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Three-dimensional head angular velocity detection from otolith afferent signals

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Abstract

Afferent signals from the otolith organs can produce compensatory eye position and velocity signals which has been described as linear vestibulo-ocular reflex (LVOR). The afferent otolith signals carry information about head orientation and changes of head orientation relative to gravity. A head orientation (tilt) related position signal can be obtained from population vector coding of tonic otolith afferent signals during static or dynamic head tilts, which in turn could produce compensatory eye position signals in the LVOR. On the other hand, eye angular velocity signals may be extracted, as proposed in this study, from the population response of tilt-velocity sensitive otolith afferents. Such afferents are shown to encode instantaneous head orientation relative to gravity at onset of a head movement and, as the movement continues, the projection of head angular velocity onto the earth-horizontal plane, indicating the instantaneous direction of movement relative to gravity. Angular velocity components along the earth-vertical direction which are not directly encoded by otolith afferents can be detected by central signal processing. Central reconstruction of 3D head angular velocity allows to obtain information about absolute head orientation in space even in the absence of semicircular canal related information. Such information is important for generating compensatory eye movements as well as for dynamic control of posture.

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References

  • Anderson JH, Blanks RHI, Precht W (1978) Response characteristics of semicircular canal and otolith systems in cat. I. Dynamic responses of primary vestibular fibers. Exp Brain Res 32:491–507

    Article  CAS  PubMed  Google Scholar 

  • Angelaki DE (1991) Dynamic polarization vector of spatially tuned neurons. IEEE Trans Biomed Eng 38:1053–1060

    Article  CAS  PubMed  Google Scholar 

  • Angelaki DE (1992) Vestibular neurons encoding multi-dimensional linear acceleration assist in the estimation of the rotational velocity during off-vertical axis rotation. Ann NY Acad Sci 656:910–913

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Baloh RW, Beykirch K, Honrubia V, Yee RD (1988) Eye movements induced by linear acceleration on a parallel swing. J Neurophysiol 60:2000–2013

    CAS  PubMed  Google Scholar 

  • Blanks RHI, Precht W (1976) Functional characteristics of primary vestibular afferents in the frog. Exp Brain Res 25:369–390

    Article  CAS  PubMed  Google Scholar 

  • Bush GA, Perachio AA, Angelaki DE (1992) Quantification of different classes of canal-related vestibular nuclei neuron responses to linear acceleration. Ann NY Acad Sci 656:917–919

    CAS  PubMed  Google Scholar 

  • Cohen B, Suzuki J, Raphan T (1983) Role of the otolith organs in generation of horizontal nystagmus; effects of selective labyrinthine lesions. Brain Res 276:159–164

    Article  CAS  PubMed  Google Scholar 

  • Correia MJ, Money KE (1970) The effect of blockage of all six semicircular canal ducts on nystagmus produced by linear acceleration in the cat. Acta Otolaryngol 62:297–308

    Google Scholar 

  • Fernández 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

    PubMed  Google Scholar 

  • Fernández C, Goldberg JM (1976b) Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. II. Directional selectivity and force response relations. J Neurophysiol 39:985–995

    PubMed  Google Scholar 

  • Fernández C, Goldberg JM (1976c) Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. III. Response dynamics. J Neurophysiol 39:996–1008

    PubMed  Google Scholar 

  • Georgopoulos AP, Schwartz AB, Kettner RE (1986) Neuronal population coding of movement direction. Science 233:1416–1419

    CAS  PubMed  Google Scholar 

  • Goldberg JM, Desmadryl G, Baird RA, Fernández C (1990) The vestibular nerve of the chinchilla. IV. Discharge properties of utricular afferents. J Neurophysiol 63:781–790

    CAS  PubMed  Google Scholar 

  • Grünwald, AK (1867) Über ‘begrenzte’ Derivationen und deren Anwendung. Z Angew Math Phys 12:441

    Google Scholar 

  • Guedry FE (1965) Orientation of the rotation axis relative to gravity: its influence on nystagmus and the sense of rotation. Acta Otolaryngol (Stockh) 60:30–48

    Google Scholar 

  • Hain TC (1986) A model of the nystagmus induced by off vertical axis rotation. Biol Cybern 54:337–350

    Article  CAS  PubMed  Google Scholar 

  • Hess BJM (1992) How does the otolith system detect three-dimensional head angular velocity? Ann NY Acad Sci 656:850–853

    CAS  PubMed  Google Scholar 

  • Hess BJM, Dieringer N (1990) Spatial organization of the maculo-ocular reflex of the rat: Responses during off-vertical axis rotation. Eur J Neurosci 2:909–919

    Article  PubMed  Google Scholar 

  • Hess BJM, Dieringer N (1991) Spatial organization of the linear vestibulo-ocular reflexes of the rat: Responses during horizontal and vertical linear acceleration. J Neurophysiol 66:1805–1818

    CAS  PubMed  Google Scholar 

  • Hess BJM, Knöpfel T, Precht W (1984) Dynamics of maculo-ocular reflexes in the frog. Neuroscience 11:645–650

    Article  CAS  PubMed  Google Scholar 

  • Lowenstein O, Saunders RD (1975) Otolith-controlled responses from first-order neurons of the labyrinth of the bullfrog (Rana catesbeiana) to changes in linear acceleration. Proc R Soc B 191:475–505

    Article  CAS  Google Scholar 

  • Macadar O, Wolfe GE, O'Leary DP, Segundo JP (1975) Response of the elasmobranch utricle to maintained spatial orientation, transitions and jitter. Exp Brain Res 22:1–12

    Article  CAS  PubMed  Google Scholar 

  • Money KE, Scott JW (1962) Functions of separate sensory receptors of non-auditory labyrinth in the cat. Am J Physiol 202:1211–1220

    CAS  PubMed  Google Scholar 

  • Myers SF, Lewis ER (1991) Vestibular afferent responses to microrotational stimuli. Brain Res 543:36–44

    Article  CAS  PubMed  Google Scholar 

  • Oldham KB, Spanier J (1974) The fractional calculus. Academic Press, Orlando

    Google Scholar 

  • Paige GD, Tomko DL (1991) Eye movement responses to linear head motion in the squirrel monkey. I. Basic characteristics. J Neurophysiol 65:1170–1182

    CAS  PubMed  Google Scholar 

  • Raphan T, Cohen B, Henn V (1981) Effects of gravity on rotatory nystagmus in monkey. Ann NY Acad Sci 374:337–346

    Google Scholar 

  • Raphan T, Schnabolk C (1988) Modeling slow phase velocity generation during off-vertical axis rotation (OVAR). Ann NY Acad Sci 545:29–50

    CAS  PubMed  Google Scholar 

  • Robinson DA (1981) The use of control system analysis in the neurophysiology of eye movements. Ann Rev Neurosci 4:463–503

    Article  CAS  PubMed  Google Scholar 

  • Schnabolk C, Raphan T (1992) Modeling 3-D slow phase velocity estimation during off-vertical axis rotation (OVAR). J Vest Res in press

  • Stevens, SS (1970) Neural events and the psychophysical law. Science 170:1043–1050

    CAS  PubMed  Google Scholar 

  • Young LR, Henn V (1975) Nystagmus produced by pitch and yaw rotation of monkeys about non-vertical axes. Fortschr Zool 23:235–246

    CAS  PubMed  Google Scholar 

Download references

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Hess, B.J.M. Three-dimensional head angular velocity detection from otolith afferent signals. Biol. Cybern. 67, 323–333 (1992). https://doi.org/10.1007/BF02414888

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  • DOI: https://doi.org/10.1007/BF02414888

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