Investigations of Disorders of Balance

Home , Balance disorder, Optokinetic drum

56856ournal ofNeurology, Neurosurgery, and Psychiatry 1995;59:568-578 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.59.6.568 on 1 December 1995. Downloaded from NEUROLOGICAL INVESTIGATIONS

Investigations of disorders of balance

P Rudge, A M Bronstein

To maintain balance in the upright position, a isfactory. Traditionally this is determined by complex and not altogether successful series of studying stance and gait with and without fixa- neurological mechanisms have evolved. These tion. Acute failure of vestibular input from one comprise visual, proprioceptive, and vestibular side results in the patient falling to that side, a systems, all of which interact, and information situation made worse by removal of fixation. which is analysed by the cerebellum, cerebral Similarly, when such a patient walks they usu- cortex, and basal ganglia. As a result of this ally veer to the side of the lesion; again this is analysis appropriate motor outputs occur in an accentuated by eye closure. Various clinical attempt to maintain posture and gait. tests with eponymous titles have been devised Dysfunction of any part can result in imbal- in an attempt to increase the accuracy in ance or a feeling of spatial disorientation. determining the side of a unilateral lesion. For In this article we consider tests primarily of example, in Unterburger's test the patient is the vestibular system, which help to determine instructed to march on the spot with the eyes what abnormalities account for a patient's closed; in the case of a unilateral lesion the symptoms. We will not consider in any detail patient rotates to the side of the lesion. research techniques or analyses that are of little Although these clinical tests may be indicative value in the clinical assessment of the patient of abnormality, their ability to predict the side at the present time. As in all branches of medi- of a unilateral lesion is poor, especially in cine it is essential to obtain an accurate history chronic, progressive, or partially compensated and to do a thorough general and neurological lesions. Removal of proprioceptive cues can examination of any patient complaining of also be useful in assessing patients especially impaired balance before embarking on exten- those with total vestibular failure. If such sive investigation; a complaint of imbalance patients are placed on a rubber mattress and may signify a wide range of possible diseases then fixation is removed they will fall as pro- including disorders of the cardiovascular and prioceptive cues function poorly under these musculoskeletal systems, as well as dysfunc- circumstances. Attempts have been made to

tion of the nervous system. improve the sensitivity and specificity of stance http://jnnp.bmj.com/ assessment by the development of various mechanical platforms (see posturography). Clinical investigation of the vestibular Of particular concern to the neurologist are system the connections to the extraocular muscle The vestibular system comprises two main nuclei which permit the vestibulo-ocular reflex components; one concerned with detection of (VOR). This reflex functions in the three car- angular acceleration (semicircular canals) and dinal planes. Stimulation or inhibition of com- on September 25, 2021 by guest. Protected copyright. one concerned with detection of linear accelera- plementary pairs of canals results in tion (otoliths). The semicircular canals com- appropriate movement of the eyes ensuring prise three pairs of accelerometers arranged adequate foveation during head movement. National Hospital for roughly in three orthogonal planes, one set on The system has a wide dynamic range suffi- Neurology and Neurosurgery, Queen each side of the head. In humans and other cient to stabilise a retinal image on the fovea Square, London, erect primates, the vertical canals are large through most movements.3 This is necessary WC1N 3BG, UK compared with those in quadrupeds, a point of as the only other mechanism available for P Rudge some relevance in that we have greater ability to image stabilisation is the pursuit optokinetic MRC Human assess canals.' system, which functions poorly above 1 Hz. Movement and the horizontal than the vertical Balance Unit, Section Whereas the adequate stimulus is acceleration, The other major part of the vestibular system ofNeuro-otology, because of the nature of flow of fluids through is that involved in gravity detection. This sys- National Hospital for narrow tubes of large radius of curvature, the tem comprises two end organs (saccule and Neurology and Neurosurgery, Queen VIIIth nerve carries velocity (first integral) utricle) which detect linear acceleration Square, London, information to the vestibular nuclei.2 Further (including gravity) by virtue of the otoconia WC1N 3BG, UK integration to position occurs at a central level that rest on hair cells of the macula. Each mac- A M Bronstein and this information is fed to various motor ula can signal acceleration in many directions Correspondence to: Dr P Rudge, National nuclei in the brain stem and cord as well as to because of the multiple orientation of hair cells Hospital for Neurology and the cerebellum and cerebral cortex.2 in the end organ.2 Connections of these linear Neurosurgery, Queen Square, London, Clinical assessment of the integrity of the accelerometers are less well determined than WC1N 3BG, UK. vestibulospinal connections is not entirely sat- those from semicircular canals but there are Investigations ofdisorders ofbalance 569 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.59.6.568 on 1 December 1995. Downloaded from connections to the neurons innervating mesencephalon, especially those involving the somatic and eye muscles. interstitial nucleus of Cajal6 and medulla; this type of tonic rotation may be suspected from a CLINICAL ASSESSMENT OF THE VOR head tilt or the eye covering test or seen from The most useful reflexes clinically to assess the tilting of the optic disc. vestibular system are the vestibulo-ocular ones. A further important finding that can be In the main, these involve activation of the made on the VOR in a clinical setting is assess- semicircular canals (VOR in the three cardinal ment of VOR suppression (VORS). In a nor- planes) by variants of the doll's head man- mal subject the VOR enables fixation to be oeuvre. It is difficult, however, clinically to maintained during head motion. If a subject is assess canal function in isolation because of the rotated through large angles, however, the presence of pursuit-optokinetic eye movements VOR is interrupted by repetitive saccadic in the light and excitation of cervical receptors. movements in the opposite sense to the slow Normal neck-eye reflexes are weak but conta- movement; this is vestibular nystagmus.The mination from them can be avoided by using a VORS is easily tested by getting the subject to swivel office chair to rotate the whole patient in fixate a long spatula gripped in the teeth while the horizontal plane; this is also of value in oscillating the head in the horizontal or verti- cases of neck rigidity or poor patient coopera- cal plane,7 or more simply by fixating their tion. Despite these limitations VOR examina- thumbs with arms outstretched while rotating tion is useful in cases of ophthalmoplegia to see at the waist or on a swivel chair. No nystagmus if restriction of gaze can be overridden by a is seen in the normal subject until the fre- rotation of the head in the appropriate plane. quency of oscillation approaches 1 Hz or the For example, in Steele-Richardson syndrome peak velocity is greater than 60°/s. Similarly, in the ophthalmoplegia is initially supranuclear peripheral disturbances the VORS is intact. In leaving the final common pathway via the many patients with cerebellar and brain stem extraocular motor nuclei intact; pursuit and lesions VORS is absent-that is, nystagmus is especially saccadic movements are limited due even seen during slow head movements. There to the disconnection of cortical pathways in the is usually a good correlation between VORS mesencephalon and brain stem. Proof that the and pursuit; absent pursuit usually results in ophthalmoplegia is indeed supranuclear is absent VORS. Using electronystagmography obtained by showing full range of movement, (ENG) and other methods of recording eye or improvement of movement, by the VOR. movement it is possible to obtain an accurate This is most easily done by getting the subject measure of the VORS (see laboratory assess- to fixate an earthbound target and rotating the ment). head in a sinusoidal fashion up and down (the direction in which limitation first occurs) and CLINICAL ASSESSMENT OF SPONTANEOUS showing improvement in the excursion of the NYSTAGMUS eye. Clearly, pursuit may play a part in this One of the cardinal signs of abnormal vestibu- improvement but the VOR is the most impor- lar function is nystagmus but not all nystag- tant factor. Information is fed from the mus signifies vestibular abnormality. To vestibular nuclei and lower brain stem to the differentiate between types of nystagmus may mesencephalic nuclei responsible for vertical require an analog or digital recording of the gaze. wave form of the movement and an assess- http://jnnp.bmj.com/ Clinically, some information on VOR func- ment of the effect of the removal of fixation on tion can be obtained by turning the patient's the nystagmus. head while observing the optic disc during Vestibular nystagmus is caused by an imbal- funduscopy.4 The patient must be instructed ance between the paired vestibular structures to maintain fixation on an object across the (end organ, VIIIth nerve, or relevant brain room. Normally, the disc remains steady in stem nuclei). Briefly, reduction of vestibular

space but if, say, the right labyrinth is hypoac- activity on one side of the brain stem causes a on September 25, 2021 by guest. Protected copyright. tive, the disc will seem to jerk during turning slow drift of the eyes to the side of that reduc- of the head (chin) to the right. When the tion. This slow movement, which is essentially vestibular loss is profound, this jerky eye linear-that is, constant velocity-is followed movement in response to turns of the head can by a rapid saccadic movement in the opposite be seen by the naked eye. In this case it is best direction. Repetition of this results in saw to instruct the patient to fixate on the exam- tooth vestibular nystagmus. The nystagmus is iner's nose. called first degree if present only when gaze is Assessment of otolith function clinically is directed towards the fast phase, second degree even less easily done. Counter rolling of the if present in the primary position, or third eyes can be seen when the head is rotated to degree if present when the eyes are deviated in the ear down on to one shoulder; the eyes the direction of the slow phase (Alexander's slowly deviate in the opposite sense and then Law).8 Removal of fixation typically enhances there is a rotatory quick phase causing tor- the nystagmus if the lesion is peripheral and sional nystagmus. This response is, however, the eyes drift markedly towards the deranged mainly dependent on the vertical semicircular side (fig 1). This can be seen clinically with canals rather than the otoliths. Skew deviation infrared apparatus or Frenzel's glasses; these of the eyes (vertical divergence of the eyes) have high dioptre convergence lenses which without nystagmus is thought to reflect tonic allow a magnified view of the eye of the otolith pathway imbalance. It can be seen with patient, without the patient being able to fixate utricular nerve lesion5 or with lesions of the due to the blur produced by the lenses. 570 Rudge, Bronstein J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.59.6.568 on 1 December 1995. Downloaded from R 300 D 300 2O00 'K Q Vert re Hor * / P le i s Figure 4 ENG ofinternuclear ophthalmoplegia showing up beat nystagmus. On the left the vertical trace (VERT) LI shows gaze paretic up beat nystagmus on looking upwards. D 5s On the right the horizontal eye movement record (HOR) for left (Ze) and right (re) eyes at rapid paper speed shows Figure 1 ENG of vestibular nystagmus due to left slow adduction velocity in the left eye and gaze paretic peripheral lesion. Note nystagmus is only apparent with nystagmus in the right eye. eyes deviated to right (R) in presence offixation but when light is extinguished at D, nystagmus is apparent in primary (P) and on left (L) gaze. The nystagmus is saw The wave form of nystagmus is not always toothed that is, has a linear slow phase, its magnitude increases with deviation of eyes in direction offast phase, saw toothed with a linear (constant) velocity, and it is always in the same direction. In allfigures for slow phase; with gaze paretic nystagmus the horizontal recordings up deflection is to right. slow phase has a roughly exponential decline interrupted by repeated fast phases (fig 2). This form of nystagmus is due to a failure of integration of the burst of actitivity arising from the saccadic generators in the parame- 300[ dian pontine reticular formation (PPRF)." This results in insufficient tonic holding activity to maintain the eyes in the eccentric position is against the orbital elastic forces tending to return the eye to the orbital mid-position. Figure 2 ENG ofgaze paretic nystagmus in cerebellar Failure of integration most commonly occurs lesion. Note exponential decline ofslow phase and some rebound nystagmus when eyes return to midline. in lesions of the brain stem or cerebellum but can also be seen if there is a failure of faithful transmission of activity through the final com- Alternatively, low amplitude nystagmus can be mon pathway to the extraocular muscles for detected with fundoscopy (which makes the example, myasthenia gravis-or if the muscles nystagmus seem reversed).4 In some patients themselves are unable to contract effectively- vigorous head shaking may generate a nystag- for example, ocular myopathy. This form of mus that is not clinically apparent. The "head nystagmus occurs in a wide variety of CNS shaking" test (20-30 full cycles at around 2 Hz conditions, many of which are associated with followed by Frenzel's glasses observation) is imbalance. At the clinical level, bidirectional claimed to be a useful addition to the clinical nystagmus in the horizontal plane is nearly vestibular examination; there is a fair correla- always associated with central dysfunction (fig tion with caloric test findings.910 3). An exception is congenital nystagmus (see oculography). Acquired nystagmus in the vertical plane http://jnnp.bmj.com/ occurs less often than horizontal nystagmus and is almost always an indication of a central disorder. Further, it is invariably accompanied by imbalance. Vertical upbeat nystagmus, especially if present in the primary position, indicates a lesion in the floor of the IVth ventricle or ventral to or the aqueduct, possibly on September 25, 2021 by guest. Protected copyright. within the superior cerebellar vermis; it is often seen in patients with bilateral internuclear ophthalmoplegia (fig 4).12 Down beat nystagmus is seen with lesions at the foramen magnum-for example, Arnold-Chiari mal- formation-or with cerebellar atrophy.'3 No cause is apparent in probably 40% of all cases; of note is the rarity of this type of nystagmus in patients with multiple sclerosis or intra-axial tumours (table 1). Characteristically, vertical nystagmus is altered by position'4 and down beat nystagmus is increased in amplitude if the eyes are deviated 300 to the left or right of the midline. Convergence can also modify vertical nystagmus. Down beating nystagmus has been associated with syringomyelia but this is not entirely true. In patients with cerebellar ectopia and a syrinx in whom there is nystag- Figure 3 ENG ofgaze paretic nystagmus to right and vestibular nystagmus to left mus (about 30% of the total) the nystagmus is (above) in patient with a right sided brain stem glioma shown in the MRI (below). often torsional, with the fast phase usually Investigations ofdisorders ofbalance 571 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.59.6.568 on 1 December 1995. Downloaded from Table 1 Causes ofdown directed towards the side of greater sensory occurs in with visual beat nystagmus'370 patients longstanding loss in the limbs-that is, clockwise fast phase failure and in lesions of the brain stem espe- Diagnosis % from the examiner's viewpoint is associated cially those involving the central tegmental Cerebellar with left sided sensory loss. Torsional nystag- tract. '7 18 In neurological practice it is most ectopia 27 mus is not confined to syringomyelia; it is also often seen in in which it is Cerebellar multiple sclerosis, degeneration typically found in lesions of the medial often associated with an internuclear ophthal- Genetic 18 vestibular nucleus (fig 5), as in Wallenberg's some workers think that Acquired 10 moplegia. Although Tumour 2 syndrome, and lesions of the cerebellum.'5 impaired visual acuity is important in the gen- Multiple sclerosis 1 There are some rarer types of nystagmus all eration of this has not Undiagnosed 42 pendular nystagmus"9 of which are often associated with imbalance. been our experience. Convergence retraction Of these, rebound nystagmus is the most fre- nystagmus due to lesions in the region of the quent.'6 If gaze-paretic nystagmus is induced quadrigeminal plate and posterior commissure on looking in one direction and the eyes are can readily be seen clinically especially using kept deviated for a prolonged period the nys- an optokinetic drum rotated downwards; it is tagmus sometimes diminishes and ceases. difficult to record without video filming. When the eyes are returned to the midline a Periodic alternating nystagmus-that is, nys- nystagmus in the reverse direction is seen for a tagmus in which the direction spontaneously short period, even though nystagmus in the and repeatedly reverses despite eye position primary position was not initially present (fig being constant-is found in various cerebellar 2). Such nystagmus is typical of cerebellar disorders and can readily be seen; it is clearly lesions. Pendular nystagmus is nystagmus in shown by prolonged horizontal eye movement which there is no clear distinction between the recordings. Finally seesaw nystagmus, in fast and slow phase. It may be symmetric- which one eye elevates and intorts and the that is, identical in each eye or highly asym- other is depressed and extorts repeatedly, indi- metric differing in amplitude, direction, or cates a lesion in the region of the peduncular both in either eye. On occasion complex tra- fossa and is probably due to damage in the jectories are followed-for example, elliptical interstititial nucleus of the medial longitudinal or figure of eight. This type of nystagmus fasiculus and the adjacent nucleus of Cajal.6 It is readily seen clinically but recordings are necessary to delineate it fully.

CLINICAL ASSESSMENT OF INDUCED H "--k NYSTAGMUS L Because many patients with imbalance do not have nystagmus, techniques for inducing nystagmus are commonly used in the clinic. The V U most valuable methods are optokinetic, rota- T__ tional, caloric, and positional stimuli. R Optokinetic nystagmus Optokinetic nystagmus can be assessed at the T,,X j\' bedside with a small striped drum rotated in L http://jnnp.bmj.com/ front of the patient. This is basically a pursuit 2 task and not surprisingly correlates well with

s other pursuit measures. It is possible to mea- 1 sure optokinetic responses with a small drum, or with a large visual field rotating about the patient using various special techniques such as electronystagmography (ENG, see later). A

common abnormality is a directional prepon- on September 25, 2021 by guest. Protected copyright. derance-that is, a greater response in one direction. Typically a right directional preponderance correlates with abnormal pursuit to the right (for example, a right cerebellar or parietal lesion results in greater optokinetic nystagmus towards the right). In normal subjects the eyes deviate in the direction of the fast phase of optokinetic nystagmus but in certain disorders of the basal ganglia the converse happens-that is, deviation is in the direction of the slow phase.20 Nystagmus induced by stimulation ofthe semicircular canals Two clinical methods are available to stimulate the semicircular canals: caloric testing and rotational stimuli. Because much information Figure 5 Horizontal (H), vertical (1<, and torsional (T) eye movement recordi.ngs can be obtained from clinical assessment of (scleral search coil technique) of a patient with predominantly torsional right beati nystagmus (top) due to a left sided lesion on thefloor ofthe IVth ventricle (bottom)ng.Te the caloric tests they will be considered next. lesion is likely to have involved the left mnedial vestibular nucleus. Sophisticated assessment of rotational stim- 572 Rudge, Bronstein J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.59.6.568 on 1 December 1995. Downloaded from uli-for example, ENG-will be considered in organ or VIIth nerve there a later damage. Secondly, section. may be a bias of the nystagmus such that the duration in one Caloric direction, say the left (with testing right cold and left hot irrigation), is greater This test depends primarily on convection set than that to the side. This is known in the relevant opposite up canal by thermal stimula- as directional and can be tion. In the clinical preponderance (DP) setting the test is most seen in peripheral disorders as well as with commonly used to measure horizontal canal lesions at any level of the nervous It function. The system. usual method is that described does, however, show that there is a vestibular by Fitzgerald and Hallpike in their classic bias in one direction and if there is a CP as paper21 in which the horizontal canal is put in well it indicates that this is not the vertical fully compen- plane with its ampulla uppermost sated. Finally, there may be hypofunction of by lying the patient horizontally on the back both horizontal canals-for example, after and flexing the neck to 300. One external mea- aminoglycoside antibiotic treatment. The tus is irrigated with water at 70 above or below advantage of caloric testing of horizontal body temperature for 40 seconds, with the canals is that function of a canal can be flow rate single being greater than 6 ml/s. This stimu- assessed, a situation that applies to no other lus sets up a convection current which flows test routinely available. The disadvan- if hot water primary up is used and stimulates the hair tages of caloric testing are that the stimulus cells; conversely the cold stimulus causes intensity varies in different subjects-for movement of endolymph away from the example, because of differences in meatal ampulla and reduces the firing rate of the diameter, and that water cannot be cells.22 Thermal stimulation irrigation of hair cells with- used if there is a defect of the tympanic mem- out any convection would also cause similar brane. effects on the hair cell firing rate but in fact Caloric can also be used to assess this testing the probably only accounts for a small propor- function of the vertical canals but in this case tion of the alteration23 (although it accounts only pairs of canals, either anterior or for all of it in conditions of poste- zero gravity such as rior, are studied. These canals are set deeper space travel).24 The interested clinician can in the petrous temporal bone than the hori- prove to himself the importance of convection zontal canals and therefore duration a caloric longer by doing test on a colleague and and more intense thermal stimuli are required. repeatedly turning the subject prone and Both ears are with and irrigated simultaneously supine showing that the nystagmus either cold (20°C) or hot (47°C) water for 60 reverses as the ampulla changes from being seconds with the head in the usual for inferior to position being superior. caloric testing. The cold stimulus causes slow The nystagmic response is used to assess downward deviation of the with the effect eyes upbeat of canal irrigation. The eyes are nystagmus and the hot stimulus the reverse. It viewed in the light while the subject fixates a is essential to perform horizontal on irrigation spot the ceiling. During and after comple- first to ensure that there is no underfunction- tion of irrigation nystagmus is induced to the ing of the horizontal canal; if there is, reduc- side opposite the irrigated ear in the case of tion of duration of of the cold irrigation relatively irrigation and vice versa for warm irriga- "normal" ear is necessary to avoid oblique tion. The test is carried out sequentially using nystagmus. Bilateral, bithermal caloric testing http://jnnp.bmj.com/ the left and right ear alternately and leaving is particularly useful in patients with ophthal- about five minutes between irrigations. This moplegias to determine if the of the interval is not paresis eye sufficient for all the thermal gra- movements is nuclear or supranuclear-for dient to disappear but is reasonably satisfac- example, Steele-Richardson syndrome.20 As tory.25 Several variables can be assessed, of will be noted from the temperature of water which duration of the nystagmus and slow used for this type of testing the cold stimulus is phase velocity are the two most common. of greater magnitude. Unfortunately it is not on September 25, 2021 by guest. Protected copyright. Only duration can be used as a clinical mea- possible to raise the temperature of the hot sure without special equipment such as ENG. stimulus above 47°C and even that is very There is no doubt that slow phase velocity is uncomfortable indeed. more physiologically meaningful, but interest- During caloric testing it is possible to assess ingly, not more clinically useful. This is visual suppression of with- because the (VORS) nystagmus variance of duration of nystagmus out contamination from other reflex eye move- is less than that of slow phase velocity.26 ments.27 2 A practicable method is to Three perform types of abnormality are seen with each irrigation with fixation and when the nys- horizontal canal irrigation. Firstly, there may tagmus ceases, to the fixation be an extinguish spot underfunctioning of one canal, conven- and view the eyes in the dark with an infrared tionally called "canal paresis" (CP). In our viewer, or to use Frenzel's In a normal a glasses. laboratory, 9% difference in the duration of subject or patients with a peripheral lesion, the nystagmus between the two sides is signifi- nystagmus will again be seen and its duration cant.* This typically occurs in peripheral without fixation gives a measure of the lesions and visual a total failure of function of one suppression. In the case of central lesions, horizontal canal is nearly always due to end especially those involving cerebellar connec-

* CP f (Lcold + - f + Lhot) (Rcold Rhot) f (Lbeating nystagmus - Rbeating CP = f + nystagmus) f (Lcold + L-hot + Rcold + DP = Rhot) f (sum alla nystagmus) Investigations ofdisorders ofbalance 573 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.59.6.568 on 1 December 1995. Downloaded from Table 2 Positional nystagmus The patient's head is rapidly lowered to below Benign Central the level of the couch and the eyes observed for any nystagmus. After an interval of 30 sec- Direction To dependent ear Any (torsional) onds, if nystagmus is not found, or after the Vertigo + + + nystagmus ceases (the test may have to be ter- Latent interval + Adaptation + minated if the nystagmus lasts longer than two Fatigue + minutes) the patient is returned to the sitting position. Again, any nystagmus is noted. The test is repeated if nystagmus is found to see if tions, visual suppression is reduced or absent there is any adaptation. After this the test is so that there is pronounced nystagmus with performed with the opposite ear dependent. fixation but when the nystagmus stops, The variables noted are latency to onset of removal of fixation does not result in a recur- nystagmus, its duration and adaptation, its rence of it. The duration of nystagmus is never direction, and finally, associated symptoms. greater with fixation than without. Broadly two types of nystagmus are seen: benign positional nystagmus and central posi- Rotational responses tional nystagmus (table 2). It is possible to obtain a general clinical Typical benign positional nystagmus indi- impression of the degree of symmetry of cates a peripheral lesion in which debris from vestibular ocular function by conducting the the otolith apparatus accumulate on the doll's head manoeuvre with careful examina- cupula of the posterior semicircular canal. tion of the eye, directly or during ophthal- Two theories have been proposed to account moscopy,4 or by manually rotating the subject for the nystagmus and both depend on inver- at a roughly constant velocity on an office sion of the posterior canal resulting in either swivel chair and observing the postrotational displacement of the cupula of that canal response. The last is essentially the original because the debris alter its specific gravity Barany test in which subjects are rotated at (cupulolithiasis)29 or the passage of debris about 90 or 1200/s (one revolution every three down that canal acting as a plunger (canal or four seconds) for 30 seconds in one direc- lithiasis).3O31 Occasionally what seems to be tion and then stopped facing the examiner to bilateral benign positional nystagmus occurs. time the duration of the observed nystagmus. Recently, benign positional nystagmus arising By comparing the postrotational response in in the horizontal canal system has been the two directions an idea of symmetry can be reported. It is elicited by brisk turning of the obtained. Although now superseded by head to one side while in the supine position.32 recording techniques and motorised equip- Typical central positional nystagmus occurs ment, this procedure is occasionally used even in a wide variety of lesions, especially those in well equipped centres when a rapid assess- involving the vestibulocerebellum. Of note is ment of vertical semicircular canal function is the fact that spontaneous vertical nystagmus, required. In this case the patient should be either upwards or downwards, can often be rotated with the head extended so that the face modified by positional testing using the con- is directed towards the ceiling; horizontal rota- ventional Hallpike manoeuvre or by placing tion of the chair then stimulates the vertical the subject supine or prone. If the nystagmus canals. Of course in this case the nystagmus is increased in the prone position it is usually http://jnnp.bmj.com/ seen is torsional and because its amplitude is decreased lying supine. Nystagmus induced by usually low the clinician should examine the canal stimulation can also be profoundly mod- subject's eyes closely under bright illumina- ified by alteration of position of the head, due tion. Asymmetries in the duration of the nys- to otolith/semicircular canal interaction.'433 34 tagmus should be 15-20% or more to be of significance.

Laboratory assessment ofpatients on September 25, 2021 by guest. Protected copyright. Positional nystagmus OCULOGRAPHY AND Nystagmus may readily be induced, or, if ELECTRONYSTAGMOGRAPHY (ENG) already present, modified by changes in posi- The techniques currently available for record- tion of the head. The conventional method is ing and the analysis of eye movement have the Hallpike manoeuvre. In this the patient sits been presented in a previous chapter in this on a couch and the examiner firmly grasps the series.35 Table 3 presents a summary of the head which is turned 600 towards one shoul- main advantages and disadvantages of these der. The patient is instructed to keep the eyes systems. From the point of view of the investi- open and to fixate the examiner's forehead. gation of the patient with a balance disorder,

Table 3 Eye movement recording techniques Electro-oculography Infrared oculography Sckeral search coil Video-oculography EOG/ENG IRO SCC VOG Signal source Comeoretinal potential Limbus infrared light Contact lens-mounted Iris/pupil image reflection search coil processing Advantages Non-invasive Non-invasive Excellent resolution (2') Non-invasive Simple/inexpensive Intermediate price Torsional recordings Torsional recordings Prolonged recordings Good resolution (10') Good resolution (10') Good linearity Disadvantages Low resolution (l1) Poor linearity Invasive Expensive Noise/drift Expensive Low temporal resolution 574 Rudge, Bronstein J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.59.6.568 on 1 December 1995. Downloaded from Table 4 Indications for eye movement recordings to investigate imbalance Congenital nystagmus 1 Assessment of eye movements in the dark (a) Is there vestibular nystagmus? (b) Vestibular function (for example, rotational test) R gaze 2 Nystagmus wave form (a) Vestibular v gaze paretic '$\'^NJir\r\r\ (b) Acquired or congenital 3 Confirmation/detection of subtle abnormalities of diagnostic value (for example, abnormal pursuit, subclinical INO) 4 Research, quantification, and follow up

in whom an investigation of vestibular responses is required, the technique generally L gaze recommended is ENG as it allows recording over a wide range of amplitudes; ENG, also called electro-oculography (EOG), is the 100 cheapest system and one not requiring a great 1 s deal of technical or scientific support. It is mainly used for investigation of horizontal eye Figure 6 Horizontal ENG recordings in a patient with congenital nystagmus. The nystagmus shows increasing movements and therefore for assessment of velocity slow phase waveforms (arrows). Compare these horizontal semicircular canal function. It can slow phase waveforms with those ofperipheral vestibular produce some reasonable recordings in the origin (which are rectilinear, figs 1 and 7) and those of vertical plane but it is totally insensitive to tor- brainstem-cerebellar origin (which arefrequently velocity sional movements-that is, those occurring decreasing, figs 2,3, and 5). around the visual axis. Thus the recording of abnormalities of eye movements in these mation of a congenital nystagmus (fig 6). planes, related to dysfunction in the vertical Oculography is also useful in characterising canal system or the otoliths, requires the use of the wave form of acquired nystagmus, espe- more complex techniques such as video ocu- cially in separating gaze evoked from vestibu- lography or the more invasive scleral search lar nystagmus (see clinical assessment of coil system. Fortunately the most common spontaneous nystagmus). abnormality affecting the vertical canal/otolith (3) Non-nystagmic oscillations can be accu- system is benign paroxysmal positional vertigo rately diagnosed with oculography. For exam- (BPPV), which does not require eye move- ple, flutter (horizontal saccades without ment recordings for its diagnosis (see posi- intersaccadic interval) or opsoclonus (polydi- tional nystagmus). rectional saccades without intersaccadic inter- It is important to consider when referral for val) can be separated from other saccadic eye movement recording is necessary (table 4). oscillations in which there is a saccadic interval (1) Recordings may be required when the (for example, square wave jerks). The length abnormality seen during clinical examination of the saccadic interval may help to decide if of the eye movement is ambiguous. For exam- the movements are voluntary as in this case ple, the presence of square wave jerks super- the intersaccadic interval exceeds 150 ms. imposed on the slow phase eye movement of (4) Eye movement recordings may be smooth pursuit may give the impression that required to see if there is any nystagmus in the pursuit is abnormal. As square wave jerks may dark in patients in whom no nystagmus is seen http://jnnp.bmj.com/ be seen in anxious but otherwise neurologi- in the light (fig 7). This is typically found in cally normal patients, the suspicion of broken patients with peripheral vestibular dysfunction pursuit may lead one incorrectly to think that (figs 1 and 7). Alternatives to recordings of eye there is structural brainstem/cerebellar dam- movement for observation of nystagmus in the age. Similarly the presence of a mild internuclear ophthalmoplegia can be difficult to Right labyrinthectomy detect clinically and separate eye recordings on September 25, 2021 by guest. Protected copyright. may be necessary to show the difference in 7 velocity between adduction and abduction days after operation Right movements (see fig 4). (2) Recording of eye movements can be t Left used to characterise the waveform of a nystag- Fixation Darkness mus or other types of ocular oscillations. A good example of the value of oculography is 28 days after operation the recognition of congenital nystagmus. Congenital nystagmus, a condition with no neurological consequences, can show various t io0L wave forms but some of them are pathogno- 1 s monic and this will be of importance when a Figure 7 Horizontal eye movement recordings (ENG) in patient who is not aware of having nystagmus a patient with a right sided labyrinthectomy. Top: develops a neurological problem. Occasionally nystagmus in the presence offixation is almost entirely with suppressed byfixation, as early as seven days patients congenital nystagmus develop postoperatively. Bottom: the process of vestibular visual symptoms in later life and the finding of compensation accounts for thefact that 28 days after the a nystagmus in these patients is of concern36. operation the nystagmus had almost entirely disappeared In cases like this eye movement recordings even in the dark. Visual suppression and vestibular compensation explain the lack ofclinicalfindings in have the value of ruling out structural brain- peripheral vestibular disorders and underline the needfor stem cerebellar disease and the positive confir- special investigations in many of these patients. Investigations of disorders of balance 575 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.59.6.568 on 1 December 1995. Downloaded from absence of optic fixation are Frenzel's glasses, siderable loss ofvestibular function can lead to infrared viewers, or an infrared camera gross underestimation of the degree of vestibu- attached to a video recorder. lar loss. As discussed in the clinical section, a (5) Eye movement recordings are necessary useful addition to the sinusoidal rotational test when quantification of eye movement perfor- is to determine suppression of the VOR by mance or abnormalities is required for visual fixation-that is, VORS. This is investi- research or in follow up of individual patients. gated by attaching a visual target to the rotating In degenerative akinetic rigid or cerebellar syn- chair so that the subjects fixate an object that dromes successive eye recordings can show moves with them during the oscillation. The progressive abnormalities. threshold of frequency or velocity at which (6) The most common reason for eye move- subjects are no longer able effectively to sup- ment recording is the investigation ofvestibular press a vestibular nystagmus or the ratio of one function without interference from visually of the nystagmus variables-for example, slow guided eye movements as detailed in the next phase velocity achieved by the stimulus with section. and without fixation-is an extremely useful addition to vestibular examination.2728 EXAMINATION OF VESTIBULAR FUNCTION Two types of abnormality are encountered Caloric response during rotational investigation in patients with Much information can be obtained by direct a balance disorder. The first is asymmetry of observation of the eyes with the caloric test. the response-DP-which, as discussed ear- Many centres have resorted to eye movement lier, simply indicates a dynamic asymmetry in recording techniques so that technical staff can the peripheral or central vestibular system. As carry out the test, to save medical time, and to these rotational responses are induced by stim- quantify the response. The interpretation of ulation of one canal at the same time as inhibi- the caloric abnormality in terms of CP or DP tion of the opposite one it is not possible to is the same but usually based on slow phase establish with certainty which labyrinth is pri- eye velocity rather than on duration of nystag- marily responsible. The second type of abnor- mus. mality is less common and comprises changes in magnitude of the induced response. A Rotational testing reduction of the induced response is the com- To obtain reliable and quantitative informa- monest finding. Clinicians often do not con- tion on vestibular function a motorised chair sider the possibility of bilateral loss of or turntable and a light-tight room are vestibular function in the differential diagnosis required. Two variables are used to define of a patient with a balance or gait disorder. In rotational stimuli: the waveform of the stimu- our recent review of bilateral vestibular failure lus, whether sinusoidal, trapezoidal, or square in a neurological hospital, in addition to well wave (impulsive), and the peak velocity known and usually suspected causes of bilat- reached during the rotation. eral vestibular loss such as meningitis or The rotational test described in the clinical antibiotic ototoxicity, many patients had section is based on the original Barany stimulus vestibular failure which was idiopathic or asso- and represents a velocity step-that is, impul- ciated with cerebellar system degenerations sive stimulus. The constant velocity rotation is or peripheral/cranial neuropathies.38 The maintained until the nystagmic response disap- converse of vestibular failure-enhanced http://jnnp.bmj.com/ pears (40-60 s) and then the patient is stopped responses-also occurs. Bilaterally enhanced with a similar sudden deceleration. After the vestibular responses can be seen usually in the induced nystagmus has ceased, the patient is course of cerebellar disease perhaps because of rotated in the opposite direction so that two disinhibition of the vestibular system.39A1 This sets of right beating responses (right start and leads to shortlasting but high velocity stop from the left) and left beating responses responses to rotational or caloric stimuli. It is

(left start and stop from the right) are collected. important to remember that patients with on September 25, 2021 by guest. Protected copyright. The actual stimulus variables used vary bilateral abnormalities of the VOR, either in (40-90°/s) but are a compromise between the the form of diminished or enhanced vestibular highest velocity necessary to detect abnormali- responses, may have visual symptoms (oscil- ties and the emetic potential of this test. lopsia) particularly during head movement Responses can be expressed in terms of dura- and thus patients with unusual visual symp- tion, peak slow phase velocity achieved, time toms related to head or body motion, espe- constant of decay of the initial peak velocity- cially if associated with unsteadiness, should that is, time to decay to about a third of the also be investigated from a vestibular point of induced velocity-or by a combination of these. view.42 Some machines are produced commercially that enable a printout of these variables. "Full" or "routine" ENG Understandably, different workers prefer to use Because balance depends on the interaction of the technique with which they have the most vestibular, visual, and proprioceptive signals it experience and there is, therefore, no consensus is customary to extend the neuro-otological on the ideal "rotational stimulus". examination to areas other than the purely If the stimulus is sinusoidal it is important vestibular. This is particularly true in terms of that a range, rather than a single, frequency is investigation of smooth pursuit, saccades, and tested to achieve a thorough investigation of optokinetic nystagmus by means of oculogra- the vestibular ocular system.'7 In our experi- phy. Although a detailed description of these ence, sinusoidal testing in a patient with con- abnormalities has been presented in a previous 576 Rudge, Bronstein J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.59.6.568 on 1 December 1995. Downloaded from Table 5 Differences between central and peripheral vestibular disorders can be visual,46 48 vestibular (for example, gal- Peripheral Central vanic),49 somatosensory, or combined for (labyrinthinelVIII nerve only) (CNS) instance, by rotational or translational dis- CNS Normal Abnormal placements of the platform.5051 The most pop- Symptoms/examination ular but expensive commercial system used Auditory Often abnormal Usually normal symptoms/examination combines disorienting somatosensory and Vertigo: visual means (acute lesion) stimuli, by of coupling the move- (chronic lesion) +l- +l- ments of the supporting surface or of the visual Oscillopsia Rare Common surround to the patient's own body sway.52 (head movement induced) (usually spontaneous) Unsteadiness: This effectively reduces the efficiency of the (acute) somatosensory or visual loops, respectively, in (chronic) +l- Nystagmus: postural control. It is claimed that when all (acute) + + stimulus combinations are studied different (chronic) +l- Trajectory Horizontal or horizontal with a Any direction patterns of abnormal postural control can be torsional component. detected which indicate the primary source of Amplitude + Wave form Rectilinear Frequently exponential disorder. In this way, if a patient cannot bal- Effect of fixation removal Appears/enhances Variable ance in the absence of visual input, or with Eye movements Normal Usually abnormal (pursuit, OKN, conflicting visual input, and when the saccades, INO) somatosensory input has been made unreli- able, a "vestibular pattern" is diagnosed. This, as well as many other claims, has not been supported by rigorous clinical studies.45 The chapter in this series,35 it should be noted here use of posturography is therefore debatable. that any significant finding on investigation of Although clearly of research interest in a spe- oculomotor functions would suggest a central cialised environment, we recommend a critical rather than a peripheral vestibular disorder. view of claims by manufacturers. The same can be said about the important visual/vestibular interaction assessed during OTOLITH FUNCTION VORS. Similarly, the diagnosis of peripheral Some patients attending balance disorder clinics vestibular disorder implies that saccades, pur- report symptoms of unsteadiness which sug- suit, optokinetic nystagmus, and VORS will be gest involvement of otolith rather than semicir- normal on clinical and ENG investigation. cular canal function..34 This may include a Table 5 gives a brief summary highlighting the sense of bobbing up and down, being carried criteria that can be used to distinguish upwards or downwards in a lift, or lateral and between peripheral and central vestibular dis- sagittal pulsions. Certain disorders of head and orders. eye coordination-for instance, the ocular tilt reaction combining head tilt and ocular skew deviation are thought to be due to interrup- Techniques being developed tion of central graviceptive otolith pathways.53 POSTUROGRAPHY Similarly, positional nystagmus, particularly of The recording of postural sway is not a widely the central type as mentioned earlier, is accepted or routine part of the examination of reduced or modified by tilt of the head with the patient with a balance disorder. Body sway respect to the gravity vector, and is therefore http://jnnp.bmj.com/ is normally assessed indirectly by recordings of interpreted as under otolith control.33 Despite the movement of the centre of foot pressure all this clinical evidence, reliable and simple while the patient stands on a force transducing tests of otolith function in humans are lacking. platform. Other motion transducers (for This is due to the difficulties in delivering the example, accelerometers) and EMG record- appropriate stimuli (whole body tilt or linear ings of the lower limbs and trunk, can be accelerations) which require large motion

added. In its simplest form, recordings of body devices and simultaneously recording a mean- on September 25, 2021 by guest. Protected copyright. sway for periods between 20 and 60 seconds ingful response (ocular torsion) which requires with eyes open and closed provide objective eye coils or video-oculography.33 Perhaps the quantification of the Romberg test but add no only technique which does not require extraor- extra information to the clinical observation of dinary equipment to investigate otolith func- that test. Patients with unilateral or even bilat- tion is that described by Gresty and eral vestibular disorders are often normal both Bronstein.54 In this procedure the subject's clinically and quantitatively on the Romberg head is placed eccentrically in front of the axis test.43 It has been reported that if the record- of rotation of a conventional rotating chair ings separate lateral and anterior/posterior while horizontal eye movements are recorded components of sway and include frequency with standard techniques. The rationale is that analysis of sway with power spectrum tech- in this position the head experiences not only niques, the information obtained can be useful angular acceleration but also a tangential com- to distinguish the various forms of cerebellar ponent along the interaural axis which gives ataxia.4 In the form described, often termed rise to stimulation of the utricular macula.55 static posturography, there is general agree- The enhanced VOR elicited in this position has ment that the technique is of no practical value been proved in experimental animals to be due in the diagnosis of balance disorders.45 When to otolith stimulation.56 Although clinical one or more motion stimuli are applied to the abnormalities can be detected,57 full evaluation subject standing on a force plate the procedure in the clinical setting has not been undertaken. is called dynamic posturography. Such stimuli Assessment of the "visual vertical" in which Investigations ofdisorders of balance 577 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.59.6.568 on 1 December 1995. Downloaded from subjects have to set a line vertical in an other- stimulate the vestibular apparatus and gener- wise totally darkened room is sensitive to acute ate a short latency (6-12 ms) inhibitory poten- peripheral or central vestibular deficits, but it tial in muscles of the neck under continuous is not proved that the abnormalities are spe- activation. Although this technique is also cific to the otolith system.3453 Indeed, semicir- under development it has the advantage that, cular canal, visual, or proprioceptive stimuli together with the caloric test and galvanic induce profound modifications of the settings stimulation of the ear, it can stimulate the of the visual vertical in normal subjects.5859 vestibular system on either side of the head The simplicity of the procedure, the inexpen- independently. The click evoked vestibular sive techniques involved, and clear abnormali- cervical potentials seem to be promising in ties in some cases make this technique an identification of patients with the Tullio phe- attractive one for the clinician, even if the nomenon (sound induced vestibular symp- meaning of abnormalities is not entirely clear. toms).668 The technology required for this procedure is currently available in most EEG SELF GENERATED ROTATIONAL STIMULI departments-that is, a click generator and an In subjects with good neck mobility the head averager as used for instance for auditory brain can be rotated about the shoulders either pas- stem evoked responses. sively by the examiner, or actively by the patient, to stimulate the semicircular canals. Eye movements can be recorded and therefore Conclusions VOR measurements can be obtained with rela- In this chapter we have considered the conse- tively simple equipment. Halmagyi et al 60 have quences of vestibular dysfunction in causing used high velocity head displacements while imbalance and discussed various methods of recording eye movements with a scleral search assessment of the vestibular system. Inevitably coil system and have shown that profound uni- these methods are heavily dependent on the lateral lesions-for example, vestibular neurec- vestibulo-ocular connections both at the clinical tomy-show a clear hypoactivity of the VOR and at the investigational level. At the outset during rotation towards the damaged side. The we stated that the neuro-otological examina- sensitivity of this technique with less complex tion could not be considered in isolation and or less invasive eye recording methods, as well in this respect we have not considered two as its general use in the balance disorder clinic, areas. Firstly, because of the close association has not been established. Self generated head of the auditory and vestibular systems, full movements can be particularly useful for the auditory function assessment is essential. In assessment of the vertical canal system but particular, middle ear and petrous bone here again there is the difficulty of having to pathology should be sought by expert ear, resort to complex eye movement recording nose, and throat surgeons. Secondly, imaging devices to measure torsion or vertical eye of the VIIIth nerve system has been revolu- motion accurately. tionised by MRI which is an essential part of the full neuro-otological assessment. Both PERCEPTUAL STUDIES OF VESTIBULAR FUNCTION these areas are omitted from the discussion, Before eye movement recordings became not because they have little importance, but widely available a great deal of the clinical and because they are not part of the remit of this research assessment of the vestibular system article. Finally, even after exhaustive docu- http://jnnp.bmj.com/ relied on psychophysical estimates.6' In the mentation of the clinical and investigative past 30 or 40 years such studies became over- findings a large proportion of patients remain shadowed by vestibulo-ocular investigations undiagnosed. Clear cut diagnoses such as but more recently interest in psychophysical Meniere's disease or cerebellopontine angle assessment has again emerged, not least tumours are relatively easy to make but in our because of the relatively poor correlation of experience a substantial proportion of patients

patient symptoms and vestibulo-ocular find- referred to a specialist neuro-otological clinic on September 25, 2021 by guest. Protected copyright. ings.6263 The simplest assessment is to enquire remain without a specific diagnosis or are about the type and intensity of the sensation given a diagnosis such as vestibular neuronitis during irrigation of the external canals in the that implies an anatomical and aetiological caloric test. Often patients describe sensations precision that is not often justified. Hopefully during the caloric test that are identical to their this unsatisfactory situation will improve with own symptoms during dizzy spells, thereby developments in imaging, neurophysiological indicating a likely vestibular origin for their techniques, and further understanding of symptoms. This can be particularly useful in symptomatology. patients with severe ocular myopathies or with congenital nystagmus in whom vestibulo-ocular function cannot be established. More 1 Spoor F, Wood B, Zonneveld F. Implications of early refined techniques are also currently being hominid labyrinthine morphology for evolution of human bipedal locomotion. Nature 1994;369:645-8. developed which allow assessment of symme- 2 Wilson VJ, Jones GM. Mammalian vestibular physiology. try of function in the vestibular system.63- 65 _New York: Plenum Preaa, 1975:365. 3 Donaghy M. The cat's vestibulo-ocular reflex. Jf Physiol 1980;300:337-5 1. SOUND EVOKED VESTIBULOCOLLIC RESPONSES 4 Zee DS. Ophthalmoscopy in examination of patients with vestibular disorders. Ann Neurol 1978;3:373-4. Colebatch and coworkers66-68 have further 5 Halmagyi GM, Gresty MA, Gibson WPR. Ocular tilt reac- described the phenomenon originally discov- tion with peripheral vestibular lesion. Ann Neurol 1979; 6:80-3. ered by Bickford et al,69 that repeated clicks 6 Halmagyi GM, Aw ST, Demaene I, Curthoys IS, Todd delivered through headphones are able to MJ. Jerk-waveform see-saw nystagmus due to unilateral 578 Rudge, Bronstein J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.59.6.568 on 1 December 1995. Downloaded from

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