Trends in Neurosciences
Volume 24, Issue 2, 1 February 2001, Pages 113-121
Journal home page for Trends in Neurosciences

Review
Changes in visual perception at the time of saccades

https://doi.org/10.1016/S0166-2236(00)01685-4Get rights and content

Abstract

We frequently reposition our gaze by making rapid ballistic eye movements that are called saccades. Saccades pose problems for the visual system, because they generate rapid, large-field motion on the retina and change the relationship between the object position in external space and the image position on the retina. The brain must ignore the one and compensate for the other. Much progress has been made in recent years in understanding the effects of saccades on visual function and elucidating the mechanisms responsible for them. Evidence suggests that saccades trigger two distinct neural processes: (1) a suppression of visual sensitivity, specific to the magnocellular pathway, that dampens the sensation of motion and (2) a gross perceptual distortion of visual space in anticipation of the repositioning of gaze. Neurophysiological findings from several laboratories are beginning to identify the neural substrates involved in these effects.

Section snippets

Saccadic suppression

Another idea to emerge early in the last century was that visual sensitivity is actively reduced during saccades. Holt 9 concluded that saccades ‘condition a momentary visual central anaesthesia’, that is, a complete loss of sensitivity. However, evidence for suppression by saccades is contradictory. Many researchers 10., 11., 12. have reported weak threshold elevation for detecting spots of light flashed briefly during saccades (two to threefold) and Krauskopf et al. 13 found no threshold

Physiological studies

Whereas psychophysical studies indicate an early site for the action of saccadic suppression, perhaps as early as LGN, direct physiological evidence is less clear. In humans, visual activity during saccades has been studied using evoked potentials (VEPs) and, more recently, with fMRI and positron emission tomography (PET) imaging. Early studies using VEP (44., 45.) showed a strong (>80%) attenuation of response amplitude to stimuli that were presented at about the same time as the start of a

Perceived position

Retinal motion is not the only problem introduced by saccades. A related (but not identical) problem is how to perceive a stable external world from extremely unstable retinal images. Helmholtz 1 believed that the constancy of perceived position was maintained during and after saccades, because both extra-retinal (the ‘effort of will’) and retinal (sensed but not perceived image motion) information were used to recalibrate the direction of gaze.

Leonard Matin and colleagues 68., 69., 70., 71.

Physiological mechanisms

Compression cannot be explained by a slow extra-retinal position signal, but instead it requires changes in the properties of receptive fields or position codes associated with them. Duhamel et al. 95 showed that there are early changes in the receptive field properties of some neurones in the lateral intraparietal area (LIP) of monkeys making saccades that anticipate their consequences (Fig. 5). LIP neurones begin to respond up to 80 ms before the onset of a saccade to stimuli that will fall

Concluding remarks

Saccades result in several physiological events in anticipation of their threat to visual stability. They suppress visual motion, an effect that is not entirely the result of ‘visual masking’ (although the motion of patterned stimuli might play an important role). Suppression is selective and particularly strong for rapid, low frequency luminance modulation, suggesting that only magnocellular function is suppressed, whereas parvocellular function is spared or even slightly enhanced. Suppression

Acknowledgements

This work was supported by grants from the Human Frontiers Science Program, the Italian Ministry of Education (MURST 40%) and the Australian Research Council.

References (101)

  • D.C. Burr

    Saccadic suppression precedes visual motion analysis

    Curr. Biol.

    (1999)
  • U.J. Ilg et al.

    Motion perception during saccades

    Vis. Res.

    (1993)
  • E.G. Gross

    Inhibition of visual evoked responses to patterned stimuli during voluntary eye movements

    Electroencephalogr. Clin. Neurophysiol.

    (1967)
  • H. Honda

    The timecourses of visual mislocalization and of extra-retinal eye position signals at the time of vertical saccades

    Vis. Res.

    (1991)
  • H. Honda

    Saccade-contingent displacement of the apparent position of visual stimuli flashed on a dimly illuminated structured backgraound

    Vis. Res.

    (1993)
  • J. Schlag et al.

    Illusory localization of stimuli flashed in the dark before saccades

    Vis. Res.

    (1995)
  • H. Honda

    Modification of saccade-contingent visual localization by the presence of a visual frame of reference

    Vis. Res.

    (1999)
  • H. Honda

    Visual mislocalization produced by a rapid image displacement on the retina: examination by means of dichoptic presentation of a target and its background

    Vis. Res.

    (1995)
  • R.M. Hansen et al.

    Accuracy of spatial locations near the time of saccadic eye movments

    Vis. Res.

    (1985)
  • P.E. Hallett et al.

    Saccadic eye movements to flashed targets

    Vis. Res.

    (1976)
  • M.A. Goodale et al.

    Separate pathways for perception and action

    Trends Neurosci.

    (1992)
  • J. Miller

    Egocentric localization of a perisaccadic flash by manual pointing

    Vis. Res.

    (1996)
  • C. Bockisch et al.

    Different motor systems use similar damped extra-retinal eye position information

    Vis. Res.

    (1999)
  • H. Deubel

    Postsaccadic target blanking prevents saccadic suppression of image displacement

    Vis. Res.

    (1996)
  • H.V. Helmholtz

    Handbuch der Physiologischen Optik (1866)

  • R.W. Sperry

    Neural basis of the spontaneous optokinetic response produced by visual inversion

    J. Comp. Physiol. Psychol.

    (1950)
  • E. Von Holst et al.

    Das Reafferenzprinzip

    Naturwissenschaften

    (1954)
  • C.S. Sherrington

    Observations on the sensual role of the proprioceptive nerve supply of the extrinsic ocular muscles

    Brain

    (1918)
  • G. Gauthier

    Ocular muscle proprioception and visual localisation in man

    J. Physiol.

    (1988)
  • R.H.S. Carpenter

    Movement of the Eyes

    (1977)
  • B. Bridgeman

    A theory of visual stability across saccadic eye movements

    Behav. Brain Sci.

    (1994)
  • E.B. Holt

    Eye movements and central anaesthesia

    Psychol. Rev.

    (1903)
  • J. Krauskopf

    Lack of inhibition during involuntary saccades

    Am. J. Psychol.

    (1966)
  • Deubel, H. et al. (1987) Saccadic eye movements and the detection of fast-moving gratings, Biol. Cybern....
  • R. Dodge

    Visual perception during eye movements

    Psychol. Rev.

    (1900)
  • R.S. Woodworth

    Vision and localization during eye movements

    Psychol. Bull.

    (1906)
  • D.C. Burr et al.

    Contrast sensitivity at high velocities

    Vis. Res.

    (1982)
  • D.J. Field

    Relations between the statistics of natural images and the response properties of cortical cells

    J. Opt. Soc. Am. A

    (1987)
  • D.C. Burr

    Selective depression of motion selectivity during saccades

    J. Physiol.

    (1982)
  • D.C. Burr

    Selective suppression of the magnocellular visual pathway during saccadic eye movements

    Nature

    (1994)
  • D.C. Van Essen

    Information processing in the primate visual system: an integrated systems perspective

    Science

    (1992)
  • B. Bridgeman et al.

    Saccadic suppression relies of luminance information

    Psychol. Res.

    (1995)
  • K. Uchikawa et al.

    Saccadic suppression to achromatic and chromatic responses measured by increment-threshold spectral sensitivity

    J. Opt. Soc. Am. A

    (1995)
  • D.M. Mackay

    Elevation of visual threshold by displacement of visual images

    Nature

    (1970)
  • D.M. MacKay

    Visual stability and voluntary eye movements

  • M.R. Diamond

    Extra-retinal control of saccadic suppression

    J. Neurosci.

    (2000)
  • F. Volkmann

    Vision during voluntary saccadic eye movments

    J. Opt. Soc. Am.

    (1962)
  • S. Shiori et al.

    Saccadic suppression of low-level motion

    Vis. Res.

    (1989)
  • E. Castet et al.

    Motion perception during saccadic eye movments

    Nat. Neurosci.

    (2000)
  • M.A. Garcı́a-Péres et al.

    Saccades, saccadic suppression and the detection of high-temporal-frequency gratings

    Invest. Ophthalmol. Vis. Sci.

    (2000)
  • Cited by (0)

    View full text