The Origin of the Acoustic Ganglion in the Sheep

The Origin of the Acoustic Ganglion in the Sheep
The Origin of the Acoustic Ganglion in the Sheep
by E. H. BATTEN 1
From the Department of Physiology, University of Bristol
WITH TWO PLATES
INTRODUCTION
I T has long been customary to regard the VII and VIII ganglia in the mammal
as originating from a common primordium—the acustico-facial crest—probably
owing to their almost simultaneous appearance and close apposition during
development (Adelmann, 1925; Bartelmez, 1922; Holmdahl, 1934; Kolmer,
1928; Politzer, 1928; Volker, 1922; and Weigner, 1901). But as long ago as 1906
Streeter drew attention to the early independence of the VII and VIII ganglia in
the human embryo and suggested that their close intimacy should be regarded as
contiguity rather than fusion. While he did not investigate the source of the
acoustic ganglion cells Streeter (1906) questioned the accepted view of their
origin from a common primordium and later (Streeter, 1912) stated that they
were not derived from the neural crest. The resolution of this problem clearly
involves the examination of a close series of embryos, particularly at stages
earlier than that at which these ganglia appear to be fused. Thus in amphibia,
where material is abundant, the formation of the acoustic ganglion from placodal
cells which detach from the walls of the otic vesicle has been traced in studies
of normal development (Brachet, 1907; Knouff, 1927, 1935; Kostir, 1924; and
Niessing, 1932). Moreover, the results of experimental work strongly support this
view since the formation of a normal acoustic ganglion is dependent on an intact
otic vesicle and is not disturbed by extirpation of the adjacent facial and glossopharyngeal neural crest (Campenhout, 1935a; Stone, 1922; and Tokura, 1925).
Nevertheless, Campenhout has admitted that this work does not absolutely prove
that the ganglion arises from the otic vesicle as the neural crest is known to
possess a marked regenerative ability. Yntema (1937) employed a Nile blue
sulphate method for tracing the migrating placodal cells and showed that the
acoustic ganglion is derived from the otic epithelium.
Few critical investigations into the origin of the acoustic ganglion have been
carried out in mammals, primarily on account of the difficulty of obtaining sufficient embryos at an early stage of development. Campenhout (1935b) in the pig
and Groth (1939) in the rabbit both describe an exclusively placodal origin for
1
Author's address: Department of Physiology, The University, Bristol 8, U.K.
[J. Embryol. exp. Morph. Vol. 6, Part 4, pp. 597-615, December 1958]
598
E. H. B A T T E N — O R I G I N O F T H E A C O U S T I C
GANGLION
this ganglion. More recently, Halley (1955) found that the acoustic ganglion in
the cat develops in large part from placodal cells and Politzer (1956) has traced
the independent anlage of the same ganglion in the human to cells which proliferate from the wall of the otic vesicle. A recent study in the sheep (Batten,
1957) indicates that the VII and VIII ganglia have an independent origin, for
the facial crest is entirely devoted to the formation of the geniculate ganglion,
and this receives contributions from an epibranchial placode for some time
before the enlarging acoustic ganglion fuses with it to produce the so-called
acustico-facial complex. The present paper describes the formation of the
acoustic ganglion from cells which detach from the placodal face of the vesicle
and offers an explanation for the marked inequality in cytological differentiation
which distinguishes the young acoustic neuroblasts from those of the adjacent
geniculate ganglion.
MATERIALS AND METHODS
Serial sections of 108 sheep embryos have been examined (Table 1). Thirty of
these embryos belong to the collection of Professor J. D. Boyd and were cut at 6 p.
and stained either in Weigert's haematoxylin and orange G, or in Heidenhain's
haematoxylin alone. A further twenty specimens were given by Professor E. C.
Amoroso and the remainder were collected locally. Bouin's fluid has been
routinely used and, after paraffin embedding, the embryos were cut at 7 p., or at
10 fx for reconstruction, and stained in Ehrlich's haematoxylin and eosin. The
later embryos of 26 mm., 28 mm., and 35 mm. were prepared by Miss P. Morgan
and loaned by Dr. R. N. Smith.
TABLE 1
Description of material used
Stage
(crown-rump
length in mm.)
Age
(in days)
11-38 somites
80-9-2
9-5-10-5
11-0-12-7
130-160
22-0-35-0
15-21
22-23
23-24
25-27
27-28
30-35
TOTAL
Number of
embryos
examined
30
26
18
21
9
4
108
The text-figures are drawings taken from graphic reconstructions of the otic
vesicle and acustico-facial complex in selected embryos. Tracings were made at
a magnification of 50 or 100 diameters using a section interval of 20 p and the
detail was transferred to a drawing board. By this method the size and distribution of the placodal spurs may be reconstructed with tolerable accuracy.
E. H. B A T T E N — O R I G I N OF T H E A C O U S T I C G A N G L I O N
599
RESULTS
12-somite—80 mm. embryos (15-22 days)
The facial neural crest can be identified as a diffuse cellular column as early
as the 12-13-somite stage, when the neural tube is still open at this level and the
otic placode is merely a flat plate of slightly thicker ectoderm. The formation of
a thick-walled otic vesicle is completed by the 26-somite (19-day) stage and the
transient connexion of the neck region with a disk of surface ectoderm is lost
slightly later (Text-fig. 1). Concurrently, the epibranchial placode of the facial
n. crest IX
ep. plac. VII
TEXT-FIG. 1. Graphic reconstruction of the otic vesicle and
adjacent ganglia in a 26-somite embryo. A. 1, mandibular arch;
A. 2, hyoid arch; ep. plac. VII, facial epibranchial placode;
ep. plac. IX, glossopharyngeal epibranchial placode; n. crest
VII, facial neural crest; n. crest IX, glossopharyngeal neural
crest; n. crest X, vagal neural crest; otic ves., otic vesicle.
nerve enters a phase of active proliferation and the developing geniculate ganglion continues to receive intermittently small cellular contributions until the
10*5 mm. stage (Batten, 1957). The differentiation of the geniculate ganglion
thus begins before there is any indication of the formation of an acoustic ganglion. Moreover, the effect of this developmental precedence of the facial nerve
becomes evident later in the marked superiority in cytological differentiation
which distinguishes the facial from the acoustic part of the VII-VIII complex.
By the 6 0-mm. (32-somite) stage the otic vesicle has grown considerably and
now has thinner walls with numerous mitotic figures in their inner layer (Textfig. 2). The basement membrane is clearly defined except along the ventral
border where two small streams of cells lying close against the rostral and lateral
external surface converge to unite in a common ventral mass. This mass repre-
600
E. H. BATTEN—ORIGIN OF THE ACOUSTIC GANGLION
sents the primordium of the acoustic ganglion and is separated from the developing geniculate ganglion by a zone of mesenchyme.
The early streams of placodal cells may be distinguished from mesenchyme by
their intimate contact with the otic epithelium and more closely packed nuclei,
and from the otic epithelium itself by nuclear orientation: the epithelial nuclei
are arranged mainly in a radial pattern whereas the placodal nuclei usually lie
at right angles to this and appear to be sweeping ventrally towards the acoustic
G IX
G. X
ep.plac. VII
A.I
TEXT-FIG. 2. Graphic reconstruction of the otic vesicle
and adjacent ganglia in a 60-mm. (32-somite) embryo.
A. 1, mandibular arch; A. 2, hyoid arch; ep. plac. VII,
facial epibranchial placode; ep. plac. IX, glossopharyngeal epibranchial placode; G. VII, geniculate ganglion;
G. VIII, placodal rudiment of acoustic ganglion; G. IX,
glossopharyngeal ganglion; G. X, vagal ganglion; otic
ves., otic vesicle.
ganglion (Plate 1, figs. A, B). Although similar flat streams of cells leading to
a minute acoustic ganglion were observed in six other embryos with 30-33
somites there is no clear indication of their precise origin. The first convincing
evidence of the emergence of these placodal streams from the otic epithelium
was found in a 7-2-mm. (36-somite) embryo with six distinct streams on the right
side. Two streams projected from the lateral wall of the vesicle as short freeending papillae, and of the four medial streams one was free-ending and the
others traced ventrally to unite with the acoustic ganglion. An early stage in the
migration of placodal cells from the otic epithelium is shown in Plate 1, fig. A 1;
this slender stream of cells appears to be interposed between the epithelium and
its basement membrane, but ends without penetrating the membrane after a
distance of 30 /x in serial section. The larger spur (Plate 1, fig. A 2) can be
E. H. B A T T E N — O R I G I N OF T H E A C O U S T I C G A N G L I O N
601
followed for 50 fx before it enters the edge of the acoustic ganglion. Unlike the
smaller spur, it is not covered by basement membrane, but lies free in a shallow
furrow in the basal layer of the otic epithelium. Two other spurs have also
broken through the membrane and extend ventrally to connect with the acoustic
ganglion.
By the 8 0-mm. stage the otic vesicle has grown into a pyriform sac which bears
endo. duct
C. VII
ep. ploc. VII
G. VIM
VII foc.n.
0.5 mm.
TEXT-FIG. 3. Graphic reconstruction of the otic vesicle and acusticofacial complex in an 80-mm. embryo, A: showing the placodal spurs
(numbered) present on the lateral wall of the vesicle, B: showing the
placodal spurs present on the medial wall, the lateral half of the vesicle
and the geniculate ganglion having been omitted to show the extent of
the acoustic ganglion, endo. duct, endolymphatic duct; ep. plac. VII,
facial epibranchial placode; G. VII, geniculate ganglion; G. VIII,
acoustic ganglion; VII fac. n., facial nerve; VII s. root, sensory root of
facial nerve.
along its thin dorso-medial border a flattened rudiment of the endolymphatic
duct. The acoustic ganglion itself is also much larger and now partially overlaps
the geniculate ganglion and spreads along its root to reach the hind-brain (Textfig. 3A). Since, however, the facial and acoustic ganglia exist as separate primordia in the previous stage their secondary union to produce the acustico-facial
complex has no developmental significance and should be regarded as the sequel
to a phase of rapid differential growth of the acoustic ganglion.
The main bulk of the acoustic ganglion lies close against the rostral face of the
ventral part of the vesicle and sends a short extension behind its medial wall
(Text-fig. 3B and Plate 2, fig. G). The rapid growth of the acoustic ganglion is
602
E. H. BATTEN—ORIGIN OF THE ACOUSTIC G A N G L I O N
due to the increment of placodal cells which detach in small streams from the
lateral and medial walls of the vesicle. Text-fig. 3 illustrates the size and distribution of nine placodal spurs present in an 8 0-mm. embryo. The migration of cells
from the lateral wall is particularly active and the two larger streams of placodal
cells (spurs 5 and 8 in Text-fig. 3A) may be traced ventrally to connect with the
acoustic ganglion. Both the smaller spurs are free-ending: spur 6 is a slender file
of cells and spur 4 a short papilla which probably represents a site of incipient
detachment. The medial wall of the vesicle bears five placodal spurs all of the
free-ending type representing sites of active cellular detachment. The cells of the
largest example (spur 1 of Text-fig. 3B) appear to be streaming from a breach in
the basement membrane, but have not yet reached the acoustic ganglion. Two
smaller spurs (2 and 3 of Text-fig. 3B) are shown in section in Plate 1, fig. B. In
shape the upper spur (Plate 1, fig. B 3) is a slender file which projects ventrally
towards the acoustic ganglion, the extreme caudal tip of which is also intercepted in this section. The cells of this file are still enclosed in a tubular extension
of basement membrane, but this appears to be broken distally at the free end.
The lower spur (Plate 1,fig.B 4) is probably in the act of detaching from the otic
epithelium since it lacks a covering of basement membrane which is well preserved on either side.
Examination of other embryos of similar age indicates that the detachment of
cells from the lateral wall is more vigorous than from the medial wall. The otic
epithelium no longer possesses a smooth contour, but is strewn with small irregular clusters of cells; some of these are entirely free and in the course of their
ventral migration (Plate 1, fig. C 5 and 6); others are about to detach from the
epithelium (Plate 1, fig. C 7 and 8). Of 14 sites of cellular detachment in this
8-2-mm. embryo, 9 were related to the lateral and 5 to the medial wall of the
vesicle. Even at low magnification the groups of migrating placodal cells are
conspicuous. In a typical coronal section through the middle of the vesicle the
placodal spurs stand out as thin streams of deeply staining cells lying close
against the lateral wall of the vesicle (Plate 1,fig.D). When traced rostrally for
a distance of 40 /J. these streams lead into the acoustic ganglion which lies at the
ventral border of the vesicle and receives from it a further placodal increment
(Plate 1,fig.E 9). A small site of impending cellular detachment is seen on the
lateral wall of the vesicle in Plate 1,fig.E 10. After the enlarging acoustic ganglion unites with the geniculate ganglion just before the 8 0-mm. stage the two
components still retain their individuality through cytological differences. The
young neuroblasts of the geniculate ganglion contrast even under low magnification with the smaller and more basophilic nuclei of the tightly packed placodal
cells of the acoustic ganglion (Plate 2,figs.F, G). While coronal sections indicate
that cells detach from the lateral and medial walls of the vesicle, it is evident in
transverse sections that the rostral wall, against which the acoustic ganglion
closely abuts, is also placodally active. Three active spurs are shown in Plate 2,
fig. F; the largest of these (spur 11) forms a connecting bridge between the otic
E. H. BATTEN—ORIGIN OF THE ACOUSTIC GANGLION
603
epithelium and the ganglion, while the other two (spurs 12 and 13) are smaller
sites of impending cellular detachment. In a section through the base of the
vesicle in the same 8 0-mm. embryo, the acoustic ganglion extends a short
distance along the medial wall and receives from it the two massive placodal
streams (Plate 2, fig. G 14 and 15). In this embryo 10 spurs were counted, 3 along
the medial wall and 7 against the rostral and lateral walls.
90-110-mm. embryos (22-25 days)
Up to the 10'0-mm. stage placodal spurs continue to form on the walls of the
vesicle and the detached cells emigrate into the enlarging acoustic ganglion. The
number of spurs recorded in these embryos usually lies between eight and ten,
endo. duct
VIII inf. vest. n.
VII gr. sup.pet.n."1
TEXT-FIG. 4. Graphic reconstruction of the otic vesicle, acoustic
and facial nerves in an 110-mm. embryo, endo. duct, endolymphatic duct; G. VII, geniculate ganglion; G. VIII pars inf.,
pars inferior of acoustic ganglion; G. VIII pars sup., pars
superior of acoustic ganglion; VII fac. n., facial nerve;
VII gr. sup. pet. n., greater superficial petrosal nerve;
VIII inf. vest, n., inferior vestibular nerve; VIII sup. vest, n.,
superior vestibular nerve.
the majority being small free-ending buds and the remainder larger streams of
the connecting type. The buds which proliferate from the lateral and rostral sides
of the vesicle contribute to the dorsal half of the ganglion which retains an intimate contact with the dorso-medial surface of the geniculate ganglion. As a
result of active budding from the ventro-medial wall the ventral half of the
acoustic ganglion gradually enlarges both in a ventral and in a medial direction
to produce a marked extension behind the otic vesicle (cf. Plate 2, figs. G, I).
604
E. H. BATTEN—ORIGIN OF THE ACOUSTIC GANGLION
About this stage the ganglion begins to show a partial subdivision which so
closely resembles that described in the human by Streeter (1906) that his terminology may conveniently be applied. Thus the dorsal part of the acoustic ganglion,
which lies close against the rostral wall of the vesicle and overrides the geniculate ganglion, may be termed the pars superior (Text-fig. 4 and Plate 2,fig.H).
In comparison with the 8 0-mm. stage this part of the ganglion shows a
vigorous dorsal growth and is now connected with the brain by a broad fibrous
root which overlaps and obscures from surface view the slender sensory root of
the facial nerve (Text-fig. 4 and Plate 2, fig. H). The remaining ventral part of
the ganglion together with its medial extension behind the base of the vesicle
constitutes the pars inferior (Text-fig. 4 and Plate 2,fig.I).
During the 9 0-mm. stage the small deeply basophilic nuclei of the placodal
cells give the pars inferior an even appearance, but by the 95-100-mm. stage
there are signs of a cytological differentiation which subdivides this part into two
regions. The nuclei of the lateral region which lies against the otic vesicle become
larger and elongate in a rostro-caudal plane. As a study of later stages reveals,
this change marks the beginning of the differentiation of these placodal cells into
neuroblasts. By contrast the cells of the medial region of the pars inferior retain
for some time the appearance of typical small placodal elements. In transverse
sections the distinction between the fusiform region of young vestibular neuroblasts and the residual placodal cells of the medial region facing the brain wall
is an impressive feature (Plate 2, fig. I). The contrast between the facial and
acoustic ganglia at this ventral level is accentuated by the more advanced differentiation of the geniculate neuroblasts which are of crest origin. The bulk of the
geniculate ganglion now overhangs the rostral face of the motor trunk and thus
begins to assume its characteristic pendant form.
Shortly after the onset of this regional differentiation the caudal edge of the
pars inferior bears a short fibrous extension which closely follows the basement
membrane of the otic epithelium. Although specific silver methods have not
been employed there is little doubt that this fibrous extension consists of nervefibres for its structure under oil immersion examination is identical with that of
adjacent cranial nerves. When the development of this outgrowth is traced back
from the later stages it can be identified as the earliest rudiment of the inferior
vestibular nerve. Initially this fine branch ends against the otic epithelium at
a point near the middle of the medial wall of the vesicle, as in Text-fig. 4 and
Plate 2,fig.I, but in other 11 -O-mm. embryos it can be followed as a fine strand
of delicate fibres into the caudal edge of the vesicle at a level where the ampulla
of the posterior canal will later develop. The rudiment of the superior vestibular
nerve regularly appears slightly later as a short fibrous stump connecting the pars
superior with the rostral margin of the otic vesicle (Text-fig. 4). Since it is rather
finer than the inferior vestibular branch it is less easy to photograph satisfactorily
at this stage, but its position is indicated in Plate 2,fig.H.
During the 10-5-mm. stage there is a decline in the extent of placodal activity
E. H. BATTEN—ORIGIN OF THE ACOUSTIC GANGLION
605
of the rostral and medial walls of the vesicle, for most embryos show only two or
three buds of small size. A typical example which is about to detach and migrate
into the pars superior is seen in Plate 2, fig. H 16. By the 110-mm. stage there
is little further evidence of contributions to the pars superior, but the scene of
placodal activity shifts to the rostral margin of the base of the vesicle where
diffuse cellular migration is commonly seen, as in Plate 2, fig. I 17. Here the
basement membrane is lost and the usual pattern is simply a diffuse outpouring
of placodal cells, although distinct spurs or slender files are occasionally found.
The placodal cells which detach from this new placodal site are not added to the
vestibular part of the pars inferior, but settle in the angle between this and the
motor root of the facial nerve.
120-160-mm. stage (26-28 days)
During the previous stage the apical region of the otic vesicle has steadily
expanded in a dorsal direction and by the 120-mm. stage has become a broad
flattened pouch with curved margins which are beginning to turn laterally. The
formation of the posterior semicircular canal is foreshadowed by the appearance
of a shallow groove which follows the caudal margin of the otic vesicle a little
way from its edge. The anterior canal is similarly outlined at a slightly later stage
and the anlage of the horizontal canal develops as a flattened outgrowth which
obliquely crosses the middle of the lateral face of the vesicle. With local resorption of parts of the closely apposed and attenuated walls both vertical canals
become recognizable features at the 14 0-mm. stage, but the horizontal canal still
lags behind in its development (Text-fig. 5).
In the acoustic ganglion the distinction between pars superior and pars inferior
is now less marked since the placodal cells of the pars superior have differentiated
into young neuroblasts. The whole of the pars superior together with the medial
zone of the pars inferior, in which precocious formation of neuroblasts was
noted at the 110-mm. stage, now constitutes the vestibular ganglion. The
superior vestibular nerve has grown into a stout trunk which bifurcates to supply
the ampullary swellings at the base of the anterior and horizontal canals. Proximally it is united with the inferior vestibular branch which now supplies several
fine nerves to the saccular region of the labyrinth before traversing its medial
wall to innervate the ampulla of the posterior canal (Text-fig. 5).
After the 12-0-mm. stage a redistribution of cells in the region of the pars
inferior leads to the formation of the cochlear lobe which is a mass of closely
packed placodal cells from which the cochlear ganglion is ultimately derived.
The development of this ganglion in the sheep appears to be more complicated
than the simple division into upper vestibular and lower cochlear ganglia
described in the pig by Campenhout (1935ft) and in the cat by Halley (1955).
Cells from two sources participate in the formation of the cochlear lobe. Firstly,
there is a gradual decrease in the number of placodal cells found in the medial
zone of the pars inferior until by the 12-5-mm. stage only the neuroblasts of the
606
E. H. BATTEN—ORIGIN OF THE ACOUSTIC GANGLION
vestibular zone remain. Examination of transverse and coronal sections indicates that this depletion is due not to differentiation of these placodal elements
into vestibular neuroblasts, but to their migration to a more ventral position
where they mobilize to form the cochlear lobe. Secondly, these residual placodal
cells originating from the pars inferior are augmented by continued placodal
I
endo. duct1
dorsal
rostral
post, canal
ont. canal
VIII inf. vest. n.
C. VII
VII fac.n.
/
VII qr. sup.pet.n.
G. VIII coch.lobe
coch. bud
0.5 mm.
TEXT-FIG. 5. Graphic reconstruction of the otic vesicle, acoustic and facial
nerves in a 140-mm. embryo, ant. canal, anterior canal; coch. bud,
cochlear bud; endo. duct, endolymphatic duct; G. VII, geniculate ganglion;
G. VIII coch. lobe, cochlear lobe of placodal cells; hor. canal, horizontal
canal; post, canal, posterior canal; VII fac. n., facial nerve; VII gr. sup.
pet. n., greater superficial petrosal nerve; VII m. root, motor root of facial
nerve; VIII inf. vest, n., inferior vestibular nerve; VIII sup. vest, n.,
superior vestibular nerve; VIII vest, g., vestibular ganglion.
proliferation along the rostral edge of the vesicle immediately ventral to the
superior vestibular nerve. In 12-0- and 13-0-mm. embryos this site shows diffuse
cellular migration as well as occasional discrete spurs and files of cells, but this
activity ends by the 14-0-mm. stage. The cochlear lobe thus lies between the
motor root of the facial nerve and the elongating base of the vesicle which is
turning medially as the cochlear bud. Although the greater part of the cochlear
lobe consists of placodal cells, a limited number of young neuroblasts are present
in the zone adjacent to the cochlear bud. A short nerve outgrowth which connects this zone with the wall of the cochlear bud probably represents the first
trace of the distal fibres of the cochlear nerve.
qr. sup.pet. n
coch. bud
VIII coch. q.
VII
O.5 mm.
fac.n
VIII inf. vest, n
VIII coch. q.
coch. bud
ant.
s.root.
VII qr. sup.pet. n.
VII
canal
TEX-FIG. 6. Graphic reconstruction of the membranous labyrinth, acoustic and facial nerves in a 260-mm. embryo, A: lateral view, B: medial view,
ant. canal, anterior canal; coch. bud, cochlear bud; endo. duct, endolymphatic duct; G. VII, geniculate ganglion; hor. canal, horizontal canal; post,
canal, posterior canal; VII fac. n., facial nerve; VII gr. sup. pet. n., greater superficial petrosal nerve; VII m. root, motor root of facial nerve; VII
s. root, sensory root of facial nerve; VIII coch g., cochlear ganglion; VIII inf. vest, n., inferior vestibular nerve; VIII sacc. n., saccular nerve; VIII
sup. vest, n., superior vestibular nerve; VIII vest, g., vestibular ganglion.
VII
VII m. r o o t
VIII sup. v
VIII vest. g.
duct
post, can
endo.
608
E. H. B A T T E N — O R I G I N OF T H E A C O U S T I C
GANGLION
22 0-35 0-mm. embryos (30-35 days)
As described in the previous stage, the rudiment of the cochlear ganglion is
represented by a lobe of placodal cells at the base of the vestibular ganglion, and
in order to follow the development of the definitive cochlear ganglion several
larger embryos of up to 35 0-mm. G.L. have been examined (Table 1). The reconstruction of a 26 0-mm. sheep embryo (Text-fig. 6) illustrates the advanced
differentiation of the membranous labyrinth which in all essential features
closely resembles the reconstruction of a 200-mm. human embryo prepared
by Streeter (1906, Plate 1, figs. 1, n). The geniculate ganglion has a markedly
pendant shape but still retains a narrow connexion with the vestibular ganglion.
As the vestibular neuroblasts are now only slightly smaller than those of the
geniculate ganglion, the cytological contrast between these ganglia is considerably diminished. The external morphology of the vestibular portion of the
membranous labyrinth now approaches the definitive pattern and the branches
of the superior and inferior vestibular nerves can be traced to innervate rudimentary cristae and maculae (Text-fig. 6A).
In comparison with the 140-mm. stage the most striking advance has been
made in the outgrowth of the cochlear duct which has completed a single spiral
turn by the 260-mm. stage and encloses in its axis the definitive cochlear ganglion. This ganglion is formed mainly by the migration of the placodal cells
of the original cochlear lobe, but there is occasional evidence in the form of
attenuated streams of cells projecting from the epithelium of the cochlear duct
which suggests a laggard placodal contribution. The majority of the cells of the
cochlear ganglion are young neuroblasts, but these are distinctly smaller than
those in the vestibular ganglion. Distally, the cochlear ganglion is intimately
connected with the inner curvature of the cochlear duct by numerous fine nervefibres and proximally the cochlear nerve may be traced across the medial surface
of the vestibular ganglion to enter the root of the acoustic nerve (Text-fig. 6B).
DISCUSSION
The principal conclusion to be drawn from this investigation is that the VII
and VIII ganglia originate from specific and initially independent cell masses
and not from a common acustico-facial crest primordium. As described elsewhere (Batten, 1957), this crest material receives a contribution from the epibranchial placode and then differentiates into the geniculate ganglion just as
Landacre (1932) found in the rat. The acoustic ganglion, however, is essentially
of placodal origin and the manner in which its cells proliferate from a dorsolateral placode incorporated in the otic vesicle confirms the findings of Campenhout (19356) in the pig and Groth (1939) in the rabbit. Since the evidence in the
sheep contradicts the widely accepted view that the acoustic ganglion arises by
subdivision of an acustico-facial primordium, as has been maintained by Adelmann (1925), Bartelmez (1922), Cameron & Milligan (1910), Da Costa (1931),
E. H. BATTEN —ORIGIN OF THE ACOUSTIC GANGLION
609
Holmdahl (1934), Kolmer (1928), Schulte & Tilney (1915), Volker (1922), and
Weigner (1901), an attempt to reconcile the opposing views might be helpful.
A partial explanation lies in the inadequacy of material: many workers have
observed the intimate fusion of these ganglia and, lacking or overlooking the
transient early stages in which the ganglia are distinctly separate, have been
misled into assuming for them a common origin. The comprehensive and influential paper of Adelmann (1925) offers an exception, but it is nevertheless
evident from a critical comparison with the parallel work of Landacre (1932)
that Adelmann is a convinced opponent of the placodal theory.
In spite of the intimate developmental apposition of the facial and acoustic
ganglia the conclusion that they develop from a common mass and, more especially, the identification of this as the 'acustico-facial neural crest' is open to
suspicion. Firstly, there is the critical difference in the functional components
which these nerves carry. Secondly, a common origin from neural crest is incompatible with Landacre's concept of the specific origin of these functional components (Landacre, 1910a, 1911,1914,1920; Stone, 1922,1924,1928 a, b, c). This
concept was founded on fish and amphibian material, but is now considered
equally valid for birds and mammals by Ariens Kappers (1941). According to
this concept the acoustic ganglion in the mammal should arise from a dorsolateral placode incorporated in the otic vesicle and not from neural crest.
Thirdly, the formation of the acoustic ganglion from neural crest is out of harmony with the pattern of its development in the lower vertebrates. As early as
1907 Brachet showed in the frog that this ganglion arose mainly from cells proliferated from the otic vesicle and later Knouff (1927, 1935) concluded that it
was entirely of placodal origin. This finding has been confirmed in other amphibia (Kostir, 1924; Niessing, 1932; Yntema, 1937) and in fish (Landacre, 19106;
Veit, 1924). Although it may be criticized as an ill-founded assumption, the view
that the acoustic ganglion may arise from neural crest in the mammal is still
current in certain textbooks. It is also surprising that the findings of Campenhout
and Groth have not attracted the attention they deserve.
The duration of placodal budding from the otic vesicle in the sheep covers the
period from the 60-mm. (32-somite) to the 140-mm. stage and thus coincides
approximately with the limits given by Campenhout (19356) for the pig. The
earliest anlage of the acoustic ganglion is formed by diffuse cellular migration
and is clearly separated from the facial crest by a zone of mesenchyme as in the
pig (Campenhout, 19356) and rabbit (Groth, 1939). After the 70-mm. stage the
evidence for the migration of cells becomes more convincing with the appearance
of distinct spurs and files of cells projecting through the basement membrane.
Since the facial crest is exclusively concerned in the formation of the geniculate
ganglion and the acoustic ganglion is developmentally independent, at any rate
initially, there is no justification for the term 'acustico-facial crest' in these
species and, as Groth (1939) has already suggested, its use should be rejected.
In the literature on human development the use of the term 'acustico-facial
610
E. H. BATTEN—ORIGIN OF THE ACOUSTIC GANGLION
ganglion' has been fostered by the reviews of Bartelmez (1922) and Bartelmez
& Evans (1926). Bartelmez (1922) agreed that the geniculate portion received a
contribution from the epibranchial placode in 4-16-somite embryos, but implied
that the remaining portion of this crest provided the acoustic ganglion. Furthermore, he regarded the possibility of the otic plate contributing cells to the ganglion as being equivocal and, in any case, of minimal significance not only in
mammals but also in other vertebrates. Recent reports, however, have shown this
opinion to be premature, for Rosenbauer (1955) found evidence of a cellular
migration from the vesicle in a single 24-somite embryo. Similarly, Politzer
(1956), in five human embryos with 26-30 somites, has traced the origin of the
rudiment of the acoustic ganglion to diffuse placodal budding from the vesicle,
which resembles events in sheep, pig, and rabbit embryos of equivalent stage.
The interpretation of this region is undoubtedly more difficult in the human
owing to the closer proximity of the facial crest to the otic vesicle. But while
Politzer's findings indicate that the early acoustic ganglion is formed from
placodal cells in the same way as in the sheep, pig, and rabbit, his assertion that
the entire ganglion arises from this source needs to be verified in later stages,
especially since Masy (1955) has noted a placodal contribution in a single
9 0-mm. embryo.
In the cat there are also conflicting reports of placodal activity. Schulte &
Tilney (1915) consider that the acoustic ganglion arises from the common crest
primordium and fail to mention any placodal activity. Halley (1955), however,
describes an active cellular migration from the otic vesicle between the 5 0- and
100-mm. stages, but owing to the presence of pycnotic debris within the acusticofacial rudiment she was unable to determine whether any neural crest cells survive to become acoustic neuroblasts or whether these are exclusively formed
from placodal cells. A careful search for similar pycnotic debris proved negative
in the sheep, and the ultimate differentiation of the placodal cells into acoustic
neuroblasts can be traced without this complication. Apparently the 'acusticofacial crest' makes contact with the vesicle rather earlier in the cat than in other
species, but it would be interesting to know if there is any diffuse cellular migration before this fusion occurs, since it is at this stage that the independent acoustic
ganglion first appears in the sheep, pig, and rabbit.
After the 8 0-mm. stage in the sheep the detachment of placodal spurs becomes
more vigorous and with the addition of these cells the rapidly enlarging acoustic
ganglion becomes closely apposed to the geniculate ganglion to establish the
so-called acustico-facial complex. The intimate association of these ganglia has
often been misinterpreted as evidence of their common origin. But since these
ganglia are developmentally independent at earlier stages and arise from specific
anlagen in the sheep, pig (Campenhout, 19356), rabbit (Groth, 1939), and human
(Politzer, 1956), their association must be regarded as a secondary event caused
by the encroachment of the acoustic upon the geniculate ganglion. This interpretation returns to Streeter's contention that the relationship involves contact
E. H. BATTEN —ORIGIN OF THE ACOUSTIC GANGLION
611
rather than fusion with implied developmental significance (Streeter, 1906). In
spite of their apposition the two ganglia may still be distinguished by cytological
differences which resemble those described in the pig and rabbit, and provide
a further argument against the view that these ganglia share a common derivation. In the latter case the two ganglia would show a uniform level of cytological
differentiation. But their cytological disparity is caused by the earlier neuroblastic differentiation of the geniculate ganglion which exists as a crest rudiment
for some time before there is any indication of the formation of an acoustic
ganglion.
The morphological transformation of the enlarging acoustic ganglion into
pars superior and pars inferior and the fate of these parts in the sheep closely
follows the account given by Streeter (1906) for the human. In the sheep, however, this early subdivision does not correspond exactly with the later differentiation into the definitive vestibular and cochlear ganglia as reported for the pig
by Lewis (1902,1906) and Campenhout (19356) and for the cat by Halley (1955).
Moreover, the earliest evidence of the differentiation of placodal cells into
acoustic neuroblasts is localized in the lateral zone of the pars inferior and
coincides with the outgrowth of the inferior vestibular nerve. In this respect the
sheep differs strongly from the pig, for Campenhout describes a cytological subdivision into an upper zone of large pale staining cells (presumably neuroblasts)
and a lower zone of small deeply staining cells identical with migrating placodal
elements. The definitive vestibular ganglion in the sheep arises from the same
material as in the human: it includes not only the pars superior, as Lewis, Campenhout, and Halley envisage, but also the lateral zone of the pars inferior in
which the earliest formation of neuroblasts is seen. The remaining medial zone
of the pars inferior migrates ventrally, as in the human, to form the rudiment of
the cochlear ganglion, but in the sheep this cochlear lobe is augmented by a
placodal contribution from the base of the vesicle during the 110-140-mm.
period. There is also some evidence of a limited diffuse migration from the walls
of the cochlear bud which has not previously been reported in other species.
Thus the formation of the cochlear ganglion in the sheep appears to be more
complicated than the simple transformation of the entire pars inferior as envisaged by Lewis (1902,1906) and Halley (1955). Both in the time of its appearance as a distinct entity and in the differentiation of its placodal cells into neuroblasts, the cochlear ganglion lags behind the vestibular ganglion in the same way
as Streeter (1906) found in the human. This retarded development contrasts
sharply with the conclusion reached by Campenhout (19356) that the cochlear
ganglion develops before the vestibular in the pig. In both the human and the
sheep the first neuroblasts appearing in the pars inferior relate to the vestibular
ganglion and, if this is so also in the pig, it would then be possible to follow
Campenhout's interpretation only by assuming that he may have identified these
cells as representing part of the cochlear ganglion, especially since he considers
the latter to arise from the entire pars inferior.
612
E. H. B A T T E N — O R I G I N OF T H E A C O U S T I C
GANGLION
Although it would be an unlikely event during the early stages when the
primordia are separate the participation of cells of neural crest origin in the
formation of the acoustic ganglion becomes theoretically possible after their
secondary fusion. Thus, postulating a definite contribution from the facial rudiment to the developing acoustic ganglion, one would expect in the latter a mixture of placodal cells and young neuroblasts equivalent to those of the geniculate
ganglion. In the present material, however, the acoustic ganglion arises from an
unmixed mass of placodal cells and even the earliest vestibular neuroblasts are of
significantly younger stage than those within the geniculate ganglion. While it is
improbable that any acoustic neuroblasts originate from the facial crest the possibility that the facial root might provide sheath cells cannot be excluded. Analysis of the development of the acoustic ganglion in the sheep strongly supports the
view given by Campenhout for the pig that, if it occurs at all, the contribution
provided by the facial crest is negligible. In this respect the acoustic ganglion can
be distinguished from the other cranial ganglia as being the only example which
is exclusively of placodal origin and in which the neuroblastic differentiation of
the placodal cells can be followed without the complication of their mixing with
crest elements. The fact that these acoustic placodal cells become neuroblasts
and sheath cells provides further support for the view that the cells derived from
the trigeminal and epibranchial placodes in the mammal may also share this
potentiality.
SUMMARY
1. The acoustic ganglion arises from placodal cells which detach from the otic
vesicle between the 6 0-mm. and 14 0-mm. stages. The accepted view that it
develops from a common 'acustico-faciaP neural crest is rejected.
2. The initial rudiment of the acoustic ganglion is a mass of detached placodal
cells which lies at the base of the vesicle and is distinctly separated from the facial
crest by a zone of mesenchyme.
3. After the 8 0-mm. stage the detachment and migration of placodal cells
becomes more vigorous and the enlarging acoustic ganglion becomes secondarily
apposed to the geniculate ganglion. Nevertheless, these ganglia retain their
separate identity through cytological differences which rest on the fact that the
young neuroblasts are already present in the geniculate ganglion before a distinct acoustic rudiment is evident. This contrast wanes gradually after the
110-mm. stage when the placodal cells begin to differentiate into acoustic
neuroblasts.
4. It is concluded that the acoustic ganglion arises exclusively from placodal
cells and the participation of facial crest cells in the root portion, if it occurs at
all, is probably negligible.
5. The definitive vestibular ganglion is derived from the pars superior together
with the lateral zone of the pars inferior in which the earliest neuroblasts appear.
E. H. B A T T E N — O R I G I N OF T H E A C O U S T I C G A N G L I O N
613
6. The definitive cochlear ganglion begins to develop rather later and arises
from the remaining medial zone of the pars inferior with the addition of further
diffuse placodal contributions from the base of the vesicle.
ACKNOWLEDGEMENTS
I am especially grateful to Professor J. D. Boyd for facilities for examining his
collection of sheep embryos, to Professor E. C. Amoroso for part of the material,
and to Dr. R. N. Smith for his collaboration in collecting material locally. I am
also indebted to Mr. R. Davies for technical assistance.
REFERENCES
ADELMANN, H. B. (1925). The development of the neural folds and cranial ganglia of the rat.
J. comp. Neurol. 39, 19-123.
ARIENS KAPPERS, J. (1941). Kopfplakoden bei Wirbeltieren. Ergebn. Anat. EntwGesch. 33,
370-412.
BARTELMEZ, G. W. (1922). The origin of the otic and optic primordia in man. / . comp. Neurol.
34, 201-32.
& EVANS (1926). The development of the human embryo during the period of somite formation, including embryos with 2-16 pairs of somites. Contr. Embryol. Carneg. Instn. 17, 1-67.
BATTEN, E. H. (1957). The behavior of the epibranchial placode of the facial nerve in the sheep.
J. comp. Neurol. 108, 393^420.
BRACHET, A. (1907). Recherches sur l'ontogenese de la tete chez les Amphibiens. Arch. Biol.
Liege et Paris, 23, 165-258.
CAMERON, J., & MILLIGAN, W. (1910). Development of the auditory nerve in Vertebrates. / . Anat.
& Physiol. Lond. 44, 111-32.
CAMPENHOUT, E. VAN (1935a). Experimental researches on the origin of the acoustic ganglion in
amphibian embryos. / . exp. Zool. 72, 175-93.
• (19356). Origine du ganglion acoustique chez le pore. Arch. Biol. Liege et Paris, 46, 271-85.
DA COSTA, CELESTINO (1931). Sur la constitution et le deVeloppement des ebauches ganglionnaires
craniennes chez les mammiferes. Arch. Biol. Liege et Paris, 42, 71-105.
GROTH, W. (1939). Der Ursprung der Labyrinthplacode und des Ganglion stato-acusticum in
Vergleich zur Genese des Riechorgans beim Kaninchen. Z. mikr.-anat. Forsch. 45, 393-442.
HALLEY, G. (1955). The placodal relations of the neural crest in the domestic cat. / . Anat. Lond.
89, 133-52.
HOLMDAHL, D. E. (1934). Neuralleiste und Ganglienleiste beim Menschen. Z. mikr.-anat. Forsch.
36,137-78.
KNOUFF, R. A. (1927). The origin of the cranial ganglia of Rana. J. comp. Neurol. 44, 259-361.
—— (1935). The developmental pattern of ectodermal placodes in Rana pipiens. J. comp.
Neurol. 62, 17-65.
KOLMER, W. (1928). Ober die Entwicklung der peripheren Nerven bei jugendlichen menschlichen
Embryonen. Z. Anat. EntwGesch. 87, 344-66.
KOSTIR, W. J. (1924). An analysis of the cranial ganglia of an embryo salamander, Amblystoma
Jeffersonianum. Ohio J. Sci. 24, 230-63.
LANDACRE, F. L. (1910a). The origin of the sensory components of the cranial ganglia. Anat. Rec.
4, 71-79.
(1910ft). The origin of the cranial ganglia in Ameiurus. J. comp. Neurol. 20, 309-411.
(1911). The theory of nerve components and the forebrain vesicle. Trans. Amer. Micr. Soc.
30, 57-66.
• (1914). Embryonic cerebral ganglia and the doctrine of nerve components. Folia Neurobiol.
8, 601-15.
•
• (1920). The origin of the cerebral ganglia. Ohio J. Sci. 20, 299-310.
• (1932). The epibranchial placode of the facial nerve of the rat. / . comp. Neurol. 56, 215-55.
614
E. H. B A T T E N — O R I G I N OF T H E A C O U S T I C G A N G L I O N
LEWIS, F. T. (1902). The gross anatomy of a 12 mm. pig. Amer. J. Anat. 2, 211-26.
(1906). The mixed cerebral nerves in mammals. /. comp. Neurol. 16, 177-82.
MASY, S. (1955). Le Systeme nerveux peripherique cranien de l'embryon humain de 9 mm.
J. Embryol. exp. Morph. 3, 30-43.
NIESSING, C. (1932). Die Entwicklung der kranialen Ganglien bei Amphibien. Morph. Jb. 70,
472-530.
POLITZER, G. (1928). Uber einen menschlichen Embryo mit 18 Ursegmentpaaren. Z. Anat. EntwGesch. 87, 674-727.
(1956). Die Entstehung des Ganglion acusticum beim Menschen. Acta Anat. 26, 1-13.
ROSENBAUER, K. A. (1955). Untersuchung eines menschlichen Embryos mit 24 Somiten, unter
besonderer Berucksichtigung des Blutgefaflsystems. Z. Anat. EntwGesch. 118, 236-76.
SCHULTE, H. VON, & TILNEY, F. (1915). Development of the neuraxis in the domestic cat to the
stage of 21 somites. Ann. N.Y. Acad. Sci. 24, 319-46.
STONE, L. S. (1922). Experiments on the development of the cranial ganglia and lateral line sense
organs in Amblystomapunctatum. J. exp. Zool. 35,421-96.
(1924). Experiments on the transplantation of placodes of the cranial ganglia in the amphibian embryo. I. Heterotopic transplantations of the ophthalmic placode upon the head of
Amblystoma punctatum. J. comp. Neurol. 38, 73-105.
(1928a). Primitive lines in Amblystoma and their relation to the migratory lateral line primordia. /. comp. Neurol. 45, 169-90.
(19286). Experiments on the transplantation of placodes of the cranial ganglia in the amphibian embryo. II. Heterotopic transplantation of the ophthalmic placode upon the head and
body of Amblystoma punctatum. J. comp. Neurol. 47, 61-116.
(1928c). Experiments on the transplantation of placodes of the cranial ganglia in the amphibian embryo. III. Pre-auditory and post-auditory materials interchanged. /. comp. Neurol.
47,117-54.
STREETER, G. L. (1906). On the development of the membranous labyrinth and the acoustic and
facial nerves in the human embryo. Amer. J. Anat. 6, 139-65.
'
(1912). The development of the nervous system. In Manual of Human Embryology, ed.
Keibel & Mall, 2,1-156. Philadelphia: Lippincott.
TOKURA, R. (1925). Entwicklungsmechanische Untersuchungen uber das Horblaschen und das
akustische sowie faciale Ganglion bei den Anuren. Folia anat. jap. 3,173-208.
VEIT, O. (1924). Beitrage zur Kenntnis des Kopfes der Wirbeltiere. II. Friihstadien der Entwicklung des Kopfes von Lepidosteus osseus und ihre prinzipielle Bedeutung fur die Kephalogenese der Wirbeltiere. Morph. Jb. 53, 319-90.
VOLKER, O. (1922). Normentafel zur Entwicklungsgeschichte des Ziesels. {Spermophilus citellus).
Normentafeln zur Entwicklungsgeschichte der Wirbeltiere, 13. Jena: Gustav Fischer.
WEIGNER, K. (1901). Bemerkungen zur Entwicklung des Ganglion acustico-faciale und des
Ganglion semilunare. Anat. Anz. 19,145-55.
YNTEMA, C. L. (1937). An experimental study of the origin of the cells which constitute the Vllth
and VHIth cranial ganglia and nerves in the embryo of Amblystoma punctatum. J. exp.
Zool. 75, 75-101.
E X P L A N A T I O N OF PLATES
PLATE 1
FIG. A. Transverse section of a 7-2-mm. sheep embryo showing two early placodal buds (1 and
2) on the medial wall of the otic vesicle. Both buds appear to be sliding ventrally between the
parent epithelium and the basement membrane, x 300.
FIG. B. Three placodal spurs associated with the rostro-medial wall of the otic vesicle in an
80-mm. sheep embryo. Spur 3 is still enclosed by a tubular evagination of the basement membrane, but spur 4 is completely detached from the epithelium. Immediately below lies the diffuse
tip of the mass of detached placodal cells which constitute the rudiment of the acoustic ganglion
(G. VIII). x300.
FIG. C. Transverse section of an 82-mm. sheep embryo showing the lateral wall of the otic
vesicle with four groups of placodal cells apparently migrating towards the acoustic ganglion.
J. Embryol. exp. Morph.
Vol. 6, Part 4
E. H. BATTEN
Plate 1
/ . Embryol. exp. Morph.
Vol. 6, Part 4
E. H. B A T T E N — O R I G I N OF T H E A C O U S T I C G A N G L I O N
615
The upper two spurs (5 and 6) are already free of the otic epithelium. Of the lower spurs, 7 consists of a cluster of cells probably about to detach and 8 is a small free spur which is attached to
the otic epithelium in the previous section, x 300.
FIG. D. Coronal section through the cranial third of the otic vesicle in an 82-mm. sheep
embryo. Note the groups of small deeply staining placodal cells apparently migrating over the
lateral face of the vesicle towards the rudiment of the acoustic ganglion (G. VIII). x 130.
FIG. E. Coronal section through the same 82-mm. embryo as Fig. D, but passing through the
cranial edge of the otic vesicle. The lateral groups of placodal cells have almost reached the
acoustic ganglion and make contact with it in the next section. The arrow (9) indicates two spurs
of placodal cells which are presumed to be streaming into the ganglion. A small bud of placodal
cells probably about to detach from the lateral wall of the vesicle is visible at 10. x 130.
PLATE 2
FIG. F. Transverse section through the ventral region of the otic vesicle in an 80-mm. sheep
embryo showing three spurs of placodal cells (11, 12, and 13). The cells of the largest spur (11) are
presumed to be migrating into the acoustic ganglion. Observe the cytological distinction between
the placodal cells of the acoustic ganglion (G. VIII) and the young neuroblasts of the geniculate
ganglion (G. VII). x 130.
FIG. G. Transverse section through the same 80-mm. embryo as Fig. F, but at a more ventral
level. The two large placodal streams (14 and 15) can be traced into the acoustic ganglion in later
sections. xl30.
FIG. H. Transverse section through the middle level of the otic vesicle in an 110-mm. sheep
embryo showing the pars superior and root portion of the acoustic ganglion. The indentation on
the lateral wall of the vesicle foreshadows the development of the posterior canal. The superior
vestibular nerve (S.V.N.) is faintly visible along the lateral wall of the vesicle with a small
placodal bud (16) immediately below it. The small bundle entering the medulla is part of the
sensory root of the facial nerve, x 130.
FIG. I. Transverse section through the same 110-mm. embryo, but 168 {>• below the level of
Fig. H. The pars inferior of the acoustic ganglion sweeps behind the medial wall of the vesicle and
is connected with it by the inferior vestibular nerve (I.V.N.). The young vestibular neuroblasts
which are differentiating in the lateral zone of the pars inferior contrast sharply with the residual
placodal cells of the medial zone which contribute to the cochlear ganglion. The rostral edge of
the vesicle shows diffuse placodal migration (17) which is added to the cochlear lobe. The section
intercepts the motor root and part of the post-trematic facial branch (VII F) of the facial nerve
and illustrates the advanced differentiation of the geniculate neuroblasts (G. VII). x 130.
(Manuscript received 11: iv: 58)
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