British Medical Bulletin 63:213-221 (2002)
© 2002 The British Council
Under-rated neuro-otological symptoms: Hoffman and Brookler 1978 revisited
Adolfo M Bronstein
Department of Neuro-otology, Division of Neuroscience and Psychological Medicine, Imperial College Faculty of Medicine, Charing Cross Hospital, London, UK
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Abstract
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In 1978, Hoffman and Brookler published an article in
The Laryngoscope to challenge prevailing views on the lack of diagnostic power
of certain symptoms often reported by patients to neuro-otologists.
Some of these ‘under-rated neuro-otological symptoms’
include complaints of non-rotational dizziness, blurred and
double vision, and the development of visual motion hypersensitivity
in patients with balance disorders. In this review, I revisit
these visual symptoms in the light of new findings from our
laboratory. Double vision due to skew eye deviation can indeed
occur in peripheral vestibular disease when there is a large,
acute peripheral imbalance of vestibular function. It is more
frequent and severe in brain stem disease. In both cases, it
is explained by disruption of the torsional vestibular ocular
reflex. It is usually assumed that damage to the otolith underlies
the emergence of skew diplopia, but recent evidence shows that
the vertical canal system is likely to be partly responsible
as well. The other ‘under-rated symptom’ revisited
here is what patients describe as dizziness when watching moving
objects or whilst walking in visually busy surroundings such
as supermarkets. Recent work has shown that this ‘visual
vertigo’ emerges in patients who, in addition to suffering
from a vestibular disorder, have increased visual dependence.
Visual dependence denotes subjects who preferentially use vision,
as opposed to vestibular or proprioceptive input, for spatial
orientation and postural control. We do not know as yet what
makes some vestibular patients become extremely visually dependent.
However, we have provided evidence for Hoffman and Brookler's
impression that visually triggered complaints should not be
summarily dismissed, as they often point to an underlying vestibular
disorder.
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Introduction
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Excellent monographs on the subject of vertigo and vestibular
disorders have appeared recently
1,2. For this reason, I will
not review the whole subject of balance disorders, but rather
concentrate on a few poorly understood vestibular symptoms which
have been the subject of recent research. Indeed, this article
was inspired by Hoffman and Brookler's paper in 1978, called
Underrated Neuro-otological Symptoms3. This publication, which
exudes clinical finesse, was structured around case reports
and set out to dispel the erroneous belief that certain symptoms
reported by patients are not useful in the diagnosis of labyrinthine
disorders. It shows that in the practice of medicine nothing
replaces the combination of a good capacity for observation
with the paying of careful attention to the patients' own description
of their symptoms.
Some of these under-rated symptoms are complaints of dizziness, light-headedness or a floating sensation. Although presented in different ways, one of the myths in neuro-otology is that these are ‘lesser’ symptoms than ‘proper’ rotational vertigo. Whilst it is true that spinning vertigo usually implies disorder of the labyrinth or its immediate central connections, the reverse implication, that these underrated symptoms do not support the diagnosis of vestibular disease, is certainly not true. As Hoffman and Brookler indicate, anyone who has done a sufficient number of caloric tests knows that people use all sorts of terms to describe the vestibular sensation induced by caloric stimulation: faintness, rocking, staggering, light headedness, waviness as well as rotational vertigo, of course. One of my patients, clearly not bothered at all by the procedure, said ‘it's like going to the pub but much cheaper’. The obvious conclusion in their paper was that: ‘the complaint of dizziness, be it nondescript of rotatory vertigo, must be taken seriously and thoroughly investigated’.
In this paper, I will revisit the two underrated neuro-otological symptoms which, in Hoffman and Brookler's opinion, relate to the visual system.
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Double vision and skew eye deviation in vestibular disease
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The first neuro-otological visual symptom Hoffman and Brookler
discussed is the vestibular patient who complains of blurred
vision and, in extreme cases, of double vision. Whilst diplopia
should always raise the possibility of brain stem involvement,
Hoffman and Brookler quote Lord Brain's article of 1938
4: ‘it
is important to remember that double vision may occur as a result
of vestibular disorder, lest this symptom should be attributed
to ophthalmoplegia and ascribed to a lesion of the nervous system.
The two images are seen one above the other and the diplopia
is doubtless due to skew deviation of the eyes, a disorder of
ocular posture emanating from the labyrinth and sometimes occurring
transitorily, as Cairns and I have shown after resection of
the auditory nerve.’ I suspect that this statement was
basically ignored for some 40 years, between 1938 and 1978 to
be precise.
The issue has been re-examined by Riordan-Eva et al5 in a robust study including 18 patients who underwent vestibular nerve section for intractable vertigo or acoustic neuroma. Patients were assessed pre- and postoperatively ophthalmologically and with measurements of the subjective visual vertical (i.e. the task of aligning a luminous straight line in the dark to the perceived gravitational vertical). It was found that 5 patients developed an ocular skew deviation (that is, a vertical squint due to a supranuclear, vertical, disconjugate misalignment of the eyes). Only three reported frank diplopia, lasting 1 day to 6 months. There was an association between large changes in ocular torsional position (ocular tilt) and tilts of the visual vertical. In turn, this was associated with lesser degrees of canal paresis on pre-operative caloric assessment. The results indicate that, as expected, the larger the vestibular imbalance produced by the surgery, the larger the tilts in ocular position and, consequently, in subjective visual vertical. They also suggest that the presence of vertical skew deviation is dependent on the presence of a large torsional change. Although prevalent wisdom dictates that such ocular skew and torsional changes are due to the acute asymmetry induced in the otolith control of eye position, alternative sources such as asymmetry in vertical canal function were mentioned.
It may be helpful to examine why the vestibular system needs to be involved in the control of vertical ocular conjugacy in the first place. Figure 1 is taken from the work of Lopez et al6. Imagine that you tilt your head slowly towards your right shoulder. As you do so, you begin to loose good visual contact with the vertically oriented visual world (e.g. try to read this article with your head tilted maximally towards the right or left shoulder). Prima facie, a good compensatory vestibulo-ocular mechanism would be to counter-rotate the eyes conjugately in the opposite direction to the head tilt and to produce a disconjugate skew deviation so that both eyes lie parallel to the horizon as we tilt (see Fig. 1). Although such mechanism is present in animals with laterally placed eyes, like the rabbit, its existence and underlying mechanisms in man are not entirely clear.
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Fig. 1 Diagram showing the compensatory eye movements which could be expected during a right ear down head tilt. The vertical ocular disconjugacy induced is usually called a skew deviation. From Lopez et al6 with permission.
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Lopez
et al6 examined patients with spontaneous torsional nystagmus
and identified the site of lesion in the contralateral vestibular
nuclei, in the pontomedullary junction. In addition to this
topographic finding, the authors examined the physiological
modulation of the nystagmus during predominantly otolith manoeuvres
(static tilt) or predominantly vertical semicircular canal manoeuvres
(head rolling movements;
Fig. 2). Since the nystagmus was mainly
modulated by the latter manoeuvres, the authors concluded that
the pathophysiological basis of torsional nystagmus is a functional
asymmetry in the central projections of the semicircular canal
system. But it was also noted that many of the patients had
ocular skew deviations as well. The presence of skew deviations
in patients with a disorder of the central semicircular canal
system (rather than of the otolithic gravitational system) was
puzzling. For this reason, it was decided to investigate the
normal physiological basis for this phenomenon, namely whether
the normal vertical canal system participates in the control
of ocular vertical alignment.
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Fig. 2 Diagram showing manoeuvres able to induce torsional eye movements and, therefore, capable of modulating a pathological torsional nystagmus. In (A), a simple head tilt to right or left produces a change in the direction of action of the gravitational vector on the otoliths. In (B), the clinical manoeuvre used to induce ocular counter-rolling activates both otolith and vertical semicircular canals; the gymbals system shown in (C) is similar. In (D), only the vertical canals are activated during rotation since the head is not re-oriented with respect to gravity. From Lopez et al6 with permission from Brain.
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In a series of experiments by Jauregui-Renaud
et al7,8, normal
subjects were whole-body rotated in roll (
i.e. about the visual
axis) with the rotational axis placed either earth-horizontal
(subjects upright;
Fig. 2C) or earth-vertical (subjects supine;
Fig. 2D). In the first condition, the compensatory vestibulo-ocular
response is mediated by the otoliths, as they continuously change
orientation with respect to the gravitational field, and by
the semicircular canals. In the second condition, since the
otolith do not undergo re-orientation with respect to gravity,
the response is only mediated by the vertical canals. For these
experiments, eye movements have to be recorded not with electro-oculography
(EOG, ENG) but with techniques able to measure vertical, horizontal
and torsional movements, such as the scleral coil technique
or video-oculography (3-D VOG). The results showed clearly that
a dynamic skew deviation occurs during the roll oscillation
and that there was no difference in the magnitude of the skew
when subjects were oscillated supine or upright. The conclusion
is that the vertical semicircular canal system exerts a dominant
influence on vertical, divergent ocular movements. Therefore,
lesions to this system, central or peripheral, have the potential
to produce pathological skew deviations in man and, consequently,
diplopia. In further studies, it was shown that, during whole
body velocity steps in the roll plane, the magnitude of the
physiological skew deviation decays with a time constant of
approximately 5 s
9. This time constant is identical to the time
constant of the vertical semicircular canal system, measured
by eye movement
9 or psychophysical
10 techniques, further indication
of the prominent role of the vertical canal system in the origin
of the dynamic skew eye deviation.
Returning to ‘under-rated neuro-otological symptoms’, it is clear that double vision can occur in peripheral vestibular disease, as a result of acute disruption to otolith and vertical canal mechanisms controlling vertico-torsional ocular alignment. Good clinical practice still dictates, however, that care should be exercised before attributing diplopia to labyrinthine disease. Furthermore, clinically obvious skew ocular deviations must be considered as secondary to CNS lesions disrupting central otolith and/or vertical canal pathways. In this regard, lesions in the vicinity of the vestibular nuclei in the pontomedullary junction usually produce hypodeviation of the ipsilateral eye (e.g. a left medullary lesion produces a skew eye deviation in which the left eye is lower than the right) and mid-brain lesions induce skew deviations with the ipsilateral eye uppermost11. When this rule of thumb does not explain the clinical findings, other mechanisms may be at work. For instance, patients may have paroxysmal skew deviations due to ‘irritative’ lesions of the brain stem which produce an abnormal increase of activity in saccadic-related areas12. Since the brain stem saccadic centres are also responsible for the generation of the fast phases of nystagmus, such skew deviations can be considered to arise from abnormally overactive quick components of vertico-torsional nystagmus. Also, cerebellar lesions (e.g. in the uvula) can produce disinhibition and instability in the vestibular vertico-torsional system13, leading to paroxysmal nystagmus with skew deviation and disabling oscillopsia (moving images) and diplopia (double vision).
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Visual influences on vestibular symptoms
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The other under-rated visual neuro-otological symptom discussed
by Hoffman and Brookler is exemplified by their ‘case
6’, a woman with a cerebello-pontine angle lesion who
presented with intolerance to visual motion.
Indeed, many patients state that their dizziness or unsteadiness is triggered or increased in surroundings with profuse visual motion or repetitive visual patterns. Patients may dislike traffic, moving crowds, supermarket aisles, watching car chases in movies, ironing striped shirts, or driving on motorways, with many patients displaying several of these triggers. Undoubtedly, in some of these patients the diagnosis is one of anxiety, phobia or panic. But this is not true for all of them, particularly when, as in patient 6 of Hoffman and Brookler, such symptoms develop after a vestibular insult. The origin of these symptoms, termed ‘space and motion discomfort’14, ‘visuo-vestibular mismatch’15, ‘visual vertigo syndrome’16 or ‘motorist disorientation syndrome’17 by different authors, has been recently investigated by Guerraz et al18.
To begin with, it should be remembered that, as soon as the vestibular system is damaged, a neural process of recovery called vestibular compensation gets under way. Guerraz et al18 speculated that, if the process of compensation from vestibular lesions is dependent on alternative sources of sensory information (visual, proprioceptive), individual differences in the functional status of these systems should have a critical influence on the clinical outcome of a vestibular disorder. Since most of these patients do not have clinically obvious visual or somatosensory disorders, Guerraz et al18 explored the possibility that minor idiosyncratic differences present in normal people could be the underlying cause. Specifically, it was decided to investigate if patients with visual vertigo were ‘visually dependent’.
In essence, a visually dependent person is someone who relies more on vision than on gravito-inertial (vestibulo-proprioceptive) cues for spatial orientation. Visually independent people do just the opposite and can quite happily disregard misleading visual information. Visually dependent and independent people represent the two ends of a continuum in the normal population. However, a patient with a vestibular disorder and visual dependency is more likely to be made dizzy by excessive or disorienting visual stimuli than a visually independent subject.
In order to examine the role of visual dependence, a group of patients with dizziness triggered by visual stimuli (visual vertigo) were probed with psychophysical and postural tasks of the type shown in Figure 3. Essentially, the tests measured how much a large field rotating disk (Fig. 3) and a statically tilted luminous frame (not shown) can alter the perception of verticality whilst seated, and postural balance whilst standing up. Questionnaires were used to measure spontaneous dizziness and autonomic symptoms as well as handicap and trait anxiety levels. In addition to visual vertigo patients, two control groups were tested – a normal control group, and a group of bilateral labyrinthine defective subjects with absence of vestibular function. The latter were included as a positive control group since labyrinthine defective subjects are by definition visually dependent.
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Fig. 3 Diagram illustrating the large rotating disk used to destabilise posture, whilst recording head sway with an electro-magnetic device (fastrak) and force platform posturography (Left). The body sway results show sway path expressed as ratios between two conditions in normal control subjects, bilateral labyrinthine defective subjects (LDS) and patients with visually induced dizziness (visual vertigo). The eyes closed/eyes open ratio (EC/EO), or Romberg quotient, represents the stabilising power of vision, i.e. how unstable subjects become with eyes closed relative to eyes in a stationary environment. The Disk/EO ratio indicates how unstable subjects become when viewing the rotating disk in comparison with eyes open in the stationary environment (the destabilising power of vision). Note that the visual vertigo patients are selectively unstable during disk rotation. Reproduced with permission from Current Opinion in Neurology20.
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The main results of this study were: (i) the majority of the
visual vertigo patients were thought to have a peripheral vestibular
disorder; (ii) levels of anxiety were similar in the two patient
groups (visual vertigo and labyrinthine defective); and (iii)
visual vertigo patients had abnormally large perceptual and
postural responses to the tilted frame and the rotating disk,
i.e. they were visually dependent. Furthermore, when the postural
sway induced by the rotating disk was expressed relative to
the static baseline sway, the visual vertigo patients had significantly
larger responses than those in the labyrinthine defective group
(
Fig. 3).
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Conclusions and key points for clinical practice
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- The findings support the view that patients whose dizzy symptoms are precipitated by disorienting visual surroundings are likely to have suffered a vestibular episode and be visually dependent.
- This combination should be highly debilitating for visual vertigo patients in disorienting visual environments when both visual and vestibular signals are unreliable.
- Clinical experience indicates that vestibular rehabilitation including repetitive optokinetic stimulation can be extremely beneficial in these patients. A formal trial has just been completed by Pavlou et al19 with very encouraging results.
- The fact that a patient may have additional anxiety or phobic symptoms should not prompt the clinician to think that all symptoms in that patient are psychological. Not surprisingly, I also agree with Hoffman and Brookler in this matter.
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Footnotes
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Correspondence to: Prof. Adolfo M Bronstein, Academic Department
of Neuro-otology, Division of Neuroscience and Psychological
Medicine, Imperial College Faculty of Medicine, Charing Cross
Hospital, Fulham Palace Road, London W6 8RF, UK
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References
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- Brandt T. Vertigo: Its Multisensory Syndromes, 2nd edn. London: Springer, 1991
- Baloh RW, Honrubia V. Clinical Neurophysiology of the Vestibular System, 3rd edn. London: Oxford University Press 2001
- Hoffman RA, Brookler KH. Underrated neurotological symptoms. Laryngoscope 1978; 88: 1127–38[Web of Science][Medline]
- Brain RW. Vertigo: its neurological, otological, circulatory, and surgical aspects. BMJ 1938; 2: 605[Free Full Text]
- Riordan-Eva P, Harcourt JP, Faldon M, Brookes GB, Gresty MA. Skew deviation following vestibular nerve surgery. Ann Neurol 1997; 41: 94–9[Web of Science][Medline]
- Lopez L, Bronstein AM, Gresty MA, Rudge P, du Boulay EP. A neuro-otological and MRI study of thirty five cases. Brain 1992; 115: 1107–24[Abstract/Free Full Text]
- Jauregui-Renaud K, Faldon M, Clarke A, Bronstein AM, Gresty MA. Skew deviation of the eyes in normal human subjects induced by semicircular canal stimulation. Neurosci Lett 1996; 205: 135–7[Web of Science][Medline]
- Jauregui-Renaud K, Faldon M, Clarke AH, Bronstein AM, Gresty MA. Otolith and semicircular canal contributions to the human binocular response to roll oscillation. Acta Otolaryngol 1998; 118: 170–6[Medline]
- Jauregui-Renaud K, Faldon M, Gresty AM. Horizontal ocular vergence and the three-dimensional response to whole-body roll motion. Exp Brain Res 2001; 136: 79–92[Web of Science][Medline]
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- Bentley CR, Bronstein AM, Faldon M et al. Fast eye movement initiation of ocular torsion in mesodiencephalic lesions. Ann Neurol 1998; 43: 729–37[Web of Science][Medline]
- Radtke A, Bronstein AM, Gresty MA et al. Paroxysmal alternating skew deviation and nystagmus after partial destruction of the uvula. J Neurol Neurosurg Psychiatry 2001; 70: 790–3[Abstract/Free Full Text]
- Furman JM, Jacob RG. A clinical taxonomy of dizziness and anxiety in the otoneurological setting. J Anxiety Disord 2001; 15: 9–26[Web of Science][Medline]
- Longridge NS, Mallinson AI, Denton A. Visual vestibular mismatch in patients treated with intratympanic gentamicin for Menière's disease. J Otol 2002; 31: 5–8
- Bronstein AM. Visual vertigo syndrome: clinical and posturography findings. J Neurol Neurosurg Psychiatry 1995; 59: 472–6[Abstract/Free Full Text]
- Page NG, Gresty MA. Motorist's vestibular disorientation syndrome. J Neurol Neurosurg Psychiatry 1985; 48: 729–35[Abstract/Free Full Text]
- Guerraz M, Yardley L, Bertholon P et al. Visual vertigo: symptom assessment, spatial orientation and postural control. Brain 2001; 124: 1646–56[Abstract/Free Full Text]
- Pavlou M, Lingeswaran A, Davies RA, Gresty MA, Bronstein AM. Machine-based vs. customised rehabilitation for the treatment of chronic vestibular patients. (Abstract Book) Monduzzi Editore. 1st World Congress of the International Society of Physical and Rehabilitation Medicine. 2001; 139
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Abstract
Introduction