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Home , Cover test, Eye movement, Hirschberg test

J7ournal ofNeurology, Neurosurgery, and Psychiatry 1995;59:115-125 115

NEUROLOGICAL INVESTIGATIONS J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.59.2.115 on 1 August 1995. Downloaded from

Eye movements

S Shaunak, E O'Sullivan, C Kennard

The clinical diagnosis of movement disor- projection of the image of the object of inter- ders requires the use of a range of investiga- est on to the most sensitive part of the , tions of varying degrees of complexity, from the fovea. Rapid conjugate eye movements, the simple cover-uncover test used at the , enable changes in the line of sight bedside in the evaluation of to the to bring the image of a new object of interest magnetic field scleral search coil oculographic on to the fovea, and the dysjunctive or ver- technique required to measure accurately gence eye movements ensure that these abnormalities of torsional eye movements.' images are simultaneously placed on both Before we consider the full range of investiga- foveae. There is also a need to stabilise the tions from the bedside to the laboratory, how- image of the object of interest on the fovea ever, it is essential to understand the use to when the object itself moves, achieved by the which the results of these investigations are system, or when the subject's put; these include clinical diagnosis, the study head or body moves as occurs during loco- of pathophysiological mechanisms, or deter- motion when the vestibular and optokinetic mination of therapeutic response. In the case ocular motor reflexes are activated. It is, there- of diplopia (an awareness of seeing the same fore, necessary to observe each of these differ- object in two different locations in visual ent types of in any assessment. space), for example, a systematic approach is We will only briefly mention the vestibular required to determine which extraocular mus- and optokinetic reflexes, as they are fully dis- cles are affected, the aetiology, and the appro- cussed in the review on balance in this series. priate management. At each stage it is essential to have a clear understanding of the anatomy and actions of the extraocular mus- The examination of static eye cles so that appropriate investigations can be movements undertaken and the results correctly inter- ACTIONS OF THE preted. Each eye is rotated by six muscles: four recti http://jnnp.bmj.com/ Although disturbances of eye position giv- and two obliques (table 1). It should be noted ing rise to diplopia are probably the most that the actions of the extraocular muscles are common eye movement disorder encountered dependent on the starting position of the eye. by clinical neurologists, evaluation of reflexive Hence the superior rectus, because of the and voluntary eye movements and identifica- anatomy of its insertion into the sclera, acts Academic Unit of tion of or some other sponta- as a pure elevator only when the is Neuroscience, Charing Cross and neous, involuntary, eye movement can abducted by 23°. With increasing adduction on September 30, 2021 by guest. Protected copyright. Westminster Medical provide important clues to the topographical of the eye from this position, the superior rec- School, London W6 diagnosis. This is possible because the neural tus acts more as an intortor and less as an ele- 8RF, UK of acts S Shaunak pathways controlling the different types vator. Similarly, the superior oblique E O'Sullivan reflex and voluntary eye movements are fairly purely as a depressor only when the eye is C Kennard well segregated in the neuraxis, at least until adducted, and more as an intortor with Correspondence to: they feed into the final common "lower" increasing abduction of the eye. To assess the Professor C Kennard, Academic Unit of motor neurons in the brainstem, which are function of all the extraocular muscles, eye Neuroscience, Charing responsible for activation of the extraocular movements should therefore be examined in Cross Hospital, Fulham Palace Road, London W6 muscles. In humans the various types of eye the nine cardinal positions of gaze. 8RF, UK. movement all subserve the same goal; the Assessment should include movements of the together, called versions, and of each eye individually, called ductions. Table 1 Action ofthe extraocular musclesfrom the primary position HERING'S AND SHERRINGTON'S LAWS Muscle Primary action Secondary action Tertiary action Sherrington's law states that whenever an Medial rectus Adduction - agonist receives a neural impulse to contract, Lateral rectus Abduction an equivalent inhibitory impulse is sent to the Superior rectus Elevation Intorsion Adduction Inferior rectus Depression Extorsion Adduction motor neurons serving the antagonist muscle Superior oblique Intorsion Depression Abduction of the same eye. Every ocular muscle has a Inferior oblique Extortion Elevation Abduction contralateral synergist and these muscles, the The superior muscles are intortors of the eye and the inferior muscles are extortors. yoke muscles, act together to move the two 116 Shaunak, O'Sullivan, Kennard

Table 2 Causes of eyes in the same direction (for example, the head posture is to turn the eyes as far as pos- J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.59.2.115 on 1 August 1995. Downloaded from increased square wave jerk frequency (greater than 15 right lateral rectus and left medial rectus both sible from the field of action of the weak mus- per minute) mediate gaze to the right). When an impulse cle. Hence, if one of the muscles that is sent to a muscle causing it to contract, an mediates conjugate gaze to the left is under- Normal elderly subjects Cerebellar disease equal impulse goes to the contralateral syner- acting, the face will also be turned to the left. Progressive supranuclear gist to maintain parallelism of the visual axes Underaction of the superior or inferior recti, palsy Multiple system atrophy (Hering's law of motor correspondence). It which act primarily to move the eyes in the Huntington's disease should be noted that the fixating eye deter- vertical plane, is compensated by head flexion Motor neuron disease Schizophrenia mines the innervational input to both eyes. or extension respectively. Torsional diplopia This is of importance in the assessment of the usually arises from underaction of the cover test, and also in the interpretation of superior or inferior oblique muscles, and investigations such as the Hess screen test. patients with this symptom often tilt their head towards the shoulder opposite to that of ABNORMALITIES OF the weak muscle. The subject's eyes should be observed in the primary position while fixing an object that Hirschberg's test requires visual discrimination. Each eye This is a rough objective test to determine the should then be occluded in turn, and any degree of tropia, and is particularly useful in abnormalities such as latent nystagmus young or uncooperative patients. The corneal observed. The use of an ophthalmoscope to reflections should be observed while the view one optic disc while the patient fixates patient fixates a light source at a distance of with the other eye will magnify any move- 33 cm with both eyes open, and then while ments seen. The most common intrusions are each eye fixates in turn. A decentration of the square wave jerks, which have an amplitude corneal reflex by 1 mm corresponds to about of 0.5-10' with refixation within 250 ms. A 70 of ocular deviation. The Krimsky test is a high frequency of square wave jerks has been variation of this in which prisms are placed in reported in cerebellar disease2 and parkinson- front of the deviated eye until the corneal ism plus syndromes,3 among other conditions reflections are symmetric. It should be noted (table 2). that a small angle will displace corneal reflections by a degree that is unlikely ASSESSMENT OF DIPLOPIA to be clinically detected. Diplopia is among the most commonly encountered neuro-ophthalmological symp- Ocular ductions and versions toms in neurological practice, and usually Ocular ductions and versions should be arises from a disparity in retinal stimulation assessed in the nine cardinal positions of between the two eyes. If diplopia is present gaze. Ductions may not show minimal muscle with one eye covered, an optical aberration weakness that can be overcome by the within the refracting media of the eye is likely patient, but versions will often show a subtle to be present, although there are other causes paresis. A limitation of movement in a partic- of this phenomenon.8 (table 3). If diplopia is ular direction may be related to paresis of the alleviated by covering one eye, a systematic agonist muscle or tethering of the ipsilateral approach to evaluation is required. As well as antagonist muscle. Apparent underaction of a

determining the nature of separation of the muscle may also arise from the phenomenon http://jnnp.bmj.com/ two images and the direction of maximal sep- termed inhibition of the contralateral antagonist. aration, enquiries as to the presence of a fam- This arises when a patient fixes with the ily history of strabismus, or a childhood paretic eye. In these circumstances the unop- history of orthoptic treatment should be posed ipsilateral antagonist of the paretic made. If the eyes are misaligned, it should be muscle requires less neural input than normal ascertained at an early stage if one is dealing to move the eye. Consequently, from with a non-comitant or comitant Hering's law, the contralateral yoke muscle

strabismus; on September 30, 2021 by guest. Protected copyright. the degree of misalignment varies with gaze also receives subnormal innervation, and position in the first, but does not vary with seems to have limited excursion. This most gaze position in the second. Non-comitance commonly causes confusion between true suggests a recent paretic or restrictive aetiol- paresis of a and ogy. Comitance is characteristic of childhood apparent paresis of the contralateral superior strabismus, and diplopia in such circum- rectus. In such a situation, however, ocular stances is usually due to decompensation of a ductions will be full in the non-paretic eye, longstanding phoria (a deviation of the visual although ocular versions may suggest limita- axes when only one eye is viewing, normally tion of movement of the contralateral kept in check by fusional mechanisms-that superior rectus if the paretic eye is fixating. is, a latent deviation). The term tropia as used later refers to a deviation of the visual axes IDENTIFICATION OF THE PARETIC MUSCLE Table 3 Causes of when both eyes are viewing, which is not kept Cover-uncover test (fig 1A) monocular diplopia in check by fusion (a manifest deviation). Cover tests rely on the fact that foveation Corneal abnormality occurs in an eye that is forced to fixate. If the abnormality Lens abnormality Head posture retinal image was not directed on to the fovea Foreign body (in aqueous or Patients with a before the took a movement vitreous humour) diplopia may adopt compen- eye up fixation, Retinal disease satory head posture, and the position of the of redress will be noted as the eye fixates, Occipital cortex pathology chin, head, and face should therefore be care- which gives an indication of the degree of Psychogenic fully observed. The purpose of an abnormal misalignment of the visual axes. Eye movements 117

A Cover-uncover test B Alternate cover test J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.59.2.115 on 1 August 1995. Downloaded from

(a) R L (a) R L (c) R L

(b) -*-= Secondary Primary deviation deviation 0////i//// (b) (d) (c) 0,,,,,,,,, .4

Figure 1 (A) Cover-uncover test, showing the presence of an . Dotted lines indicate the position of the eye when under cover. (a) At rest the visual axes are aligned correctly. (b) When the cover is placed before the left eye, the eye no longerfixates, and moves inwards. (c) On removal of the cover the eye moves outwards to take up fixation, indicating an esophoria. (B) The alternate cover test, showing the presence of an . (a) At rest, with both eyes viewing, there is a manifest inward deviation ofthe left eye. (b) A cover placed before the non-fixating left eye causes no movement. (c) When the right eye is occluded, the left eye isforced to fixate, and a movement of redress occurs (the primary deviation). The resulting additional innervation to the contralateralyoke muscle leads to deviation of the sound eye under the cover (the secondary deviation). Note that the secondary deviation is greater than the primary deviation. (d) When the cover is transferred to the left eye both eyes assume their original position.

The cover-uncover test should be per- Alternate cover test (fig IB) formed both before and after the correction The alternate cover test is more dissociating of any abnormal head posture, and with the than the cover-uncover test, and should be eyes in the nine cardinal positions of gaze. A used to fully dissociate the eyes and show the clearly defined fixation target at a distance of maximal deviation. While the patient fixates a 6 m should be used, and the test repeated target the occluder is quickly switched from with a near target at a distance of 33 cm to eye to eye to prevent binocular viewing, determine the effect of and accom- allowing sufficient time for the eyes to settle modation on any response seen. The test is in their new position. The alternate cover test performed by occluding one eye at a time, should also be performed in the nine cardinal and initially observing the movements of the positions of gaze to determine the direction of http://jnnp.bmj.com/ uncovered eye. If the uncovered eye moves to gaze that elicits the maximal deviation, and take up fixation, it can be assumed that under the eye in which fixation in that field of gaze binocular conditions the eye was not aligned causes the greater deviation. It is important with fixation, and a manifest deviation was that the patient should never be allowed to present (a tropia). Inward movement of the regain fusion while the occluder is being uncovered eye indicates an , and out- transferred. The examiner should note the as ward movement an esotropia. A vertical devia- movement of the uncovered eye the on September 30, 2021 by guest. Protected copyright. tion may be either a hypotropia or a occluder is changed from one eye to the , depending on whether the eye other. Movement of the uncovered eye may moves up or down respectively. The exam- indicate either a heterotropia or a heteropho- iner should determine whether the tropia is ria, and the alternate cover test will not differ- comitant or non-comitant by seeing if the entiate between these possibilities. The magnitude of the deviation varies in the dif- cover-uncover test must therefore be per- ferent positions of gaze. If no tropia is pre- formed first to determine if a tropia is pre- sent, and the covered eye is noted to move to sent. assume fixation just after it is uncovered, a The size of the deviation of the paretic eye latent deviation (a ) is present, when under cover, with the non-paretic eye and this may also be classified as an exopho- fixating, is termed the primary deviation. ria, esophoria, hypophoria, or a hyperphoria When the paretic eye is forced to fixate, addi- depending on the direction of the deviation. tional innervation is required to overcome the The test is then repeated, and the same paresis. This excessive innervation is also, by observations made while covering the other Hering's law, equally transmitted to the con- eye. It should be noted that the convention is tralateral synergist, which consequently over- that if there is a vertical deviation of the eyes, acts. This overaction is termed the secondary the higher of the two is referred to as hyper- deviation, and is greater than the primary tropic/hyperphoric, regardless of which eye is deviation. The alternate cover test best shows actually at fault. the difference in size between the primary 118 Shaunak, O'Sullivan, Kennard

and secondary deviation, and this finding can that orthophoria (the condition of perfect J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.59.2.115 on 1 August 1995. Downloaded from be used to identify the weak muscle in a yoke alignment of the visual axes) is a physiologi- pair by comparing the movements of redress cally unusual state, and normal people often in the two eyes. It should be noted that the have a small comitant phoria. movement of redress is equal in both eyes in the case of comitant strabismus. Parks-Bielschowsky testfor vertical diplopia Prisms can be used in conjunction with the The Parks-Bielschowsky test is used to ascer- alternate cover test (prism and cover test) to tain the weak muscle in patients with vertical quantify the deviation by determining the or torsional diplopia. The first step is to prism strength that nullifies or just reverses determine with the cover-uncover test the movement of redress. This test measures whether there is a right or left hypertropia in the total deviation and does not separate the primary position and after correction of tropia from phoria. any abnormal head posture. A right hyper- tropia, for example, may arise from underac- The red glass test tion of the depressors of the right eye (right This technique allows the patient with inferior rectus and superior oblique). diplopia to readily differentiate between the Alternatively, the left eye may be hypotropic images from each eye. A red filter is placed in because of weakness of the elevators of that front of one eye (by convention the right) so eye (left inferior oblique and superior rectus). that the subject with diplopia sees two differ- The alternate cover test should then be used ent coloured images. The separation of these to determine whether the amount of vertical images can then be reported by the patient in deviation increases in right or left gaze. If the the nine cardinal positions of gaze, and in hypertropia increases on left gaze, the right head tilts to the right and left. The red image superior oblique or left superior rectus are is towards the right (uncrossed) with an underacting. Further differentiation between esotropia, and towards the left (crossed) with these alternatives is possible by asking the an exotropia. The separation of the two subject to look up and down in left gaze. An images becomes maximal in the direction of increase in hypertropia in gaze downwards gaze of the paretic muscle, with the image implicates the superior oblique as the weak from the paretic eye projected more peripher- muscle. ally. Finally, the vertical deviation should be compared with the alternate cover test in The Maddox rod test right and left head tilt positions. The degree This technique provides a subjective method of misalignment will increase when the head of measuring ocular deviations and depends is tilted to the side of the paretic muscle if the on dissociation of the eyes by presenting a ipsilateral intortors (superior oblique and point source of light to one eye and a line superior rectus) are weak, and to the opposite image to the other eye. The Maddox rod side if the extorting muscles (inferior oblique device consists of small glass rods with a red and inferior rectus) are weak. In practice, an filter, and has the effect of transforming a increased misalignment on head tilt is usually point source of light into a line perpendicular indicative of an ipsilateral superior oblique to the axes of the cylinder; hence the rods palsy, although the test will help to differenti- may be oriented according to the desired ate this from apparent weakness of the con- http://jnnp.bmj.com/ plane of testing. The test is particularly useful tralateral superior rectus arising from the in torsional diplopia where superior or infe- phenomenon of inhibition of the contralateral rior oblique muscle weakness is suspected. In antagonist (see earlier). The test is less often the case of a suspected right superior oblique positive with palsies of the vertical recti or palsy, for example, the rod is held horizon- inferior oblique muscles. tally before the right eye while the left eye The explanation for the effect lies in the

views a white point source of light. The fact that a head tilt to either shoulder induces on September 30, 2021 by guest. Protected copyright. patient will report that the red line is lower an ocular counter rolling, which is mediated than the point source, and relatively intorted, by the ipsilateral intortors (superior rectus and the separation of the images will be maxi- and superior oblique), and the contralateral mal on looking down and to the left. By rotat- extortors (inferior rectus and inferior ing the rods in their frame until the red line is oblique). If, for example, the ipsilateral supe- vertical the amount of (torsional rior oblique is paretic, the superior rectus on deviation) can be determined. A variation of the same side receives excessive innervation the test uses both red and white lenses so that to intort the eye, and by virtue of its relatively the subject can compare the position and ori- unopposed primary action elevates the eye. entation of two lines, rather than a line and point source. The Hess screen test The Maddox rod test primarily detects the This test is used in the investigation of non- presence of phorias, because the red lens used comitant strabismus to assess the paretic ele- produces very dissimilar images and therefore ment, and depends on the use of mirrors or prevents fusional vergence. It should be noted filters to dissociate the eyes and show the that some patients may be able to fuse the position of the non-fixing eye when the other two images in the red glass test, and a phoria eye is fixing in specified positions of gaze.9 can therefore be overlooked. For this reason, The test is invaluable in providing a perma- the results of the Maddox rod test are usually nent record of ocular motility that can be more reliable. The clinician should be aware used to monitor progress and treatment. Two Eye movements 119

test objects are presented in the field of view contralateral synergist to the primarily paretic J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.59.2.115 on 1 August 1995. Downloaded from and the patient is required to place them in muscle remains slightly greater than that of such a fashion that they seem to be superim- the ipsilateral antagonist may help to identify posed (the haploscopic principle). the muscle that was initially paretic. In the Lee's screen adaptation of the test, the apparatus consists of two glass screens at The Lancaster red-green test 900 to each other, which are bisected by a The Lancaster red-green test makes use of double sided plane mirror. A grid on each the same basic principles, but uses red and screen is marked with dots at 50 intervals, green filters to dissociate the eyes.'0 The which are connected to form inner and outer patient wears reversible goggles with a red fil- fields at displacements of 150 and 300 respec- ter in front of the right eye and a green filter tively. The subject fixates with one eye in front of the left eye, and therefore sees only through the mirror the dots on one of the the image of a red light with the right eye, screens which is illuminated, and the exam- and the image of a green light with the left iner uses a pointer to indicate the position of eye. The examiner projects the linear image a dot in the field of this eye. The patient is of a red torch on to a screen in the nine cardi- required to place his pointer on the non-illu- nal positions of gaze and the patient is asked minated screen, viewed with the other eye, so to superimpose the image of a green torch on that it is superimposed over the foveal image to the screen so that the two images seem to of the fixating eye. The blank screen is then him to exactly coincide. If there is a deviation briefly illuminated, and the position of the of the visual axes the two images will be sepa- pointer recorded on a chart that is a copy of rated on the screen. The effect of fixating the grid on the screen. As the innervation of with either eye can be investigated by either the extraocular muscles of both eyes is deter- reversing the goggles, or simply by the patient mined by the fixating eye, any muscle under- and examiner exchanging torches. action or overaction in the non-fixating eye can be identified. The procedure is per- RESTRICTIVE MUSCLE DISEASE formed in the cardinal positions of gaze, and Forced duction testing then repeated with the other eye fixating. The forced duction test is used to determine The charts from the two eyes are assessed the presence of a mechanical restriction to by comparing the plotted fields with each eye movements. This may occur in, for exam- other and with the normal fields on the chart. ple, thyroid ophthalmopathy," Brown's supe- A difference in the size of the fields shows rior oblique tendon sheath syndrome,'2 or non-comitance, which usually indicates the after orbital blowout fractures (table 4). Local recent onset of paresis. The smaller of the or general anaesthesia is required. Two pairs two fields indicates the primarily affected eye. of forceps are applied to diametrically If the fields are displaced but of the same size, opposed limbal points, and horizontal, comitance is present, and this suggests a oblique, and vertical rotations of the globe are longstanding deviation or a non-paretic aeti- performed. Failure of movement or retraction ology. of the globe into the indicates a restric- Each field is then compared with the nor- tive process. Care must be taken that the mal field. The position of the central dot in globe is not inadvertently pushed back into the smaller field indicates the primary devia- the orbit, as this increases the relative length http://jnnp.bmj.com/ tion (the result of fixating with the unaffected of the tethered muscle, and may mask a posi- eye), and its position in the larger field indi- tive result. cates the secondary deviation (the result of An alternative, less invasive, procedure, fixating with the affected eye). Underaction is which may also be used in an uncooperative identified as inward displacement of the dots, patient, is to measure intraocular pressures in and overaction as outward displacement; the primary position and again with gaze in

maximum displacement will occur in the the direction of the limitation of movement. on September 30, 2021 by guest. Protected copyright. direction of action of the overacting contralat- An increase in pressure of greater than 6 mm eral synergist. A narrow, symmetric field with Hg suggests a mechanical limitation. restriction in opposite directions implies a mechanical restriction of ocular movement. THE TENSILON TEST The outer field should also always be exam- may mimic any single or ined; this may show a defect when the central combined extraocular muscle palsy, or fields appear normal, particularly when a infranuclear or supranuclear ophthalmople- mechanical defect is present, or in cases of gia, and must therefore be considered in the slight paresis. differential diagnosis of any puzzling acquired Secondary changes may occur with time ocular motility disturbance. Although the that make determination of the primarily paretic muscle difficult (spread of comitance), and the Hess chart in such circumstances will Table 4 Causes ofrestrictive ophthalmopathy become increasingly comitant. As well as Thyroid disease overaction of the contralateral synergist, over- Brown's syndrome: congenital or acquired Duane's syndrome action of the ipsilateral antagonist due to con- Blow-out fractures tracture, and inhibition of the contralateral Infiltration: for example, metastases, lymphoma, amyloid, orbital myositis, pseudotumour antagonist will appreciably alter the appear- Caroticocavernous fistula ance of the Hess chart. In these circum- Extraocular muscle fibrosis stances the fact that the overaction of the Prolonged muscle weakness with secondary contracture 120 Shaunak, O'Sullivan, Kennard

Tensilon test remains an important tool in phrenia, 18 Huntington's disease, "I progressive J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.59.2.115 on 1 August 1995. Downloaded from the diagnosis of this condition, the clinician supranuclear palsy, and corticobasal degener- must be aware of the limitations and potential ation,20 and motor neuron disease.7 Predictive pitfalls of the procedure.'4 In particular, it is saccades can be tested by alternately raising a important that a definite goal or end point be finger of one hand and then the other in a chosen such as a quantifiable change in the predictable regular pattern, and asking the degree of ptosis or ocular misalignment (for patient to make saccades to the target. example, pretest and post-test Hess charts or Finally the patient should be observed for cover and prism tests). any head movements or blinks before making a , as occurs in Huntington's disease5 and ocular motor apraxia.2' Bedside examination of dynamic eye movements SMOOTH PURSUIT After examination of static eye movements Smooth pursuit can be tested by asking the the various dynamic eye movement systems, patient to track a small target at a distance of including saccades, pursuit, vestibulo-ocular about 1 m while keeping their head still. reflex (VOR), and optokinetic nystagmus Assessment of both horizontal and vertical (OKN) should be tested, firstly at the bedside smooth pursuit should be performed. The and then if necessary by oculography. It target should be moved initially at a slow uni- should be noted that oculomotor perfor- form speed and the pursuit eye movements mance may be modulated by the patients' observed to determine whether they are age, attentiveness, and concurrent medica- smooth, or broken up by catch up saccades. tion. This is a non-specific sign if present in both directions-for example, due to aging22 or SACCADES cerebellar disease,23 or it may indicate a Voluntary saccade initiation should be focal posterior cortical lesion if only present assessed by instructing the patient to look in one direction.24 The speed should be grad- from side to side. The patient is then asked to ually increased, but at high velocities all fixate two targets alternately-for example, a smooth pursuit eye movements will be broken pen in one hand and a raised finger in the up by saccades, even in normal subjects. other-each time they are briefly moved. The These saccadic intrusions occur as the distance between the two objects is varied. smooth pursuit velocity of the eye fails to This generates reflexive saccades, which are match that of the target-that is, the pursuit tested in both horizontal and vertical planes, gain (pursuit velocity divided by target veloc- and the examiner should observe saccadic ity) is reduced. variables such as speed of initiation (latency), The OKN drum and tape actually stimu- accuracy, and velocity. Saccadic accuracy can late pursuit eye movements rather than opto- be determined by noting the size and direc- kinetic nystagmus.' They are useful in testing tion of any corrective saccades. Careful for pursuit asymmetries (pursuit which is observation allows detection of saccades as worse in one direction), and reversed pursuit small as 0.50. Normal subjects often show a in which the fast phases are in the direction of minor degree of saccadic undershoot, which the drum rotation, as in congenital nystag- is more often found with larger gaze shifts. mus.25 If the smooth pursuit gain is reduced http://jnnp.bmj.com/ Any slowing of saccades can be accentu- to one side, the eyes will deviate less quickly ated by using an optokinetic striped drum or from their primary position, so fewer quick tape, when the repositioning saccades will phases are seen when the subject observes an appear slowed. This is of particular help OKN drum. when showing slowed adduction in a partial If a target is tracked by head movements internuclear ophthalmoplegia.'5 Another the VOR will act to generate eye movements

method to accentuate this abnormality is to that would compensate for the head move- on September 30, 2021 by guest. Protected copyright. use oblique targets. Because the velocity is ments. These are in an inappropriate direc- slowed in one plane the resulting saccade will tion and are therefore normally suppressed. be L shaped, because the normal vertical Studies in normal subjects26 and patients27 component is completed before the abnormal have led to the belief that the suppression of horizontal one. the VOR is derived from the smooth pursuit Other types of saccades can also be gener- system, and that patients with abnormal ated at the bedside.'6 For example, antisac- smooth pursuit have impaired suppression of cades (saccades in the opposite direction to the VOR. This may be tested by asking the the target) can be tested by holding up both patient to fixate their thumbnail with their hands on either side of the patient and asking arms outstretched while rotating their head them not to look at the finger that is moved and trunk in harmony.28 Impaired cancella- but instead to look in the opposite direction. tion of the VOR and hence abnormal pursuit If the patient repeatedly makes a reflexive sac- are shown by observing the eye repeatedly cade to the finger that has moved rather than moving off fixation due to the VOR, followed in the opposite direction a high level of dis- by refixation saccades. This is a particularly tractibility (impaired ability to suppress useful technique for testing pursuit in patients reflexive saccades) is shown. Elevated antisac- with gaze evoked nystagmus. cade error rates are associated with dysfunction, and have been reported in OPTOKINETIC NYSTAGMUS patients with frontal lobe lesions,'7 schizo- As discussed earlier the optokinetic system Eye movements 121

cannot as part of a clinical examina- both with and without fixation to assess the be tested J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.59.2.115 on 1 August 1995. Downloaded from tion because the OKN drum and tape com- degree of suppression of the nystagmus by monly used actually test smooth pursuit and fixation. Frenzel goggles can be used to not the optokinetic system. remove fixation.

VESTIBULAR SYSTEM The patient should be observed for nystag- Oculographic techniques mus with and without fixation and also after Although a correct diagnosis of many eye shaking the head for 15 seconds.29 Frenzel movement disorders can be ascertained by goggles may be useful for studying eye move- the bedside methods already described, it is ments without the subject fixating. only by using oculographic recording tech- If the vestibulo-ocular system is function- niques that more subtle abnormalities can be ing normally passive rotation of the patient's detected by the quantitative analysis and eval- head should result in a slow eye movement so uation they afford. In particular the develop- that the eyes deviate in the opposite direction ment of very precise behavioural paradigms in to that of the head movement. This is known the laboratory evoking saccadic and pursuit as the doll's head (oculocephalic) manoeuvre eye movements has shown disturbances pre- and should be performed both horizontally viously undetected at the bedside. and vertically. This technique is not only valuable for assessing vestibular function, but THE IDEAL SYSTEM also for differentiating between nuclear and When considering the various techniques supranuclear gaze palsies, and in the evalua- available it is necessary to be clear about the tion of brainstem function in comatose requirements for an ideal eye movement patients. It should be noted that the eye recording system.3' These are: (a) easy, non- movements elicited by this procedure in traumatic application, ideally with no contact unconscious patients largely reflect the with the eye. (b) No interference with normal integrity of the semicircular canals and their vision, and a sufficiently large field of vision. central connections, although in conscious (c) Simultaneous measurement of horizontal, patients the effects of visual input on eye vertical, and torsional eye movements. (d) movements may influence the response to High accuracy and repeatability, with a wide head rotation. linear range of over 900 of eye position. (e) A rough estimate of any deterioration of High resolution allowing detection of eye vestibular gain (head velocity divided by eye movements as small as a few seconds of arc. velocity) can be obtained by asking the (f) Good stability with no baseline drift. (g) patient to read a Snellen chart while their Good dynamic measuring range (frequency head is being passively rotated. If there is an bandwidth) of zero to a few hundred Hertz. abnormality the will show a (h) Insensitivity to translational head move- deterioration compared with the acuity ments, and thus no need for rigid head fixa- obtained with the head still. With an ophthal- tion. (zT) Insensitivity to surrounding levels of moscope the examiner can observe the illumination, and to artefacts arising from patient's optic disc while they fixate a distant blinks and electromyographic or electro- object and shake their head from side to mechanical interference.

side.30 If the gain of the VOR is unity the Unfortunately none of the current tech- http://jnnp.bmj.com/ examiner will not see any movement of the niques fulfil all these criteria, although some patient's disc. of the four main methodologies in current use Vestibular nystagmus can be elicited by fulfil most of them. rotating the patient in a swivel chair at a con- stant velocity. By altering head position hori- ELECTRO-OCULOGRAPHY zontal, vertical and torsional nystagmus can The most commonly used technique and the be shown. Postrotatory nystagmus will be one that has been available for the longest on September 30, 2021 by guest. Protected copyright. seen if the chair is suddenly stopped. This period is electro-oculography (EOG). As a will be emphasised if the patient wears method to provide a simple visual record of Frenzel goggles, so removing fixation and an eye movement disorder EOG is the sim- allowing the examiner to estimate the dura- plest and cheapest. If high resolution analysis tion of the postrotatory nystagmus. of eye movements, particularly saccades is Caloric stimulation can also be used to test required, however, this technique has numer- the vestibulo-ocular system. The test is per- ous disadvantages. It relies on the fact that formed with the patient supine. The external the globe acts as an electrostatic dipole, with auditory meatus is checked to ensure that the the 0-4-1 0 mV positive with respect tympanic membrane is intact. The head is to the posterior pole. Electrodes are placed flexed to 300 to allow maximum stimulation on the skin on either side of the eye and the of the horizontal semicircular canals. One to magnitude of the potential recorded depends two hundred millilitres of either warm water on the proximity of the cornea to the elec- (44°C) or cold water (30°C) is infused into trode.32 A major disadvantage is the variability the patient's ear. The normal response in an of the corneoretinal potential, particularly in awake patient is for a slow phase response relation to ambient illumination.33 This towards the side of the cold water irrigation results in drifting of the baseline, and it is, (or away from the warm water) with the fast therefore, necessary to dark adapt the subject phase away from the cold water (or towards for 15-20 minutes before testing. There is the warm water). The test is best performed also a rather high baseline noise level due 122 Shaunak, O'Sullivan, Kennard

netic field. Both horizontal and vertical eye both to electromagnetic interference and peri- J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.59.2.115 on 1 August 1995. Downloaded from orbital muscle activity.34 This necessitates the position may be measured simultaneously, use of low pass filtering with a differential and with appropriate windings of the wire coil amplifier and great care with the placement of so may torsional eye movements. The the electrodes. Its sensitivity is at best 0.50 method has low noise levels and high sensitiv- and more usually only 1-2°. ity in the order of a few seconds of arc,3940 There are advantages to EOG over other and its linear range is ±200, greater if a sine techniques. There is a large measurement function correction is used. range of up to ±60° horizontally and ±400 There are, however, two main disadvan- vertically, although the vertical movement tages of the method. Firstly, the subject has recordings are subject to error and only pro- to wear a scleral contact lens held to the eye vide qualitative assessment; the analogue out- by suction.41 Although topical local anaes- put is linear over a range of ±30° 34; there are thetic is used, some subjects find the insertion no limitations of the fields of vision and the and removal of the coil unpleasant. As the subjects can wear their spectacles; and coil can only be left in place for up to 30 min- recordings can be made with the eyelids utes this can limit the number of tests per- closed, which is useful during vestibular and formed. The second main disadvantage is caloric testing. cost. Most complete systems are expensive as are the coils, which usually last for only about INFRARED LIMBUS REFLECTION OCULOGRAPHY five subjects. The second technique that is being increas- It becomes apparent that none of the cur- ingly used both for routine eye movement rently available techniques meets the full set assessment and research is the infrared lim- of ideal criteria discussed earlier. The method bus reflection (IRLR) technique. The eye is chosen rather depends on the clinician's diffusely illuminated with infrared, which is requirements. If, for example, a record of a differentially reflected by the iris and the patient's nystagmus is required, then a sclera back to photocells positioned near the straightforward video recording would be limbus.35 As the sclera reflects better than the appropriate, perhaps with an EOG chart iris the output from the photocells will be record. For recording slow eye movements directly proportional to the position of the such as VOR or OKN the use of EOG is ade- eye. The positioning of the infrared emitters quate, but if a detailed analysis of saccadic and the photocells is crucial for accurate and metrics is required IRLR or MFSSC would linear recordings.36 The other problem is fixa- be more appropriate. The cheapest method is tion of the head, which is necessary if the EOG and MFSSC is the most expensive. If recorded eye movement is to be an accurate large eccentric eye movements are to be representation of direction of gaze. Infrared recorded then EOG is best, as it is for record- oculography systems are generally linear ing patients with their eyes closed, required in within a horizontal range of ± 150, and a ver- testing vestibular function, or when uncon- tical range of ± 100, although satisfactory ver- scious. tical recordings can be difficult.37 It has been Although it is possible to perform some claimed that sensitivity for this technique is of quantification of eye movement records the order of 3 minutes of arc, but in practice directly from the chart records, the analogue

it is not quite so impressive. signal produced by the oculographic equip- http://jnnp.bmj.com/ ment is usually digitised and the data analysis HIGH SPEED VIDEO RECORDERS proceeds off line at a later date with interac- A third technique is high speed television tive computer programs. recording, which with the rapid advances in technology, and therefore of temporal resolu- tion, is likely to become increasingly used for Laboratory investigation of dynamic eye oculography. These systems usually locate the movements centre using software algorithms for SACCADES on September 30, 2021 by guest. Protected copyright. each frame.38 Currently the spatial resolution Essentially when saccadic eye movements are is very good in both horizontal and vertical investigated in the laboratory, the same para- axes, and is highly suitable for recording two digms described earlier are tested. A range of dimensional scanpaths, but temporal resolu- more behaviourally demanding saccadic para- tion is still inadequate for full analysis of sac- digms such as the antisaccade, predictive sac- cadic metrics. cade, and remembered saccade tasks may be used in the laboratory, and may show a disso- MAGNETIC FIELD SCLERAL SEARCH COIL ciation in performance in different patient TECHNIQUE groups.16 The measurement of saccades in the Finally, probably the most accurate system is laboratory also allows both more controlled the magnetic field scleral search coil presentation of the stimuli and more accurate (MFSSC) method.39 The subject is seated so measurement of the variables mentioned. The that their head is located in an alternating beginning and end of a saccade are defined magnetic field. The subject wears a ring arbitrarily, often when the eye velocity rises shaped contact lens in which is embedded a above or falls below 200/s respectively. coil of wire. An alternating current is thereby Rapid refixation gaze movements are induced in the wire, which is proportional to largely achieved by a saccade that covers the sine of the angle between the planes of about 90% of the required distance (primary the search coil and the direction of the mag- saccade), followed by a series of secondary Eye movements 123

Figure 2 Recordings of A amplitude until it saturates at about 20-30°. J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.59.2.115 on 1 August 1995. Downloaded from horizontal eye movements This consistent relation between saccadic taken from two subjects 15 performing the antisaccade Target I degrees amplitude and peak velocity is known as the task (magnetic field scleral main sequence (fig 3).42 Clinical laboratories search coil technique). should derive their own normative values for Upward displacements indicate movement ofthe saccadic variables, as these vary depending on eye or target to the right the precise details of the test procedures and and downward the oculographic equipment. displacement movements to Eye X l X XI degrees the left. (A) Control subject; the subject is SMOOTH PURSUIT (FIG 4) performing the paradigm Laboratory evaluation of smooth pursuit uses correctly, and making saccades in the opposite many different types of stimulus presentation, direction to the target. (B) some of which cannot be tested at the bed- Subject withfrontal lobe side. Usually the stimulus is a small bright dysfunction. The arrows B spot of light, the position of which is con- denote the onset ofreflexive which is saccades in the same degrees trolled by mirror galvanometers, and direction as the target, Target projected on to a screen. Alternatively a spot which are corrected in all screen be cases by saccades in the on a computer may used although opposite direction. 4' + 4 ; 4 this method does not allow testing of such a large range of movements. Eye | The most commonly used pursuit stimuli degrees are either constant velocity (ramp stimulus) or sinusoidal waveforms. A range of different velocities or frequencies are tested. 2500 Interactive computer programs allow the ms analysis of smooth pursuit to calculate such pursuit variables as velocity gain (eye veloc- ity/target velocity). The maximum gain aver- saccades until the target is foveated. Accuracy aged from a series of cycles or the gain of the primary saccade is expressed as sac- averaged as the eye passes the primary posi- cadic gain. This is the value of the primary tion is measured. For sinusoidal targets both saccadic amplitude divided by the target gain and phase can be measured. The gain is amplitude, so that a perfectly accurate pri- calculated from peak eye velocity/peak target mary saccade has a gain of 1 0. Often the gain velocity. The gain is known to be dependent of the primary saccade and also the gain of on the peak acceleration of the target.43 These the final eye position (FEP) after the sec- stimuli mainly test the maintenance of pur- ondary saccades are recorded. Figure 2 shows suit, although another aspect of the pursuit an example of a laboratory recording of per- system of interest is pursuit initiation.44 formance in a saccadic task. The peak velocities of saccades show a OPTOKINETIC NYSTAGMUS unique feature; there is a progressive expo- Adequate assessment of the optokinetic sys- nential increase in velocity with saccadic tem requires a stimulus that fills the patient's http://jnnp.bmj.com/

Figure 3 Main sequence: 500 r a graph of the peak velocity ofsaccadesfrom 11 normal subjects plotted 450 H as afunction oftheir amplitude. 400 H on September 30, 2021 by guest. Protected copyright.

350 H (A Co 0) 01) 300 F * . . . 03) 0L) ; * ': 040 1 . ..0 .. 250 H a.8 0 0-a) 0) 200 H :,0

a) 150 H

100 H

50 H

01 1 2 3 4 5 6 7 8 9 10 1 1 12 13 14 15 Saccade amplitude (degrees) 124 Shaunak, O'Sullivan, Kennard

Figure 4 Oculographic A B J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.59.2.115 on 1 August 1995. Downloaded from recordings ofsmooth pursuitfrom two subjects Target tracking a target moving horizontally at a constant velocity of200 (magnetic field scleral search coil 22g5 technique). (A) Tracing degrees from a normal subject showing accurate tracking. (B) Tracingfrom a patient with motor neuron disease Eye showing poor tracking with frequent catch up saccades. IdegreesT22.5

Velocity 1degrees/sI 150

2000 ms

field of vision and induces the sense of self ceases the response should continue. This is rotation (circularvection). One method is to known as optokinetic afternystagmus rotate the patient at a constant velocity in the (OKAN). The optokinetic system acts as a light for more than a minute. This allows the velocity storage mechanism during the pres- VOR to decay and so the nystagmus is solely ence of the stimuli and when this is no longer due to visual input. Another method is to sit visible the nystagmus continues in the same the patient inside a large optokinetic drum. direction for a few seconds with a declining The eye movements stimulated are conjugate slow phase velocity. eye movements of constant velocity in the When studying OKN the nystagmus seen direction of the stimulus, interspersed with in the presence and absence of visual stimuli quick phases in the opposite direction. The should be studied. This is most easily done by way in which the patient is instructed deter- turning out the lights after a period of optoki- mines the type of response. If the patient is netic stimulation, often after the drum has asked to follow the stripes look nystagmus, rotated at 60°/s for 60 seconds. The velocity which consists of prolonged slow phases with gain (eye velocity/target velocity) and the large corrective saccades, is seen. If the sub- symmetry of the response are measured for ject is asked to stare ahead at the stripes stare both OKN and OKAN. The time constant of nystagmus is induced, which is characterised the slow phase eye movements of the OKAN by smaller and more frequent quick phases. can also be measured. Both the smooth pursuit system and the Because of the great variability in the mea- optokinetic system contribute to the surement of a subject's OKAN eye velocity

response. During the initial few seconds and time constant, repeated measures are http://jnnp.bmj.com/ smooth pursuit constitutes the more impor- needed.45 Alternatively the build up of the tant component. When the visual stimulus slow phase velocity of the OKAN can be monitored by briefly turning out the lights during frequent, two second periods of dark- ness during the stimulation.46 To prevent Table S Clinical and investigative approach to eye movement abnormalities contamination of the data by smooth pursuit the first one second of each two second Bedside assessment Laboratory investigation on September 30, 2021 by guest. Protected copyright. period should be discarded. Static eye movements (diplopia) Ocular ductions and versions Hess screen test Hirschberg/Krimsky test Red glass test Cover-uncover test Lancaster red-green test Alternate cover test Maddox rod test Conclusion Parks-Bielschowsky test Tensilon test The intention of this review has been to pro- Forced ductions vide the clinician with an overview of the clin- Dynamic eye movements ical assessment and appropriate investigation Saccades: EOG, IRLR, MFSSC, high speed video of a patient presenting with a disturbance of Variables studied: eye movements (table 5). Because many neu- Fixation stability Primary saccade gain Latency, accuracy, velocity FEP gain rological conditions may cause abnormalities Distractibility (for example, antisaccades) Latency, velocity of ocular motility, a rational approach to this Distractibility Smooth pursuit: EOG, IRLR, MFSSC, high situation remains of great importance to the speed video practising neurologist. Although a variety of Variables studied: Saccadic intrusions Velocity gain specialised investigations are available, an Symmetry/asymmetry saccadic intrusions appreciation of the basic anatomical and Vestibulo-ocular reflex suppression Phase Vestibulo-ocular reflex: physiological principles involved is necessary, Doll's head manoeuvre See Balance review both for an adequate bedside assessment and Caloric stimulation Optokinetic nystagmus: for such investigations to be appropriately OKN drum Full field visual stimulation employed and interpreted. These findings (actually tests smooth pursuit; see text) must of course be viewed in conjunction with Eye movements 125

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