Cranial nerves III, IV, and VI (a brief summary is at the end of this presentation):
General. Cranial nerves III, IV, and VI, innervate the extraocular muscles. The
extraocular muscles are the striated muscles that attach external to the eyeball. They
are to be differentiated from the intraocular muscles, which, in our domestic mammals,
are smooth muscle and internal to the eyeball. The innervation of the ocular muscles
is significant in examining the animal as “eye movement and the resting position of
the eyes; and appearance of the pupil” are three of the clues that we use routinely.
See the list at the end of Nervous System 2.
The third cranial nerve is the oculomotor (eye-motor) nerve; the fourth is the trochlear
nerve, named after the pulley-like (trochlear) arrangement of its tendon with the
trochlear cartilage: and the sixth is the abducent nerve, named according to its
abducting action in turning the eyeball so that the gaze is lateral. In addition to
muscles that move the eyeball, the oculomotor innervates the levator palpebrae
superioris, which elevates the upper eyelid, and the oculomotor nerve also provides
parasympathetic innervation to the smooth muscle of the interior of the eyeball: the
constrictor muscle of the pupil; and the ciliary muscle, which changes lens curvature
in the process of accommodation, the bringing of light rays to a focus on the retina.
In the domestic mammals, the striated muscles that move the eyeball are the four
rectus muscles, medial, lateral, dorsal and ventral; the dorsal and ventral oblique
muscles, and the retractor bulbi muscle. Of these muscles, all but the dorsal oblique,
lateral rectus and retractor bulbi are innervated by the oculomotor nerve. The dorsal
oblique is innervated by the trochlear nerve. The lateral rectus and retractor bulbi are
innervated by the abducent nerve (that is, according to some workers; several
European texts state that only the lateral part of the retractor is supplied by the
abducent, the remaining medial portion by the oculomotor). With respect to the
retractor, it arises always directly medial to the lateral rectus. This is not determinative
of the question but lends some support to the idea that the retractor is split off the
lateral rectus and that both muscles receive their motor innervation from the abducent
nerve alone.
The eyeball and its attaching extraocular muscles are conical in form and are
enclosed within the periorbital membrane, which extends from the margin of the orbit
to the perimeter of the optic canal and orbital fissure. Medially the periorbital
membrane is fused with the periosteum of the bony orbital wall. Within the periorbita,
the eyeball rests on a fat pad and is freely movable, its movements determined by the
balance of impulses to opposing muscles: Dorsal and ventral rectus muscles, which
turn the eyeball so that the gaze is upward or downward, respectively; medial and
lateral rectus muscles, which turn the eyeball’s gaze medially and laterally,
respectively; and impulses to the oblique muscles, which are not strictly, but nearly,
antagonistic. All of these muscles, except the ventral oblique, take origin internal to
the periorbita from the perimeter of bone at the margin of the optic canal and orbital
fissure (the orbital fissure is incorporated in the foramen orbitorotundum in swine and
cattle) and insert in the fibrous sclera of the eyeball. The rectus muscles are the
largest and strongest muscles attaching to the eyeball and each inserts by a thin, flat
tendon anterior to the eyeball’s equator. The retractor bulbi, which is not present in
humans, some other primates, and birds, arises medial to the lateral rectus at the
lateral margin of the orbital fissure and divides into four fascicles, which insert
posterior to the equator; in the dog, at dorsomedial, dorsolateral, ventromedial, and
ventrolateral positions. The retractor is deep to the rectus muscles. It is an expanded,
thin muscle that envelops the eyeball and optic nerve posteriorly and draws the
eyeball toward the muscle’s origin at the orbital fissure. This increases pressure within
the space enclosed by the periorbital membrane and pushes out the third eyelid,
which is loosely attached. When extruded, the third eyelid covers the ventromedial
exposed aspect of the eyeball. The phenomenon has significance in tetanus infection
in the horse in which the retractor is hyperactive and the third eyelid flashes each time
that the muscle contracts.
Fig. 1. Extraocular muscles of the horse, lateral view of the orbit with periorbital
membrane largely cut away. The appearance is similar in all the domestic mammals.
Figure is from Topographische Anatomie des Pferdes, W. Ellenberger u. H. Baum: 1896,
Verlag Paul Parey
lacrimal gland
ventral oblique m.
dorsal rectus m.
lateral rectus m.
ventral rectus m.
periorbital membrane, partly
removed and reflected
medial rectus m.
Fig. 2. Deep dissection of the extraocular muscles of the horse, lateral view of the orbit
with lacrimal gland removed and periorbital membrane largely cut away. The appearance
is similar (but not the same) in all the domestic mammals. Figure is from Topographische
Anatomie des Pferdes, W. Ellenberger u. H. Baum: 1896, Verlag Paul Parey. The artist
has moved the dorsal oblique a little dorsally to show the muscle more fully than it would
normally be exposed in a strict lateral view.
dorsal rectus m. (cut)
ventral oblique m.
trochlea
dorsal oblique m.
lateral rectus m.
retractor bulbi
m. lbimm
ventral rectus m.
The dorsal oblique arises at the medial margin of the optic canal. It is smaller and
weaker than the rectus muscles, spindle-shaped, and lies internal to the periorbita
against the dorsomedial orbital wall. It is directed rostrodorsally toward the orbital
margin and a depression of the medial wall that is bridged by the trochlear cartilage.
The muscle tapers as it passes between the medial wall and the cartilage and,
emerging between the two, turns posterolaterally to its attachment dorsally on the
sclera; at its attachment, the tendon is posterior to the equator of the eyeball and
lateral to the optic axis. The tendon is deep to the dorsal rectus muscle. Contraction
of the muscle turns the dorsal aspect of the eyeball forward and medially. Since the
attachment is to a spherical eyeball, the gaze is directed ventrolaterally. The ventral
oblique arises from the medial wall of the orbit; in the dog, on the fibrous membrane
that covers a small regularly appearing separation of the palatomaxillary suture at the
medial wall of the maxillary foramen. The muscle passes laterally, ventral to the
ventral rectus, and inserts posterior to the equator and lateral to the optic axis. The
tendon inserts deep to the lateral rectus muscle on the lateral aspect of the eyeball.
Its contraction rotates the eyeball, turning its dorsal aspect laterally and the gaze a
little upward (dorsally).
Eye movement due to the oblique muscles is not easily detected on observing the
animal as the movement is slight and is incorporated in the total movement of the
eyeball. Paralysis of the dorsal oblique muscle is rare. It results in an unopposed
contraction of the ventral oblique with an exaggerated upward gaze of the affected
eye. With oculomotor nerve (ventral oblique; medial, dorsal and ventral rectus)
paralysis, lateral strabismus is the predominant sign.
Fig. 3A, Dorsal view, attachment of the dorsal oblique in humans; Fig. 3B, lateral
view, attachment of the ventral oblique in humans. To the writer’s knowledge, no
detailed work comparable to the work providing these figures has been done on the
anatomy of our domestic animals. Figures are from
http://www.cybersight.org/data/1/rec_docs/87_Ch%203%20%20Summary%20of%20the %20Gross%20Anatomy%20of%20the%20Extraocular%20M
uscles,%20p.%2038-51.pdf.
Fig. 3A
Fig. 3B
dorsal (super.)
oblique tendon
Fig. 4. Skull, canine. Lateral view with zygomatic arch removed. The depression
bridged by the trochlea of the dorsal oblique and the origin of the ventral oblique
are marked.
depression bridged by trochlea
gap in the palatomaxillary suture, in
life, covered by membrane from
which the ventral oblique takes origin
Contraction of the rectus and oblique muscles is utilized to effect the delicate
movements that keep the area of visual interest centered on the macular area of the
retina. The innervation of these muscles and their action on the eyeball become
significant chiefly in cases of paralysis but will be a consideration in the case of a
muscle’s not functioning for any reason. Thus, with paralysis of the abducent nerve,
the gaze on the affected side remains always medial, and so on.
Movements of the eyeball are coordinated to maintain the area of visual interest
focused on the macular area, or the area of the retina providing most acute vision,
which varies in form according to species. These movements are often quite precise
and the motor unit of each motor nerve fiber will be small. Different from the
innervation of muscles that effect coarse movements, e.g., the bicep femoris, the
triceps brachii, in which a single nerve fiber may innervate more than one thousand
myofibers, a single nerve fiber of cranial nerves III, IV, and VI innervates perhaps only
10 myofibers. Moreover, the eye muscles provide a rich source of neuromuscular
spindles, which furnish the necessary feedback of muscle length that enables
precision in coordinate contraction and relaxation of muscle fibers. The proprioceptive
fibers that innervate the extraocular muscles are all from the trigeminal. Thus, in
addition to its motor innervation, every extraocular muscle receives as well trigeminal
fibers, which mediate proprioception (Proprioceptive knowledge of eye position,
Steinbach, M.J., Vision Research, 27, 1737 – 1744, 1987) and, probably, pain. These
sensory fibers probably reach cranial nerves III, IV, and VI, as those nerves pass in
proximity to the ophthalmic nerve in relation to the cavernous sinus or through the
orbital fissure.
Oculomotor Nerve. The oculomotor nerve passes from the ventromedial aspect of
the crus cerebri, perforates the arachnoidea and the dura mater of the floor of the
cranial vault and enters the orbital fissure, accompanied by the trochlear, abducent,
and ophthalmic nerves, and the emissary vein of the orbital fissure, which joins the
cavernous venous sinus to the orbital plexus of veins (dog, cat, Equidae; in ruminants
and swine, the homologous vein is designated the emissary vein of the foramen
orbitorotundum).
As it emerges from the medial part of the orbital fissure, the oculomotor nerve divides
into a dorsal branch, which supplies the dorsal rectus and levator of the upper eyelid,
and the medial rectus and a ventral branch which supplies the ventral rectus and the
ventral oblique, and bears the parasympathetic fibers which form the parasympathetic
root of the ciliary ganglion. The arrangement of these branches, excepting the
parasympathetic root of the ciliary ganglion, is shown in yellow in Fig. 5. The position
of the ciliary ganglion is shown in Fig. 5.
The parasympathetic nucleus of the oculomotor nerve occupies the ventrolateral
periaqueductal gray of the midbrain just dorsal to the oculomotor nucleus. Its position,
as it appears in the red kangaroo, can be seen in Fig. 6. The smaller animals are
closer to the ground and have a greater use of the muscle of accomodation for
focussing on near-objects. The smooth muscle of accomodation is better developed
in the dog and cat than in the horse and a greater number of ganglion cells that
supply the muscle is reasonably expected. Ellenberger-Baum (1943) states that the
ganglion is absolutely largest in the cat.
Parasympathetic ganglia generally receive three kinds of fibers: 1. Preganglionic
parasympathetic fibers, the “parasympathetic root”; 2. Sensory fibers, the sensory
“root”; and 3. Sympathetic fibers make up the sympathetic “root”. Parasympathetic
fibers synapse in the ganglion; sensory and sympathetic fibers pass through the
ganglion without synapse. The ciliary ganglion’s parasympathetic root passes from
the ventral branch of the oculomotor; its sensory root, from the long ciliary nerve, a
branch of the nasociliary branch of the opththalmic, and the sympathetic root is
thought to proceed from the nerve of the pterygoid canal. The nerves that pass from
the ganglion--- in the case of the ciliary ganglion, the short ciliary nerves--- are a
common path for the three kinds of fibers. The short ciliary nerves perforate the sclera
in a circular arrangement around the optic nerve and enter the choroidea.
Sympathetic fibers supply the dilatator of the pupil; parasympathetic fibers supply the
constrictor muscle of the pupil and the muscle of accomodation; sensory fibers form
neuroreceptor synapses with receptors for pain, touch and pressure.
Reflexes mediated by the autonomic (sympathetic, parasympathetic) fibers of the
ciliary nerves:
1. determine the size of the pupil in response to light and darkness;
2. provide the narrowing of the pupil associated with accomodation;
3. provide the changes in the curvature of the lens in the process of
accomodation.
The sensory fibers of the ciliary nerves mediate the oculocardiac reflex in which
increasing pressure within the eyeball results in a slowing of the heart rate. In the text
Human Physiology (Bernardo Houssay et al.: 1955, McGraw Hill) is recited the
physiological correspondence of intraocular pressure and blood pressure. The
oculocardiac reflex appears to be general; that is, placing digital pressure on the
eyeball of an animal results in a slowing of the heart rate.
Fig. 5. Canine, anterior view of structures at the apex of the orbit.
m. levator palpebrae superioris
m. rectus dorsalis
m. retractor bulbi
oculomotor n.,
dorsal branch
ventral branch
branch to m.
obliquus ventralis
m. obliquus dorsalis
m. rectus lateralis
optic n.
m. rectus medialis
position of
ciliary ganglion
m. rectus ventralis
Fig. 6. Myelin-stained section at the level of the rostral midbrain of the red kangaroo
(from: Brain Biodiversity Bank, Michigan State University:
www.msu.edu/~brains/brains/redkangaroo/sections/redroo_sec1103.jpg).
parasympathetic nucleus
of the oculomotor nerve
oculomotor
nucleus
red nucleus
oculomotor nerve fibers; they
pass through the medial part
of the red nucleus and
emerge from the midbrain
medial to the crus cerebri
crus cerebri
Fig. 7. Canine brain, lateral view with left hemisphere removed. The
origin of the oculomotor, trochlear, trigeminal, and abducent nerves is
indicated.
IV
V
crus cerebri
III
VI
Fig. 8. Canine brain, dorsal view with hemispheres (in part) and
cerebellum (entirely) removed. The origin of the trochlear and trigeminal
nerves is indicated.
IV
V
Fig. 9. Canine brain, ventral view. The olfactory bulb (designated I, here)
and the origin of the optic, oculomotor, trochlear, trigeminal (V), and
abducent nerves is indicated.
I
II
III
IV
V
VI
Trochlear Nerve. The trochlear nerve arises from the midbrain at the level of the
caudal (posterior) colliculus. The trochlear nucleus is ventral to the periaqueductal
gray in a paramedian position at rostral (anterior) levels of the caudal colliculus. It is
separated from the oculomotor nucleus by an interval of perhaps .5 cm in the dog.
Fig. 10. Canine brain, sagittal section, myelin hematoxylin stain. From The Brain
of the Dog in Section, Plate 60, Marcus Singer, 1962: Saunders.
nuclei of the oculomotor and
trochlear nerves in the ventrolateral
periaqueductal gray
Fibers pass caudally from the trochlear nucleus and enter the anterior (rostral)
medullary velum of the fourth ventricle where they incline sharply medially,
decussating with the contralateral fibers. Following decussation, the fibers emerge
dorsally from the midbrain beneath the caudal colliculus and, within the subarachnoid
space, pass laterally and turn rostroventrally alongside the midbrain. They perforate
the dura of the tentorium cerebelli and continue rostrally with the third, fifth, and sixth
cranial nerves in relation to the cavernous sinus. The third, fourth, and sixth cranial
nerves and the ophthalmic branch of the fifth with the emissary vein of the orbital
fissure continue rostrally through the orbital fissure, emerging at the apex of the orbit
where the trochlear nerve enters the dorsal oblique muscle.
Fig. 11. Sheep brain at the level of the decussation of the trochlear nerve in the
rostral medullary velum. Myelin stain. The rostral end of the fourth ventricle can be
seen ventral to the velum.
trochlear nerve
Fig. 12. Canine brain, median section.
mesencephalic aqueduct
rostral colliculus
caudal colliculus
decussation of trochlear
nerve within the rostral
medullary velum
cerebellum
Fig. 13. Equine orbit, deep dissection, lateral view. The dorsal rectus is
removed in part to expose the dorsal oblique, which the artist has moved
a little dorsally in what would otherwise be a strict lateral view. In this
figure, the dorsal oblique is emphasized and the trochlear nerve is shown
in yellow. Figure is from Topographische Anatomie des Pferdes, W.
Ellenberger u. H. Baum: 1896, Verlag Paul Parey.
medial rectus m.
dorsal rectus m. (cut)
trochlea
frontal n.
dorsal oblique m.
infratrochlear n.
trochlear n.
ethmoidal n.
fFig.14. Canine, rostral view of the nerves, vessels, and muscles at the level of the
optic canal and orbital fissure. The optic canal transmits the optic nerve and
internal ophthalmic artery (not shown in this figure); the orbital fissure transmits
other vessels and nerves that supply the orbit: emissary vein of the orbital fissure,
oculomotor, trochlear (not shown in this figure), abducent, and ophthalmic nerves.
ophthalmic nerve:
lacrimal,
frontal,
ethmoidal,
nasociliary,
long ciliary
abducent nerve
ethmoidal artery
aaa
emissary vein, orbital fissure
optic n.
oculomotor nerve
nerve
The trochlear nerve is not shown in Figs. 5 or 14 and I have not traced it. In humans,
it passes medially from the orbital fissure caudal to the origin of the levator palpebrae
and the dorsal rectus, then onto the dorsolateral aspect of the dorsal oblique and
extends along the deep, lateral, aspect of the muscle, which it enters. Paralysis of the
dorsal oblique leaves the ventral oblique unopposed and the gaze is directed dorsally.
Fig. 15. Canine, left orbit, with much of the tissues removed to show the veins of
the medial orbital plexus. Note that the ethmoidal a./v. pass medial to the dorsal
oblique muscle; the ethmoidal n., lateral to the dorsal oblique, then between it and
the medial rectus to enter the more ventral of the two ethmoidal foramina.
venous trunk joining angular vein of the eye
and the emissary vein of the orbital fissure
dorsal oblique m.
ethmoidal a./v.
angular vein of the eye
ethmoidal n.
medial rectus m.
emissary vein of
the orbital fissure
optic nerve
emissary vein of
the round foramen
(enters the rostral
alar foramen)
deep facial vein
ethmoidal foramina
optic canal
orbital fissure
rostral alar foramen
Abducent Nerve. The nucleus of the abducent nerve is located at the pontomedullary
junction a little below the floor of the fourth ventricle. The nucleus is ventrolateral to
the genu of the facial nerve and lateral to the medial longitudinal fasciculus. Its fibers,
all of them motor, pass ventrally, emerging at the caudolateral angle of junction of the
pyramid and trapezoid body. From this point the nerve passes forward in the
subarachnoid space and perforates the dura, joining the 3rd, 4th and 5th cranial nerves
in relation to the cavernous sinus. With the ophthalmic branch of the trigeminal and
the emissary vein, all depart the cranial cavity at the orbital fissure and enter the
apical part of the orbit. The abducent nerve is most lateral as it emerges from the
fissure and gives off branches to the retractor bulbi and the deep, medial, surface of
the lateral rectus.
Fig. 16. Canine brain, cross-section at pontomedullary junction, hematoxylin stain.
From The Brain of the Dog in Section, Marcus Singer, 1962: Saunders. Inset is
taken from the main figure and labeled particularly for the abducent nucleus.
genu, facial nerve
medial longitudinal fasciculus
abducent nucleus
abducent nerve fibers
Fig. 16. Canine brain, lateral view with left hemisphere removed. Trapezoid
body, pyramid, and abducent nerve are marked.
trapezoid body
abducent nerve
pyramid
Fig. 17. Relations at the orbital fissure.
position of
orbital fissure
(dashed line)
ophthalmic nerve branches
abducent n.
oculomotor n.
lateral rectus and
retractor bulbi
emissary v. of the
orbital fissure
Summary: The 3rd, 4th, and 6th cranial nerves innervate the striated muscles that are
responsible for movements of the eyeball. The 3rd cranial nerve also innervates the
striated proper levator of the upper eyelid and the pupillary constrictor and ciliary
smooth muscle.
1. When a nerve supplying any striated (skeletal) muscle is injured, myofibers
affected will cease to function at once and these myofibers will begin to
atrophy. In the case of nerves supplying smooth muscle, in general, only its
regulation is lost. In the case of the pupillary constrictor, it loses its regulation
but the pupillary dilator is still receiving innervation and is functional. The
result is a dilated pupil that does not constrict in response to light. Loss of
ciliary smooth muscle innervation with failure of accommodation is not
generally detected in our animals; loss of accomodation would be a source of
complaint by persons, who would find be unable to focus on near-objects on
the affected side.
2. Injury to the oculomotor nerve peripherally, depending on location of the
injury and the degree of involvement, is most obvious as a lateral strabismus
(the affected eye directed laterally), mild drooping of the upper eyelid, and a
dilated pupil on the affected side. If the injury is central, depending on the
size and location of the injury, a number of additional signs could be present.
In this regard, it should be noted that most or all of the fibers supplying the
dorsal rectus come from the contralateral oculomotor nucleus. This would be
of no consequence in the case of a peripheral oculomotor lesion but, with a
central lesion, would affect oculomotor eye muscles of the affected side save
for the dorsal rectus which would be paralyzed on the opposite side.
3. Peripheral injury to the trochlear nerve with loss of dorsal oblique function
results in an unopposed ventral oblique and an upward deviated eye. If the
injury is central, depending on the location and extent of the injury, a number
of additional signs could be present.
4. Peripheral injury to the abducent nerve results in a medial strabismus and
inability to retract the eyeball. Again, as with the oculomotor and trochlear
nerves, if the injury is central, a number of additional signs could be present.
This concludes this presentation.