Readaptation of the vestibulo-ocular reflex relieves the mal de debarquement syndrome

Mingjia Dai, Bernard Cohen, Eric Smouha, Catherine Cho, Mingjia Dai, Bernard Cohen, Eric Smouha, Catherine Cho

Abstract

The mal de debarquement syndrome (MdDS), a continuous feeling of swaying, rocking, and/or bobbing, generally follows travel on the sea. The associated symptoms cause considerable distress. The underlying neural mechanisms are unknown, and to date there have been no effective treatments for this condition. Results in monkeys and humans suggested that MdDS was caused by maladaptation of the vestibulo-ocular reflex (VOR) to roll of the head during rotation. We studied 24 subjects with persistent MdDS (3 males, 21 females; 19.1 ± 33 months). Physical findings included body oscillation at 0.2 Hz, oscillating vertical nystagmus when the head was rolled from side-to-side in darkness, and unilateral rotation during the Fukuda stepping test. We posited that the maladapted rocking and the physical symptoms could be diminished or extinguished by readapting the VOR. Subjects were treated by rolling the head from side-to-side while watching a rotating full-field visual stimulus. Seventeen of the 24 subjects had a complete or substantial recovery on average for approximately 1 year. Six were initially better, but the symptoms recurred. One subject did not respond to treatment. Thus, readaptation of the VOR has led to a cure or substantial improvement in 70% of the subjects with MdDS. We conclude that the adaptive processes associated with roll-while-rotating are responsible for producing MdDS, and that the symptoms can be reduced or resolved by readapting the VOR.

Keywords: Fukuda stepping test; bobbing; optokinetic; posturography; rocking; swaying; velocity storage.

Figures

Figure 1
Figure 1
Schematic diagram of the treatment paradigm. The subject’s head was passively rolled at her rocking frequency while watching the stripes moving to the left to act against the maladapted VOR component to the right. H is the velocity of the horizontal optokinetic stimulus; V is the component of the optokinetic stimulus in the head sagittal plane; P represents the maladapted vertical component; Head positions: A, on the left, B, in the center, and C, on the right. Arrows show the direction of the horizontal and vertical slow phase velocity.
Figure 2
Figure 2
(A) Posturographic recordings of body rocking, and (B) recordings of arm movements at the perceived frequency of rocking. Both body movement and arm movement were at the same frequency of about 0.2 Hz.
Figure 3
Figure 3
Vertical (pitch) eye position (C) and velocity (B) induced by head roll (A) at about 0.2 Hz in darkness. (B) The dark traces show the slow phase eye velocity and the gray traces the quick phases, blinks and fluttering of the eyelid. The peak velocity of the vertical eye oscillations was about ±4°/s estimated by a sine function approximation. The vertical dash line shows the relationship between the head position in roll and slow phase vertical eye velocity and position. The slow phase eye velocity was upward when the head was rolled to the right and down when the head was rolled to the left.
Figure 4
Figure 4
Measurement of the displacement of center of pressure (COP) before (red traces) and after treatment (blue traces) for rocking and swaying with posturography in two subjects. Subject A had both rocking and swaying whereas subject B mainly had rocking. After treatment, the rhythmic oscillations present before the treatment disappeared.

References

    1. Darwin E. Zoonomia. London: J. Johnson; (1796).
    1. Gordon CR, Spitzer O, Shupak A, Doweck I. Survey of mal de debarquement. BMJ (1992) 304:544.10.1136/bmj.304.6826.544
    1. Brown JJ, Baloh RW. Persistent mal de debarquement syndrome: a motion-induced subjective disorder of balance. Am J Otolaryngol (1987) 8:219–2210.1016/S0196-0709(87)80007-8
    1. Cha YH, Brodsky J, Ishiyama G, Sabatti C, Baloh RW. Clinical features and associated syndromes of mal de debarquement. J Neurol (2008) 255:1038–4410.1007/s00415-008-0837-3
    1. Cha YH. Mal de debarquement. Semin Neurol (2009) 29:520–7
    1. Hain TC, Hanna PA, Rheinberger MA. Mal de debarquement. Arch Otolaryngol Head Neck Surg (1999) 125:615–2010.1001/archotol.125.6.615
    1. Dai M, Raphan T, Cohen B. Adaptation of the angular vestibulo-ocular reflex to head movements in rotating frames of reference. Exp Brain Res (2009) 195:553–6710.1007/s00221-009-1825-2
    1. Raphan T, Matsuo V, Cohen B. Velocity storage in the vestibulo-ocular reflex arc (VOR). Exp Brain Res (1979) 35:229–4810.1007/BF00236613
    1. Cohen B, Helwig D, Raphan T. Baclofen and velocity storage: a model of the effects of the drug on the vestibulo-ocular reflex in the rhesus monkey. J Physiol (1987) 393:703–25
    1. Guedry FE, Jr, Graybiel A. Compensatory nystagmus conditioned during adaptation to living in a rotating room. J Appl Physiol (1962) 17:398–404
    1. Bonanni M, Newton R. Test-retest reliability of the Fukuda stepping test. Physiother Res Int (1998) 3:58–6810.1002/pri.122
    1. Brandt T, Krafczyk S, Malsbenden I. Postural imbalance with head extension: improvement by training as a model for ataxia therapy. Ann N Y Acad Sci (1981) 374:636–4910.1111/j.1749-6632.1981.tb30907.x
    1. Demura S, Kitabayashi T, Noda M. Power spectrum characteristics of sway position and velocity of the center of pressure during static upright posture for healthy people. Percept Mot Skills (2008) 106:307–1610.2466/pms.106.1.307-316
    1. Schmitke RT. Ship sway, roll, and yaw motions in oblique seas. SNAME Transactions. The Society of Naval Architects & Marine Engineers; (1978). p. 26–46
    1. Anderson J. Fundamentals of Aerodynamics. McGraw-Hill; (2011).
    1. Raphan T, Cohen B. The vestibulo-ocular reflex (VOR) in three dimensions. Exp Brain Res (2002) 145:1–2710.1007/s00221-002-1067-z
    1. Dichgans J. Circularvektion, optiche pseudo-coriolis effekte und optokinetischer nachnystagmus:Eine vergleichede untersuchung subjectiver und objectiver optokinetischer nacheffekte. Albrecht Von Graefes Arch Klin Exp Ophthalmol (1972) 184:42–5710.1007/BF00410494
    1. Zee DS, Yee RD, Robinson DA. Optokinetic responses in labyrinthine-defective human beings. Brain Res (1976) 113:423–810.1016/0006-8993(76)90955-0
    1. Maekawa K, Simpson JA. Climbing fiber responses evoked in the vestibulo-cerebellum of rabbit from visual system. J Neurophysiol (1973) 36:649–66
    1. Yakushin SB, Gizzi M, Reisine H, Raphan T, Buttner-Ennever J, Cohen B. Functions of the nucleus of the optic tract (NOT). II. Control of ocular pursuit. Exp Brain Res (2000) 131:416–3210.1007/s002219900302
    1. Llinas RR. Inferior olive oscillation as the temporal basis for motricity and oscillatory reset as the basis for motor error correction. Neuroscience (2009) 162:797–80410.1016/j.neuroscience.2009.04.045
    1. Marsh E, Baker R. Normal and adapted visuooculomotor reflexes in goldfish. J Neurophysiol (1997) 77:1099–118

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