Improved visual sensitivity during smooth pursuit eye movements

When we view the world around us, we constantly move our eyes. This brings objects of interest into the fovea and keeps them there, but visual sensitivity has been shown to deteriorate while the eyes are moving. Here we show that human sensitivity for some visual stimuli is improved during smooth pursuit eye movements. Detection thresholds for briefly flashed, colored stimuli were 16% lower during pursuit than during fixation. Similarly, detection thresholds for luminance-defined stimuli of high spatial frequency were lowered. These findings suggest that the pursuit-induced sensitivity increase may have its neuronal origin in the parvocellular retino-thalamic system. This implies that the visual system not only uses feedback connections to improve processing for locations and objects being attended to, but that a whole processing subsystem can be boosted. During pursuit, facilitation of the parvocellular system may reduce motion blur for stationary objects and increase sensitivity to speed changes of the tracked object.

[1]  D. H. Kelly Spatiotemporal variation of chromatic and achromatic contrast thresholds. , 1983, Journal of the Optical Society of America.

[2]  F A Wichmann,et al.  Ning for Helpful Comments and Suggestions. This Paper Benefited Con- Siderably from Conscientious Peer Review, and We Thank Our Reviewers the Psychometric Function: I. Fitting, Sampling, and Goodness of Fit , 2001 .

[3]  C. F. Stromeyer,et al.  Colour is what the eye sees best , 1993, Nature.

[4]  M. Roy,et al.  Contrast dependency of VEPs as a function of spatial frequency: the parvocellular and magnocellular contributions to human VEPs. , 2001, Spatial vision.

[5]  M. Morrone,et al.  Extraretinal Control of Saccadic Suppression , 2000, The Journal of Neuroscience.

[6]  D H Kelly,et al.  Luminous and chromatic flickering patterns have opposite effects. , 1975, Science.

[7]  P. Thier,et al.  Visual tracking neurons in primate area MST are activated by smooth-pursuit eye movements of an "imaginary" target. , 2003, Journal of neurophysiology.

[8]  C. A. Burbeck,et al.  Contrast gain measurements and the transient/sustained. , 1981, Journal of the Optical Society of America.

[9]  D. Flitcroft The interactions between chromatic aberration, defocus and stimulus chromaticity: Implications for visual physiology and colorimetry , 1989, Vision Research.

[10]  Akihiro Yagi,et al.  Improvement of chromatic temporal resolution during smooth pursuit eye movement , 2010 .

[11]  D. Burr,et al.  Selective suppression of the magnocellular visual pathway during saccadic eye movements , 1994, Nature.

[12]  R. Wurtz Response of striate cortex neurons to stimuli during rapid eye movements in the monkey. , 1969, Journal of neurophysiology.

[13]  J. Robson,et al.  Application of fourier analysis to the visibility of gratings , 1968, The Journal of physiology.

[14]  Saumil S. Patel,et al.  The temporal impulse response function in infantile nystagmus , 2003, Vision Research.

[15]  Dirk Kerzel,et al.  Improved visual sensitivity during smooth pursuit eye movements , 2010 .

[16]  Eileen Kowler,et al.  Shared attentional control of smooth eye movement and perception , 1986, Vision Research.

[17]  Karl R Gegenfurtner,et al.  Chromatic contrast sensitivity during optokinetic nystagmus, visually enhanced vestibulo-ocular reflex, and smooth pursuit eye movements. , 2009, Journal of neurophysiology.

[18]  R. Sperry Neural basis of the spontaneous optokinetic response produced by visual inversion. , 1950, Journal of comparative and physiological psychology.

[19]  S G Lisberger,et al.  Temporal properties of visual motion signals for the initiation of smooth pursuit eye movements in monkeys. , 1994, Journal of neurophysiology.

[20]  William H. Merigan,et al.  Spatio-temporal vision of macaques with severe loss of Pβ retinal ganglion cells , 1986, Vision Research.

[21]  P. Thier,et al.  Posterior Parietal Cortex Neurons Encode Target Motion in World-Centered Coordinates , 2004, Neuron.

[22]  Kathleen A Turano,et al.  Eye movements affect the perceived speed of visual motion , 1999, Vision Research.

[23]  G. Legge Sustained and transient mechanisms in human vision: Temporal and spatial properties , 1978, Vision Research.

[24]  Mitsuo Ikeda,et al.  Temporal Summation of Positive and Negative Flashes in the Visual System , 1965 .

[25]  A. Tomlinson,et al.  A comparison of saccadic and blink suppression in normal observers , 1997, Vision Research.

[26]  J. McCann,et al.  Visibility of low-spatial-frequency sine-wave targets: Dependence on number of cycles. , 1975, Journal of the Optical Society of America.

[27]  Harold E Bedell,et al.  Signals of eye-muscle proprioception modulate perceived motion smear. , 2008, Journal of vision.

[28]  E. Kaplan,et al.  The dynamics of primate M retinal ganglion cells , 1999, Visual Neuroscience.

[29]  R J Krauzlis,et al.  Shared motor error for multiple eye movements. , 1997, Science.

[30]  P. van Donkelaar,et al.  The allocation of attention during smooth pursuit eye movements. , 2002, Progress in brain research.

[31]  P. Schiller,et al.  Properties and tectal projections of monkey retinal ganglion cells. , 1977, Journal of neurophysiology.

[32]  A. Leventhal,et al.  Signal timing across the macaque visual system. , 1998, Journal of neurophysiology.

[33]  D. Burr,et al.  Selective depression of motion sensitivity during saccades. , 1982, The Journal of physiology.

[34]  Michael E. Goldberg,et al.  Effect of stimulus position and velocity upon the maintenance of smooth pursuit eye velocity , 1994, Vision Research.

[35]  R. Wurtz,et al.  Use of an extraretinal signal by monkey superior colliculus neurons to distinguish real from self-induced stimulus movement. , 1976, Journal of neurophysiology.

[36]  Junji Watanabe,et al.  Veridical perception of moving colors by trajectory integration of input signals. , 2007, Journal of vision.

[37]  Martina Poletti,et al.  Miniature eye movements enhance fine spatial detail , 2007, Nature.

[38]  C. Rashbass The visibility of transient changes of luminance , 1970, The Journal of physiology.

[39]  H. Levitt Transformed up-down methods in psychoacoustics. , 1971, The Journal of the Acoustical Society of America.

[40]  D. Kerzel,et al.  Visual short-term memory during smooth pursuit eye movements. , 2005, Journal of experimental psychology. Human perception and performance.

[41]  F A Bilsen,et al.  The influence of the number of cycles upon the visual contrast threshold for spatial sine wave patterns. , 1974, Vision research.

[42]  R. Wurtz,et al.  Guarding the gateway to cortex: attention in visual thalamus , 2008, Nature.

[43]  Shozo Tobimatsu,et al.  The effect of spatial frequency on chromatic and achromatic steady-state visual evoked potentials , 1999, Clinical Neurophysiology.

[44]  D. Burr,et al.  Temporal Impulse Response Functions for Luminance and Colour During Saccades , 1996, Vision Research.

[45]  K. Hoffmann,et al.  Responses of Neurons of the Nucleus of the Optic Tract and the Dorsal Terminal Nucleus of the Accessory Optic Tract in the Awake Monkey , 1996, The European journal of neuroscience.

[46]  Paul R. Martin,et al.  Extraclassical Receptive Field Properties of Parvocellular, Magnocellular, and Koniocellular Cells in the Primate Lateral Geniculate Nucleus , 2002, The Journal of Neuroscience.

[47]  D. Kiper,et al.  Chromatic properties of neurons in macaque area V2 , 1997, Visual Neuroscience.

[48]  P. Thier,et al.  Inability of Rhesus Monkey Area V1 to Discriminate Between Self‐induced and Externally Induced Retinal Image Slip , 1996, The European journal of neuroscience.

[49]  Dirk Kerzel,et al.  Effects of attention shifts to stationary objects during steady-state smooth pursuit eye movements , 2008, Vision Research.

[50]  P. Lennie,et al.  Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. , 1984, The Journal of physiology.

[51]  J. Kulikowski,et al.  Pattern and flicker detection analysed by subthreshold summation. , 1975, The Journal of physiology.

[52]  M. Hawken,et al.  Smooth pursuit eye movements to isoluminant targets. , 2008, Journal of neurophysiology.

[53]  A. Watson Probability summation over time , 1979, Vision Research.

[54]  G. Rizzolatti,et al.  Reorienting attention across the horizontal and vertical meridians: Evidence in favor of a premotor theory of attention , 1987, Neuropsychologia.

[55]  S. Nishida,et al.  Human Visual System Integrates Color Signals along a Motion Trajectory , 2007, Current Biology.

[56]  WH Merigan,et al.  Chromatic and achromatic vision of macaques: role of the P pathway , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[57]  S. B. Hutton,et al.  The effects of dividing attention on smooth pursuit eye tracking , 2005, Experimental Brain Research.

[58]  M. Pinsk,et al.  Attention modulates responses in the human lateral geniculate nucleus , 2002, Nature Neuroscience.

[59]  P. Cavanagh,et al.  Position-based motion perception for color and texture stimuli: effects of contrast and speed , 1999, Vision Research.

[60]  N. Logothetis,et al.  Functions of the colour-opponent and broad-band channels of the visual system , 1990, Nature.

[61]  K. Hoffmann,et al.  Neural Mechanisms of Saccadic Suppression , 2002, Science.

[62]  D. Burr,et al.  Changes in visual perception at the time of saccades , 2001, Trends in Neurosciences.

[63]  S. B. Stevenson,et al.  Dependence of visual suppression on the amplitudes of saccades and blinks , 1986, Vision Research.

[64]  E. J. Morris,et al.  Visual motion processing and sensory-motor integration for smooth pursuit eye movements. , 1987, Annual review of neuroscience.

[65]  R. Reid,et al.  Saccadic Eye Movements Modulate Visual Responses in the Lateral Geniculate Nucleus , 2002, Neuron.

[66]  R H Wurtz,et al.  Comparison of effects of eye movements and stimulus movements on striate cortex neurons of the monkey. , 1969, Journal of neurophysiology.

[67]  A. Watson,et al.  A standard model for foveal detection of spatial contrast. , 2005, Journal of vision.

[68]  M Concetta Morrone,et al.  Saccadic eye movements cause compression of time as well as space , 2005, Nature Neuroscience.

[69]  G. Schwarz Estimating the Dimension of a Model , 1978 .

[70]  John B. Shoven,et al.  I , Edinburgh Medical and Surgical Journal.

[71]  William Bialek,et al.  Time Course of Precision in Smooth-Pursuit Eye Movements of Monkeys , 2007, The Journal of Neuroscience.

[72]  I. Bodis-Wollner,et al.  Visual contrast sensitivity , 1988, Neurology.

[73]  E. Holst,et al.  Das Reafferenzprinzip , 2004, Naturwissenschaften.

[74]  D. H. Kelly,et al.  Retinal inhomogeneity. I. Spatiotemporal contrast sensitivity. , 1984, Journal of the Optical Society of America. A, Optics and image science.

[75]  Karl R Gegenfurtner,et al.  Temporal contrast sensitivity during smooth pursuit eye movements. , 2007, Journal of vision.

[76]  Alexander Thiele,et al.  Speed skills: measuring the visual speed analyzing properties of primate MT neurons , 2001, Nature Neuroscience.

[77]  David Burr,et al.  Suppression of the magnocellular pathway during saccades , 1996, Behavioural Brain Research.

[78]  S. Lisberger,et al.  Initial tracking conditions modulate the gain of visuo-motor transmission for smooth pursuit eye movements in monkeys , 1994, Visual Neuroscience.

[79]  Stephen G. Lisberger,et al.  Regulation of the gain of visually guided smooth-pursuit eye movements by frontal cortex , 2001, Nature.

[80]  S. Lisberger,et al.  Role of arcuate frontal cortex of monkeys in smooth pursuit eye movements. I. Basic response properties to retinal image motion and position. , 2002, Journal of neurophysiology.

[81]  R. Marrocco,et al.  Monkey superior colliculus: properties of single cells and their afferent inputs. , 1977, Journal of neurophysiology.

[82]  Karl R. Gegenfurtner,et al.  Contrast sensitivity during the initiation of smooth pursuit eye movements , 2007, Vision Research.

[83]  D. Pollen,et al.  Striate cortex increases contrast gain of macaque LGN neurons , 2000, Visual Neuroscience.

[84]  Mingsha Zhang,et al.  The proprioceptive representation of eye position in monkey primary somatosensory cortex , 2007, Nature Neuroscience.

[85]  K. Gegenfurtner,et al.  Memory modulates color appearance , 2006, Nature Neuroscience.

[86]  Karl R. Gegenfurtner,et al.  Temporal and chromatic properties of motion mechanisms , 1995, Vision Research.

[87]  P. Lennie,et al.  Chromatic mechanisms in lateral geniculate nucleus of macaque. , 1984, The Journal of physiology.

[88]  W. Merigan,et al.  Spatial resolution across the macaque retina , 1990, Vision Research.

[89]  D. Burr Motion smear , 1980, Nature.

[90]  K. Uchikawa,et al.  Temporal integration of chromatic double pulses for detection of equal-luminance wavelength changes. , 1986, Journal of the Optical Society of America. A, Optics and image science.

[91]  M. Landy,et al.  Properties of second-order spatial frequency channels , 2002, Vision Research.

[92]  K. Nakayama,et al.  Two Distinct Visual Motion Mechanisms for Smooth Pursuit: Evidence from Individual Differences , 2007, Neuron.

[93]  Harold E. Bedell,et al.  Asymmetry of perceived motion smear during head and eye movements: Evidence for a dichotomous neural categorization of retinal image motion , 2005, Vision Research.

[94]  P. Schiller,et al.  Composition of geniculostriate input ot superior colliculus of the rhesus monkey. , 1979, Journal of neurophysiology.

[95]  Seiji Ono,et al.  Extraretinal signals in MSTd neurons related to volitional smooth pursuit. , 2006, Journal of neurophysiology.

[96]  H. Barlow Temporal and spatial summation in human vision at different background intensities , 1958, The Journal of physiology.

[97]  Eli Brenner,et al.  Mislocalization of flashes during smooth pursuit hardly depends on the lighting conditions , 2006, Vision Research.

[98]  W. Newsome,et al.  Deficits in visual motion processing following ibotenic acid lesions of the middle temporal visual area of the macaque monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[99]  B. Knight,et al.  Contrast gain control in the primate retina: P cells are not X-like, some M cells are , 1992, Visual Neuroscience.

[100]  B. Wandell,et al.  Matching color images: the effects of axial chromatic aberration , 1994 .

[101]  Harry J. Wyatt,et al.  Detecting saccades with jerk , 1998, Vision Research.

[102]  J. Pokorny,et al.  Spatial frequency processing in inferred PC- and MC-pathways , 2003, Vision Research.

[103]  D. Heeger,et al.  Center-surround interactions in foveal and peripheral vision , 2000, Vision Research.

[104]  D. Hubel,et al.  The role of fixational eye movements in visual perception , 2004, Nature Reviews Neuroscience.

[105]  David R. Anderson,et al.  Model selection and multimodel inference : a practical information-theoretic approach , 2003 .

[106]  V. Casagrande A third parallel visual pathway to primate area V1 , 1994, Trends in Neurosciences.

[107]  R. Wurtz Neuronal mechanisms of visual stability , 2008, Vision Research.

[108]  J. Maunsell,et al.  The effects of parvocellular lateral geniculate lesions on the acuity and contrast sensitivity of macaque monkeys , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[109]  Saumil S. Patel,et al.  The temporal impulse response function during smooth pursuit , 2009, Vision Research.

[110]  David C. Burr,et al.  Impulse-response functions for chromatic and achromatic stimuli , 1993 .

[111]  V. S. Ramachandran,et al.  Perception of shape from shading , 1988, Nature.

[112]  J J Koenderink,et al.  Spatiotemporal contrast detection threshold surface is bimodal. , 1979, Optics letters.

[113]  E. Sutter,et al.  M and P Components of the VEP and their Visual Field Distribution , 1997, Vision Research.

[114]  Leslie G. Ungerleider,et al.  The role of striate cortex in the guidance of eye movements in the monkey , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[115]  Joel Pokorny,et al.  Responses to pulses and sinusoids in macaque ganglion cells , 1994, Vision Research.

[116]  T. Freeman,et al.  Extra-Retinal Vision: Firing at Will , 2007, Current Biology.

[117]  W. Newsome,et al.  Motion selectivity in macaque visual cortex. I. Mechanisms of direction and speed selectivity in extrastriate area MT. , 1986, Journal of neurophysiology.

[118]  Richard E. Kronauer,et al.  Temporal properties of the red-green chromatic mechanism , 1994, Vision Research.

[119]  Gunnar Blohm,et al.  Direct evidence for a position input to the smooth pursuit system. , 2005, Journal of neurophysiology.

[120]  M. Hawken,et al.  Psychophysics: Threshold Measurements Interaction of Motion and Color in the Visual Pathways , 2022 .

[121]  R. Hess,et al.  The functional area for summation to threshold for sinusoidal gratings , 1978, Vision Research.

[122]  Harold E Bedell,et al.  Suppression of motion-produced smear during smooth pursuit eye movements , 1996, Current Biology.

[123]  K. Uchikawa,et al.  Saccadic suppression of achromatic and chromatic responses measured by increment-threshold spectral sensitivity. , 1995, Journal of the Optical Society of America. A, Optics, image science, and vision.

[124]  O E Favreau,et al.  Perceived velocity of moving chromatic gratings. , 1984, Journal of the Optical Society of America. A, Optics and image science.

[125]  P. O. Bishop,et al.  Spatial vision. , 1971, Annual review of psychology.

[126]  H. Akaike A new look at the statistical model identification , 1974 .

[127]  David W. Royal,et al.  Correlates of motor planning and postsaccadic fixation in the macaque monkey lateral geniculate nucleus , 2005, Experimental Brain Research.

[128]  Harold E. Bedell,et al.  Direction and extent of perceived motion smear during pursuit eye movement , 2007, Vision Research.

[129]  J. Maunsell,et al.  Macaque vision after magnocellular lateral geniculate lesions , 1990, Visual Neuroscience.

[130]  L Mitrani,et al.  Dependence of visual suppression on the angular size of voluntary saccadic eye movements. , 1970, Vision research.

[131]  David C. Burr,et al.  Compression of visual space before saccades , 1997, Nature.

[132]  M. Ibbotson,et al.  Enhanced motion sensitivity follows saccadic suppression in the superior temporal sulcus of the macaque cortex. , 2006, Cerebral cortex.

[133]  J. Movshon,et al.  Chromatic properties of neurons in macaque MT , 1994, Visual Neuroscience.