On the extrinsic eye muscles of the whale, withspecial remarks upon the innervation andfunction of the musculus retractor bulbi

BY
HIROSHI HOSOKAWA

Department of Anatomy (Prof. Dr. T. Ogawa),
Medical School, University of Tokyo.

While I was engaged in the anatomical study on the visual organsof the whale, special attention was directed to the musculi palpebrales,
which are in the cetacea, as some anatomists said, of an unique existence
throughout the animal kingdom. Next to that, my special interest was
rendered to the well-developed musculus retractor bulbi, the existenceof which is never characteristic for the cetacea, but is rather common
for almost all vertebrates except the cyclostoma and fishes (Haller v.
Hallerstein, 1934; Franz, 1934 etc.) 1 • Meanwhile I encountered in thewhale a peculiar feature concerning the innervation of the retractor
bulbi and tried to explain it by various means of researches, which
will be related in order in the following paragraphs. As the result, I
came to the conclusion that the inn.ervation of the cetacean retractor
bulbi is never essentially different from that in other vertebrates,
though it exhibits a noteworthy peculiarity at first sight.
Relating to this problem, I tried to know the functional meaningof this muscle and studied also its original nucleus in the brain-stem,
experimenting on the cat.
At the end, my observations on the sensory nerves of the retractor
and of other extrinsic eye muscles in the cetacea will be mentioned.
MATERIALS

MYSTACOCETI:
1) Sei whale (Balaenoptera borealis, Lesson): adult 1 (45 feet,
female), fetus 1 (7 feet, male)2) Blue whale (B. musculus, L.): fetuses 2 (6 feet, female; 7 feet,male)3) Fin whale (B. physalus, L.) : fetuses 3 (3 feet, male; 8 feet,
female; 13 feet, male)1) Even among the fishes some teleostei are said to have slight indication of thismuscle.

2

HIROSHI HOSOKAWAODONTOCETI :4) Sperm whale (Physeter catodon, L.): fetuses 2 (3 feet, female;
5 feet, male)5) Pilot whale (Globicephalus melas, Traill): adult 1 (17 feet, male)6) A dolphin (Prodelphinus caeruleo-albus, Meyen) : adults 2, fetuses 3.
Other mammals used for comparison:
1) cats 52) dogs 23) rabbits 2
1. The extrinsic eye muscles of the whale
In the cetacea the extraocular muscles consist of two oblique, four
straight ones and of the retractor bulbi. Of them, it is noteworthy
that the greater part of each of four recti muscles extends forwards
over the eyeball and inserts into the eyelid, delivering only a small
muscle branch to the eyeball (Fig. 1, 2). While the ocular portions

Fasciculus opticus

M. obliq. inf.

Fig. 1. Extrinsic eye muscles of Globicephalus::melas(17 feet, male) (left eye)of the recti muscles are relatively well preserved in the Globiceph alus,
they are very rudimentary in the Sei and other baleen whales. For

On the extrinsic eye muscles of the whale3

this reason, these muscles of the cetacean eye do not deserve well thename "Mm. recti bulbi", but the name "Mm. palpebrales" is for themmore preferable, as Weber (1886fand Putter (1903) called them.
M. palpebralis sup.

M, rectus sup.

M. palp. inf.

M. orbicularis oculi

M. rectus inf.
ConjuJ1ctival glandFig. 2.

Median section through eye and palpebrae of Globicephalus melas

The peculiarity of the musculi palpebrales of the cetacea has been
well known since Weber, but the meaning of it is not yet fully determined. Weber was of the opinion that they might serve for themechanical protection of the eyeball against - water pressure, while
Putter ascribed them a hydrodynamic function, assuming that theymight efficiently work against cooling down of the eyeball producihg
heat by their contraction.
The smallness of the ocular attachment$ o{ the recti muscles is

HIROSHI HOSOKAWA

4generally thought to have much to do with the decline of the oculomotor function in the whale.
Concerning the obliqui muscles nothing special is found in the
cetacean eye, except that the ocular insertion of the inferior obliquus
is sometimes divided into two portions, as shown in Fig. 3.

Op!iq.
sup.

Obliq. inf.

a, fetm1 of Sei whale

Obliq. inf.

b, adult Sei whale

Fig. 3. Diagram to show the insertions of the oblique muscles(right eye, posterior view)

The retractor bulbi will be described at length later on.
THE INNERVATION of the obliqui and recti muscles is in thewhale intrinsically the same as in other animals; namely the inferior
obliquus and all the recti except the lateral rectus are supplied by theoculomotorius, while the superior obliquus and the lateral rectus are
innervated respectively by the trochlearis and the abducens. These
muscles and nerves are illustrated in Fig. 4 (a-g). Fig. 5 (a-e) shows
the intramuscular distribution of nerve fibres in each muscle. Fig. 6
is a diagram showing the innervations.
GANGLION CILIARE. In old times, more than a century ago,
Burns (1832) and Rapp (1837) could not find the ciliary ganglion in
Phocaena communis, but Stannius (1842) saw it in the same porpoise(cited from Schwalbe, 1879). Weber (1886), not finding it in Hyperoodon and other toothed whales, thought that this ganglion might be
missing or at least very rudimentary in them. In the whales treatedin the present work, both in the baleen and toothed ones, the existenceof this ganglion was ascertained, though they are usually very smallin size (Fig. 5, c). The radix brevis, connecting this ganglion withthe trunk of the oculomotor nerve, consists of one or two thin bundles,
sometimes very short, while in other cases it is considerably longer.

On the extrinsic eye muscles of the whale

,,/'

5

/ M. obliq. sup.

/,, M. palp. sup.
/IIaFig. 4. Extrinsic eye muscles and their innervations of the Sei whale(fetus, 7 feet) (right eye)

The radix longa, the connection with the ophthalmic nerve, is always
present, while the sympathetic root could not be seen.
The size of this ganglion is as follows;
1) Blue whale(fetus, 6 feet, left)
3x1.8x1.5 mm
2)
,,
,,
( ,,
7 feet, 1.)
1.1x0.8 x 0.8 mm
3) Fin whale( ,,8 feet, 1.)
3x2x1.2 mm
4),,,,( ,, 13 feet, right) 1.7x1.3.x 1.0 mm5) Sperm whale ( ,,3 feet, r.)
1.5x1.0 x 0.8 nim

HrnosH1 Roso KA w A

IV.l<'ig.~[4. bComparison with the ciliary ganglion of the cat (3.5 x 1.9 x 1.5 mm;
3.0x1.8x1.5 mm), dog (3.0x1.7 x 1.5 mm) and of the rabbit (0.8 x 0.6
x 0.5 mm) shows how small it is in the whale.
2.

General view of the retractor bulbi

The retractor bulbi is in the whale, as illustrated in Figs. 1 and 2,
composed of not very distinctly separated four portions. They insert
to the eyeball, as shown in Fig. 7, nearer the posterior pole of theeyeball than the recti muscles, and each portion is situated between
two of the latters. So I would call them respectively Pars superior
medialis, Pars superior lateralis, Pars inferior medialis and Pars
inferior lateralis. As generally known, the retractor is well developedOn the extrinsic eye inuscies of the whaie

V1, b

V1a

Fasciculus opticus

M. palp. lat. ,..........................

'''

....

' Fascia orbitalis

Fig. 4. cin amphibia and reptilia, while in birds the musculus pyramidalis andmusculus buralis s. quadratus are probably homologous to it. Also inmammals the retractor has a wide distribution ; only a few of themincluding man are devoid of this muscle. According to Halier v.
Hallerstein, these exceptional mammals are Orycteropus, Pteropus andPrimates1.
As in the whales, the mammalian retractor is often divided into
four portions. But it is sometimes not readily divisible into portions,for example in some domestic animals such as horse, ox, sheep and pig.
Many authors have studied the retractor, calling it with various
names, for instance, m. retractor bulbi s. oculi, m. suspensor[ius]oculi, m. choanoides, Grundmuskel, muscle en etonnoir, posterior rectus
etc.
1) Nussbaum (1893) and Fleischer (1907) described as anomalous cases a rudimentary retractor in the human being.

8

HIROSHI HOSOKA WA

VI'

V1, b

;

\

III
'\

Fasciculus opticus

\

\

/

/
/

Mm. retractores(Pars Iat. sup. et inf.)
Fig. 4. d

3.

Historical review on the motor innervation of the retractor bulbi

Before mentioning the nerves of the retractor in the whale, I
will review briefly the literature of the problem for various kinds ofanimals. Concerning lower vertebrates, previous authors said unanimously that it is supplied by the abducent nerve (Corning, 1902;
Nishi, 1922, 1938). As to the mammals, however, remarkable discrepancies have prevailed among the authors, of which the details werealready reported by Hopkins (1919) and Cords (1924). Table 1 represents the brfef summary of them. As shown in this table, the authors
might be classified into two groups, the one saying that the retractor
is innervated merely by branches from the abducens, and the otherattributing two or more nerve sources for this muscle. It is interesting to note that many of veterinary anatomists belong to the lattergroup. Most of them insisted on the dual innervation by the abducens

, • eye. mu scl.es of the whale
On the extrms1c
M. palpebralis sup.

M. obliq. sup.

/ Bulbus oculi
/

/

/

/

M. rectus lat.
/

/

/

/

~/

M. palp. me d.

/// M. palp. !at.

//

/

/

- '·

Arcus zygomaticus''

M. obliq. inf.

' M. palp. et reetus inf.

Fig. 4. e

M. oblig. sup.

V1, a
\

M. palp.
sup.

I

I

· / M. palp. Iat.

,,
MaxillaI\

M. obliq. inf.

Fig. 4. f//lirnosHI ltosoKA wA

10

M. palpebralis sup.
l\r. obliq. sup.
Il\rrn. retractores///

M. palp. rned.

l\r. rectus

Arcus zygornaticus

Fig. 4. gand the oculomotorius.
This remarkable disagreement attracted naturally the attentionof some anatomists, and especially Hopkins and Cords, in order todecide this problem, dissected many kinds of mammals repeatedly,using the binocular microscope. They found then no indication offilaments either from the superior or from the inferior division of theoculomotor nerve to the retractor, and so concluded that the mammalian
retractor is supplied exclusively by the abducent nerve just like inlower vertebrates. They said with confidence that all the statements
attributing the oculomotorius or other motor source were incorrect
for this muscle.

4.

Motor innervation of the cetacean· retractor bulbi

As shown in Table 1, Rapp (1837) and Stannius (1842) stated thatthe retractor of Phocaena communis is supplied by the abducent nerve1 •1) They described also a nerve supply from the ophthalmic nerve.
a sensory innervation I will state later in Chapter 8.

About such

On the extrinsic eye inuscies of the whaieii

Weber (1886) mentioned the same for Hyperoodon and other whales,
and Cords (1924) was also of the same opinion, when he dissected ayoung specimen of Delphinus phocaena.
In the present study, however, an interesting fact was seen that theretractor of the whale, especially its medial portions receive decidedly
branches from the inferior division of the oculomotor nerve, while
the lateral portions of this muscle are supplied without doubt bybranches of the abducens (Figs. 5, 8 and 9 a). I confirmed this fact
in all the whales treated in the present paper. There exists, concerning this point, no exception, although the branches are quantitatively
variant to some extent according to individuals or to species.

llI

VI

b

L-y-'
I

'--r' ;
/

\'

/

\

._,_,..,,... ~ '-r' 7-"
1 \,'<-::::>/,,; 'f Pars lat. inf. }'i / ". " Pars med. inf. m. retractoris~-- Pars Iat. sup.

M, palp, et rect. med. ;Pars med. sup.
M. palp. et rect. sup. m. retractoris

'

'I

l/

M. palp. et rect. !at.

Fig. 5. (1) Motor innervation of the extrinsic eye muscles(fetus of the l<'in whale, 13 feet, male) (right eye)12

llrnosm HosOKAWA
c

e

IV

Ggl. ciliare·

M. palp. et rect. in!.

dFig. 5. (2)

Jv·
III

VI

Palp. e~Rect. lat.

ubllq. inf,

Palp. et Reet.
inf.

Fig. 6. Diagram to show the innervation of the extrinsic
eye muscles in the whale (left eye, anterior view)

On the extrinsic eye muscles of the whale

Facies dorsalis-

R.s.

O.s.

13

Facies superior/

Ret. (s. m.)o.s.

P. m. --

-R. 1.

Facies inferior

Faeies medialis/ R.m.
,,
1

Ro i . . :. __--R.nt.
Ret. (i. I.) ---... ____ _.

Ret. (i. m.)

Facies lateralis

R.s. --

O. a.---Ret. (s. 1.)

Fig. 7.

-- ... ---- ----P. s. ; M. palpebralis superior
P. i. ; M. palp.
inferior
P. m. :. M. palp.
medialis
P. 1. ; M. palp.
lateralis
R. s. ; M. rectus superior, R. i. R~ i. ; M. rect. inferior
R. m. ; M. rect. medialk
R. I. ; M. rect. Iateralis
Ret. (s. m.); M. retractor bulb'(Pars superior medialis)Ret. (s. l.) ;_ /1 (P. sup. lat.)Ret. (i. m.); /1 (P. inf. med.)
Ret. (i. i.) ; /1 (P. inf. !at.)Insertions of the extrinsic eye muscles of the whale(Fetus of Sei whale, 7 feet) (right eye)Moreover, in all cases an anastomsis is existent between thetrunk of the abducens and the inferior division of the oculomotor
nerve near the top of the orbital cone. The anastomosing nerve
bundle comes proximally from the abducens and passes distally into
the oculomotorius. It is illustrated in Fig. 5, 8 and 9 a. Fig. 9 b isa simplified diagri:im to show the relation.

HIROSHI HOSOKAWA

14

Table

1.

Opinions of the previous authors upon the innervation of M. retractor bulbi in mammals
VI and other nerves

VI (N. abducens) only__A_u_t_h_o_r_s__ ,l _ _M_a_t_e_r_ia_I_s__ _ _ _ _A_u_t_h_or_s___ I Innervation

Materials

1

Stannius (1846) (comparative
anatomy)1

Foltz ('62)

horse, rabbit

Owen ('68)(comp. anat.)

Milne-Edwards! (comp. anat.)

Rapp (1838)
Stannius ('42)

VI+ V1

Phocaena comm.

Chauveau ('57)

VI + III

domestic animals

Krause ('68)

III only{ VI only

Gurlt ('73)

VI+ IIIrabbit etc.
cat, young ox(comp. anat.)

Schwalbe ('79)

VI+ III

II('76)

Wilder &Gage ('86)

domestic animals

Weber ('87)

Phocaena comm.,
Sei whale

sheep, ox, dog,
rabbit etc.
domestic animals

Leisering ('85)

Motais ('87)
Ellenberger &dog
Baum ('91, '96)
III onlyFrank ('94)
domestic animals
VI+ III
Nussbaum ('93) (comp. anat.)
Reute ('97)
fetus of pig
I I + II
Bradley('97)(veterinary
anat.)
I I + II
Gegenbaur(comp. anat.)
Varaldi ('99)
(
II
II )
('98)
I I + II
Du-Bois Reymonddog, cat, rabbit
I I + II
& Silex ('99, '07)
cat
Corning ('02)
dog, cat
Reighard etc. (1901)
III only
M'Fadyan ('02)
I VI+ III horse
Wiedersheim(comp. anat.)domestic animals
Struska ('03)
I JI+ II
('06)
II
II
Martin ('04)
I I + II
Share-Jones ('06)
III+ IV+ VI horse
III onlyman (anomaly)
Fleischer ('07)
Ellenberger &VI + III
domestic animals
Montanedomestic animals
Baum ('08, '12)
Bourdelle ('13)
horse, ox, sheep, Strangeway ('09) I VI+ x (III?) (veterinary anat.)I
Hopkins ('17) pig, dog, cat, Zimmerl ('09)
VI + III (II
JI )rabbit, etc.
Bensley ('10)!
JI + /1
rabbitCords ('24)
many kinds of
Bradley ('12)
III only
dog
mammals includ4
VI+III
domestic
ammalsiing Phocaena
I Sisson ('l )Mivart ('89)

cat

I

1

I

J

Key-A.bergs
('34)

comm.
rabbitImai ('34, '36)

I monkey, cat

I
I

I

I

On the extrinsic eye muscles of the whale

15

M. palp. med.

Ggl. ciliare---- M. palp. sup.

Fig. 8. Innervation of M. retractor bulbi (1)Fetus of Blue whale (7 feet) (left eye)Now, it occurs naturally the question whether the nerve fibres of
the anastomosis (a in Fig. 9 b) continue directly into the branches ofthe oculomotor nerve to the medial portions of the retractor (b inthe same figure). In other words, the branches in question may belong intrinsically to the abducens, like the branches to the lateral
portions, passing only temporarily via the oculomotorius. But becauseof the close adhesion of fiber bundles, it was impossible for me toseparate and trace the distal extention of the bundle a macroscopically.
So, I tried to settle 'the problem from various viewpoints.
A. CALCULATION OF NERVE FIBERS
First of all, the nerve fibres were calculated in the anastomosis
and in the branches of the oculomotorius going to the retractor. The
result upon a fetus of the Blue whale is shown in Table 2. The
medullated fibers of the bundle a amount to 768, while those of thebundle b are 806, exceeding thus the former by about 5%. If Kolliker

16

HIROSHI HOSOKAWA

III VIIIIVIyM. palp. et.
reet. sup. ---------

M. retractor(Pars med.)

"- 1/

--~

-~

M. pa!p. et/reet. inf. //M. obliq.
inf.

Pars medialis Pars lateralis
M. retractor(Pars !at.)a, Fetus of Blue Whale

M.retractorbulbib, Scheme

Fig. 9. Innervation of M. retractor bubli (2)(1867) and Sherrington (1894) be right in their remarks that the nerve
fiber does not bifurcate during its course in relatively thick nerve
trunk, which is macroscopically recognizable, one could admit that atleast some of the fibers in b are probably derived from the oculomotor
nerve itself. But my further calculation of fibers in the trochlear nerve in the same whale, showed that the nerve trunk contains in
the distal part more fibers than in the proxim.al part, the difference
amounting to 10% approximately.
Moreover, I found in a cat that a distal portion of the abducens
possesses about 20% more fibers than a proximal portion. And as
between the two points examined no addition of nerve fibers fromoutside to the nerve trunk occurred, this increase of nerve fibers in
number is very probably due to bifurcation or dichotomizing of anerve fiber within the nerve trunk. Eccles and Sherrington (1930)
insisted statistically, on the branching of both the afferent and efferent
fiber within the nerve trunk with unequivocal illustrations of bifurcating fibers. Other authors such as Dllnn (1902), BjOrkmann and Wohlfart (1936), Takagi (1948) etc. have also suggested or confirmed theincrease of nerve fibers distalwards in the nerve trunk.

On the extrinsic eye muscles of the whale

17

Table 2.
Fiber-analysis of N. III and N. VI of a Blue whale fetus(6 feet, left eye)~s

. k ness* 0 f
Parts[ total number I thic
shown in 1
fib
a fiberFig. 9, b I of nerve
res I

I

9247

j

thickness

numberI

401,_ _ _4_ _medium-sized \

5791

63

thick

x

%
I
I fibresnumberofof eachto the total
1

I
I
1

------!-----'

fi_n_e_~j ___3_o5_5___ ,___3_3_ _ j,_ _ _ _ _ _ _ _ _ _ , _ _
1

thick

l--y---l----70_4_1_ _

a

b

c

769

806

1160

* thick fibres:
medium-sized f.:fine fibres:

I

199

3

__
thick

34

4

med.-sized

549

71

fine

186

25

thick

18

2

med.-sized

548

72

fine

204

26

thick

18

2

med.-sized

901

78

fine

241

20

,

:~= m=:=:=~-s_iz_e_d~ -1= = -:_:=:=:= = :~= = :=:= = illarger than 5.0 µ (in diameter)
between 5.0 and 2.5 µ ( JI )smaller than 2.5 1,( JI )

Anyway, now that the distal increase of nerve fibers in number
along the nerve trunk is certain, all the nerve fibers in the bundle bof the whale may possibly be derived from the anastomosis a, though
at the same time we cannot deny also the possibility that some of
the fibers in b may belong originally to the oculomotorius. Thus itbecame clear that the numerical calculation of nerve fibers does notafford any reliable basis to decide the problem.
B. FIBER-ANALYSIS OF THE NERVE BUNDLES IN QUESTIONAs the second step, fiber-analysis was undertaken upon the nerve
bundles in question. Namely, all of the fiber-constituents were clas-

HIROSHI HoSOKAWA

18

sifted into three classes according to their diameter; thick, mediumsized and thin fibers, each being respectively more than 5 µ, between
5 ai'id 2.5 µ and less than 2.5 µin diameter. I determined the numberof fibers belonging to eachclass
in the bundles a, b, Y
80 ·,,and X as indicated in Fig. 9 b.
My data are given in Table 2.
70
Fig. 10 shows the result diagrammatically.
Thus,
the
60
bundle b displays nearly thesame fiber-composition as the60bundle a and also the same as40
the trunk of the abducens (Y).
If otherwise the trunk of the30
oculomotor nerve (X) exhibited· a different fiber-compositiono----<> x
20
from these three, it would tello------------0 yalmost undoubtedly that theo--------o a0-···-···· .. ·-·······•"-0 b
110bundle b is nothing but the distal extention of the bundle or·
anastomosis a.
fine fibres
medium-sized fibres
thick fibres
In reality, however, aFig. 10. Fiber-analysis of N. III and N.
striking resemblance was foundVI of a Blue Whale fetus
to exist as to the fiber-composition between the abducens (Y) and the trunk of the oculomotorius (X),and therefore, it became impossible for me to know the relation between the bundles b and a by means of the fiber-analysis 1 •"'C.

NERVE ENDINGS OF THE ABDUCENS, COMPARED WITH
THOSE OF THE OCULOMOTORIUS

Thirdly, nerve endings were examined in each of the eye musclesin the whale. For, if there be, concerning this point, any noticabledifference between the abducens and the oculomotorius, though thisassumption is rather unplausible, it might be helpful for determining
the nature of the bundle b, which innervates the medial portions of
the retractor. Some of the nerve endings stained by the Bielschowsky
method are illustrated in Fig. 11 (m. palpebralis lat.), in Fig. 12 (m.
1) Fig. 10 shows that the bundle b contains somewhat less fibers of larger diameter than the bundle a. It may be caused by the distal caliber-decrease of nerve
fi.bers testified by Eccles, Sherrington (1930), Bjorkmann and Wohlfart (1936).

13. ·~ ·~J ~

. '·1

<••

' '

t ,, •

If ~. ,,

'\·

4

2

'·~

ti ~ U'.__,;

Fig. 11. Nerve endings in M. palbebralis lateralis of Prodelphinus caeruleo-albus,;, ~ \

" ~· ~ '4.

l:l

.....
<.C

iD

po

~
P"'

~

.+

H>

0

rn

(!)

!ilg.

3

~
(!)

('$'

5·
rn

'"I

.+

~

(!)

(!)

P"'

.+

0

20

HIROSHI HosOKAWA

;;

..,,,
'::l
_, ·
~l
_.,,~

"""-\

__...,1

2

1

a, Pars medialisb, Pars lateralis
Fig. 18. Nerve endings in M. retractor bulbi of Prodelphinus caeruleo-albus

32!:\:)· •

.....

Cl)

:a::r'·
.....
""

(1)

::r'·

..,.

H>,

(D'

'"'
"'0

i::
,.,,

s

"<
(1)

(1)

~··

"'

5··

>-;

..,.>I

(1)

(1)

::r'

..,.

::;:!

0

HrnosHI HosoKA w A

22

palp. med.) and in Fig. 13 (m. retractor bulbi). A precise descriptionof these endings and the comparative anatomical discussions upon them
are not needed here, for we find no remarkable. difference or peculiarity, compared with them in other animals.
The motor nerve endings in the extrinsic eye muscles have beenstudied by many authors, viz. Retzius (1892), Hamada (1928), Hines(1931), Woollard (1931), Yokomatsu (1932) etc., for various kinds ofanimals, but never for the whale. In the huge amounts of literature,
however, no remarkable difference has ever been reported as to theanatomy of nerve endings between the trochlearis, the abducens andthe oculomotorius. For, all of the previous authors who have studied
this problem treated always the eye muscles as a whole, without
paying attention to each muscle separately. I myself compared theterminal branchings, terminal buttons etc. between the abducens in
m. palpebralis lateralis and pars lateralis m. retractoris bulbi and theoculomotorius in m. palpebralis medialis. But I failed to see any
noteworthy difference between the two. All of these muscles exhibitedvery similar nerve endings, notwithstanding whether the examinedmuscle bundle belongs to pars medialis of the retractor, the medial
palpebralis, to the lateral palpebralis or to pars lateralis of the retractor. The same histological research was performed also on theextraocular muscles of the cat, but with the similar results.
D.

MICRODISSECTION OF THE NERVE BUNDLES IN A DOLPHIN, PRODELPHINUS CAERULEO-ALBUS

A kind of the sharply snouted dolphin, Prodelphinus caeruleo-albus
Meyen, is very common to the sea near Izu Peninsula. And a good
opportunity was given me to dissect the extrinsic eye muscles of thisdolphin, and I found that, though the relations of nerves and muscles
in question are quite the same as in other whales, branches from theoculomotorius to the retractor are relatively simple in this dolphin
and the distance between the anatomosis a and the branching of
bundle b is considerably shorter than in other whales. So I endeavoured
to separate and trace the distal course of the bundle a along theoculomotor nerve. Using sharp pointed pincettes and needles underthe binocular microscope, the bundle a was dissected distalwards. The
result is shown in Fig. 14, which indicates clearly that the branches
innervating the medial portions of the retractor are really continuouswith the abducent nerve via the anastomosis.

On the extrinsic eye muscles of the whale

23

Thus finally I believe to have succeeded in proving that all portions of the retractor are innervated also in the whale by the abducens,though some of the nerve fibers supplying the medial portions of thismuscle run temporarily in the trunk of the oculomotorius and look
like branches from the latter apparently.
Ill

1tf

VI

VI

(

''
''
''
'•

;/~

"\\

: /

/"'/

\

!'

(Par~ latoralis).

,1,. ... "'M. retractor(Pars lateralis)'

M. retractor

'

'' ''
\f

right

M. retractor(Pars medialis)left

Fig. 14. Innervation of the M. retractor bulbi of Prodelphinus ·caeruleo-albus

5.

Comparative anatomical study upon the innervation of the retractor
bulbi

Then it occurred to me the question, whether the same relation
holds good also in other animals. If so, the divergent statements ofthe previous authors reviewed in Chapter 3 might be easy to understand. In other words, if the anastomosis a, being situated in thedepth of the orbita, be missed in observation, the peripheral branches
would be taken very possibly for branches of the oculomotor nerve
itself. For this sake the eyes of cats, dogs and rabbits were dissectedwith greatest caution. But, as shown in Figs. 15 and 16, such relations as seen in the whale were never present in these animals.
Neither the anastomosis between the abducens and the oculomotorius
nor branches which, arising from the latter, innervate the retractor
were found. Hence this type of innervation of the retractor is forltmosm itosoKAW'A

24

a

HI

VI

lil

b

III

VI

c

VI

V1
Rect. sup.

R.·s.

Rect. med.

R.m.

Reet. inf.

l..,--1

Obliq. inf.

,

Retractor'

Retraetor

R.1.
Retractor

Fig. 15. Innervation of the M. retractor bulbi of cat (a), dog (b) andrabbit (c)Fig. 16. Diagram to show the innervation of the extrinsic eye muscles ofcat (a) and rabbit (b) (left eye, anterior view)

the present to be considered as peculiar to the whales 1 •Additionally I wish to mention a bold assumption upon the cause
why a number of authors such as Schwalbe (1879), Du-Bois Reymond(1907) etc. have incorrectly thought of the dual innervation of theretractor from the abducens and the oculomotorius. In the mammals
1) For me it is difficult to understand, why Rapp, Stannius, Weber and Cords did
not find this peculiarity in the whale. Phocaena and Hyperoodon which they used as
the materials may lack in this peculiaritry. But I can hardly surmise such a possibility.

25

On the extrinsic eye muscles of the whale

examined by me, cat, dog and rabbit, some of the nervi ciliares
breves arising from the . ciliary ganglion go winded around the retractor or penetrate this before they reach the optic nerve. Becauseof this somewhat confusing course, they might have been taken as
terminating in the retractor itself1 •6.

Physiological studies upon the retrr·actor· bulbi of the cat
A.

INNERVATION OF THE RETRACTOR

According to Hopkins and Nishi, Foltz (1862) and Key-Abergs (1934)
examined physiologically the innervation of the retractor respectively
in the horse and in the rabbit. I myself carried out a few physiologicalexperiments upon the retractor bulbi of the cat. The result is shownin Fig. 17. When the trunk of the abducens is stimulated with electri-i·,1,6 volt

a. Electric stimulation of
the N. abducens

b. Electric stimulation of
the N. oculomotorius

Fig. 17. Experimental study upon the innervation of the M. retractor
bulbi (cat)city, the retractor contracts intensely, while it does not show any
contraction by stimulation of the oculomotor nerve. This observationis quite consistent with the macroscopic dissection illustrated in Fig. 15.
In Fig. 17 b one sees a slight contraction of the retractor by stimulation of the oculomotorius. Perhaps, this may be due to collateralcurrent, presence of which could be proven with the tester.
1) Cords said the same thing, too, though briefly (p. 243, foot-note 2).

26

HIROSHI HOSOKAWA

B.

THE FUNCTION OF THE RETRACTOR BULBI

Together with the above mentioned experiments, I attempted toknow the real function of the retractor muscle, for the name "m.
retractor bulbi s. oculi" is one which was given by the anatomists
such as Stannius, Benz, Gegenbaur etc. probably from purely morphological standpoint, and we have had seemingly no definite, physiological proof to show the appropriateness of this name. According toCords, some authors assumed other functions for this muscle ; for example, Milne-Edwards, Stannius, Straus-Durkheim, Le Double, Ellenberger-Baum thought that it· might merely cooperate with the recti
mu:3cles. Motais and Martin supposed, on the other hand, that it
might serve to support the eyeball for the purpose to allow the higher
activity of the straight and oblique muscles (m. suspensorius oculi).
To answer this problem, I stimulated the nerves and muscles individually with the electrode, examining the movements of the eyeball. The details of my resultsareomitted here. The concluRetraction
Rotationsive remarks are representedof theof theBulbus oculi
Bulbus octili
by Fig. 18; that is, the recti
When the straightand obliqui muscles rotate theor oblique muscle
eyeball by their contraction,
contracts
but do not retract the eyebali
When theM. retractor
at all, while the retractor
bulbi contracts
muscle pulls backward the eyeball strikingly, without causing
Fig. 18. Experimental study upon the
any rotation.
function of the M. retractor bulbi (cat)Thus, it became doubtlessthat the retractor bulbi serves almost exclusively for the retractionof the eyeball ; in other words, it deserves the name quite adequately
also from the physiological aspect.

7.

III

±

±

III

Motor nucleus of the retractor bulbi in the brain-stem

The intramedullar location of the motor nucleus for the retractor
bulbi has not yet been determined. According to Kappers, Huber andCrosby (1936), some authors have accounted the so-called accessory
nucleus of the abducens for it. But this nucleus, which gene;ally
exists in mammals including man (Terni, Preziuss, Addens etc.), andon the other side interpreted as the "dorsal facial nucleus" (vanValkenberg, Kappers), does not seem in reality to send fibers eitherOn the extrinsic eye muscles of the whale27

in the facial or in the abducent' nerve. Furthermore, if we recollectthat the retractor bulbi is absent in the primates including man, while
this cell group is well developed in them, it is quite unreasonable to·regard those nerve cells as the nucleus innervating the retractor. In
my opinion, such a nucleus may exist somewhere in the brain-stem,
probably occupying a portion in the nucleus nervi abducentis. The
reason, why I supposed so, is thus:
The fibers of the abducens going to the retractor amount to about
2,000 in a fetus of the Blue whale, making nearly one third or one
fourth of all the fibers of this nerve (Table 2), and they can be followed proximalward as relatveiy definite parts within the trunk of
the abducens 1• In other words, the nerve fibers supplying the retractor
are well localized within the abducens. I guess, such a localization
may also exist in its original nucleus.
So I studied at first the comparative anatomy of the abducens
nucleus by serial sections stained with the Pal-Weigert method, paying
special attention to the morphological difference of this nucleus between
animals with and without the -retractor muscle. But no remarkabledifference could be found, which is available for this purpose2 •Secondly, I performed degeneration-experiments using a few catsas the material. Because of technical difficulty, however, the operative
removal of the retractor bulbi was not successful. So the lateral
rectus muscle of one side was extirpated together with its nervous
insertions; the retractor with its nerves remained intact. After thelapse of ten or fourteen days the cat was killed and the brain-stem
was fixed in alcohol, 20 µ thick sections were prepared serially andstained with thionin. At the same time, utilizing the osmic acid, theretrograde degeneration of the lateral rectus fibers of the abducens
and the intactness of the retractor fibers were examined. The serial
sections of the brain-stem revealed, however, no marked change either
in the root fibers of the abducens or in the nerve cells of the original
nucleus of the abducens.
It seems, injuries on such peripheral extremities of root fibers do
not bring forth any remarkable tigrolysis in their original nerve cells.
But the cells in the rostral portion of the abducens nucleus showed a1) In the abducent nerve of the cat, I found the retractor supplying fibers
numbered about 300, occupying approximately one fourth of the total fibers of about
1200.
2) Concerning the comparative anatomical study of the nucleus n. abducentis,
Fuse's detailed work published in 1912 teaches us very much.

28

Hrnosm .HosoKAWA

slight tencency of tigrolysis on the operated side, whereas the caudal
portion looked perfectly intact. At present I am inclined to think,that the rostral part of this nucleus may supply fibers to the lateral
rectus, while the caudal portion may send them to the retractor
muscle. Naturally I can have no definite opinion upon this problem.
8. · Sensory fibers of the retractor bulbi and of other extrinsic eye
muscles in the whale

Though the retractor bulbi is said to have no sensory innervation(Huber, 1899, 1900, etc.), I observed in this muscle of the whales aswell as of the cat many nerve endings, which are very much like thesensory ones. Some of them are illustrated in Fig. 13 (b, 2, 3). These
endings, especially that shown in Fig. 13, b, 3 resembles to a highdegree the grape-like ending (terminaison en grappe) described by
Tschiriew (1879), who explained them as a young, undeveloped formof the motor end-plate. Retzius (1892) too called such endings as"atypical" motor ones. On the other hand, Bremer (1882), Huber(1899), etc, took them, being situated epilemmally, for sensory endingsin the skeletal muscles, and also in Dogiel's excellent work on thesensory endings in the extrinsic eye muscles (1906) similar endings
were described as sensory and illustrated very precisely. Thoughsome recent anatomists, Hines (1931) etc., were of the opinion thatthose endings, lying sometimes hypolemmally or coming from an axis
cylinder which constitutes a medullated nerve fiber continuing to motor
end-plates, might be motor in nature, it is more generally believedthat at least some of those grape-like endings are of the sensory
character (Kulchitsky, 1925 ; Hinsey, 1927; Woollard, 1931 etc.) 1 ' 2 •My macroscopic:U observations upon the sensory nerves to theretractor of the whale, are shown in Fig. 19; the ophthalmic nerve(V1 in this figure) is seen supplying thin branches to the retractor 3 • In
1) Boeke (1927) said that, though the most of grape-like endings are either motor
or sensory, some of them are of the sympathetic nature.
2) In relation to the sensory endings in the extrinsic eye muscles, Cooper, Danieland Whitteridge's recent paper (1949) is very important. By recording impulses in
the nerve from the inferior obliquus of goats during stretch or active contraction of
the muscle, they obtained physiological evidence for the presence of proprioceptors inthis muscle. They ascribed however such a proprioceptive function to the muscle
spindles.
3) The ophthalmic nerve of the whale is composed of two main branches. Oneof them takes the course similar to the nasociliary nerve in other mammals and man(Via in Fig. 19), while the other appears to correspond to the lacrimal nerve (V 1b in
Fig. 19).

On the extrinsic eye muscles of the whale, Portio major } V,'
Portio minor
I

Gg1. semilunare
!

I

I

/

/

/

Va

Fig. 19. Sensory innervation of the external eye muscles of
the whale (1) (Fetus of the Sperm whale)from Vrn

IV

vr
D

I

M. rectus sup.
M. obliq. sup.
M. rectus lat.
D : direct insertion
I : indirect insertion
Fig. 20. Sensory innervation of the external eye muscles of the whale (2)

r

29

30

HIROSHI HosoKA w A

this figure, furthermore, the sensory branches to other extrinsic eye
muscles are illustrated. Examining these nerves, a remarkable featurequite different from the case in man is noticed. For, as described wellin Schwalbe's textbook (1881), in man the sensory fibers to the extrinsic
eye muscles, branching from the trunk of the ophthalmic nerve near
the sinus cavernosus or at the entrance of the orbita, go immediately
into the trunk of the oculomotorius, trochlearis or of the abducens
and run together with those motor nerves until their destinations.
In the whale, on the contrary, the sensory nerves course independently
for a long distance until very near their insertions to the muscle.
Though sometimes they run along with the motor nerves, the adhesionor union takes place only in the very vicinity of their terminations(indirect insertion in Fig. 20). Even in such cases, some of the sensory
nerves reach the muscle quite independently from the motor nerves(direct imertion in Fig. 20).
Concerning the sensory fibers of the extrinsic eye muscles of rabbit,
cat and monkey, Tozer and Sherrington (1910) stated that nearly allof them run from beginning to end of their ocurse within the motor
nerves such as trochlearis, oculomotorius and abducens, while thetrigeminal nerve has nothing to do with the sensory innervation ofthese muscles. Woollard (1931) and Hines (1931) also said the samefor rabbit, dog, cat,. rat etc. Their reason for this conclusion is, that
almost all of the intramuscular nerve endings, both of motor andsensory nature, disappeared, after the motor nerves were severed attheir exits from the brain-stem. According to Hines, those sensory
nerves have their origin in the upper portion of the nucleus mesencephalicus of the trigeminal nerve.
In the present work no definite evidence was obtained to settle
the problem, whether the extraocular muscles of tne whale receive
also such sensory fibers other than the above mentioned branches
issuing from the ophthalmic nerve.
Summary1) The musculi palpebrales of the cetacean eye are of an uniqueexistence throughout the animal kingdom. The motor innervation ofthem is quite the same as that of four straight muscles,· which insert
to the eyeball; namely, the lateral palpebralis is supplied by the abducens, while the other three are innervated by the oculomotorius.
2) . The musculi obliqui and the innervations of them show nothingOn the extrinsic eye muscles of the whale31

peculiar in the cetacea, with one exception that the ocular insertionof the inferior obliquus is sometimes divided into two portions.
3) The ciliary ganglion, the preSE!nce of which has not yet beenclarified in the cetacea, exists in all of Mystaco- and Odontoceti treatedin the present work, though always rather in vestigial conditions.
4) The retractor bulbi is remarkably well developed in the whales,
and is .divided into four portions: Pars superior medialis and lateralis,
Pars inferior medialis and lateralis.
5) The retractor bulbi of the whale is apparently innervateddoubly by the abducens and by the oculomotorius, each nerve supplying
the lateral and medial portions of this muscle respectively. But thebranches innervating the medial portions are, though they appear toarise from the oculomotorius, nothing but fibers which belong essentiallyto the abducens and have coursed orily temporarily in the trunk of
the oculomotorius. Namely, all the portions of the retractor aresupplied in the whale exclusively by the abducens just like in allother animals, whose retractor receives direct branches from the ab·ducens only. Such a temporary course of the abducens fibers via theoculomotorius trunk is very peculiar for the cetacea. ·6) The name "musculus retractor bulbi" is appropriate for thismuscle, as my experiments on the cat's eye resulted, that its contraction caused a striking retraction of the eyeball, while the recti andobliqui muscles brought forth merely rotating movements of the eyeball.
7) There seems to be some possibility that the nerve cells supplying motor fibers to the retractor are localized in the caudal partof the nucleus n. abducentis.
8) The retractor bulbi as well as the other extrinsic eye muscles
receives in the whale sensory innervation from the ophthalmicus.
9) The sensory nerves of the extrinsic eye muscles show in the
cetacea a different feature from those in man. In the former theyrun from the ophthalmic nerve quite independently until their insertions
to the muscles, while in the latter the sensory nerves course nearlythrough the whole length united with the motor nerves, viz. oculomotorius, trochlearis, and abducens.

32

HIROSHI HosOKAWA

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On the extrinsic eye muscles of the whale

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s.