23

Ocular Motor Nerves

CHAPTER SUMMARY
The Nerves, 243 The Near Response, 246
Oculomotor Nerve, 243 The Far Response, 246
Trochlear Nerve, 244 Notes on the Sympathetic Pathway to the Eye, 247
Abducens Nerve, 244 Control of Eye Movements, 247
Nerve Endings, 245 Gaze Shifting, 248
Motor Endings, 245 Gaze Holding, 249
Sensory Endings, 245 Clinical Panel
Pupillary Light Reflex, 245 Ocular Palsies, 249
Accommodation Reflex, 246

STUDY GUIDELINES
are ‘yoked’ and work together to keep both eyes in their
General
cardinal position of gaze.
Because of the immense diagnostic and therapeutic importance
2. Indicate the nerve supply to the six muscles that move the
of ocular muscle innervation, and because of its inherent
eyeball and describe how the CN III elevates the upper
complexity, neuro-ophthalmology has become its own branch
eyelid.
of medicine.
3. Contrast the effects of the sympathetic and parasympathetic
It is especially important to describe the way in which
autonomic nerve supply to the eye; explain the changes
premotor centres can operate bilaterally to keep the gaze on
and anatomic pathways that are responsible for the
target, even when the head is moving.
pupillary changes noted in a dark room, in a well-lit
Specific
room, and when focusing on an object held close to
1. Describe the function of cranial nerves (CN) III, IV, and one’s nose.
VI on eye movements; identify which extraocular muscles

THE NERVES The nerve passes through the tegmentum of the midbrain
The ocular motor nerves comprise the oculomotor (CN III), and emerges into the interpeduncular fossa. It crosses the apex
trochlear (CN IV), and abducens (CN VI) nerves. They provide of the petrous temporal bone, pierces the dural roof of the
the motor nerve supply to the four recti and two oblique muscles
controlling movements of the eyeball on each side (Fig. 23.1). The
oculomotor nerve contains two additional sets of neurons: one to
supply the levator of the upper eyelid and the other to control the Superior oblique
sphincter muscle of the pupil and the ciliary muscle.
Superior rectus
The nuclei serving the extraocular muscles (extrinsic muscles
of the eye) belong to the somatic efferent cell column of the Optic nerve
brainstem, in line with the nucleus of the hypoglossal nerve.
The oculomotor nucleus has an additional, parasympathetic
nucleus that belongs to the general visceral efferent cell column. Medial rectus

Lateral rectus
Oculomotor Nerve
The nucleus of the third nerve is at the level of the superior colli-
culus of the midbrain. It is partly embedded in the periaqueduc-
tal grey matter (Fig. 23.2A). It is composed of five individual Inferior rectus
subnuclei, which supply striated muscles (ipsilateral subnuclei Inferior oblique
innervate the inferior rectus, inferior oblique, and medial rectus,
and the contralateral superior rectus muscle; the levator palpeb-
rae superioris is innervated by a single midline nucleus) and one
parasympathetic nucleus. Fig. 23.1 Extrinsic ocular muscles.

243
Downloaded for Pablo López (pilopez3@uc.cl) at Pontifical Catholic University of Chile from ClinicalKey.com by Elsevier on
November 06, 2022. For personal use only. No other uses without permission. Copyright ©2022. Elsevier Inc. All rights reserved.
244 CHAPTER 23 Ocular Motor Nerves

A
B

Peri-aqueductal
Superior colliculus Aqueduct grey matter Abducens nucleus
Trochlear nerve
Facial colliculus
Inferior colliculus
Facial nerve

Oculomotor nerve
Red nucleus Decussation of superior
cerebellar peduncles
A Upper midbrain
B Lower midbrain
Abducens nerve

C Lower pons

Fig. 23.2 (A C) Transverse sections of the brainstem showing the origins of the ocular motor nerves.

cavernous sinus (Fig. 23.3), runs in the lateral wall of the sinus,
and divides into an upper and a lower division within the
superior orbital fissure. The upper division supplies the super-
ior rectus and the levator palpebrae superioris; the lower divi-
sion supplies the inferior and medial recti and the inferior
oblique.
The parasympathetic fibres originate in the Edinger
Westphal nucleus. They accompany the main nerve into the
orbit and then leave the branch to the inferior oblique to
synapse in the ciliary ganglion. Postganglionic fibres
emerge from the ganglion in the short ciliary nerves, which
pierce the lamina cribrosa (‘sieve-like layer’) of the sclera
and supply the ciliary and sphincter (constrictor) pupillae
muscles.
Trochlear Nerve
The nucleus of the fourth nerve is at the level of the inferior col-
liculus of the midbrain. The nerve itself is unique in two respects
(Fig. 23.2B): it is the only nerve to emerge from the dorsum of
the brainstem and the only nerve to fully decussate.
The CN IV winds around the crus of the midbrain and tra-
vels in the wall of the cavernous sinus accompanied by CN III
(Fig. 23.3). It passes through the superior orbital fissure and
supplies the superior oblique muscle.
Abducens Nerve
The nucleus of the sixth nerve is in the floor of the fourth
ventricle, at the level of the facial colliculus in the lower pons
(Fig. 23.2C). The nerve descends to emerge at the lower border
of the pons (pontomedullary junction) and runs up the pontine
subarachnoid cistern beside the basilar artery. It angles over the
apex of the petrous part of the temporal bone and passes
through the cavernous sinus inferolateral to the internal carotid
artery (Fig. 23.3). It enters the orbit through the superior orbital
fissure and supplies the lateral rectus muscle, which abducts
the eye.

Downloaded for Pablo López (pilopez3@uc.cl) at Pontifical Catholic University of Chile from ClinicalKey.com by Elsevier on
November 06, 2022. For personal use only. No other uses without permission. Copyright ©2022. Elsevier Inc. All rights reserved.
 CHAPTER 23 Ocular Motor Nerves 245

Optic chiasm Internal carotid artery Hypophysis

Pituitary stalk Ophthalmic artery Pituitary stalk

Optic tract
Cavernous
Vii sinus
Vi III
Plane of IV
section in B
VI Vi
Viii
III Vii
IV
VI

Sphenoidal air sinus

Sympathetic plexus Internal carotid artery

A B

Fig. 23.3 (A) Middle cranial fossa with cavernous sinuses removed. (B) Coronal section in the plane of the hypophysis with the cavernous sinuses
in place. III, Oculomotor nerve; IV, trochlear nerve; VI, abducens nerve; Vi, Vii, Viii, ophthalmic, maxillary, mandibular divisions of trigeminal nerve.

NERVE ENDINGS provide proprioceptive information rather than contribute to

Motor Endings
All the ocular motor units are small, containing 5 to 10 muscle
fibres (compared with 1000 or more in the tibialis anterior mus-
cle). These motor units can be divided into three groups, of
which two are most relevant: motor neurons that form single
‘en plaque’ endings that innervate muscle fibres and respond
with a fast twitch and those that form multiple small ‘en grappe’
endings on muscle fibres that respond with a slow tonic con-
traction. The fast twitch muscle fibres are likely involved with
saccadic or rapid eye movements, while the slow twitch fibres
are involved in gaze holding (e.g. fixation, smooth pursuit). As
extraocular muscles execute multiple functions it is likely to
occur through unique groupings of motor units that allow inde-
pendent activation to produce a repertoire of actions.
Sensory Endings
Neuromuscular spindles and Golgi tendon organs are not
prominent in the extraocular muscles of humans. However,
other assumed sensory axons approach the central portion of
slow twitch muscle fibres, but then turn back towards the distal
muscle zone forming a spiral of nerve endings around their tips.
This unique nerve ending type, the palisade ending, is believed
to provide such proprioceptive information and contribute to
the monitoring of eye position.
The cell bodies of these palisade ending nerves and the cell
bodies of the motor neurons that innervate the slow twitch mus-
cle fibres are most likely found around the periphery of the cra-
nial motor nuclei. If these motor neurons function in the same
role as γ motor neurons, then the palisade ending neurons
would function in a similar manner to a muscle spindle and
eye movement.
There are other sensory afferents from extraocular muscles
(some may provide proprioceptive information, others nocicep-
tion or vasodilatation), which travel through the ophthalmic
nerve to the trigeminal ganglion. The trigeminal ganglion also
receives proprioceptive terminals from the neck muscles and
projects both to the ipsilateral cerebellum and to the contralat-
eral superior colliculus. The conjunction of ocular and cervical
proprioceptive information presumably assists in the coordina-
tion of simultaneous movements of the eyes and head.
PUPILLARY LIGHT REFLEX (FIG. 23.4)
Constriction of the pupils in response to light optimises visual
acuity and protects the retina from overexposure to bright light.
It involves four sets of neurons:
1. The afferent limb commences in melanopsin-containing
retinal ganglion cells (small subset of ganglion cells that
provide luminance information; intrinsically photosensitive
retinal ganglion cells, ipRGC) that generate an electrical
signal, independent of rod or cone synaptic input, and
travels within the optic nerve.
2. Fibres leaving the optic chiasm enter both optic tracts and
terminate in the pretectal nuclei, situated just rostral to the
superior colliculus on each side (Fig. 17.19).
3. Each pretectal nucleus is linked by interneurons to both
Edinger Westphal (parasympathetic) nuclei; the two
nuclei are connected by the posterior commissure (PC).
4. Preganglionic parasympathetic fibres enter the oculomotor
nerve, exit through the inferior division of the oculomotor
nerve, and synapse in the ciliary ganglion.

Downloaded for Pablo López (pilopez3@uc.cl) at Pontifical Catholic University of Chile from ClinicalKey.com by Elsevier on
November 06, 2022. For personal use only. No other uses without permission. Copyright ©2022. Elsevier Inc. All rights reserved.
246 CHAPTER 23 Ocular Motor Nerves

Midbrain ACCOMMODATION REFLEX

Pretectal nucleus
The Near Response
When the eyes view a near object, the ciliary muscles contract
2
reflexively, thereby relaxing the suspensory ligament of the lens
Edinger–Westphal (Fig. 23.5). Because the lens at rest is somewhat flattened or
nucleus
stretched by tension exerted on the lens capsule by the suspen-
Optic tract sory ligaments, the lens bulges passively when the ciliary muscle
1 3
contracts. The thicker lens has the greater refractive power
required to bring near objects into focus on the retina. This
Ciliary ganglion response of the lens is termed accommodation.
This accommodation reflex, as understood clinically,
4 involves two additional features. The sphincter pupillae con-
tracts to eliminate passage of light through the peripheral, thin-
Short ciliary nerves ner part of the lens. At the same time, the visual axes of the two
eyes converge, as a result of increased tone in the medial rectus
muscles. The convergence is clinically known as vergence.
The three features described are also known as the near
Sphincter pupillae response:
• The lens becomes more biconvex.
Retinal ganglion cell • The pupil constricts.
• The eyes converge.
Fig. 23.4 Pupillary light reflex. For numbers, see text.

Pathway for the Accommodation Reflex. To execute the

Cornea
Sphincter pupillae
Dilator pupillae Iris
Ciliary muscle Suspensory ligament
Fig. 23.5 Intrinsic muscles of the eye.
near response, a stereoscopic analysis of the object is carried out
at the level of the visual association cortex. The afferent limb of
the reflex passes from the retina to the occipital lobe via the lat-
eral geniculate body. The efferent limb passes from the occipital
lobe to the midbrain, where some fibres activate the Edinger
Westphal nucleus and others activate vergence (convergence)
cells in the reticular formation. The convergence cells activate
the nuclear groups serving the medial recti, with the effect of
fixating the object onto the fovea centralis of each eye. The
(con)vergence response is called the fixation reflex.
Pupillary constriction can be caused by light and by accom-
modation. A bright light stimulus usually produces greater
pupillary constriction than accommodation. When the light
reflex pathway is damaged, but the near reflex pathway remains
intact, a condition known as light-near dissociation results. The
near reflex results in a (greater) pupillary constriction compared
to light. The most common cause of light-near dissociation is
blindness from optic neuropathy. The condition may also result
from lesions in the dorsal midbrain that interrupt the afferent
optic nerve fibres where they travel to the Edinger Westphal
nucleus but not those of the near reflex that reach this nucleus
via a more ventral route. While other causes for light-near
Lens
dissociation exist, two need to be specifically mentioned: Argyll
Robertson pupil that classically results from the inflammatory
response of neurosyphilis disrupting the light pathway in the
midbrain and Adie tonic pupil from an idiopathic (unknown)
injury to the parasympathetic ciliary ganglion.

5. Postganglionic fibres run in the short ciliary nerves and
enter the iris to supply the sphincter (constrictor) pupillae
(Fig. 23.5). The normal response is consensual; that is,
both pupils constrict equally when the light is applied to
one eye only.
The Far Response
Just as the state of the pupil depends upon the balance of sympa-
thetic and parasympathetic activity, so does the state of the lens.
At rest both are in midposition. The resting focal length of the
lens averages 1 metre (with considerable variation between

Downloaded for Pablo López (pilopez3@uc.cl) at Pontifical Catholic University of Chile from ClinicalKey.com by Elsevier on
November 06, 2022. For personal use only. No other uses without permission. Copyright ©2022. Elsevier Inc. All rights reserved.

individuals). This is because the ciliary muscle is tonically
active. To bring a distant object into focus, the ciliary muscle
must be inhibited, so that the suspensory ligament becomes taut
and the lens flat. The sphincter of the pupil is inhibited as well.
The sympathetic system innervates all the intrinsic muscles.
It has a dual mode of action. It causes contraction of the dilator
pupillae via α receptors on the muscle fibres, and it causes
relaxation of the ciliary muscle and pupillary sphincter via β
receptors. This dual effect constitutes the far response, and it is
used to focus the eyes upon objects at a distance. (Note: The
unqualified use of α and β receptors signifies α1 and β2,
respectively.)
In stressed individuals, heightened sympathetic activity may
interfere with the normal process of accommodation. For exam-
ple, nervous students taking an important written test may have
difficulty in bringing the questions into proper focus.
NOTES ON THE SYMPATHETIC PATHWAY TO
THE EYE
The great length of the sympathetic pathway to the eye is indi-
cated in Fig. 23.6.
1. Central fibres descending from the hypothalamus cross to
the other side in the midbrain. In the pons and medulla,
they are joined by ipsilateral fibres descending from the
reticular formation.
Internal carotid artery
Superior tarsal Hypothalamus
muscle of Muller
(within the aponeurosis
of levator palpebrae
superioris)
3 movements under the control of the cerebral cortex,
Dilator pupillae
SCG
1
2
Spinal cord
T1 ventral nerve root
Fig. 23.6 Sympathetic innervation of the eye; three neuron pathways
from the hypothalamus to the eye. Arrows indicate directions of
impulse conduction. SCG, Superior cervical ganglion. For numbers, see
text.
Downloaded for Pablo López (pilopez3@uc.cl) at Pontifical Catholic University of Chile from ClinicalKey.com by Elsevier on
November 06, 2022. For personal use only. No other uses without permission. Copyright ©2022. Elsevier Inc. All rights reserved.
CHAPTER 23 Ocular Motor Nerves 247
2. Preganglionic fibres emerge in the first thoracic ventral
nerve root and run up in the sympathetic chain to the
superior cervical ganglion.
3. Postganglionic fibres from the superior cervical ganglion
run along the external and internal carotid arteries and
their branches.
Interruption of this ‘three-neuron’ oculosympathetic path-
way anywhere along its course can result in Horner syndrome
(small pupil (miosis), ipsilateral ptosis, and variable anhidrosis
depending on the site of the lesion; Chapter 13). The external
carotid sympathetic fibres accompany all the branches of the
external carotid artery. Those accompanying the facial artery
supply the arterioles of the cheek and lips and are particularly
responsive to emotional states. Those accompanying the maxil-
lary artery supply the cavernous tissue covering the nasal con-
chae (turbinate bones).
Two sets of sympathetic fibres accompany the internal
carotid artery. One set leaves it to join the ophthalmic division
of the CN V in the cavernous sinus, then leaves this in the long
and short ciliary nerves to supply the vessels and smooth mus-
cles of the eyeball (ptosis results from paralysis of the smooth
muscle fibres within the aponeurosis of the levator palpebrae
superioris, the superior tarsal muscle of Muller). The second set
forms a plexus around the internal carotid artery and its
branches, including the ophthalmic artery. The ophthalmic
artery gives off supratrochlear and supraorbital branches, which
carry sympathetic fibres to the skin of the forehead and scalp.
Interruption of the postganglionic (sympathetic internal
carotid plexus) fibres near the jugular foramen (see jugular fora-
men syndrome, Chapter 18), or in the cavernous sinus, produces
anhidrosis (loss of sweating) on the forehead and scalp.
CONTROL OF EYE MOVEMENTS
The eyes normally move as a pair. This conjugate movement is
of two fundamentally different kinds, as follows:
1. Gaze shifting. Cortical and subcortical areas are responsible
for these volitional eye movements.
a. Saccadic are conjugate, high velocity, ballistic eye
particularly the frontal and parietal eye fields, that
redirect fixation to a new object of interest and onto the
fovea of the eye. During this rapid eye movement, visual
acuity is diminished, reestablishing itself once the target
is again on the fovea, but this change in acuity goes
unnoticed as this discontinuity is ‘filled in’ by the visual
system.
b. Vergence are dysconjugate eye movements that shift the
gaze from far to near targets (e.g. fixation reflex).
2. Gaze holding. The visual system (retina to visual cortex)
provides feedback with respect to the position of the target
of gaze and the eye position that keeps the target on the
retina (fovea) when the target or we move. (While the eyes
may appear stationary, there are involuntary, fast, but
small fixational eye movements that continue to occur,
shifting the projection of an object over different retinal
receptors, and facilitating feature extraction. If the retina
248 CHAPTER 23 Ocular Motor Nerves
were truly immobile, the visual system would function
poorly as it is relatively insensitive to unchanging input.)
a. Tracking, or smooth pursuit, occurs as the eyes follow
an object of interest that is moving slowly across the
visual field; eye velocity matches that of the visual target
and maintains visual acuity by keeping the image on
the fovea. (Without an object to track, it is not possible
for an individual to volitionally move his or her eyes at
such a slow speed. Attempts to do so result in small
saccadic eye movements.)
b. Vestibuloocular reflex occurs when the gaze is held on
an object of interest during movements of the head and
is dependent upon displacement of endolymph in the
kinetic labyrinth (Chapter 19).
Gaze Shifting
Four separate gaze centres in the brainstem pick out motor neu-
rons appropriate to the direction of movement—leftwards,
rightwards, upwards, or downwards—and are involved in both
shifting and gaze-holding eye movements. The centres are small
nodes in the reticular formation. They contain burst cells, which
discharge at 1000 Hz (impulses/s) and entrain the appropriate
motor neurons momentarily at this rate because it is necessary
to overcome the elastic properties of the orbit to initiate eye
movements.
The paired centres (left and right) for horizontal eye move-
ments are in the paramedian pontine reticular formation
(PPRF; Fig. 17.15). When each is activated, it will result in a
conjugate (both eyes) movement to its own side (Fig. 23.7); for
example, activation of the left PPRF moves both eyes so that
they gaze to the left. The midbrain contains a bilateral centre for
vertical eye movements located at the rostral end of the medial
longitudinal fasciculus (MLF), at the level of the pretectal
nucleus, called the rostral interstitial nucleus of the MLF
(riMLF); perhaps its neurons for upgaze are more dorsal, for
downgaze more ventral (Fig. 17.19). (Other nuclei that are often
mentioned for vertical eye movements include the interstitial
nucleus of Cajal (INC), which is at the same level but a little ven-
tral and plays a role in integrating information from the medulla
and pons. The nucleus of the posterior commissure (PCom) con-
tributes to upward gaze generation and coordination with eyelid
movements.)
Automatic scanning movements are activated through the
superior colliculus on receipt of visual information from the
retina through the optic tract. Examples of automatic scanning
include the quick sideward glance towards an object attracting
attention in the peripheral visual field. The tectoreticular pro-
jections concerned cross the midline before engaging the gaze
centres. Saccadic accuracy is controlled by the midregion
(vermis) of the cerebellum, which receives afferents from the
superior colliculi and projects to the vestibular nucleus. The
posterior parietal cortex is likely involved in shifting gaze to
such novel targets, and the parietal eye field (Brodmann area
7a) is involved when exploring visual scenes via visually
guided saccades; both areas have significant interaction with
the frontal eye fields.
Downloaded for Pablo López (pilopez3@uc.cl) at Pontifical Catholic University of Chile from ClinicalKey.com by Elsevier on
November 06, 2022. For personal use only. No other uses without permission. Copyright ©2022. Elsevier Inc. All rights reserved.
Frontal eye field
To R medial rectus
1
To L lateral rectus 3
Oculomotor nucleus
Crossover
Paramedian
pontine
reticular Abducens
formation nucleus
2
Fig. 23.7 Pathways involved in a voluntary ocular saccade to the left.
(1) A projection from the right frontal eye field activates the left
paramedian pontine reticular formation (PPRF). (2) Some PPRF
neurons activate adjacent abducens neurons. (3) Other PPRF neurons
send heavily myelinated (fast) internuclear fibres along the medial
longitudinal bundle to activate oculomotor neurons serving the right
medial rectus. Simultaneous contraction of the respective medial
rectus muscles yields a saccade to the left.
Voluntary saccadic eye movements are better understood for
horizontal eye movements and multiple areas exist in the frontal
cortex (frontal eye field: voluntary saccades, memory-guided
saccades, and vergence movements; supplementary eye field:
planning and learning saccadic eye movements; and dorsolat-
eral prefrontal cortex: planned saccades to remembered targets),
which have reciprocal interactions with parietal cortical areas
to produce such voluntary eye movements (Chapter 28).
Projections from the frontal eye fields descend in the anterior
limb of the internal capsule, and most of these fibres cross over
before terminating in the contralateral brainstem gaze centres.
Other projections from the frontal cortex end in basal ganglia
(caudate, substantia nigra) and help to maintain a ‘balance’
between reflex and volitional saccades to prevent unwanted sac-
cades and act through a group of neurons distributed through
the midbrain and pons (omnipause neurons). The ipsilateral
superior colliculus is also activated at the same time, to reinforce
the excitation of the appropriate gaze centre.
There is hemispheric control of horizontal saccades, but the
left hemisphere is responsible for saccadic eye movements to
the right side and vice versa. Some patients who experience
an acute frontal lobe lesion (usually an ischemic stroke) may
 CHAPTER 23 Ocular Motor Nerves 249

temporally exhibit an inability to volitionally look to the side
opposite the lesion (gaze paralysis or acquired oculomotor
apraxia) while their vestibuloocular reflex remains intact.
This gaze paralysis usually vanishes within a week, even if the
hemiplegia remains profound. Unilateral parietal lobe lesions,
especially of the right side, may cause delayed or hypometric
(short of the planned target) saccades to the side contralateral
(opposite) to the lesion (Chapter 32).
Gaze Holding
The neural mechanisms for tracking are complex because of the
following basic requirements: (1) intact visual pathways to mon-
itor the position of the object throughout the movement; (2)
neurons to signal the rate of movement of the object (velocity
detectors); (3) neurons to coordinate movements of the eyes and
head (neural integrator); and (4) a system to monitor smooth
execution of the tracking movement. An example of this system
for horizontal smooth pursuit would include the following:
• Object movement detection begins in the retina and through
the optic nerve projects to the lateral geniculate nucleus and
from there to the primary visual cortex. With further cortical
input from the frontal, parietal, and temporal cortex, it
converges on the temporoparietooccipital junction (TPO) that
projects ipsilaterally to the pons.
• The ipsilateral dorsolateral pontine nucleus (DLPN) receives
that input and projects to the contralateral cerebellar flocculus,
which projects to the vestibular nucleus.
• The vestibular nuclei project back (same side of origin of the
cortical response) to the pons and the PPRF so the result is a
conjugate horizontal movement of the eyes. It is important
to remember that smooth pursuit movements are ipsilateral;
the right hemisphere is responsible for rightward smooth
pursuit movements and vice versa.
Vertical eye movements are generated bihemispherically
with projections to the riMLF, which then projects to the
respective motor neurons of cranial nerves III and IV. The INC
integrates additional information from vestibular, pons, and
medulla neurons, and the PCom further contributes with
respect to upgaze and eyelid movement.
The vestibuloocular reflex is signalled by the dynamic laby-
rinth and is integrated with spatial and velocity information in
the nucleus prepositus hypoglossi, a node of the reticular forma-
tion that helps to position and hold the eyes steady in an eccen-
tric position of gaze. The nucleus prepositus hypoglossi projects
to the PPRF or, for vertical eye movements, the riMLF, which
integrates conjugate eye movements. Cortical input (frontal,
parietal, and insular) further modulates these responses. As a
reflex, it also needs to be suppressed when a target and the head
(and eyes) are moving synchronously in the same direction;
otherwise the reflex would move the eyes in a direction opposite
to the head movement!
The dynamic labyrinth and cerebellum cooperate to keep the
eyes on target during movement of the head, as described in
Chapter 19.

CLINICAL PANEL 23.1 Ocular Palsies

One or more of the three ocular motor nerves may be paralysed by disease within the brainstem (e.g. multiple sclerosis, vascular occlusion), in the subarachnoid
space (e.g. meningitis, aneurysm in the circle of Willis, distortion by an expanding intracranial lesion), in the cavernous sinus (e.g. thrombosis of the sinus, aneu-
rysm of the internal carotid artery there), or by microvascular ischemia to the nerve in the setting of atherosclerotic risk factors. There is a significant prevalence
of structural lesions, and it may be prudent to consider contrast-enhanced MRI for all patients presenting with acute, isolated ocular motor mononeuropathies
irrespective of age.

Oculomotor Nerve
Complete III Nerve Palsy
Characteristic signs of complete third nerve paralysis (left eye) are shown in Fig. 23.8A. They are:
1. Complete ptosis of the upper eyelid (held open by the examiner in this figure so the position of the left eye can be seen).
2. A fully dilated, non-reactive pupil (unopposed dilator pupillae).
3. A fully abducted eye (unopposed lateral rectus), which is also depressed (unopposed superior oblique).

A LEFT B LEFT

Fig. 23.8 (A) Complete left III nerve paralysis. The closed eyelid has been raised by the examiner’s finger. (B) Complete left VI nerve paralysis.

Downloaded for Pablo López (pilopez3@uc.cl) at Pontifical Catholic University of Chile from ClinicalKey.com by Elsevier on
November 06, 2022. For personal use only. No other uses without permission. Copyright ©2022. Elsevier Inc. All rights reserved.
250 CHAPTER 23 Ocular Motor Nerves

Partial III nerve palsy

The pupils are always monitored when cases of head injury come to medical attention. Rapidly increasing intracranial pressure, resulting from an acute extradur-
al or subdural hematoma (Chapter 5), often compresses the third nerve against the crest of the petrous temporal bone. The parasympathetic fibres are superfi-
cially placed and are the first to suffer, and the pupil dilates progressively on the affected side. Pupillary dilatation is an urgent indication for surgical
decompression of the brain.
Trochlear Nerve
The IV nerve is rarely paralysed alone. The cardinal symptom is diplopia (double vision) on looking down, such as when going downstairs. This happens because
the superior oblique normally assists the inferior rectus in pulling the eye downwards, especially when the eye is in an adducted position.
Abducens Nerve
The effect of a complete VI nerve paralysis is shown in Fig. 23.8B (right eye is affected and in this diagram the individual is attempting to look towards their
right). The eye is fully adducted by the unopposed pull of the medial rectus. The abducens nerve has the longest course in the subarachnoid space of any cranial
nerve. It also bends sharply over the crest of the petrous temporal bone. A space-occupying lesion affecting either cerebral hemisphere may cause compression
and paralysis of one abducens nerve.
‘Spontaneous’ paralysis of the VI nerve may be caused by an arterial aneurysm at the base of the brain, atherosclerosis of the internal carotid artery in the
cavernous sinus, or microvascular ischemia to the nerve in the setting of atherosclerotic risk factors.

Internuclear Ophthalmoplegia (INO)

Interruption of the linkage between the abducens nucleus and the contralateral oculomotor nucleus, via the MLF, gives rise to a disorder of conjugate gaze
referred to as internuclear ophthalmoplegia.
As an example, a lesion of the right MLF is shown in Fig. 23.9 and would leave the gaze to the right unaffected, whereas attempting to gaze to the left,
the right eye adducts minimally and the contralateral left eye abducts, but nystagmus (towards the left) is seen. On looking to the left the left abducens nucleus is

Right Left
Midposition

Saccade to right

Attempted saccade to left

Vergence

Fig. 23.9 Right internuclear ophthalmoplegia.

Downloaded for Pablo López (pilopez3@uc.cl) at Pontifical Catholic University of Chile from ClinicalKey.com by Elsevier on
November 06, 2022. For personal use only. No other uses without permission. Copyright ©2022. Elsevier Inc. All rights reserved.
 CHAPTER 23 Ocular Motor Nerves 251

activated (causing contraction of the left lateral rectus muscle and abduction of the left eye) and the PPRF also projects into the right MLF that would normally
activate the right oculomotor nucleus and result in contraction of the right medial rectus (and adduction of the right eye), but this pathway is blocked so, the
right medial rectus does not contract. The individual experiences diplopia when looking to the left (two images side-by-side). Integrity of the III nucleus and the
right medial rectus is shown by its normal behaviour during the vergence component of the near response (this involves a different and unaffected pathway).
Below the age of 40, the chief cause of internuclear ophthalmoplegia is a demyelinating plaque from multiple sclerosis disrupting the MLF. Above the age
of 60, the chief cause is a stroke from an occlusion of a pontine branch of the basilar artery causing an ischemic injury to the MLF.

Ocular Sympathetic Supply

Any one of the three sequential sets of neurons depicted in Fig. 23.6 may be interrupted by local pathology.
1. The central set may be interrupted by a vascular lesion of the pons or medulla oblongata or by demyelinating disease (multiple sclerosis). The usual picture is
one of Horner syndrome (ptosis and miosis, as described in Chapter 13) with cranial nerve involvement on one side, together with motor weakness and/or
sensory loss in the limbs on the contralateral side. Horner syndrome is associated with anhidrosis—absence of sweating—in the face and scalp on the
same side, together with congestion of the nose (engorged turbinates).
2. The preganglionic set is most often interrupted by infection/tumour of the lung, by trauma, or cervical spine disease. Horner syndrome is again associated
with anhidrosis of the face and scalp (and nasal congestion) on the same side.
3. The postganglionic set accompanying the external carotid artery can be injured by disease of the carotid artery (dissection of the carotid artery) or by a
tumour of the base of the skull. The set accompanying the internal carotid artery may be interrupted as part of a jugular foramen syndrome (Chapter 18) or
by pathology in the cavernous sinus. Horner syndrome is now accompanied by anhidrosis of the forehead and anterior scalp (territory of the supraorbital and
supratrochlear arteries).

Core Information
Oculomotor Nerve
Somatic efferent fibres of cranial nerve (CN) III arise from the main nucleus
at the level of the superior colliculus. The nerve passes in the wall of the
cavernous sinus and its two divisions exit the cranium through the superior
orbital fissure. The upper division supplies the superior rectus and levator
palpebrae superioris muscles; the lower division supplies the inferior oblique
as well as the inferior and medial recti muscles.
Parasympathetic fibres emerge from the Edinger Westphal nucleus,
travel in the main nerve, and synapse in the ciliary ganglion to supply the
sphincter pupillae and ciliary muscles. Paralysis of CN III causes dilation of
the pupil, ptosis, and divergent squint.
Trochlear Nerve
The nucleus of the CN IV is at the level of the inferior colliculus. The nerve
crosses the midline before emerging below the inferior colliculus. It passes in
the lateral wall of the cavernous sinus to supply the superior oblique muscle.
Paralysis is characterised by diplopia on looking down.
Abducens Nerve
The nucleus is at the level of the facial colliculus in the pons. The CN VI runs
in the subarachnoid space from lower border of the pons to the apex of the
petrous part of the temporal bone and passes through the cavernous sinus and
the superior orbital fissure to supply the lateral rectus muscle. Paralysis is char-
acterised by convergent squint with inability to abduct the affected eye.
(A simple memory device useful to remember which nerve innervates
which eye muscle is: LR6(SO4)3. This fictitious chemical formula reminds us
that the lateral rectus (LR) is innervated by the VI nerve, the superior oblique
(SO) is innervated by the IV nerve, and the rest of the eye muscles are inner-
vated by the III nerve.)
Sympathetic
Muscles stimulated (via α1 receptors) are the dilator pupillae, a smooth
muscle in the anterior deeper part of the levator palpebrae superioris
(known as the tarsal muscle of Muller). Paralysis is characterised
by ptosis with a constricted pupil (Horner syndrome). Muscles inhibited
(via β2 receptors) are the sphincter pupillae and the ciliary muscles.
Parasympathetic
Muscles stimulated are the sphincter (constrictor) pupillae and the ciliary
muscles.
Reflex Pathways
For the pupillary light reflex: from the retina to the pretectal nucleus, to both
Edinger Westphal nuclei, to the ciliary ganglion, and finally, the sphincter
pupillae muscle.
For the accommodation reflex: from the retina to the lateral geniculate
body, to the occipital cortex, to the Edinger Westphal nucleus, to the ciliary
ganglion, and then to the ciliary muscles.
Oculomotor controls
Gaze shifting (saccadic) eye movements are locally activated by six gaze
centres. Most important clinically is the paramedian pontine reticular
formation (PPRF), which operates to pull the ipsilateral lateral rectus and
contralateral medial rectus conjugately to its own side. Automatic scanning
is controlled by the superior colliculi and voluntary scanning by the frontal
eye fields. Gaze holding is complex and involves the occipital cortex,
dynamic labyrinth, cerebellum, superior colliculus, and reticular formation.

SUGGESTED READINGS Binda P, Morrone MC. Vision during saccadic eye movements.
Annu Rev Vis Sci. 2018;4:193 213.
Bae YJ, Kim JH, Choi BS, et al. Brainstem pathways for horizontal Detwiler PB. Phototransduction in retinal ganglion cells. Yale J Biol
eye movement: pathologic correlation with MR imaging. Med. 2018;91:49 52.
RadioGraphics. 2013;33:47 59. Kim SH, Zee DS, du Lac S, et al. Nucleus prepositus hypoglossi
Baird-Gunning JJD, Lueck CJ. Central control of eye movements. lesions produce a unique ocular motor syndrome. Neurology.
Curr Opin Neurol. 2018;31:90 95. 2016;87:2026 2033.

Downloaded for Pablo López (pilopez3@uc.cl) at Pontifical Catholic University of Chile from ClinicalKey.com by Elsevier on
November 06, 2022. For personal use only. No other uses without permission. Copyright ©2022. Elsevier Inc. All rights reserved.
252 CHAPTER 23 Ocular Motor Nerves

Larsen RS, Waters J. Neuromodulatory correlates of pupil dilation.
Front Neural Circuit. 2018;12:21.
Martin TJ. Horner Syndrome: a clinical review. ACS Chem Neurosci.
2018;9:177 186.
Paduca A, Bruenech JR. Neuroanatomical structures in human
extraocular muscles and their potential implication in the devel-
opment of oculomotor disorders. J Pediatr Ophthalmol
Strabismus. 2018;55:14 22.
Pretegiani E, Optican LM. Eye movements in Parkinson’s disease
and inherited Parkinsonian syndromes. Front Neurol. 2017;8:592.
Rucci M, Victor JD. The unsteady eye: an information-processing
stage, not a bug. Trends Neurosci. 2015;38:195 206.
Spering M, Carrasco M. Acting without seeing: eye movements reveal
visual processing without awareness. Trends Neurosci. 2015;
38:247 258.
Takahashi M, Shinoda Y. Brain stem neural circuits of horizontal
and vertical saccade systems and their frame of reference.
Neuroscience. 2018;392:281 328.
Tamhankar MA, Volpe NJ. Management of acute cranial nerve 3, 4
and 6 palsies: role of neuroimaging. Curr Opin Ophthalmol.
2015;26:464 468.
Tarnutzer AA, Straumann D. Nystagmus. Curr Opin Neurol. 2018;
31:74 80.

Downloaded for Pablo López (pilopez3@uc.cl) at Pontifical Catholic University of Chile from ClinicalKey.com by Elsevier on
November 06, 2022. For personal use only. No other uses without permission. Copyright ©2022. Elsevier Inc. All rights reserved.