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HYPOTHESIS PAPER
WHAT BÁRÁNY’S CALORIC TEST MIGHT
HAVE OVERLOOKED: THE PRIMARY FACTOR
MAY BE THE MIDDLE EAR MUSCLES
1
Eccles Institute of Neuroscience; John Curtin School of Medical Research; The Australian
National University; Canberra, ACT 2601; Australia
A - Research concept and design; B - Collection and/or assembly of data; C - Data analysis and interpretation; D - Writing the article; E - Critical revision of the article; F - Final approval of article;
Publication date: 2019-12-31
Corresponding author
Andrew Bell
Andrew Bell, Eccles Institute of Neuroscience, John Curtin School of Medical Research, The Australian National University, Canberra, ACT 2601, Australia; email: andrew.bell@anu.edu.au
Andrew Bell, Eccles Institute of Neuroscience, John Curtin School of Medical Research, The Australian National University, Canberra, ACT 2601, Australia; email: andrew.bell@anu.edu.au
J Hear Sci 2019;9(4):9-22
KEYWORDS
ABSTRACT
The caloric test of vestibular function, originating from Bárány in the early 1900s, has conventionally been understood as a test of the effect of temperature on the horizontal semicircular canals of the inner ear. Warm water introduced into the external auditory meatus will, if the
vestibular system is intact, cause back-and-forth beating of the eyes (nystagmus) in one direction; cold water will cause beating in the reverse
direction. The text-book explanation is that the eye movements are caused by a thermal gradient across the horizontal canal, which in turn
causes convection in the fluid within. The convective motion stimulates the vestibular hair cells, causing nystagmus, dizziness, nausea, and often vomiting. But here an alternative mechanism is proposed: warm or cold water causes the tensor tympani muscle in the middle ear to increase in tension (warm water) or decrease in tension (cold water), and in this way changes the force exerted by the ossicles on the inner ear
fluids behind the oval window. Altered force on the stapes therefore means a change of hydraulic pressure inside the sealed labyrinth, and
this pressure could directly stimulate hair cells within the inner ear – including the semicircular canals – and so generate nystagmus. If correct, this means the caloric test is really a test of the temperature sensitivity of the middle ear muscles, although the vestibular system still
needs to be intact in order to register a positive response. The new hypothesis explains a range of anomalies surrounding the caloric test, and
these are systematically reviewed.
REFERENCES (101)
1.
Bárány R. Some new methods for functional testing of the vestibular apparatus and the cerebellum. Nobel Lectures, Physiology or Medicine, 1914. Available at https://www.nobelprize.org/pri....
2.
Lorente de No R. Facets of the life and work of Professor Robert Bárány (1886–1936). In: Graham MD, Kemink JL, editors. The Vestibular System: Neurophysiologic and Clinical Research. New York: Raven Press; 1987. p. 1–16.
3.
Stahle J. Controversies on the caloric response: from Bárány’s theory to studies in microgravity. Acta Otolaryngol, 1990; 109: 162–7.
4.
Lopez C, Blanke O. Nobel Prize centenary: Robert Bárány and the vestibular system. Curr Biol, 2014; 24: R1026–R1028.
5.
Cawthorne T, Cobb WA. Temperature changes in the perilymph space in response to caloric stimulation in man. Acta Otolaryngol, 1954; 44: 580–8.
6.
Harrington JW. Caloric stimulation of the labyrinth: experimental observations. Laryngoscope, 1969; 79: 777–93.
7.
Baloh RW. Robert Bárány and the controversy surrounding his discovery of the caloric reaction. Neurology, 2002; 58: 1094–9.
8.
Barin K. Background and technique of caloric testing. In: Jacobson GP, Shepard NT, editors. Balance Function Assessment and Management (2nd ed). San Diego: Plural; 2016. p. 283–317.
9.
Barin K. Interpretation and usefulness of caloric testing. In: Jacobson GP, Shephard NT, editors. Balance Function Assessment and Management (2nd ed). San Diego: Plural; 2016. p. 319–45.
10.
Carpenter D, Kaylie D, Piker E, Frank-Ito D. A pilot study to investigate the relationship between interaural differences in temporal bone anatomy and normal variations in caloric asymmetry. Am J Audiol, 2018; 27: 110–20.
11.
Curthoys IS, Manzari L. Clinical application of the head impulse test of semicircular canal function. Hearing Balance and Communication, 2017; 15: 113–26.
12.
Rambold HA. Testing of the semicircular canal function in vertigo and dizziness. In: Bahmad F, editor. Up to Date on Meniere’s Disease: IntechOpen; 2017. p. 119–35.
14.
O’Neill G. The caloric stimulus: mechanisms of heat transfer. Br J Audiol, 1995; 29: 87–94.
15.
Hill DK. The effect of temperature in the range 0–35° C on the resting tension of frog’s muscle. J Physiol, 1970; 208: 725–39.
16.
Bell A. How do middle ear muscles protect the cochlea? Reconsideration of the intralabyrinthine pressure theory. J Hear Sci, 2011; 1(2): 9–23.
17.
Coats AC, Smith SY. Body position and the intensity of caloric nystagmus. Acta Otolaryngol, 1967; 63: 515–32.
18.
Bell A. Middle ear muscle dysfunction as the cause of Meniere’s disease. J Hear Sci, 2017; 7(3): 9–25.
19.
Bell A. New perspectives on old ideas in hearing science: intralabyrinthine pressure, tenotomy, and resonance. J Hear Sci, 2018; 8(4): 19–25.
20.
Scherer H, Clarke AH. The caloric vestibular reaction in space. Acta Otolaryngol, 1985; 100: 328–36.
21.
Scherer H, Brandt U, Clarke AH, Merbold U, Parker R. European vestibular experiments on the Spacelab-1 mission: 3. Caloric nystagmus in microgravity. Exp Brain Res, 1986; 64: 255–63.
22.
Kassemi M, Oas JG, Deserranno D. Fluid–structural dynamics of ground-based and microgravity caloric tests. J Vestib Res, 2005; 15: 93–107.
23.
Oosterveld WJ, Greven AJ, Gursel AO, De Jong HAA. Caloric vestibular test in the weightless phase of parabolic flight. Acta Otolaryngol, 1985; 99: 571–6.
24.
Bergstedt M. The effect of gravitational force on the vestibular caloric test. Acta Otolaryngol, 1961; 53: 551–62.
25.
Arai Y, Yakushin SB, Cohen B, Suzuki J-I, Raphan T. Spatial orientation of caloric nystagmus in semicircular canal-plugged monkeys. J Neurophysiol, 2002; 88: 914–28.
26.
Kassemi M, Deserranno D, Oas JG. Fluid–structural interactions in the inner ear. Computers & Structures, 2005; 83: 181–9.
27.
Valli P, Buizza A, Botta L, Zucca G, Ghezzi L, Valli S. Convection, buoyancy or endolymph expansion: what is the actual mechanism reponsible for the caloric response of semicircular canals? J Vestib Res, 2002; 12: 155–65.
28.
Rabbitt RD. Semicircular canal biomechanics in health and disease. J Neurophysiol, 2019; 121: 732–55.
29.
McGarvie LA, Curthoys IS, MacDougall HG, Halmagyi GM. What does the dissociation between the results of video head impulse versus caloric testing reveal about the vestibular function in Meniere’s disease? Acta Otolaryngol, 2015; 135: 859–65.
30.
McGarvie LA, Curthoys IS, MacDougall HG, Halmagyi GM. What does the head impulse test versus caloric dissociation reveal about vestibular dysfunction in Meniere’s disease? Ann N Y Acad Sci, 2015; 1343: 58–62.
31.
Feldmann H, Huttenbrink KB, Delank KW. Transport of heat in caloric vestibular stimulation. Conduction, convection or radiation? Acta Otolaryngol, 1991; 111: 169–75.
32.
Nishizawa S. Observations on conduction of caloric stimulation to the middle ear cavity by thermoscanning. Laryngoscope, 2002; 112: 504–8.
33.
Pau HW, Sievert U, Just T, Wild W. Heat radiation during caloric vestibular test: thermographic demonstration in temporal bone experiments. Ann Otol Rhinol Laryngol, 2001; 110: 1041–4.
34.
Myrhaug H. The incidence of ear symptoms in cases of malocclusion and temporo-mandibular joint disturbances. Br J Oral Surg, 1964; 2: 28–32.
35.
Baumgarten Rv, Benson A, Berthoz A, Brandt T, Brand U, Bruzek W, et al. Effects of rectilinear acceleration and optokinetic and caloric stimulations in space. Science, 1984; 225: 208–12.
36.
O’Neill G. The influence of temporal bone anatomical variation upon the caloric stimulus. Clin Otolaryngol, 1987; 12: 277–82.
37.
McLeod ME, Meek JC. A threshold caloric test: results in normal subjects. Pensacola, FL: NASA R-47; 1962.
38.
Jongkees LBW. The caloric test and its value in evaluation of the patient with vertigo. Otolaryngol Clin North Am, 1973; 6: 73–93.
39.
Ifediba MA, Rajguru SM, Hullar TE, Rabbitt RD. The role of 3-canal biomechanics in angular motion transduction by the human vestibular labyrinth. Ann Biomed Eng, 2007; 35: 1247–63.
40.
Rabbitt RD, Boyle R, Highstein SM. Sensory transduction of head velocity and acceleration in the toadfish horizontal semicircular canal. J Neurophysiol, 1994; 72: 1041–8.
41.
Yamauchi A, Rabbitt RD, Boyle R, Highstein SM. Relationship between inner-ear fluid pressure and semicircular canal afferent nerve discharge. J Assoc Res Otolaryngol, 2001; 3: 26–44.
42.
Iversen MM, Rabbitt RD. Wave mechanics of the vestibular semicircular canals. Biophys J, 2017; 113: 1133–49.
43.
Shen S, Liu Y-W, Sun X-M, Zhao W, Su Y, Yu S, et al. A biomechanical model of the inner ear: numerical simulation of the caloric test. Scientific World Journal, 2013; 2013: e160205.
44.
Zangemeister WH, Bock O. The influence of pneumatization of mastoid bone on caloric nystagmus response. Acta Otolaryngol, 1979; 88: 105–9.
45.
Patki AU, Ronen O, Kaylie DM, Frank-Ito DO, Piker EG. Anatomic variations in temporal bones affect the intensity of nystagmus during warm caloric irrigation. Otol Neurotol, 2016; 37: 1111–6.
46.
Longridge NS, Mallinson AI, Pothier DD. Development and understanding of caloric responses: an overview of the first hundred years. J Otolaryngol ENT Res, 2015; 3(2): e00056.
47.
Jongkees LBW. Origin of the caloric reaction of the labyrinth. Arch Otolaryngol, 1948; 48: 645–57.
48.
Borries GVT. Studies on normal caloric nystagmus. Acta Otolaryngol, 1922; 4: 8-20.
49.
Schubert MC, Shepard NT. Practical anatomy and physiology of the vestibular system. In: Jacobson GP, Shepard NT, editors. Balance Function Assessment and Management. San Diego: Plural; 2016. p. 1–16.
50.
Coupland ME, Ranatunga KW. Force generation induced by rapid temperature jumps in intact mammalian (rat) skeletal muscle fibres. J Physiol, 2003; 548.2: 439–49.
51.
Ranatunga KW, Offer G. The force-generation process in active muscle is strain sensitive and endothermic: a temperatureperturbation study. J Exp Biol, 2017; 220: 4733–42.
52.
Ranatunga KW. Temperature effects on force and actin–myosin interaction in muscle: a look back on some experimental findings. Int J Mol Sci, 2018; 19: e1538.
53.
Offer G, Ranatunga KW. The endothermic ATP hydrolysis and crossbridge attachment steps drive the increase of force with temperature in isometric and shortening muscle. J Physiol, 2015; 593.8: 1997–2016.
54.
Ranatunga KW, Sharpe B, Turnbull B. Contractions of a human skeletal muscle at different temperatures. J Physiol, 1987; 390: 383–95.
55.
Bell A. A fast, “zero synapse” acoustic reflex: middle ear muscles physically sense eardrum vibration. J Hear Sci, 2017; 7(4): 33–44.
56.
Josephson EM. Spasm of the auditory accommodative mechanism: a functional basis of ear-drum retraction and of deafness for low tones. Arch Otolaryngol Head Neck Surg, 1931; 13: 166–9.
57.
Bance M, Mai M, Tomlinson D, Rutka J. The changing direction of nystagmus in acute Meniere’s disease: pathophysiological implications. Laryngoscope, 1991; 101: 197–201.
58.
West R, Barlow RA. The neuromuscular mechanism of hearing. Arch Otolaryngol, 1929; 9: 645–53.
59.
Bance M, Makki FM, Garland P, Alian WA, van Wijhe RG, Savage J. Effects of tensor tympani muscle contraction on the middle ear and markers of a contracted muscle. Laryngoscope, 2013; 123: 1021–7.
60.
Düwel P, Jüngling E, Westhofen M, Lückhoff A. Potassium currents in vestibular type II hair cells activated by hydrostatic pressure. Neuroscience, 2003; 116: 963–72.
61.
Bento RF, Fonseca ACO. A brief history of mastoidectomy. Int Arch Otorhinolaryngol, 2013; 17: 168–78.
62.
McKenzie W. Vertigo after radical mastoidectomy. J Laryngol Otol. 1949; 63: 511–9.
63.
Klockhoff I. Middle ear muscle reflex tests for otologic diagnosis. Trans Am Acad Ophthalmol Otolaryngol, 1963; 67: 777–84.
64.
Klockhoff I. Impedance fluctuation and a “tensor tympani syndrome”. Fourth International Symposium on Acoustic Impedance Measurements; 1981; Lisbon: Universidade Nova de Lisboa.
65.
Klockhoff I, Anderson H. Reflex activity in the tensor tympani muscle recorded in man: preliminary report. Acta Otolaryngol, 1960; 51: 184–8.
66.
Westcott M, Sanchez TG, Diges I, Saba C, Dineen R, McNeill C, et al. Tonic tensor tympani syndrome in tinnitus and hyperacusis patients: a multi-clinic prevalence study. Noise Health, 2013; 15: 117–28.
67.
Downs DW, Crum MA. The hyperactive acoustic reflex. Arch Otolaryngol. 1980; 106: 401–4.
68.
Gurkov R, Pyyko I, Zou J, Kentala E. What is Meniere’s disease? A contemporary re-evaluation of endolymphatic hydrops. J Neurol, 2016; 263: S71–S81.
69.
McCaslin DL, Rivas A, Jacobson GP, Bennett ML. The dissociation of video head impulse test (vHIT) and bithermal caloric test results provide topological localization of vestibular system impairment in patients with “definite” Meniere’s disease. Am J Audiol, 2015; 24(3): 1–10.
70.
Park HJ, Migliaccio AA, Della Santina CC, Minor LB, Carey JP. Search-coil head-thrust and caloric tests in Meniere’s disease. Acta Otolaryngol, 2005; 125: 852–7.
71.
Lee S-U, Kim H-J, Koo J-W, Kim J-S. Comparison and caloric and head-impulse tests during the attacks of Meniere’s disease. Laryngoscope, 2017; 127: 702–8.
72.
Agrawal Y, Minor LB. Physiologic effects on the vestibular system in Meniere’s disease. Otolaryngol Clin North Am, 2010; 43: 985–93.
73.
Loader B, Beicht D, Hamzavi J-S, Franz P. Tenotomy of the middle ear muscles causes a dramatic reduction in vertigo attacks and improves audiological function in definite Meniere’s disease. Acta Otolaryngol, 2012; 132: 491–7.
74.
Reichmayr C, Sterrer E, Bachtiar A, Layr M, Loader B. Tenotomy of the middle ear muscles. Wien Klin Wochenschr, 2019; 131: 87–91.
75.
Trevino Gonzalez JL, Rios YH. Meniere’s disease. Annals Clin Cytol Pathol, 2016; 2: e1044.
76.
Baumgarten Rv, Boehmer G, Brenske A, Reiser M. A nonthermoconvective mechanism generating caloric nystagmus: similarities between pressure-induced and caloric nystagmus in the pigeon. In: Graham MD, Kemink JL, editors. The Vestibular System: Neurophysiologic and Clinical Research. New York: Raven Press; 1987. p. 51–9.
77.
Ingelstedt S, Ivarsson A, Tjernström Ö. Vertigo due to relative overpressure in the middle ear. Acta Otolaryngol, 1974; 78: 1–14.
78.
Saxena RK, Tandon PN, Sinha A, Kacker SK. Auditory functions in raised intracranial pressure. Acta Otolaryngol, 1969; 68: 402–10.
79.
Marchbanks RJ, Reid A. Cochlear and cerebrospinal fluid pressure: their inter-relationship and control mechanisms. Br J Audiol, 1990; 24: 179–87.
80.
Büki B, Chomicki A, Dordain M, Lemaire JJ, Wit HP, Chazal J, et al. Middle-ear influence on otoacoustic emissions. II: contributions of posture and intracranial pressure. Hear Res, 2000; 140: 202–11.
81.
Parker DE, Tjernström Ö, Ivarsson A, Gulledge WL, Poston RL. Physiological and behavioral effects of tilt-induced body fluid shifts. Aviat Space Environ Med, 1983; 54: 402–9.
82.
de Kleine E, Wit HP, Avan P, van Dijk P. The behavior of evoked otoacoustic emissions during and after postural changes. J Acoust Soc Am, 2001; 110: 973–80.
83.
de Kleine E, Wit HP, Van Dijk P, Avan P. The behavior of spontaneous otoacoustic emissions during and after postural changes. J Acoust Soc Am, 2000; 107: 3308–16.
84.
Büki B, Avan P, Lemaire JJ, Dordain M, Chazal J, Ribári O. Otoacoustic emissions: a new tool for monitoring intracranial pressure changes through stapes displacements. Hear Res, 1996; 94: 125–39.
85.
Büki B, de Kleine E, Wit HP, Avan P. Detection of intracochlear and intracranial pressure changes with otoacoustic emissions: a gerbil model. Hear Res, 2002; 167: 180–91.
86.
Avan P, Büki B, Maat B, Dordain M, Wit HP. Middle ear influence on otoacoustic emissions. I. Noninvasive investigation of the human transmission apparatus and comparison with model results. Hear Res, 2000; 140: 189–201.
87.
Avan P, Giraudet F, Chauveau B, Gilain L, Mom T. Unstable distortion-product otoacoustic emission phase in Meniere’s disease. Hear Res, 2011; 277: 88–95.
88.
Parker DE, Tubbs RL, Ritz LA, Wood DL. Effects of Sound on the Vestibular System. Ohio: Aerospace Medical Research Laboratory; 1976.
89.
Parker DE, Reschke MF. Mechanisms of acoustical vestibular stimulation. Minerva Otorinolaringol, 1972; 22: 240–9.
90.
Reschke MF, Homick J, Landreth J. Acoustical vestibular stimulation in man. Minerva Otorinolaringol, 1974; 24: 253–60.
91.
Kwee HL. The occurrence of the Tullio phenomenon in congenitally deaf children. J Laryngol Otol, 1976; 90: 501–7.
92.
Erlich MA, Lawson W. The incidence and significance of the Tullio phenomenon in man. Otolaryngol Head Neck Surg, 1980; 88: 630–5.
93.
Ades HW, Graybiel A, Morrill SN, Tolhurst GC, Niven JI. Non-auditory effects of high intensity sound stimulation on deaf human subjects. Aviation Medicine, 1958; 29: 454–67.
94.
Rosengren SM, Kingma H. New perspectives on vestibular evoked myogenic potentials. Curr Opin Neurol, 2013; 26: 74–80.
95.
Timmer FCA, Zhou G, Guinan JJ, Kujawa SG, Herrmann BS, Rauch SD. Vestibular evoked myogenic potential (VEMP) in patients with Meniere’s disease with drop attacks. Laryngoscope, 2006; 116: 776–9.
96.
Böhmer A, Dillier N. Experimental endolymphatic hydrops: are cochlear and vestibular symptoms caused by increased endolymphatic pressure? Ann Otol Rhinol Laryngol, 1990; 99: 470–6.
97.
Oman CM, Young LR. The physiological range of pressure difference and cupula deflections in the human semicircular canal. Acta Otolaryngol, 1972; 74: 324–31.
98.
Bell A. Detection without deflection? A hypothesis for direct sensing of sound pressure by hair cells. J Biosci, 2007; 32: 385–404.
99.
Bell A. The pipe and the pinwheel: is pressure an effective stimulus for the 9+0 primary cilium? Cell Biol Int, 2008; 32: 462–8.
100.
Kondrachuk AV, Boyle R. Intralabyrinthine pressure and function of cupula–endolymphatic system. Life in Space for Life on Earth Symposium; 22–27 June 2008; Angers, France, 2008.
101.
Kachar B, Parakkal M, Fex J. Structural basis for mechanical transduction in the frog vestibular sensory apparatus: I. The otolithic membrane. Hear Res, 1990; 45: 179–90.
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