Skip to main content
Log in

Human ocular responses to translation of the observer and of the scene: dependence on viewing distance

  • Original Paper
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Recent experiments on monkeys have indithat-—the eye movements induced by brief translation of either the observer or the visual scene are a linear function of the inverse of the viewing distance. For the movements of the observer, the room was dark and responses were attributed to a translational vestibulo-ocular reflex (TVOR) that senses the motion through the otolith organs; for the movements of the scene, which elicit ocular following, the scene was projected and adjusted in size and speed so that the retinal stimulation was the same at all distances. The shared dependence on viewing distance was consistent with the hypothesis that the TVOR and ocular following are synergistic and share central pathways. The present experiments looked for such dependencies on viewing distance in human subjects. When briefly accelerated along the interaural axis in the dark, human subjects generated compensatory eye movements that were also a linear function of the inverse of the viewing distance to a previously fixated target. These responses, which were attributed to the TVOR, were somewhat weaker than those previously recorded from monkeys using similar methods. When human subjects faced a tangent screen onto which patterned images were projected, brief motion of those images evoked ocular following responses that showed statistically significant dependence on viewing distance only with low-speed stimuli (10°/s). This dependence was at best weak and in the reverse direction of that seen with the TVOR, i.e., responses increased as viewing distance increased. We suggest that in generating an internal estimate of viewing distance subjects may have used a confounding cue in the ocular-following paradigmthe size of the projected scene - which was varied directly with the viewing distance in these experiments (in order to preserve the size of the retinal image). When movements of the subject were randomly interleaved with the movements of the scene - to encourage the expectation of ego-motion - the dependence of ocular following on viewing distance altered significantly: with higher speed stimuli (40°/s) many responses (63%) now increased significantly as viewing distance decreased, though less vigorously than the TVOR. We suggest that the expectation of motion results in the subject placing greater weight on cues such as vergence and accommodation that provide veridical distance information in our experimental situation: cue selection is context specific.

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

    PubMed  CAS  Google Scholar 

  • Biguer B, Prablanc C (1981) Modulation of the vestibulo-ocular reflex in eye-head coordination as a function of target distance in man. In: Fuchs AF, Becker W (eds) Progress in oculomotor research. Elsevier North-Holland, New York, pp 525–530

    Google Scholar 

  • Blakemore C, Donaghy M (1980) Co-ordination of head and eyes in the gaze changing behaviour of cats. J Physiol (Lond) 300:317–335

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Busettini C, Miles FA, Schwarz U (1991) Ocular responses to translation and their dependence on viewing distance. II. Motion of the scene. J Neurophysiol 66:865–878

    PubMed  CAS  Google Scholar 

  • Cohen B, Matsuo V, Raphan T (1977) Quantitative analysis of the velocity characteristics of optokinetic nystagmus and optokinetic after-nystagmus. J Physiol (Lond) 270:321–344

    CAS  Google Scholar 

  • Collewijn H, Van Der Mark F, Jansen TC (1975) Precise recordings of human eye movements. Vision Res 15:447–450

    Article  PubMed  CAS  Google Scholar 

  • Crist C, Robinson DL (1989) A large-field screen with even texture for vision research. Vis Neurosci 2:415–417

    PubMed  CAS  Google Scholar 

  • Eubank RL (1988) Spline smoothing and nonparametric regression. (Statistics: textbooks and monographs, vol 90) Dekker, New York

    Google Scholar 

  • Gellman RS, Carl JR, Miles FA (1990) Short latency ocular-following responses in man. Vis Neurosci 5:107–122

    Article  PubMed  CAS  Google Scholar 

  • Goldberg JM, Fernandez C (1975) Responses of peripheral vestibular neurons to angular and linear accelerations in the squirrel monkey. Acta Otolaryngol 80:101–110

    PubMed  CAS  Google Scholar 

  • Gresty MA, Bronstein AM (1986) Otolith stimulation evokes compensatory reflex eye movements of high velocity when linear motion of the head is combined with concurrent angular motion. Neurosci Lett 65:149–154

    Article  PubMed  CAS  Google Scholar 

  • Gresty MA, Bronstein AM, Barratt H (1987) Eye movement responses to combined linear and angular head movement. Exp Brain Res 65:377–384

    Article  PubMed  CAS  Google Scholar 

  • Hays AV, Richmond BJ, Optican LM (1982) A UNIX-based multiple process system for real-time data acquisition and control WESCON Conf. Proc. 2:1–10

    Google Scholar 

  • Hine T, Thorn F (1987) Compensatory eye movements during active head rotation for near targets: effects of imagination, rapid head oscillation and vergence. Vision Res 27:1639–1657

    Article  PubMed  CAS  Google Scholar 

  • Israël I. Berthoz A (1989) Contribution of the otoliths to the calculation of linear displacement. J Neurophysiol 62:247–263

    PubMed  Google Scholar 

  • Lisberger SG, Miles FA, Optican LM, Eighmy BB (1981) Optokinetic response in monkey: underlying mechanisms and their sensitivity to long-term adaptive changes in vestibuloocular reflex. J Neurophysiol 45:869–890

    PubMed  CAS  Google Scholar 

  • Matsuo V, Cohen B (1984) Vertical optokinetic nystagmus and vestibular nystagmus in the monkey: up-down asymmetry and effects of gravity. Exp Brain Res 53:197–216

    Article  PubMed  CAS  Google Scholar 

  • Miles FA, Busettini C (1992) Ocular compensation for self motion: visual mechanisms. Ann NY Acad Sci 656:220–232

    Article  PubMed  CAS  Google Scholar 

  • Miles FA, Kawano K, Optican LM (1986) Short-latency ocular following responses of monkey. I. Dependence on temporospatial properties of the visual input. J Neurophysiol 56:1321–1354

    PubMed  CAS  Google Scholar 

  • Miles FA, Schwarz U, Busettini C (1991) The parsing of optic flow by the primate oculomotor system. In: Gorea A (ed) Representations of vision: trends and tacit assumptions in vision research. Cambridge University Press, Cambridge, pp 185–199

    Google Scholar 

  • Miles FA, Schwarz U, Busettini C (1992) The decoding of optic flow by the primate optokinetic system. In: Berthoz A, Graf W, Vidal PP (eds) The head-neck sensory-motor system. Oxford University Press, New York, pp 471–478

    Google Scholar 

  • Paige GD (1989) The influence of target distance on eye movement responses during vertical linear motion. Exp Brain Res 77:585–593

    Article  PubMed  CAS  Google Scholar 

  • Paige GD, Tomko DL (1991) Eye movement responses to linear head motion in the squirrel monkey. II. Visual-vestibular interactions and kinematic considerations. J Neurophysiol 65:1183–1196

    PubMed  CAS  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) Developments in neuroscience, vol 1. Elsevier/North-Holland, Amsterdam, pp 37–47

    Google Scholar 

  • Raphan T, Matsuo V, Cohen B (1979) Velocity storage in the vestibulo-ocular reflex arc (VOR). Exp Brain Res 35:229–248

    Article  PubMed  CAS  Google Scholar 

  • Robinson DA (1963) A method of measuring eye movement using a scierai search coil in a magnetic field. IEEE Trans Biomed Eng 10:137–145

    PubMed  CAS  Google Scholar 

  • Rodenburg M, Kasteel-van Linge A, Maas AJJ (1987) Coordination of head and eye position during fixation. In: O’Regan JK, Lévy-Schoen A (eds) Eye movements : from physiology to cognition. Elsevier/North-Holland, Amsterdam, pp 211–218

    Google Scholar 

  • Schwarz U, Miles FA (1991) Ocular responses to translation and their dependence on viewing distance. I. Motion of the observer. J Neurophysiol 66:851–864

    PubMed  CAS  Google Scholar 

  • Schwarz U, Busettini C, Miles FA (1989) Ocular responses to linear motion are inversely proportional to viewing distance. Science 245:1394–1396

    Article  PubMed  CAS  Google Scholar 

  • Sedgwick HA (1986) Space perception. In: Boff KR, Kaufman L, Thomas JP (eds) Sensory processes and perception. (Handbook of perception and human performance, vol I) Wiley, New York, pp 21.1–21.57

    Google Scholar 

  • Snyder LH, King WM (1992) Effect of viewing distance and location of the axis of head rotation on the monkey’s vestibuloocular reflex. I. Eye movement responses. J Neurophysiol 67:861–874

    PubMed  CAS  Google Scholar 

  • Vakkur GJ (1967) Studies of optics and neurophysiology of vision. (MD Thesis), University of Sydney

  • Viirre E, Tweed D, Milner K, Vilis T (1986) Reexamination of the gain of the vestibuloocular reflex. J Neurophysiol 56:439–450

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Busettini, C., Miles, F.A., Schwarz, U. et al. Human ocular responses to translation of the observer and of the scene: dependence on viewing distance. Exp Brain Res 100, 484–494 (1994). https://doi.org/10.1007/BF02738407

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02738407

Key words

Navigation