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Dynamics of Visual Motion Processing pp 239–257Cite as

Intrasaccadic Motion: Neural Evidence for Saccadic Suppression and Postsaccadic Enhancement

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Abstract

Primates have relatively small foveas within their retinas. There are sufficient photoreceptors only in the fovea to allow high spatial resolution vision. Thus, to obtain high-resolution images in the entire visual field, there is a need to point the fovea at targets of interest, and this is achieved using saccadic eye movements. Humans make around three saccades per second. How is smooth, uninterrupted visual perception maintained in the face of the frequent image displacements generated by saccades? It has been known for many years that visual perception is modified before, during, and after saccades and, more recently, evidence has accumulated showing how neural activity is also modulated. This review will describe some of the recent electrophysiological work that shows how neural activity in the visual brain changes at the time of saccades. The review is divided into three sections. The first section describes theories relating to the saccadic suppression and some of the neural evidence to support and refute those theories. The second section describes the recently discovered alterations to the timing of visual responses in the nervous system. It turns out that the latencies of visual responses are reduced at the time of saccades, providing possible explanations for the changes in the time perception that have been observed. The third section describes how neural responsiveness is increased after saccades. Recent findings have shown that when visual stimuli are presented within the receptive fields of visual neurons soon after saccades, responses are larger than that occurring in the absence of saccades. This enhanced responsiveness persists for approximately the same duration as typical intersaccadic periods. Thus, visual responsiveness is normally enhanced between saccades. Conversely, during long periods of fixation visual sensitivity is relatively low. These latter findings suggest that the motor and visual systems work closely together to maximize the sensitivity and efficiency of the visual system.

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References

  • Battaglini PP, Galletti C, Aicardi G, Squatrito S, Maioli MG (1986) Effect of fast moving stimuli and saccadic eye movements on cell activity in visual areas V1 and V2 of behaving monkeys. Arch Ital Biol 124:111–119

    PubMed  CAS  Google Scholar 

  • Bremmer F, Kubischik M, Hoffmann KP, Krekelberg B (2002) Neural dynamics of saccadic suppression; Program No. 57.2. Abstract Viewer/Itinerary Planner. Society for Neuroscience, Washington, DC. Online

    Google Scholar 

  • Bruce CJ, Goldberg ME (1985) Primate frontal eye fields I. Single neurons discharging before saccades. J Neurophysiol 53:603–635

    PubMed  CAS  Google Scholar 

  • Burr DC, Morrone MC (2006) Perception: transient disruptions to neural space-time. Curr Biol 16:R847–R849

    Article  PubMed  CAS  Google Scholar 

  • Burr DC, Holt J, Johnstone JR, Ross J (1982) Selective depression of motion sensitivity during saccades. J Physiol (London) 333:1–15

    CAS  Google Scholar 

  • Burr DC, Morrone MC, Ross J (1994) Selective suppression of the magnocellular visual pathway during saccadic eye movements. Nature 371:511–513

    Article  PubMed  CAS  Google Scholar 

  • Carpenter RHS (1988) Movements of the eyes, 2nd edn. Pion Press, London

    Google Scholar 

  • Castet E, Masson GS (2000) Motion perception during saccadic eye movements. Nat Neurosci 3:177–183

    Article  PubMed  CAS  Google Scholar 

  • Castet E, Jeanjean S, Masson GS (2001) ‘Saccadic suppression’-no need for an active extra-retinal mechanism. Trends Neurosci 24:316–317

    Article  PubMed  CAS  Google Scholar 

  • Celebrini S, Newsome WT (1994) Neuronal and psychophysical sensitivity to motion signals in extrastriate area MST of the macaque monkey. J Neurosci 14:4109–4124

    PubMed  CAS  Google Scholar 

  • Celebrini S, Newsome WT (1995) Microstimulation of extrastriate area MST influences performance in a direction discrimination task. J Neurophysiol 73:437–448

    PubMed  CAS  Google Scholar 

  • Cucchiaro JB, Uhlrich DJ, Sherman SM (1993) Ultrastructure of synapses from the pretectum in the A-laminae of the cat’s lateral geniculate nucleus. J Comp Neurol 334:618–630

    Article  PubMed  CAS  Google Scholar 

  • Diamond MR, Ross J, Morrone MC (2000) Extraretinal control of saccadic suppression. J Neurosci 20:3449–3455

    PubMed  CAS  Google Scholar 

  • Findlay JM, Gilchrist ID (2003) Active vision: the psychology of looking and seeing. Oxford, Oxford University Press

    Book  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 

  • Holt EB (1903) Eye movements and central anaesthesia. Psychol Rev 4:3–45

    Google Scholar 

  • Ibbotson MR, Mark RF, Maddess T (1994) Spatiotemporal response properties of direction-selective neurons in the nucleus of the optic tract and dorsal terminal nucleus of the wallaby, Macropus eugenii. J Neurophysiol 72:2927–2943

    PubMed  CAS  Google Scholar 

  • Ibbotson MR, Crowder NA, Price NSC (2006) Neural basis of time changes around the time of saccades. Curr Biol 16:R834–R836

    Article  PubMed  CAS  Google Scholar 

  • Ibbotson MR, Price NSC, Crowder NA, Ono S, Mustari MJ (2007) Enhanced motion sensitivity follows saccadic suppression in the superior temporal sulcus of the macaque cortex. Cereb Cortex 17:1129–1138

    Article  PubMed  CAS  Google Scholar 

  • Ilg UJ, Hoffmann KP (1993) Motion perception during saccades. Vis Res 33:211–220

    Article  PubMed  CAS  Google Scholar 

  • Kaplan E, Shapley RM (1986) The primate retina contains two types of ganglion cells, with high and low contrast sensitivity. Proc Natl Acad Sci U S A 83:2755–2757

    Article  PubMed  CAS  Google Scholar 

  • Kaplan E, Lee BB, Shapley RM (1990) New views of primate retinal function. Prog Retin Res 9:273–336

    Article  Google Scholar 

  • Kawano K (1999) Ocular tracking: behavior and neurophysiology. Curr Opin Neurobiol 9:467–473

    Article  PubMed  CAS  Google Scholar 

  • Kawano K, Miles FA (1986) Short-latency ocular following responses of monkey II. Dependence on a prior saccadic eye movement. J Neurophysiol 56:1355–1380

    PubMed  CAS  Google Scholar 

  • Kawano K, Shidara M, Yamane S (1992) Neural activity in dorsolateral pontine nucleus of alert monkey during ocular following responses. J Neurophysiol 67:680–703

    PubMed  CAS  Google Scholar 

  • Kawano K, Shidara M, Watanabe Y, Yamane S (1994) Neural activity in cortical area MST of alert monkey during ocular following responses. J Neurophysiol 71:2305–2324

    PubMed  CAS  Google Scholar 

  • Kawano K, Inoue Y, Takemura A, Kitama T, Miles F (1997) A cortically mediated visual stabilization mechanism with ultra-short latency in primates. In: Thier P, Karnath H-O (eds) Parietal lobe contributions to orientation in 3D space. Springer, Heidelberg, pp 185–199

    Google Scholar 

  • Krauskopf J, Graf V, Gaarder K (1966) Lack of inhibition during involuntary saccades. Am J Psychol 79:73–81

    Article  Google Scholar 

  • Kufler SW (1953) Discharge patterns and functional organization of mammalian retina. J Neurophysiol 16:37–68

    Google Scholar 

  • Latour PL (1962) Visual threshold during eye movements. Vis Res 2:261–262

    Article  Google Scholar 

  • Lee D, Malpeli JG (1998) Effects of saccades on the activity of neurons in the cat lateral geniculate nucleus. J Neurophysiol 79:922–936

    PubMed  CAS  Google Scholar 

  • Leichnetz GR (1989) Inferior frontal eye field projections to the pursuit-related dorsolateral pontine nucleus and middle temporal area (MT) in the monkey. Vis Neurosci 3:171–180

    Article  PubMed  CAS  Google Scholar 

  • Leon MI, Shadlen MN (2003) Representation of time by neurons in the posterior parietal cortex of the macaque. Neuron 38:317–327

    Article  PubMed  CAS  Google Scholar 

  • Masson GS, Castet E (2002) Parallel motion processing for the initiation of short-latency ocular following in humans. J Neurosci 22:5149–5163

    PubMed  CAS  Google Scholar 

  • Maunsell JH, Gibson JR (1992) Visual response latencies in striate cortex of the macaque monkey. J Neurophysiol 68:1332–1344

    PubMed  CAS  Google Scholar 

  • Mazer JA, Vinje WE, McDermott J, Schiller PH, Gallant JL (2002) Spatial frequency and orientation tuning dynamics in area V1. Proc Natl Acad Sci U S A 99:1645–1650

    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 visual input. J Neurophysiol 56:1321–1354

    PubMed  CAS  Google Scholar 

  • Miller JM, Bockisch C (1997) Visual perception – where are the things we see? Nature 386:550–551

    Article  PubMed  CAS  Google Scholar 

  • Morrone MC, Ross J, Burr DC (2005) Saccadic eye movements cause compression of time as well as space. Nat Neurosci 8:950–954

    Article  PubMed  CAS  Google Scholar 

  • Newsome WT, Pare EB (1988) A selective impairment of motion perception following lesions of the middle temporal visual area (MT). J Neurosci 8:2201–2211

    PubMed  CAS  Google Scholar 

  • Park J, Schlag-Rey M, Schlag J (2003) Voluntary action expands perceived duration of its sensory consequence. Exp Brain Res 149:527–529

    PubMed  Google Scholar 

  • Petersen SE, Baker JF, Allman JM (1985) Direction-specific adaptation in area MT of the owl monkey. Brain Res 346:146–150

    Article  PubMed  CAS  Google Scholar 

  • Price NSC, Ibbotson MR (2001) Pretectal neurons optimised for the detection of saccade-like movements of the visual image. J Neurophysiol 85:1512–1521

    PubMed  CAS  Google Scholar 

  • Price NSC, Ibbotson MR, Ono S, Mustari MJ (2005) Rapid processing of retinal slip during saccades in macaque area MT. J Neurophysiol 94:235–246

    Article  PubMed  CAS  Google Scholar 

  • Raiguel SE, Lagae L, Gulyas B, Orban GA (1989) Response latencies of visual cells in macaque areas V1, V2 and V5. Brain Res 493:155–159

    Article  PubMed  CAS  Google Scholar 

  • Raiguel SE, Xiao DK, Marcar VL, Orban GA (1999) Response latency of macaque area MT/V5 neurons and its relationship to stimulus parameters. J Neurophysiol 82:1944–1956

    PubMed  CAS  Google Scholar 

  • Ramcharan EJ, Gnadt JW, Sherman SM (2001) The effects of saccadic eye movements on the activity of geniculate relay neurons in the monkey. Vis Neurosci 18:253–258

    Article  PubMed  CAS  Google Scholar 

  • Reppas JB, Usrey WM, Reid RC (2002) Saccadic eye movements modulate visual responses in the lateral geniculate nucleus. Neuron 35:961–974

    Article  PubMed  CAS  Google Scholar 

  • Richards W (1969) Saccadic suppression. J Opt Soc Am 59:617–623

    Article  PubMed  CAS  Google Scholar 

  • Riggs LA, Merton PA, Morton HB (1974) Suppression of visual phosphenes during saccadic eye movements. Vis Res 14:997–1011

    Article  PubMed  CAS  Google Scholar 

  • Ross J, Morrone MC, Goldberg ME, Burr DC (2001a) Changes in visual perception at the time of saccades. Trends Neurosci 24:113–121

    Article  PubMed  CAS  Google Scholar 

  • Ross J, Morrone MC, Goldberg ME, Burr DC (2001b) Response: ‘saccadic suppression’ – no need for an active extra-retinal mechanism. Trends Neurosci 24:317–318

    Article  CAS  Google Scholar 

  • Rushton WA (1965) Visual adaptation. Proc R Soc Lond B 16:20–46

    Article  Google Scholar 

  • Schiller PH, Logothetis NK, Charles ER (1990) Functions of the colour-opponent and broad-band channels of the visual system. Nature 343:68–70

    Article  PubMed  CAS  Google Scholar 

  • Schmidt M (1996) Neurons in the cat pretectum that project to the dorsal lateral geniculate nucleus are activated during saccades. J Neurophysiol 76:2907–2918

    PubMed  CAS  Google Scholar 

  • Shioiri S, Cavanagh P (1989) Saccadic suppression of low-level motion. Vis Res 29:915–928

    Article  PubMed  CAS  Google Scholar 

  • Snippe HP, Poot L, van Hateren JH (2000) A temporal model for early vision that explains detection thresholds for light pulses on flickering backgrounds. Vis Neurosci 17:449–462

    Article  PubMed  CAS  Google Scholar 

  • Snyder AW, Pask C (1973) The stiles-crawford effect-explanation and consequences. Vis Res 13:1115–1137

    Article  PubMed  CAS  Google Scholar 

  • Stiles WS, Crawford BS (1933) The luminous efficency of rays entering the eye pupil at different points. Proc R Soc Lond B 112:428–450

    Article  Google Scholar 

  • Thiele A, Henning P, Kubischik M, Hoffmann KP (2002) Neural mechanisms of saccadic suppression. Science 295:2460–2462

    Article  PubMed  CAS  Google Scholar 

  • Thilo KV, Santoro L, Walsh V, Blakemore C (2004) The site of saccadic suppression. Nat Neurosci 7:13–14

    Article  PubMed  CAS  Google Scholar 

  • Tolias AS, Moore T, Smirnakis SM, Tehovnik EJ, Siapas AG, Schiller PH (2001) Eye movements modulate visual receptive fields of V4 neurons. Neuron 29:757–767

    Article  PubMed  CAS  Google Scholar 

  • Toyama K, Kimura M, Komatsu Y (1984) Activity of the striate cortex cells during saccadic eye movements of the alert cat. Neurosci Res 1:207–222

    Article  PubMed  CAS  Google Scholar 

  • Wurtz RH (1969) Comparison of effects of eye movements and stimulus movements on striate cortex neurons of the monkey. J Neurophysiol 32:987–994

    PubMed  CAS  Google Scholar 

  • Yarrow K, Rothwell JC (2003) Manual chronostasis: tactile perception precedes physical contact. Curr Biol 13:1134–1139

    Article  PubMed  CAS  Google Scholar 

  • Yarrow K, Haggard P, Heal R, Brown P, Rothwell JC (2001) Illusory perceptions of space and time preserve cross-saccadic perceptual continuity. Nature 414:302–305

    Article  PubMed  CAS  Google Scholar 

  • Zuber BL, Stark L (1966) Saccadic suppression: elevation of visual threshold associated with saccadic eye movements. Exp Neurol 16:65–79

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

Some of the work presented here was conducted using funds from the Australian Research Council Centre of Excellence in Vision Science (CE0561903) and two NIH grants (EY06069; RR0165). Thanks go to Professor Mustari, Drs Cloherty, Price, Crowder, Hietanen and Ono and to Tracey Broznya, Katia Peixoto and Anthony Gazy for help with experiments and animal care.

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Authors and Affiliations

  1. Visual Sciences, Research School of Biological Sciences, Australian National University, Canberra, Australia

    Michael R. Ibbotson

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  1. Michael R. Ibbotson
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Correspondence to Michael R. Ibbotson .

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  1. Hertie Inst. Klinische Gehirnforschung, Abt. Neurodegenerative Krankheiten, Universität Tübingen, Otfried-Müller-Str. 27, Tübingen, 72076, Germany

    Uwe J. Ilg

  2. CNRS, Inst. Neurosciences Cognitives de la, Université de la Méditerranée, Chemin Joseph Aiguier 31, Marseille CX 20, 13402, France

    Guillaume S. Masson

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Ibbotson, M.R. (2009). Intrasaccadic Motion: Neural Evidence for Saccadic Suppression and Postsaccadic Enhancement. In: Ilg, U., Masson, G. (eds) Dynamics of Visual Motion Processing. Springer, Boston, MA. https://doi.org/10.1007/978-1-4419-0781-3_11

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