible nerynx (nasal) ---~ 5 ——- ----- Nasal concha o ; / if Integumentum Nares Nasal septum (cartilage)

Fig. 17. In the fetus of 40 mm. (9 weeks) all structures which will become part of, or related to, the ear of the adult, are present in a stale of recognizable incipiency.

The cartilaginous otic capsule is a preosseous element of the chondrocranium; within it the reticular tissue, which replaced precartilage, has in turn been resorbed to produce the intercommunicating system of the perilymphatic (periotic) labyrinth. Lodged within this labyrinth is that of epithelia ducts, the endolymphatic (otic) labyrinth.

The parts of the adult external ear are represented by the auricle (in which cartilage is already developing) and by the primordial stalk of ectoderm which, upon rearrangement and disappearance of cells, will become the external acoustic meatus.

In the middle ear the auditory ossicles are lodged in primitive mesenchymal tissue; they are still wholly cartilaginous, and will remain so until the fetus has reached the 117-mm. stage, at which time ossification appears first in the incus.

The facial canal and the primordium of the stapedial muscle have changed little since the 28-mm. stage, advancement being limited to separation of the stapedius from the source-structure, the laterohyale. Segregation is complete in the 43-mm. fetus, and conversion of the undifferentiated mesenchymal cells of the laterohyale into muscle tissue is under way.

In specimen of the same age, fibers from the facial nerve pass to the muscle blastema — an observation which led some investigators to conclude that innervation bu this nerve from the second arch spelled origin of the stapes from the same branchial source. HANSON ET AL.—AUDITORY OSSICLES 377

Be ise, as r edie of ™ pista: edial


  • 3

Vestibul Fig. 18. In the 21-week stage the ossicles are still cartilaginous al the insertion of the tendon and the incudostapedial joint is still mesenchymal. The ossification center in the slapes is advancing toward the head, having already converted the crura and the tympanic part of the base into perichondral bone.

The stapedial tendon is inserted into both the long crus of the incus and the head of the stapes (an arrangement which was encountered in 30 of 198 series, fetal and adult). 378 QUARTERLY BULLETIN, N.U.M:S.




Tendon of stapedial . muscle.=






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Fig. 19. In the newborn the ossicles are, in all major features, adult elements of the human skeleton. The stapes, for example, retains a mere remnant of its fetal structure, namely marrow limited to the

interior of the cervical and capital parts and to the inner circumference of the base.

Evident likewise in this and many other postnatal specimens (including some to the age of 70 years) is the occurrence of double insertion of the stapedial tendon. This. means that the early association with the incus (compare fig. 18) is not lost as the ossicles mature and as the incudostapedial joint

is formed.

These observations are interpreted to mean that the manubrium of the malleus and long crus of

the incus, as well as the greater part of the stapes, are derived from the second branchial arch. HANSON ET AL.—AUDITORY OSSICLES 379



-Anterior process of malleus

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Fig. 20. In the fetus of 161 mm. (19 weeks) Meckel’s cartilage is beginning to undergo ossification near the zone in which altered tissue will differentiate into that of the anterior ligament of the malleus (fig. 20a). Three weeks later, in the fetus of 190 mm. (22 weeks) the anterior process of the malleus has become attached to the neck of the ossicle (fig. 20b, at arrows).

In the 215-mm. (24-week) stage, Reichert’s cartilage, continuous with the otic capsule, forms part of the wall of the facial canal (fig. 20c). In early infancy, the cartilage (a derivative of the laterohyale) is a mere remnart (fig. 20d). Newly-formed membrane bone and expanding tympanic cavity

(at : in both figs. 20c and 20d) intervene between the contents of the canal and the residual, invested, cartilage.




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