Vyšetření očních pohybů je důležitou součástí neurologického vyšetření, které poskytuje významné poznatky o funkci centrálního i periferního nervového systému, okohybných svalech a orbitě. Pečlivé, systematické a přesné vyšetření musí být provedeno během několika minut. Neurolog by měl být schopen interpretovat jeho nález, provést syndromologickou a topickou diagnostickou rozvahu a naplánovat další cílená vyšetření. Cílem tohoto přehledu je připomenout anatomicko-fyziologické podklady očních pohybů, ukázat postup jejich vyšetření a prezentovat hlavní patologické nálezy.
Klíčová slova: vyšetření očních pohybů – nervus oculomotorius – nervus trochlearis – n. abducens – vestibulo-optokinetický systém
C. Bonnet 1; J. Hanuska 2; A. Dombrowski 3; E. Ruzicka 1
Department of Neurology and Centre for Clinical Neurosciences, Charles University, Prague, First Faculty of Medicine and General University Hospital, Prague, Czech Republic
1; Student, Charles University, Prague, First Faculty of Medicine and General University Hospital, Prague, Czech Republic
2; Freelance Artist, Bad Bramstedt, Germany
Cesk Slov Neurol N 2011; 74/107(5): 518-526
Examination of eye movements is an essential part of any comprehensive neurological examination, providing important information about the function of the central and peripheral nervous systems, the eye muscles and the orbit. A careful, systematic and precise examination may be carried out within only a few minutes. The neurologist should be able to interpret signs, to adopt a topological or syndrome-based approach and to direct diagnostic procedures. The aim of this review is to provide a basic anatomo-physiological account of eye movements, followed by an account of the examination of eye movements and a summary of the principal abnormalities that may be disclosed.
Key words: eye movement examination - oculomotor muscles - oculomotor nerve - trochlear nearve - abducens nerve - vestibular-optokinetic system
movements can be measured with extreme precision and provide a wide
range of important information. The results of such eye examinations
are usually rich in terms of derivable parameters, are
well-documented in normal adults and in patients suffering from brain
lesion, and may be used as one means of testing the functional
integrity of the cortico-cortical and cortico-subcortical circuits.
Examination of eye movements is an essential part of the neurological
examination and places only few cognitive demands on subjects. The
neurologist must be able to interpret the results that drive the
diagnostic approach. The aim of this review is to provide practical
information about the clinical examination of eye movements and the
interpretation of potential findings.
movements are triggered and controlled by a number of cortical
and subcortical areas, apart from the vestibulo-ocular reflex and
quick phases of all nystagmus, which are generated in the brain stem.
Some of the cortical areas
involved in the management of eye movement are the frontal eye field,
the supplementary eye field, the pre-supplementary motor area, the
parietal eye field, the dorsolateral prefrontal cortex and the
posterior parietal cortex. These areas project directly to the
superior colliculus and indirectly through basal ganglia and the
substantia nigra pars reticulata (SNpr), to the pontine nuclei
(nucleus reticularis tegmenti pontis) and the cerebellum .
The vertical and horizontal gaze
centres are situated in the brainstem. Vertical and torsional
conjugate eye movements are generated in the midbrain, in the rostral
interstitial nucleus of the medial longitudinal fasciculus (riMLF)
. The paramedian pontine reticular formation (PPRF), known in the
past as the para-abducens nuclear group, is the organizing centre for
horizontal gaze . Vertical and horizontal gaze centres project to
neurons of the oculomotor, trochlear and abducens nuclei, where the
corresponding cranial nerves arise (Fig. 1).
The oculomotor nerve begins in
the midbrain at the level of the superior colliculus with a cluster
of somatic and visceral nerve nuclei. Somatic motor nuclei provide
fascicles to the extrinsic ocular muscles: the superior and inferior
recti, the medial rectus, the inferior oblique and the levator
palpebrae superioris. The visceral motor nucleus, also known as the
Edinger-Westphal nucleus or the accessory oculomotor nucleus,
provides parasympathetic fibres to intrinsic ocular muscles: the
sphincter pupillae that regulates pupillary constriction in response
to light, and the ciliary muscle that enables the lens to accommodate
for near vision. The third intrinsic eye muscle, the dilatator
pupillae, receives sympathetic innervation via the carotid plexus.
Each subunit of the oculomotor nerve is paired, apart from the caudal
subunit which supplies the two levator palpebrae superioris muscles.
This interesting configuration explains why it is comparatively
difficult to open only one eye while the other eye remains closed
. The oculomotor nucleus receives inputs from the contralateral
abducens nucleus via the medial longitudinal fasciculus (MLF) for the
innervation of the medial rectus muscle, allowing conjugate
horizontal eye movements. The fascicles of cranial nerve (CN) III
exit ventrally through the brainstem into the interpeduncular cistern
[4,5], pass the basilar artery, superior cerebellar artery, and
travel in close proximity to the posterior communicating artery.
CN III then enters the cavernous sinus, where it is in close
proximity to CN IV, CN V, CN VI, and the carotid artery. In the
cavernous sinus, the nerve divides into superior and inferior
elements and enters the orbital apex through the superior orbital
fissure together with the ophthalmic artery, CN II, CN VI, and
the nasociliary branch of CN V1 [4,5].
The nucleus of the trochlear
nerve (CN IV) is
located in the tegmentum of the midbrain, at the level of the
inferior colliculus . The trochlear nerves decussate in the roof
of the aqueduct before exiting from the dorsal aspect of midbrain,
and run between the posterior cerebral and superior cerebellar
arteries before entering the cavernous sinus. CN IV enters the orbit
through the superior orbital fissure and crosses medially over the
levator palpebrae superioris and superior rectus muscles before
reaching the superior oblique muscle.
The nucleus of the abducens
nerve (CN VI) is
located in the pons, ventral to the floor of the fourth ventricle and
lateral to the MLF. The nerve contains two groups of neurons: the
internuclear neurons and the motor neurons. The internuclear neurons
cross the midline, ascend in the MLF to the oculomotor nerve nuclei
and ensure innervation of the contralateral medial rectus muscle. The
motor neurons are made up of the principal fascicle of the abducens
nerve, which innervates the ipsilateral lateral rectus muscle . CN
VI travels between the pons and the clivus, then pierces the dura
mater before continuing between the dura and the skull. At the top of
the petrous temporal bone, the abducens nerve makes a sharp turn
forwards to enter the cavernous sinus. In the cavernous sinus it runs
alongside the internal carotid artery and enters the orbit through
the superior orbital fissure.
The oculomotor, trochlear and
abducens nerves control the six small extrinsic ocular muscles
responsible for precise eye movement: four rectus muscles and two
obliques. The medial rectus muscle adducts the eye (inwards) and the
lateral rectus abducts it (outwards). The superior rectus muscle
elevates-adducts and slightly rotates the eye inwards, whereas the
inferior rectus muscle depresses-adducts and slightly rotates the eye
outwards. The oblique muscles have a predominantly rotatory
pulling function. The superior oblique is the most important inward
rotator, as well as depressing and slightly abducting the eye. The
inferior oblique muscle rotates the eye outward, and also elevates
and abducts (Fig. 2).
imaging of an object requires steady fixation of its image on the
central, foveal (macular) region of the retina, which contains the
highest concentration of cone photoreceptors. Two main groups of eye
movements facilitate this stabilization of an image on the retina and
allow the line of sight to change when a new object of interest
appears and needs to be directed to the fovea [2,7]. The eye
movements that stabilize the image on the retina are the optokinetic
reflex, the vestibulo-ocular reflex, and smooth pursuit:
The optokinetic reflex (OKR) is induced when an entire visual scene drifts across the retina, eliciting eye rotation in the same direction at a velocity that minimizes the motion of the image on the retina. When the eyes rotate in the direction of a stimulus, their motion is periodically interrupted by rapid rotations in the opposite direction (quick phases or saccades), which reset the position of the eye for a new period of steady rotation .
The vestibulo-ocular reflex (VOR) is a response analogous to head motion, with input coming from the vestibular system rather than the retina [7,8]. It responds to rotational and translational acceleration detected by two different structures, firstly the semicircular canals, which respond to angular (rotational) acceleration, with movement in the plane of the stimulated canal, and secondly the otolith organs, which respond to linear (translational) acceleration and sustained lateral tilt of the head. The VOR implies an intact trineuronal arc composed of the vestibular ganglion, the vestibular nuclei and the ocular motor nuclei .
Smooth pursuit stabilizes an image when slow movement of an object is directed to the fovea . Smooth pursuit needs to suppress the VOR because in moving the head, the VOR will normally move the eyes in the opposite direction to that of movement, disturbing vision .
The eye movements that change the
line of sight are known as the saccades and vergence:
Saccades are rapid eye movements that move the line of sight through successive points of fixation [2,13]. They are among the most well-understood eye movements, possessing dynamic properties that are easily measured, and have become a popular means of studying motor control, cognition and several neurological diseases . Saccades are the quick phases of nystagmus. They may be reflexive, triggered externally by a visual target appearing suddenly, or intentional, triggered internally by a visual target already present for a period of time, perceived a moment before (memory-guided saccade), or expected at a specific location (predictive saccade). Antisaccades, made in the direction opposite to a suddenly-appearing visual target, are also voluntary .
Vergence is the movement of the two eyes in different directions to enable binocular fixation of a single object. There are two main types of vergence movements, termed fusional and accommodative. The alignment of the eyes is maintained by fusional vergence and the reflex is driven by retinal image disparity. In the normal state, retinal image disparity produces diplopia. Motor fusion then triggers a vergence response to align the images of the object of regard on the two foveae. Accommodative vergence is stimulated by loss of image focus on the retina and occurs in association with accommodation of the lens and pupillary constriction [2,15–17].
accurate patient history is essential to the examination of eye
movements, including how long the symptoms have been present, whether
pathological findings are evident in old photographs, and records of
also supplementary data: video on https://el.lf1.cuni.cz/ocularmovementsexam/)
The examiner should stand
slightly to the side of the patient, since patients with cognitive
impairment are accustomed to looking at the face or eyes of the
examiner, and do not respond to verbal commands. The patient should
be asked to sit or stand, hold the head erect and to look straight
ahead. The examination starts with fixation, followed by pursuit,
vergence, saccades and VOR.
of the eyes in primary position. The patient should view an object
that requires visual discrimination on the other side of the room.
Ocular alignment is determined by carefully observing the reflection
of light on the cornea, which must be at the same height. This can be
especially helpful in patients with ptosis or facial asymmetry.
Careful inspection of the symmetry of both eyelids, pupils and head
Each eye is then examined
individually with the cover test, which may disclose heterotropia,
a misalignment of the visual axes when both eyes are viewing
a single target. A target that requires visual
discrimination (e.g. an “E”) is placed at a distance of 6 m
and another at 35
cm. Firstly, with the eyes in the central position, the right eye is
covered and corrective movements of the uncovered left eye are
monitored. If no movement is detected, the cover is removed and the
left eye covered. This test is repeated with the eyes brought to the
nine cardinal positions of gaze and the whole process undertaken
again with the near target .
examiner’s finger or a small target such as a pen,
even a mirror, may be used for this part of the examination. The
target is held approximately 60 cm in front of the patient’s face
and the patient asked to avoid moving the head. The target is moved
horizontally then vertically, at a uniformly low speed
(10–30/s), and the patient asked to follow it. Both eyes together
are observed. The patient should be able to follow the target
smoothly at an appropriate velocity. After this, each eye is observed
separately to examine the eye muscles. Each eye is should be able to
trace a capital “H” (Fig. 3).
Examination of the pursuit system
includes assessment of VOR suppression, which is an essential
component of the smooth pursuit task during motion. The patient is
asked to follow a rotating object while the head is maintained
in a fixed direction (e.g. the patient stretches the hands
forward, holding them together, and maintains the gaze on them while
seated in a chair that is rotating). The eyes should remain
stable in the orbit, through visual fixation and suppression of VOR
patient is asked to maintain the gaze on an accommodative target that
requires focus, something that is slowly brought to the bridge of the
nose along the sagittal plane. The patient is also asked to shift the
point of fixation alternately between a far target and a near
target. Pupillary changes during convergence are noted.
is placed approximately 60 cm in front of the patient’s nose,
and the patient asked to look at it. The target is moved away from
centre and presented to one side, and the patient asked to change
line of sight and view the target again. Avoiding large movements,
this procedure is repeated centre-right-centre-left-centre, three or
four times. The vertical saccades are then examined by alternating
(Fig. 5). Saccades are usually fast, accurate and conjugate. Most
patients are able to initiate the saccadic eye movement (latency) as
quickly as they are asked to look at the target. Latency, velocity,
accuracy and conjugated movement of both eyes are noted.
Vestibulo-ocular reflex and optokinetic reflex
and vertical VOR are examined by means of the head-impulse test,
after Halmagyi & Curthoys (Fig. 6) . The patient’s head
is held still in two hands and the patient asked to fix the gaze on
the examiner’s nose; the head is then directed rapidly and
horizontally to the left and to the right. To examine vertical VOR,
the patient’s head is directed vertically up and down.
Rotation of the head in a healthy subject should lead to rapid
compensatory eye movements in the opposite direction, leaving the
patient still looking at the examiner’s nose.
Dynamic visual acuity is the
ability to resolve visual detail while the observer is moving. Motion
reduces visual acuity relative to static conditions. This test
provides a clinical functional measure of the vestibulo-ocular
reflex (VOR) during horizontal or vertical sinusoidal head rotations
at frequencies of at least 2 Hz and a rate greater than
120/s . To start with, static acuity is assessed by means of
the standard Snellen chart, asking the patient to read the smallest
legible line on the chart. Then the patient’s head is moved at
about 2 Hz, at an amplitude of only 5–10 degrees in the horizontal
and then the vertical, and the patient asked to read the smallest
line on the chart that can be discerned. To avoid interference from
the patient’s memory, a different but equally difficult
chart may be employed or the patient may be asked to read the line
backwards during the dynamic part of the test. When the VOR
system is impaired, visual acuity degrades during head movement .
A common method of testing
the optokinetic reflex is to sit the patient inside a large,
patterned optokinetic drum or to rotate the patient at a constant
velocity for more than a minute with the eyes open in an
illuminated room. Small-field motion induced by a drum or tape,
with stripes that rotate horizontally or vertically, does not test
the optokinetic system adequately, but primarily assesses the pursuit
is essential to record all information concerning signs and symptoms
revealed by examination of eye movement. Definitions must be kept
clear in order to avoid incorrect diagnosis. Definitions of the
principal abnormalities and their origins appear above.
tend to seek medical advice when an eye movement disorder causes
visual discomfort and/or leads to dizziness or instability.
is the sensation of seeing an object at two different locations in
space. The patient should be asked if it is horizontal, vertical or
torsional, and elicitation extended to the direction of gaze in which
the diplopia is more marked, and if it is worse for near or distant
viewing. Monocular diplopia is rare and may be caused by astigmatism,
refractive errors, cataract, corneal irregularity, lens dislocation
or eye trauma. Patients who complain of little or no visual
disturbance despite an obvious ocular misalignment have usually had
strabismus from an early age. Patients with acquired strabismus tend
to close one eye to avoid diplopia .
is an illusion of movement of the perceived world, often associated
with poor visual acuity, reported by many patients with neurological
disorders. This commonly occurs while the patient is walking, during
head movement, driving or even when the head is still. Oscillopsia
very often results from an impaired vestibulo-?-ocular
reflex due to bilateral, peripheral or central vestibular
dysfunction; from abnormal eye movements such as nystagmus; or from
paresis of the extraocular muscles .
perception of self-motion or object-motion, as well as an unpleasant
distortion of static gravitational orientation.
complaints may be revealed by the clinical examination, among them
eyelid abnormalities, ptosis, retractions, lid nystagmus, lid opening
apraxia or synkinesis.
misalignment of the visual axes causing the two images of an object
to fall on non-corresponding areas of the two retinas, usually giving
rise to diplopia.
misalignment of the eyes caused by damage to the prenuclear
vestibular input to the oculomotor nuclei. Skew deviation may arise
out of a lesion in the utricle, the MLF, the midbrain, the
cerebellum, the vestibular cortex or the thalamus. It may also be
a transient finding associated with raised intracranial pressure
associated with supratentorial tumours or pseudotumours.
deviation, ear to shoulder, appears in some patients with skew
deviation. This reaction is usually attributed to peripheral or
central lesions disrupting otolithic inputs [2,20].
rhythmic, involuntary oscillation of the eyes initiated by slow
phases. Although the direction of nystagmus is defined by the
direction of the fast corrective phase, it is the slow phase that
reflects the underlying disorder .
Description of nystagmus needs to
include the direction of beat, the degree, the effect of visual
fixation and other provocation manoeuvres. The direction of eye
motion should be described from the patient’s perspective. For
example, clockwise torsional rotations should correspond to
rotation of the top poles of the patient’s eyes to the
patient’s right. The planes in which the nystagmus occurs
(horizontal, vertical, torsional, mixed) should be noted for each
eye. Horizontal nystagmus is most often congenital or
peripheral-vestibular in origin, commonly associated with a torsional
component. Torsional nystagmus is usually associated with medulla
oblongata lesions, such as syringobulbia and Wallenberg´s syndrome.
Downbeat nystagmus commonly occurs with degeneration affecting the
vestibulocerebellum, lesions near the craniocervical junction,
vertebral ectasia and with drug intoxications, especially lithium.
Upbeat nystagmus is less well localized than downbeat nystagmus,
reported largely with paramedian lesions of the medulla oblongata,
but also with pontine and midbrain abnormalities .
Nystagmus may be also of
a pendular or jerk type: (1) pendular nystagmus: sinusoidal
oscillations of approximately equal amplitude and velocity; (2) jerk
nystagmus: slow initiating phase with a fast corrective phase
The oscillations of each eye
should be compared (synchrony or asynchrony). When the direction of
the oscillations differ in each eye, the condition is known as
The degree of nystagmus is
1st grade, nystagmus only in the direction of gaze;
2nd grade, nystagmus also present in primary position;
3rd grade, nystagmus also present in the opposite direction of gaze.
Further examination involves the
effect of removing fixation with Frenzel goggles. This is a sensitive
method for detecting spontaneous nystagmus, in fact nystagmus due to
peripheral vestibular imbalance may only be apparent under these
circumstances. Fixation can also be eliminated by examining one eye
with an ophthalmoscope (while the other eye is covered) and
simultaneously checking for movements of the optic papilla or retinal
vessels. Since the retina is behind the axis of rotation of the
eyeball, the direction of any observed vertical or horizontal
movement is opposite to that of the nystagmus detected with this
method, i.e. a downbeat nystagmus causes a rapid upward
movement of the optic papilla or retinal vessels . Other clinical
tests, depending on the clinical question, are positional testing,
hyperventilation, the Valsalva manoeuvre and head shaking. The
neuro-otologist usually induces nystagmus by caloric, galvanic or
vibratory stimuli .
of the eye that is only present in certain directions of gaze,
gaze-evoked nystagmus is often a side-effect of medication
(anticonvulsants, benzodiazepines) or toxins (alcohol). A horizontal
gaze-evoked nystagmus may indicate a structural lesion in the
brain stem or cerebellum. A dissociated horizontal gaze-evoked
nystagmus may be present in internuclear ophthalmoplegia ,
whereas vertical gaze-evoked nystagmus is observed in midbrain
lesions involving the interstitial nucleus of Cajal.
jerks are small saccades, from 0.5° to 5°, that cause the eyes to
oscillate around the primary position. They can increasingly occur in
progressive supranuclear palsy and certain cerebellar syndromes.
rapid bursts of oscillations without intersaccadic interval,
occurring in only one direction, usually horizontal.
of oscillations without intersaccadic interval, occurring in combined
horizontal, vertical, and torsional directions; ocular flutter and
opsoclonus occur in various settings, such as encephalitis,
paraneoplasia (neuroblastoma in children or other tumours in adults),
meningitis, intracranial tumours, hydrocephalus, thalamic
haemorrhage, multiple sclerosis, systemic disease, and drug
pursuit is a very brisk function that varies with subject age
and the ability to direct visual attention, and is influenced by
medication [23–28]. Even healthy persons exhibit a slightly
saccadic smooth pursuit during vertical downward gaze. For these
reasons, a saccadic smooth pursuit does not always allow either
an exact topographical or etiological classification . Pursuit
movements that do not match the target velocity necessitate
corrective saccades, making the pursuit saccadic. Impaired smooth
pursuit is observed in intoxication (anticonvulsants,
benzodiazepines, alcohol), cerebellar or extrapyramidal
neurodegenerative disorders, hereditary cerebellar diseases, cerebral
lesions, and even in extraocular muscle palsy [21,29–31].
Abnormalities of smooth pursuit may also be encountered in some
individuals with congenital forms of nystagmus . Failure of VOR
suppression, investigated as a part of the examination of smooth
pursuit, results in an incompletely cancelled VOR that appears as
a jerk nystagmus beating in the direction of rotation.
of CN III may be complete or partial. A complete CN III lesion
causes ptosis, a fixed, dilated pupil with paralysis of
accommodation, resting eye position (“down and out”), and the
inability to elevate, depress or adduct the eye. The opposite eyelid
may droop slightly, reflecting the bilateral innervation of the
lids by CN III. Incomplete CN III palsy is more common and may result
from lesion at various sites along the course of the nerve from the
nucleus to the muscle [2,32].
with CN IV palsy usually report vertical and torsional diplopia
aggravated by looking downwards and inwards, especially when reading
or climbing stairs . The head may be tilted away from
affected side to reduce blurred vision (the Bielschowsky sign).
Accordingly, double vision increases markedly when the head is
upright or tilted to the affected side (Bielschowsky test).
VI nerve palsy
nerve palsy is the most common of all ocular motor palsies. Patients
usually present binocular, uncrossed, horizontal diplopia at its
greatest when viewing distant objects and looking ipsilaterally.
Abduction is restricted or slowed, and there is an esotropia (the
eyes are “crossed” – while one eye looks straight ahead, the
other eye is turned in toward the nose). Patients often turn the head
to the affected side to minimize diplopia.
specific gaze abnormality, resulting from a lesion in the MLF,
is characterized by impaired horizontal eye movement with weak
adduction of one eye and abduction ataxic nystagmus of the
contralateral eye. The adduction deficit identifies the INO as being
either left or right, and is ipsilateral to the MLF lesion. Vertical
saccades and convergence are normal.
uncommon syndrome occurs if a lesion affects the paramedian
pontine reticular formation (PPRF) and the medial longitudinal
fasciculus on the same side. The eyes cannot move horizontally,
except the eye contralateral to the lesion side, which can abduct.
Convergence is unaffected.
most common vergence disorder is convergence insufficiency associated
with diplopia, eye strain, fatigue, loss of concentration while
reading, motion sickness, and headaches. Other vergence and
accommodative anomalies are convergence excess, divergence
insufficiency or excess, and vergence or accommodative insufficiency.
Convergence insufficiency may be
present in some forms of childhood strabismus. Acquired disorders of
vergence include the effect of some sedative drugs and alcohol,
Parkinson’s disease, progressive supranuclear palsy, midbrain
lesions and parietal lesions . One rare condition is spasm of
convergence, in which the eyes intermittently converge or turn
towards each other. This phenomenon causes diplopia, blurred vision,
miosis and episodic adduction of one or both eyes. It may be a sign
of an organic lesion or of a functional disorder. Organic forms
include thalamic esotropia, brainstem and cerebellar disorders,
Wernicke-Korsakoff syndrome, vertebrobasilar ischemia, Chiari
malformations, posterior fossa tumours, multiple sclerosis, and
metabolic disturbances .
of saccadic velocity
Saccades of small amplitude, appearing too fast (increased peak velocity- amplitude relationship), may be seen in myasthenia gravis, tumours of the globe, flutter and opsoclonus.
Slow saccades are present in abnormalities of the extraocular muscles, oculomotor nerve palsy, internuclear ophthalmoplegia, in central neurological disorders and in pharmaceutical intoxication, especially that of anticonvulsants or benzodiazepines.
Slowing of horizontal saccades is generally observed in pontine lesions after dysfunction of the ipsilateral PPRF.
Slowing of vertical saccades indicates a midbrain lesion in which the rostral interstitial nucleus of the MLF is involved, such as in ischemic, inflammatory and neurodegenerative diseases, especially progressive supranuclear palsy.
of saccadic accuracy
Hypermetric saccades are saccades of high amplitude; the patient will look over and past the target (overshoot), and will need a corrective back saccade to re-attempt to find the target. These indicate lesions of the cerebellum (especially the vermis) or the cerebellar pathways. Patients with Wallenberg syndrome make hypermetric saccades in the direction of the side of the lesion.
Hypometric saccades are saccades of low amplitude; the subject will need to make more than one saccade to attempt to find the target. These occur in a variety of cerebellar, cerebral hemisphere and brain stem disorders.
of saccadic initiation
latencies increase in patients with amblyopia and hemispheric
lesions, especially those affecting the cortical eye fields.
Bilateral frontoparietal lesions produce a severe defect of
saccade initiation known as ocular motor apraxia. Other disorders
causing increased latencies are Huntington’s disease and
corticobasal degeneration [2,21].
involving the neuronal substrate of the VOR gives rise to changes in
gain, direction of VOR and postural imbalance . During the
examination the patient will be not able to maintain target fixation.
The patient will perform a corrective (catch-up) saccade to fix
the target again, or will not move the eyes at all. Frequent causes
of abnormalities of the VOR are:
unilateral peripheral vestibular disorder, lesion of the labyrinth or of the vestibular nerve;
bilateral peripheral vestibular disorders, due to bilateral eighth nerve section, aminoglycoside intoxication, or toxic, infectious, neoplastic, autoimmune, traumatic or inflammatory processes;
central vestibular disorders due to infarct, haemorrhage, tumour, trauma or infection.
are three main ways in which to record eye movements to a high
degree of accuracy:
electro-oculography: a large range of horizontal movements may be recorded by quantifying the corneo-retinal potential using skin surface electrodes. This method is applicable for children and poorly cooperative patients. Disadvantages are common lid artefacts, the requirement for repeat calibration, adaptation to level of ambient lighting and its inability to measure vertical eye movements;
magnetic search coil technique: allows the measurement of eye movements in all directions using the scleral annulus, but is expensive and invasive;
video-based infrared oculography (infra-red eye tracking) is the most frequently used method. A light source is used to produce reflections on the surface of the eye. Tracking the relative movements of these images gives an eye position signal. A video image is digitized and analyzed with computer software to calculate the position of the pupil and its centre. This method allows rapid and reliable recording of horizontal and vertical eye movements.
Different oculomotor paradigms
are used in the laboratory to measure eye movements. We measure
smooth pursuit and saccades (velocity, latency and accuracy).
Saccades may be tested using visually stationary or moving targets,
combined with head movements, both reflexive and memory-guided. The
control of voluntary saccades may be tested with an antisaccade
paradigm. In this task, the subject is required to suppress a saccade
towards a stimulus that appears at the periphery of vision, and
instead to generate a voluntary saccade of equal size towards
the opposite side . (Fig. 7, 8)
of eye movement must be systematic, accurate, easy to perform, and
place few demands on patients. The examination should begin by
exploring fixation and smooth pursuit, and go on to investigate
vergence. If vergence is abnormal the lesion will be probably be
nuclear (CN III) or infranuclear. Finally, the saccades should
be explored: if these are normal, the examination may cease. If they
are abnormal, VOR is next. Should VOR be normal, the origin of the
eye movement disorder will be probably be supranuclear, whereas if
VOR is abnormal, the problem should be nuclear or infranuclear. (Fig.
9, adapted from Vignal et al )
Note: Supplementary data (video)
associated with this article is available on the website of Charles
University, Prague, First Faculty of Medicine and General University
Hospital, Prague, Czech Republic:
Bonnet’s work on this article was supported by Czech Ministry
of Education research project MSM0021620849
would also like to thank Sophie Rivaud-Pechoux, Dr. Claudia Brockmann
and Chris Harris for their critical review of the manuscript. We also
extend our thanks to Olga Kucerova for her contribution, Miriam
Kovalikova for her help preparing the video, and Aaron Rulseh, MD,
for preliminary English language correction.
of Neurology Charles
University, Prague, First
Faculty of Medicine and
General University Hospital Katerinska
St. 30 120
00 Prague 2 e-mail:
for review: 21. 1. 2011 Accepted
for print: 13. 3. 2011
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