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Brain 2005 128(7):1475-1477; doi:10.1093/brain/awh566
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© The Author (2005). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For Permissions, please email: journals.permissions@oupjournals.org

From the Archives

Studies in human vestibular function: I. Observations on the directional preponderance of caloric nystagmus (‘nystagmusbereitschaft’) resulting from cerebral lesions. II. Observations on the directional preponderance of caloric nystagmus (‘nystagmus-bereitschaft’) resulting from unilateral labyrinthectomy. III. Observations on the clinical features of ‘Ménière's’ disease: with especial reference to the results of the caloric tests. By Gerald Fitzgerald and C. S. Hallpike (I); T. E. Cawthorne, Gerald Fitzgerald and C. S. Hallpike (II and III), Research Unit, National Hospital, Queen Square, London. Brain 1942; 65: 115–37, 138–60 and 161–80.

Three papers from Dr Charles Hallpike, Sir Terence Cawthorne and a young research fellow, Dr Gerald Fitzgerald, illuminated the neurology of giddiness and allowed measurement of the human vestibular system to become routine clinical practice in the 1940s. Paper I explains the standardized techniques and describes observations in the clinical setting of cerebral lesions. Paper II addresses the neuro-otology of peripheral and brainstem connections of the vestibular system and offers a fresh analysis of the functional neuroanatomy of their circuits. Paper III reconsiders the problem of Ménière's disease in the light of these discoveries, based on meticulous analysis of 50 cases attending the National Hospital, Queen Square, London.

Fitzgerald and Hallpike start from the positionxs that experimental removal of one cerebral hemisphere increases sensitivity of the ipsilateral labyrinth both to rotation and direct stimulation using hot water calorics, but with a different effect for cold water. They suggest that cerebral lesions result in central facilitation of induced labyrinthine nystagmus in a particular direction. The authors trace the development of caloric testing from original observations by R. Bárány (Arch Ohrenheilk 1906; 68: 1–30), who noted the reversal of direction dependent on head position and the effect of water temperature on the induced nystagmus. Fitzgerald and Hallpike made technical modifications aimed at restricting stimulation to one semicircular canal within each labyrinth: water at 30°C and 44°C; 8 ozs delivered from a 2 pint douche can through rubber tubing to the posterior wall of the external auditory meatus at a pressure of 2 ft H2O through a 4 mm nozzle over 40 s, each procedure taking around 4 min to complete; two tests at each temperature with a ‘washout’ period between hot and cold of 5 min; and nystagmus observed in the straight ahead position with the patient supine and the head at 30°, without Bartels glasses. Normally, the responses last ~1.3–2.1 min, cold water producing nystagmus of slightly longer duration than hot. Directional preponderance is usually indicated by two independent but complementary clues, each provided by the reactions of each ear. Canal paresis describes a disturbance in relationship of the cold hot reactions from one ear. More complex abnormalities reflect the combination of directional preponderance and canal paresis (see Figures). In 20 patients with cerebral hemisphere lesions, Fitzgerald and Hallpike show an absolute correlation between directional preponderance and the presence of a temporal lobe lesion (10 cases). There are no exceptions.



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Fig. 1 (A) The normal caloric response to cold (30°C) and hot (44°C) water: each line represents 3 min divided into 1 min, 20 and 10 s intervals. The dashed arrows indicate the direction and duration of the nystagmus observed in the left eye and right eye, respectively. (B) Directional preponderance to the right and left. (C) Canal paresis to the left and right. (D) Compensation of canal paresis following labyrinthectomy: before the procedure, and after 3 and 30 weeks. (E) Combined right utricular and right canal paresis (without dominance). (F) The vestibular system: one eye is shown (for convenience) innervated by the oculomotor nerve nuclei (O.N.); these are connected to the vestibular nuclei (V.N.), which are, in turn, influenced by the labyrinth (L) and the temporal lobes (T.L.).

 
Cawthorne, Fitzgerald and Hallpike start their discussion of directional preponderance in paper II by reminding readers that the effects of unilateral labyrinthectomy differ experimentally from those seen in the clinical setting, perhaps as a result of chronicity and compensation. Nystagmus occurs to the opposite side in both situations, but rotation of the head and neck brings the normal labyrinth uppermost in experimental animals and the affected organ uppermost in man. The authors set out to reconcile these discrepancies by observations in nine individuals undergoing surgical destruction of the labyrinth for Ménière's disease, thus combining acute destruction with chronic adaptive change. Preoperatively, seven had canal paresis and two showed directional preponderance towards the better ear. Postoperatively, for around 1 week, all nine lay with the affected ear uppermost and showed nystagmus to the opposite side. Thereafter, the intact ear showed an exaggerated hot and a diminished cold water caloric response. This resolved partially over the following 17 months. Thus, unilateral labyrinthectomy produced or enhanced pre-existing directional preponderance. Bárány based his analysis of functional vestibular neuroanatomy on J. R. Ewald's law (Physiologische Untersuchungen über das Endorgan des Nervus octavus. Wiesbaden; 1892); this stated that endolymph sensitivity of the cupula lying within the external canal is unidirectional and larger with ampullopetal than ampullofugal flow. But, here, Dr Hallpike's team hit a problem. According to Ewald, hot water calorics stimulate ampullopetal flow and should generate a larger response than ampullofugal stimulation of cold water. But the opposite was observed. Because the cases had been studied before and after vestibular destruction, more confidence was placed in the clinical observations than in Ewald's theory. Therefore, sensitivity of the human ear is normally bidirectional but becomes unidirectional after labyrinth destruction until the central connections compensate. A. Högyes had suggested that, in labyrinthine disease, ipsilateral tonic effects are lost, leading to facilitation of impulses emanating from the opposite vestibular apparatus and its central connections (Uber den Nervenmechanismus der assoziierten Augenbewegungen; 1881. Translated by M. Súgar. Berlin: Urban and Schwarzenberg; 1913. p. 134). W. Bechterew's observations on cases with different intervals between unilateral and bilateral vestibular destruction helped in understanding the nature of compensation (Archiv für die gesammte Physiologie des Menschen und der Thiere 1883; 30: 312–47): the initial loss of stimulation is followed by increased sensitivity of the deafferented vestibular nuclei, so that the subsequent contralateral lesion creates a new imbalance not seen when bilateral labyrinthectomy is carried out simultaneously. For Cawthorne and colleagues, vestibular function involves phasic signals from the utricle resulting from rotational or thermal stimuli; and the major supranuclear influence is from the temporal lobes, the ‘vestibular cortex’.

Thus far, Charles Hallpike and colleagues had explored the properties of cerebral and destructive labyrinthine lesions. Utricular damage alone produced directional preponderance, whereas canal paresis abolished both the hot and cold water responses. But what would happen if these occurred together, and in various combinations from the two sides? In paper III, the authors start by reminding readers that the patient described by Ménière (1861) died within 3 days of onset and most certainly did not have Ménière's disease (Gaz Méd Paris 1861; 16: 597–601). Subsequent working clinical definitions and pathological data allowed consensus among clinicians that a disorder characterized by intermittent vertigo, deafness and tinnitus was associated `with extreme dilation of the endolymph system ... a distended saccule filling the cavity of the vestibule ... Reissner's membrane thrown back upon the bony wall of the scala vestibule and protruded through the helicotrema with obliteration of the perilymph spaces'. Therefore, their concept was strictly mechanical with no contribution from the inflammation that had confounded the original case series of suppurative middle ear disease. Hallpike and colleagues describe 50 cases: 43 had bilateral cochlear deficits and 47 abnormal calorics; 35 were deaf and had ipsilateral defects of vestibular function; 5 had crossed abnormalities of cochlear function and caloric responses; 7 had normal hearing but abnormal calorics; 3 were deaf but had normal vestibular function. The Rinné and Weber tests indicated conductive deafness. Audiometry showed high tone hearing loss. The response to labyrinthectomy was better than the use of phenobarbital (8/9 versus 19/24). Turning to details of the caloric responses, 10 had unilateral utricular lesions (directional preponderance), 29 had canal paresis and 8 had both—either showing equivalent derangements or an emphasis of canal paresis. But more detailed scrutiny led the authors to propose that for ‘unilateral’ one should read ‘bilateral with unilateral preponderance’; Ménière's disease is a bilateral but asymmetric disorder, thus accounting for the occasional combination of cochlear and vestibular defects on opposite sides. Cawthorne, Fitzgerald and Hallpike firmly tilted wavering ideas on Ménière's disease as a brain disorder towards a seat in the vestibular apparatus: ‘in the majority of cases of Ménière's disease there occurs a lesion of the external canal without utricular involvement. In a considerable number (about 20 percent), utricular paresis occurs alone, and nearly as often in combination with a paresis of the external canal’. Thus, measurement of a complex neuroanatomical system had achieved a new synthesis and informed the nature of giddiness—a symptom equally ominous for sufferers and those asked to manage the complaint.

Alastair Compston

Cambridge, UK


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