Skip to main content
Log in

Linear acceleration perception in the roll plane before and after unilateral vestibular neurectomy

  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Summary

The ability of 33 patients to perceive the direction, relative to the body long axis, of a linear acceleration vector acting in the coronal plane, rolltilt perception, was studied at various times, before and from 1 week to 6 months after unilateral, selective vestibular neurectomy for Meniere's disease, acoustic neuroma or intractable paroxysmal vertigo. The results of these patients were compared with the results of 31 normal subjects and two control patients who had both vestibular nerves surgically sectioned. Rotating on a fixed-chair centrifuge in an otherwise darkened room, each observer was required to indicate his perception of the direction of the resultant gravito-inertial vector by setting a small, motor-driven, illuminated bar, attached to the chair but rotatable in the frontoparallel plane, to the perceived gravitational horizontal. Normal subjects accurately align the bar with respect to the gravito-inertial resultant vector which, in the dark, they assume to be the gravitational vertical. This percept has been called the oculogravic illusion. Accurate roll-tilt perception is due to vestibular (probably mainly otolithic) sensory information since patients with bilateral vestibular neurectomies do not perceive the resultant vector accurately. Whereas normal subjects perceive resultant vectors directed to the right and to the left equally accurately, roll-tilt perception was invariably asymmetrical one week after unilateral vestibular neurectomy. Even at rest there was an asymmetry in the baseline settings, so that patients set the bar down on the side of the operated ear, in order for it to appear gravitationally horizontal: if a patient had a right vestibular nerve section then he set the bar clockwise (from the patient's view) below the true gravitational horizontal. With increasing gravitoinertial resultant angles there was an increasing asymmetry of roll-tilt perception due both to decreased sensitivity to roll-tilt stimuli directed towards the operated ear and to transiently increased sensitivity to roll-tilt stimuli directed towards the intact ear. A progressive decrease in both perceptual asymmetries followed, rapidly in the first 3 weeks, more slowly in the next 6 months. Based on these results, which are consistent with what is known about the responses of primary and secondary otolithic neurons to linear acceleration, we propose: (1) that the asymmetric roll-tilt perceptual response following unilateral vestibular neurectomy is an otolithic analogue of Ewald's second law; (2) that the perceptual asymmetries may be due to decreased spontaneous activity in the deafferented lateral vestibular nucleus; (3) that the progressive recovery of roll-tilt perceptual symmetry after vestibular neurectomy may be part of the otolithic component of the total recovery phenomenon known as vestibular compensation; (4) that ocular torsion caused by the unilateral vestibular neurectomy is a major factor contributing to the systematic errors in baseline settings to the gravitational horizontal one week after operation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Baloh RW, Honrubia V, Konrad, HR (1977) Ewald's second law re-evaluated. Acta Otolaryngol 83: 475–479

    Google Scholar 

  • Brandt T, Dieterich M (1987) Pathological eye-head coordination in roll: tonic ocular tilt reaction in mesencephalic and medullary lesions. Brain 110: 649–666

    Google Scholar 

  • Clark B (1967) The oculogravic illusion as a test of otolith function. Third Symposium on the role of the vestibular organs in space exploration. U.S. Naval Aerospace Medical Institute, Pensacola

    Google Scholar 

  • Clark B Graybiel A (1951) Visual perception of the horizontal following exposure to radial acceleration on a centrifuge. J Comp Physiol Psychol 44: 525–534

    Google Scholar 

  • Clark B, Graybiel A (1962) Visual perception of the horizontal during prolonged exposure to radial acceleration on a centrifuge. J Exp Psychol 63: 294–301

    Google Scholar 

  • Clark B, Graybiel A (1963) Perception of the postural vertical in normals and subjects with labyrinthine defects. J Exp Psychol 65: 490–494

    Google Scholar 

  • Clark B, Graybiel A (1964) Perception of the postural vertical following prolonged bodily tilt in normals and subjects with labyrinthine defects. Acta Otolaryngol 58: 143–148

    Google Scholar 

  • Clark B, Graybiel A (1966a) Factors contributing to the delay in the perception of the oculogravic illusion. Am J Psychol 79: 377–388

    Google Scholar 

  • Clark B, Graybiel A (1966b) Perception of the visual horizontal in normal and labyrinthine defective observers during prolonged rotation. Am J Psychol 79: 608–612

    Google Scholar 

  • Clark B, Graybiel A (1967) Egocentric localization of the visual horizontal in normal and labyrinthine-defective observers as a function of head an body tilt. Percept Psychophys 2: 609–611

    Google Scholar 

  • Cremer P, Henderson C, Curthoys I, Halmagyi G (1987) Horizontal vestibulo-ocular reflexes in humans with only one horizontal canal. Adv Oto-Rhino-Laryngol 42: 180–184

    Google Scholar 

  • Dai MJ, Curthoys IS, Halmagyi GM (1988) A model of otolith stimulation. Biol Cybern (in press)

  • Day RH, Wade NJ (1966) Visual spatial after effect from prolonged head-tilt. Science 154: 1201–1202

    Google Scholar 

  • Diamond SG, Markham CH (1981) Binocular counterrolling in humans with unilateral labyrinthectomy and in normal controls. Ann NY Acad Sci 374: 69–79

    Google Scholar 

  • Diamond SG, Markham CH (1983) Ocular counterrolling as an indicator of vestibular otolith function. Neurology 33: 1460–1469

    Google Scholar 

  • Dichgans J, Diener HC, Brandt Th (1974) Optokinetic-graviceptive interaction in different head positions. Acta Otolaryngol 78: 391–398

    Google Scholar 

  • Ewald EJR (1892) Physiologische Untersuchungen über das Endorgan des Nervus octavus. Bergmann, Wiesbaden (as quoted by Baloh et al. 1977)

    Google Scholar 

  • Fernandez C, Goldberg JM (1976a) Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. I. Response to static tilts and to long-duration centrifugal force. J Neurophysiol 39: 970–984

    Google Scholar 

  • Fernandez C, Goldberg JM (1976b) Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. II. Directional selectivity and force-response relations. J Neurophysiol 39: 985–95

    Google Scholar 

  • Fetter M, Zee DS (1988) Recovery from unilateral labyrinthectomy in monkeys. J Neurophysiol 59: 370–393

    Google Scholar 

  • Fisch U (1973) The vestibular response following unilateral vestibular neurectomy. Acta Otolaryngol 76: 229–238

    Google Scholar 

  • Flock, A (1964) Structure of the macula utriculi with special reference to directional interplay of sensory responses as revealed by morphological polarization. J Cell Biol 22: 413–431

    Google Scholar 

  • Friedmann G (1970) The judgement of the visual vertical and horizontal with peripheral and central vestibular lesions. Brain 93: 313–328

    Google Scholar 

  • Friedmann G (1971) The influence of unilateral labyrinthectomy on orientation in space. Acta Otolaryngol 71: 289–298

    Google Scholar 

  • Goldberg JM, Fernandez C (1971) Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. I. Resting discharge and response to constant angular accelerations. J Neurophysiol 34: 635–660

    Google Scholar 

  • Graybiel A (1952) The oculogravic illusion. Arch Ophthalmol 48: 605–615

    Google Scholar 

  • Graybiel A (1956) The importance of the otolithic organs in man based on a specific test for utricular function. Ann Otolaryngol 65: 470–487

    Google Scholar 

  • Graybiel A (1974) Measurement of otolith function in man. In: Kornhuber HH (ed) Vestibular system part 2: psychophysics, applied aspects and general interpretations. [Handbook of sensory physiology, Vol VI/2. Springer, Berlin Heidelberg New York pp 233–266

    Google Scholar 

  • Graybiel A, Clark B (1965) Validity of the oculogravic illusion as a specific indicator of otolith function. Aerospace Med 36: 1173–1180

    Google Scholar 

  • Graybiel A, Niven JI (1953) The absence of residual effects attributable to the otolith organs following unilateral labyrinthectomy in man. Laryngoscope 63: 18–30

    Google Scholar 

  • Graybiel A, Niven JI, Walsh TE (1952) The differentiation between symptoms referable to the otolith organs and semicircular canals in patients with nonsuppurative labyrinthitis. Laryngoscope 62: 924–933

    Google Scholar 

  • Graybiel A, Miller EF, Newsom BD, Kennedy RS (1968) The effect of water immersion on the perception of the oculogravic illusion in normal and labyrinthine defective subjects. Acta Otolaryngol 65: 599–610

    Google Scholar 

  • Halmagyi, GM, Gresty MA, Gibson WPR (1978) Ocular tilt reaction with peripheral vestibular lesion. Ann Neurol 6: 80–83

    Google Scholar 

  • Harner SG, Ebersold MJ (1985) Management of acoustic neuromas 1978–1983. J Neurosurg 63: 175–179

    Google Scholar 

  • Lacour M, Gianni S, Manzoni D, Pompeiano O, Xerri C (1985) Central compensation of vestibular deficits. III. Response characteristics of lateral vestibular neurons to roll tilt after contralateral labyrinth deafferentation. J Neurophysiol 54: 988–1005

    Google Scholar 

  • Lindeman HH (1969) Studies on the morphology of the sensory regions of the vestibular apparatus. Adv Anat Embryol Cell Biol 42: 1–113

    Google Scholar 

  • Lowenstein O, Wersall J (1959) A functional interpretation of the electron-microscopic structure of the sensory hairs in the cristae of the elasmobranch Raja clavata in terms of directional sensitivity. Nature 184: 1807

    Google Scholar 

  • Mach E (1875) Grundlinien der Lehre von den Bewegungsempfindungen. Engelmann Leipzig, (quoted by Young 1984b)

  • Miller EF, Graybiel A (1966) Magnitude of gravitational force: an independent variable in egocentric visual localization of the horizontal. J Exp Psychol 71: 425–460

    Google Scholar 

  • Morant RB, Aronoff J (1966) Starting position, adaptation, and visual framework as influencing the perception of verticality. J Exp Psychol 39: 538–547

    Google Scholar 

  • Nelson JR, House WF (1971) Ocular countertorsion as an indicator of otolith function: effects of unilateral vestibular lesions. Trans Am Acad Ophthalmol Otol 75: 1313–1321

    Google Scholar 

  • Noble CE (1949) The perception of the vertical. III. The visual vertical as a function of centrifugal and gravitational forces. J Exp Psychol 39: 839–850

    Google Scholar 

  • O'Connell DC, Lathrop RG, Weintraub DJ, McHale TJ (1967) Apparent verticality: psychological error versus sensorytonic theory. J Exp Psychol 73: 347–353

    Google Scholar 

  • Precht W, Dieringer N (1985) Neuronal events paralleling functional recovery (compensation) following peripheral vestibular lesions. In: Berthoz A, Melvill Jones G (eds) Adaptive mechanisms in gaze control: facts and theories. Elsevier, Amsterdam, pp 251–268

    Google Scholar 

  • Ruttum M, von Noorden GK (1983) Adaptation to tilting of the visual environment in cyclotropia. Am J Opthalmol 96: 229–237

    Google Scholar 

  • Schaltenbrand G, Bailey P (1959) Introduction to stereotaxis with an atlas of the human brain. Georg Thieme, Stuttgart

    Google Scholar 

  • Schone H, Lechner-Steinleitner S (1978) The effect of preceding tilt on the perceived vertical. Acta Otolaryngol 85: 68–73

    Google Scholar 

  • Schuknecht H (1982) Behavior of the vestibular nerve following labyrinthectomy. Ann Otol Rhinol Laryngol Suppl 91: 16–32

    Google Scholar 

  • Smith PF, Curthoys IS (1988a) Neuronal activity in the contralateral medial vestibular nucleus of the guinea pig following unilateral labyrinthectomy. Brain Res 444: 295–307

    Google Scholar 

  • Smith PF, Curthoys IS (1988b) Neuronal activity in the ipsilateral medial vestibular nucleus of the guinea pig following unilateral labyrinthectomy. Brain Res 444: 308–319

    Google Scholar 

  • Taylor MM (1963) Visual discrimination and orientation. J Opt Soc Am 53: 763–765

    Google Scholar 

  • Winer BJ (1962) Statistical principles in experimental design. McGraw-Hill, New York

    Google Scholar 

  • Wolfe JW, Kos CM (1977) Nystagmic responses of the rhesus monkey to rotational stimulation following unilateral labyrinthectomy: final report. Trans Am Acad Ophthal Otolaryngol 84: 38–45

    Google Scholar 

  • Xerri C, Gianni S, Manzoni D, Pompeiano O (1983) Central compensation of vestibular deficits. I. Response characteristics of lateral vestibular neurons to roll tilt after ipsilateral labyrinth p deafferentation. J Neurophysiol 50: 428–448

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dai, M.J., Curthoys, I.S. & Halmagyi, G.M. Linear acceleration perception in the roll plane before and after unilateral vestibular neurectomy. Exp Brain Res 77, 315–328 (1989). https://doi.org/10.1007/BF00274989

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00274989

Key words

Navigation