Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Two-dimensional coding of linear acceleration and the angular velocity sensitivity of the otolith system

  • 132 Accesses

  • 56 Citations

Abstract

There exist otolith-sensitive vestibular nuclei neurons with spatio-temporal properties that can be described by two response vectors that are in temporal and spatial quadrature. These neurons respond to the component of a stimulus vector on a plane rather than a single axis. It is demonstrated here that these “two-dimensional” linear accelerometer neurons can function as one-dimensional angular velocity detectors. The two-dimensional property in both space and time allows these neurons to encode the component of the stimulus angular velocity vector that is normal to the plane defined by the two response vectors. The angular velocity vector in space can then be reconstructed by three populations of such neurons having linearly independent response planes. Thus, we propose that these two-dimensional spatio-temporal linear accelerometer neurons, in addition to participating in functions of the otolith system that are based on detection of linear acceleration, are also involved in the generation of compensatory ocular responses during off-vertical axis rotations.

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

References

  1. Angelaki DE (1991) Dynamic polarization vector of spatially tuned neurons. IEEE Trans Biom Eng 38:11:1053–1060

  2. Angelaki DE (1992a) Spatio-temporal convergence (STC) in otolith neurons. Biol Cybern 66:38–96

  3. Angelaki DE (1992b) Detection of rotating gravity signals. Biol Cybern 67

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

  5. Angelaki DE, Bush GA, Perachio AA (1991) Horizontal canal-sensitive vestibular nuclei neurons encoding multi-dimensional linear acceleration assist in the estimation of rotational velocity during off-vertical axis rotation. Eur J Neuroscience [Suppl] 4:58

  6. Angelaki DE, Bush GA, Perachio AA (1992) A model for the characterization of the spatial properties in vestibular neurons. Biol Cybern 66:231–240

  7. Benson AJ, Barnes GR (1973) Responses to rotating linear acceleration vectors considered in relation to a model of the otolith organs. In: Fifth symposium on the role of the vestibular organs in space exploration, Government printing office, Washington pp 221–236

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

  9. Benson AJ, Guedry FE, Melvill Jones G (1970) Response of semi-circular canal dependent units in vestibular nuclei to rotation of a linear acceleration vector without angular acceleration. J Physiol (Lond) 210: 475–494

  10. Bush GA, Perachio AA, Angelaki DE (1991) Spatial and temporal properties of otolith-sensitive horizontal canal (HC) neurons in the vestibular nucleus as a function of linear acceleration frequency. Soc Neurosci Abstr 17:315

  11. Chan YS, Cheung YM, Hwang JC (1987) Response characteristics of neurons in the cat vestibular nuclei during slow and constant velocity off-vertical axes rotations in the clockwise and counter-clockwise rotations. Brain Res 406:294–301

  12. 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

  13. Correia MJ, Guedry FE (1966) Modification of vestibular responses as a function of the rate of rotation about an earth horizontal axis. Acta Otolaryngol 62:297–308

  14. Correia MJ, Money KE (1970) The effect of blockage of all six semicircular canal ducts on nystagmus produced by dynamic linear acceleration in the cat. Acta Otolaryngol 69:7–16

  15. Darlot C, Denise P (1988) Nystagmus induced by off-vertical rotation axis in the cat. Exp Brain Res 73:78–90

  16. Darlot C, Denise P, Droulez J, Cohen B, Berthoz A (1988) Eye movements induced by off-vertical axis rotation (OVAR) at small angles of tilt. Exp Brain Res 73:91–105

  17. Fanelli R, Raphan T, Schnabolk C (1990) Neural network modelling of eye compensation during off-vertical-axis roation. Neural Networks 3:265–276

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

  19. Fernandez C, Goldberg JM, Abend WK (1972) Response to static tilts of peripheral neurons innervating otolithg organs of the squirrel monkey. J Neurophysiol 35:978–997

  20. Goldberg JM, Fernandez C (1981) Physiological mechanisms of the nystagmus produced by rotation about an earth-horizontal axis. Ann NY Acad Sci 374:40–43

  21. Goldberg JM, Fernandez C (1982) Eye movements and vestibular nerve responses produced in the squirrel monkey by rotations about an earth-horizontal axis. Exp Brain Res 46: 393–401

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

  23. Goldstein H (1950) Classical Mechanics, Addison-Wesley Publishing Company, Reading, Massachusetts

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

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

  26. Harris LR (1987) Vestibular and optokinetic eye movements evoked in the cat by rotation about a tilted axis. Exp Brain Res 66:522–532

  27. Haslwanter Th, Hess BJM (1991) Ocular responses to off vertical axis rotations: directional specifiecity of 3D angular velocity. Europ J Neurosci [Suppl] 4:60

  28. Hess BJM (1992) Three-dimensional head angular velocity detection from otolith afferent signals. Biol Cybern 67:323–333

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

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

  31. Hess BJM, Haslwanter Th (1991) 3D ocular responses to off-vertical axis rotation: Directional selective modulation of 3D eye position. Europ J Neurosci [Suppl] 4:59

  32. Janecke JB, Jongkees LBW, Oosterveld WJ (1970) Relationship between the otoliths and nystagmus. Acta Otolaryngol 69:1–6

  33. Loe PR, Tomko DL, Werner G (1973) The neural signal of angular head position in primary afferent vestibular nerve axons. J Physiol (Lond) 219:29–50

  34. Melvill Jones G, Milsum JH (1969) Neural response of the vestibular sytem to translational acceleration. In: Supplement to conference on systems analysis approach to neurolophysiological problems. Brainerd, [Suppl] pp 8–20

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

  36. Raphan T, Cohen B, Henn V (1981) Effects of gravity on rotatory nystagmus in monkeys. Ann NY Acad Sci 374:44–55

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

  38. Raphan T, Waespe W, Cohen B (1983) Labyrinthine activation during rotation about axes tilted from the vertical. Adv Oto-Rhino-Laryngol 30:226–229

  39. Reichardt W (1961) Autocorrelation, a principle for the evaluation of sensory information by the central nervous system. In: Rosenblith WA (eds) Principles of sensory communication, Wiley, New York, pp 303–317

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

  41. Schor RH, Miller AD, Tomko DL (1984) Responses to head tilt in cat central vestibular neurons. I. Direction of maximum sensitivity. J Neurophysiol 51:136–146

  42. Schor RH, Miller AD, Timerick JB, Tomko DL (1985) Responses to head tilt in cat central vestibular neurons. II. Frequency dependance of neural response vectors. J Neurophysiol 53:1444–1452

  43. Van Santen JPH, Sperling G (1985) Elaborated Reichardt detectors. J Opt Soc Am A 2:300–321

  44. Wilson VJ, Melvill Jones G (1979) Mammalian vestibular physiology, Plenum Press, New York

  45. Young LR, Henn V (1975) Nystagmus produced by pitch and yaw rotation of monkeys about non-vertical axes. Fortsch Zool 23(1):235–246

Download references

Author information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Angelaki, D.E. Two-dimensional coding of linear acceleration and the angular velocity sensitivity of the otolith system. Biol. Cybern. 67, 511–521 (1992). https://doi.org/10.1007/BF00198758

Download citation

Keywords

  • Angular Velocity
  • Vestibular Nucleus
  • Linear Acceleration
  • Response Vector
  • Response Plane