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Influence of otolithic stimulation by horizontal linear acceleration on optokinetic nystagmus and visual motion perception

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Summary

Several studies in the past have demonstrated the existence of an Otolith-Ocular Reflex (OOR) in man, although much less sensitive than canal ocular reflex. The present paper 1 confirms these previous results. Nystagmic eye movements (L-nystagmus) appear in the seated subject during horizontal acceleration along the interaural axis in the dark for an acceleration level (1 m/s2) about ten times the perception threshold with a sensitivity of about 0.035 rad/m.

When sinusoidal linear acceleration is combined with optokinetic stimulation, the recorded nystagmus slow phase velocity exhibits strong periodic modulation related to subject motion. This marked effect of linear acceleration on the optokinetic nystagmus (OKN) appears at a level (0.1 m/s2) close to the acceleration perception threshold and has a 4-fold higher sensitivity than L-nystagmus. Modulation of OKN can reach a peak-to-peak amplitude as great as 20 °/s; for a given optokinetic field size it increases with the velocity of the optokinetic stimulus, i.e. with the slow phase eye velocity. In parallel with changes in OKN slow phase velocity, linear acceleration induces a motion related decrease in the perceived velocity of the visual scene and modifications in selfmotion perception.

The results are interpreted in terms of a mathematical model of visual-vestibular interaction. They show that sensory interaction processes can magnify the contribution given to the control of eye movements by the otolithic system and provide a way of exploring its function at low levels of acceleration.

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References

  • Baarsma EA, Collewijn H (1975) Eye movements due to linear acceleration in the rabbit. J Physiol (Lond) 245: 227–247

    Google Scholar 

  • Babiiak VI (1978) Les composantes sensorielles du nystagmus optocinétique sous l'action des accélérations angulaires. Kosm Biol Aviakosmicheskaya Med 1: 66–71

    Google Scholar 

  • Baker R, Precht W, Berthoz A (1973) Synaptic connections to trochlear motoneurons determined by individual vestibular nerve branch stimulation in the cat. Brain Res 64: 402–406

    Google Scholar 

  • Barnes GR, Benson AG, Prior ARJ (1978) Visual vestibular interaction in the control of eye movement. Aviat Space Environ Med 49: 557–564

    Google Scholar 

  • Benson AJ, Bodin MA (1966) Interaction of linear and angular acceleration on vestibular receptors in man. Aerosp Med 37: 144–154

    Google Scholar 

  • Berthoz A, Pavard B, Young LR (1975) Perception of linear horizontal self motion induced by peripheral vision (linear vection). Basic characteristics and visual vestibular interactions. Exp Brain Res 23: 471–489

    CAS  PubMed  Google Scholar 

  • Berthoz A, Buizza A, Schmid R (1977) Visual vestibular interaction during linear motion. ESA SP- 130: 117–125

    Google Scholar 

  • Buizza A, Schmid R, Zanibelli A., Mira E, Semplici P (1978) Quantification of vestibular nystagmus by an interactive computer program. ORL 40: 147–159

    Google Scholar 

  • Buizza A, Léger A, Berthoz A, Schmid R (1979) Otolithicacoustic interaction in the control of eye movement. Exp Brain Res 36: 509–522

    Google Scholar 

  • Carpenter MB (1960) Fiber projections from descending and lateral vestibular nuclei in the cat. Am J Anat 107: 1–22

    Google Scholar 

  • Cohen B, Highstein SM (1972) Cerebellar control of the vestibular pathways to oculomotor neurons. In: Brodai A, Pompeiano O (eds) Basic aspects of central vestibular mechanisms. Amsterdam, Elsevier (Progress of brain research, vol 37, pp 411–428)

    Google Scholar 

  • Crampton GH (1966) Does linear acceleration modify cupular deflection?, II Symp. on the Role of Vestibular Organs in Space Exploration. NASA SP-115: 169–184

    Google Scholar 

  • Dichgans J (1977) Optokinetic nystagmus as dependent on the retinal periphery via the vestibular nucleus. In: Baker R, Berthoz A (eds) Control of gaze by brain stem neurons. Amsterdam, Elsevier North-Holland, pp 261–267

    Google Scholar 

  • Dichgans J, Brandt T (1978) Visual vestibular interaction: Effects on self-motion perception and in postural control. In: Held R, Leibowitz H, Teuber HL (eds) Perception. Springer, Berlin Heidelberg New York (Handbook of sensory physiology, vol 8, pp 755–804)

    Google Scholar 

  • Fernandez C, Goldberg JM (1976) Physiology of peripheral neurons innervating otolith organs in the squirrel monkey. III. Response dynamics. J Neurophysiol 39: 970–1008

    Google Scholar 

  • Fluur E (1960) Vestibular compensation after labyrinthine destruction. Acta Otolaryngol (Stockh) 52: 367–375

    Google Scholar 

  • Fluur E (1970) Utricular stimulation and oculomotor reactions. Laryngoscope 70: 413–431

    Google Scholar 

  • Galoian VP, Zenkin GM (1976) Etude des mouvements de torsion de l'œil. Biofizika 21: 570–577

    Google Scholar 

  • Graybiel A, Patterson JL (1955) Thresholds of stimulation of the oblith organs as indicated by the oculagravic illusion. J Appl Physiol 7: 666–670

    Google Scholar 

  • Graybiel A (1974) Measurement of otolith function in man. In: Kornhuber HH (ed) Task. Springer, Berlin Heidelberg New York (Handbook of sensory physiology, vol 4/2, pp 233–266)

    Google Scholar 

  • Grüsser OJ, Grüsser-Cornells U (1972) Interaction of vestibular and visual inputs in the visual system. In: Brodal A, Pompeiano O (eds) Basic aspects of central vestibular mechanisms. Elsevier, Amsterdam, pp 573–583

    Google Scholar 

  • Guedry F (1974) Psychophysics of vestibular sensation. In: Kornhuber HH (ed) Vestibular systems. Springer, Berlin Heidelberg New York (Handbook of sensory physiology, vol 6, pp 3–154)

    Google Scholar 

  • Guedry FE Jr, Lentz JM, Jell RM (1978) Visual vestibular interaction: influence of peripheral vision on suppression of the vestibular ocular reflex and visual acuity. WASA, NAMRL 1246

  • Gundry MJ (1978) Threshold of perception for periodic linear motion. Aviat Space Environ Med 49: 679–686

    Google Scholar 

  • Helmholtz H von (1896) Handbuch der physiologischen Optik. Voss, Hamburg Leipzig

    Google Scholar 

  • Hunte M (1786) The use of the oblique muscle. In: Nicol G, Johnson J (eds) Observations on certain parts of the animal oeconomy. London, pp 209–212

  • Jongkees LBW, Philipszoon AT (1962) Nystagmus provoked by linear accelerations. Acta Physiol Pharmacol Neerl 10: 238–247

    Google Scholar 

  • Jung R (1977) Introduction: an appreciation of early work on gaze control in man and of visuo-vestibular research before 1940. In: Baker R, Berthoz A (eds) Control of gaze by brain stem neurons. Elsevier, Amsterdam, pp 1–10

    Google Scholar 

  • Koenig E, Allum JHJ, Dichgans J (1978) Visual vestibular interaction upon nystagmus slow phase velocity in man. Acta Otolaryngol 85: 397–410

    Google Scholar 

  • Léger A, Buizza A, Berthoz A, Schmid R (1978) Otolith contribution to ocular pursuit of acoustic targets. Exp Brain Res 32: R 25

    Google Scholar 

  • Lestienne F, Soechting J, Berthoz A (1977) Postural readjustments induced by linear motion of visual scenes. Exp Brain Res 28: 363–384

    Google Scholar 

  • Levison WH, Zacharias GL (1978) Motion cue models for pilot vehicle analysis. Aerospace Med Res Lab TR-78-2

  • Mach E (1875) Grundlinien der Lehre von den Bewegungsempfindungen. Engelmann, Leipzig

    Google Scholar 

  • Masse, D (1976) Le contrôle des mouvements oculaires. Thèse, Université de Grenoble

  • Meiry JL (1966) The vestibular system and human dynamic space orientation. NASA CR-628

  • Niven SI, Hixson CE, Correia MJ (1965) Elicitation of horizontal nystagmus by periodical acceleration. Acta Otolaryngol 62: 429–441

    Google Scholar 

  • Ormsby CC (1974) Model of human dynamic orientation. Ph. D. Thesis. MIT, Cambridge

    Google Scholar 

  • Ormsby CC, Young LR (1976) Perception of static orientation in a constant gravito inertial environment. Aviat Space Environ Med 47: 159–164

    Google Scholar 

  • Pavard B, Berthoz A (1977) Linear acceleration modifies the perceived velocity of a moving visual scene. Perception 6: 529–540

    Google Scholar 

  • Pompeiano O, Walberg F (1957) Descending connections to the vestibular nuclei on experimental study in the cat. J Comp Neurol 108: 465–503

    Google Scholar 

  • Precht W (1977) The functional synaptology of brain stem oculomotor pathways. In: Baker R, Berthoz A (eds) Control of gaze by brain stem neurons. Elsevier, Amsterdam, pp 131–142

    Google Scholar 

  • Precht W, Llinás R (1969) Functional organization of the vestibular afferents to the cerebellar cortex of the cerebellar cortex of frog and cat. Exp Brain Res 9: 30–52

    Google Scholar 

  • Precht W, Volkind R, Maeda M, Giretti ML (1976) The effects of stimulating the cerebellar nodulus in the cat on the vestibular neurons. Neuroscience 1: 301–312

    Google Scholar 

  • Raphan T, Cohen B, Matsuo V (1977) A velocity storage mechanism responsible for optokinetic nystagmus (OKN) optokinetic after nystagmus (OKAN) and vestibular nystagmus In: Baker R, Berthoz A (eds) Control of gaze brain stem neurons. Elsevier, Amsterdam, pp 37–48

    Google Scholar 

  • Robinson DA (1977a) Linear addition of optokinetic and vestibular signals in the vestibular nucleus. Exp Brain Res 30: 447–450

    Google Scholar 

  • Robinson DA (1977b) Vestibular and optokinetic symbiosis: an example of explaining by modelling. In: Baker R, Berthoz A (eds) Control of gaze by brain stem neurons. Elsevier, Amsterdam, pp 49–58

    Google Scholar 

  • Schmid R, Zambarbieri D, Sardi R (1979) A mathematical model of the optokinetic reflex. Biol Cybern 34: 215–225

    Google Scholar 

  • Schmid R, Buizza A, Zambarbieri D (1979) A non-linear model for visual-vestibular interaction during body rotation in man. Biol Cybern (in press)

  • Schwindt PC, Richter A, Precht W (1973) Short latency utricular and canal input to ipsilateral abducens motoneurons. Brain Res 60: 259–262

    Google Scholar 

  • Shillinger GL, Baumgarten RJ von, Baldrighi G (1973) The gravity reference response, the rotation sensation and other illusory sensations experienced in air craft and space flight. Space Life Sci 4: 368–390

    Google Scholar 

  • Stark L (1971) The control system for versional eye movements. In: Bach-Y-Rita P, Collins CC, Hyde JE (eds) The control of eye movements. New York, Academic Press, pp 363–428

    Google Scholar 

  • Steer R W (1967) The influence of angular and linear acceleration and thermal stimulation on the human semi-circular canal. Sc. D. Thesis. MIT, Cambridge

    Google Scholar 

  • Suzuki JI (1972) Vestibulooculomotor relations: static responses. In: Brodal A, Pompeiano O (eds) Basic aspects of central vestibular mechanism. Elsevier, Amsterdam (Progress of brain research, vol 37, pp 507–514)

    Google Scholar 

  • Szentágothai J (1964) Pathways and synaptic articulation patterns connecting vestibular receptors and oculomotor nuclei. In: Bender MB (ed) The oculomotor system. Harper and Row, New York, p 556

    Google Scholar 

  • Ter Braak JWG (1936) Untersuchungen über optokinetischen Nystagmus. Arch Neurol Physiol 21: 309–376

    Google Scholar 

  • Ter Braak JWG (1937) Kann der Bewegungsapparat durch geradlinige Beschleunigung gereizt werden? Pflügers Arch 238: 327–332

    Google Scholar 

  • Timm C (1953) Physikalische Vorgänge bei der Labyrinthreizung. Z Laryngol Rhinol 32: 237–251

    Google Scholar 

  • Tokunaga O (1977) The influence of linear acceleration on optokinetic nystagmus in human subjects. Acta Otolaryngol (Stockh) 84: 338–343

    Google Scholar 

  • Vidic TR, Barlow JS, Oman CM, Tole JR, Weiss AD, Young LR (1976) Human eye tracking during vertical and horizontal motion. Neurosci Abstr 2: 1026

    Google Scholar 

  • Woellner RC, Graybiel A (1959) Counterrolling of the eyes and its dependence on the magnitude of gravitational or inertial force acting laterally on the body. J Appl Physiol 14: 632

    Google Scholar 

  • Yasui S (1973) Nystagmus generation, oculomotor tracking and visual motion perception. Ph. D. Thesis, Department of Aeronautics and Astronautics. MIT, Cambridge

    Google Scholar 

  • Young LR, Meiry JL (1967) A revised dynamic otolith model. NASA SP 152: 363–368

    Google Scholar 

  • Young L, Dichgans J, Murphy R, Brandt Th (1973) Interaction of optokinetic and vestibular stimuli in motion perception. Acta Otolaryngol (Stockh) 76: 24–31

    Google Scholar 

  • Zacharias GL (1977) Motion sensation dependence on visual and vestibular cues. Ph. D. Thesis. MIT, Cambridge

    Google Scholar 

Download references

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Buizza, A., Léger, A., Droulez, J. et al. Influence of otolithic stimulation by horizontal linear acceleration on optokinetic nystagmus and visual motion perception. Exp Brain Res 39, 165–176 (1980). https://doi.org/10.1007/BF00237547

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