Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-24T18:31:34.055Z Has data issue: false hasContentIssue false
  • English
  • Français

Improved visual sensitivity during smooth pursuit eye movements: Temporal and spatial characteristics

Published online by Cambridge University Press:  01 May 2009

ALEXANDER C. SCHÜTZ ,
DORIS I. BRAUN  and
KARL R. GEGENFURTNER
ALEXANDER C. SCHÜTZ*
Affiliation:
Abteilung Allgemeine Psychologie, Justus-Liebig-Universität, Giessen, Germany
DORIS I. BRAUN
Affiliation:
Abteilung Allgemeine Psychologie, Justus-Liebig-Universität, Giessen, Germany
KARL R. GEGENFURTNER
Affiliation:
Abteilung Allgemeine Psychologie, Justus-Liebig-Universität, Giessen, Germany
*
*Address correspondence and reprint requests to: Abteilung Allgemeine Psychologie, Justus-Liebig-Universität, Otto-Behaghel-Str. 10F, 35394 Giessen, Germany. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Recently, we showed that contrast sensitivity for color and high–spatial frequency luminance stimuli is enhanced during smooth pursuit eye movements (Schütz et al., 2008). In this study, we investigated the enhancement over a wide range of temporal and spatial frequencies. In Experiment 1, we measured the temporal impulse response function (TIRF) for colored stimuli. The TIRF for pursuit and fixation differed mostly with respect to the gain but not with respect to the natural temporal frequency. Hence, the sensitivity enhancement seems to be rather independent of the temporal frequency of the stimuli. In Experiment 2, we measured the spatial contrast sensitivity function for luminance-defined Gabor patches with spatial frequencies ranging from 0.2 to 7 cpd. We found a sensitivity improvement during pursuit for spatial frequencies above 2–3 cpd. Between 0.5 and 3 cpd, sensitivity was impaired by smooth pursuit eye movements, but no consistent difference was observed below 0.5 cpd. The results of both experiments are consistent with an increased contrast gain of the parvocellular retinogeniculate pathway.

Keywords

Smooth pursuit eye movementsTemporal contrast sensitivityTemporal Impulse ResponseSpatial contrast sensitivityColor contrast sensitivitySensitivity enhancement
Type
Research Articles
Information
Visual Neuroscience , Volume 26 , Issue 3 , May 2009 , pp. 329 - 340
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Akaike, H. (1974). A new look at the statistical model identification. IEE Transactions on Automatic Control AC 19, 716–723.CrossRefGoogle Scholar
Arakawa, K., Tobimatsu, S., Tomoda, H., Kira, J. & Kato, M. (1999). The effect of spatial frequency on chromatic and achromatic steady-state visual evoked potentials. Clinical Neurophysiology 110, 1959–1964.CrossRefGoogle ScholarPubMed
Barlow, H.B. (1958). Temporal and spatial summation in human vision at different background intensities. The Journal of Physiology 141, 337–350.CrossRefGoogle ScholarPubMed
Baseler, H.A. & Sutter, E.E. (1997). M and P components of the VEP and their visual field distribution. Vision Research 37, 675–690.CrossRefGoogle ScholarPubMed
Bedell, H.E. & Lott, L.A. (1996). Suppression of motion-produced smear during smooth pursuit eye movements. Current Biology 6, 1032–1034.CrossRefGoogle ScholarPubMed
Bedell, H.E., Ramamurthy, M., Patel, S.S. & Vu-Yu, L.P. (2003). The temporal impulse response function during smooth pursuit. Journal of Vision 3, 210a.CrossRefGoogle Scholar
Bedell, H.E., Ramamurthy, M., Patel, S.S., Subramaniam, S., Vu-Yu, L.P. & Tong, J. (2008). The temporal impulse response function in infantile nystagmus. Vision Research 48, 1575–1583.Google Scholar
Benardete, E.A. & Kaplan, E. (1999). The dynamics of primate M retinal ganglion cells. Visual Neuroscience 16, 355–368.CrossRefGoogle ScholarPubMed
Benardete, E.A., Kaplan, E. & Knight, B.W. (1992). Contrast gain control in the primate retina: P cells are not X-like, some M cells are. Visual Neuroscience 8, 483–486.CrossRefGoogle ScholarPubMed
Braun, D.I., Mennie, N., Rasche, C., Schutz, A.C., Hawken, M.J. & Gegenfurtner, K.R. (2008). Smooth pursuit eye movements to isoluminant targets. Journal of Neurophysiology 100, 1287–1300.CrossRefGoogle ScholarPubMed
Burbeck, C.A. & Kelly, D.H. (1981). Contrast gain measurements and the transient/sustained. Journal of the Optical Society of America 71, 1335–1342.CrossRefGoogle ScholarPubMed
Burnham, K.P. & Anderson, D.R. (2002). Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. New York: Springer.Google Scholar
Burr, D.C. (1980). Motion smear. Nature 284, 164–165.CrossRefGoogle ScholarPubMed
Burr, D.C., Holt, J., Johnstone, J.R. & Ross, J. (1982). Selective depression of motion sensitivity during saccades. The Journal of Physiology 333, 1–15.Google Scholar
Burr, D.C. & Morrone, M.C. (1993). Impulse-response functions for chromatic and achromatic stimuli. Journal of the Optical Society of America A 10, 1706–1713.Google Scholar
Burr, D.C. & Morrone, M.C. (1996). Temporal impulse response functions for luminance and colour during saccades. Vision Research 36, 2069–2078.CrossRefGoogle ScholarPubMed
Burr, D.C., Morrone, M.C. & Ross, J. (1994). Selective suppression of the magnocellular visual pathway during saccadic eye movements. Nature 371, 511–513.CrossRefGoogle ScholarPubMed
Campbell, F.W. & Robson, J.G. (1968). Application of Fourier analysis to the visibility of gratings. The Journal of Physiology 197, 551–566.CrossRefGoogle Scholar
Cavanagh, P., Tyler, C.W. & Favreau, O.E. (1984). Perceived velocity of moving chromatic gratings. Journal of the Optical Society of America A 1, 893–899.CrossRefGoogle ScholarPubMed
Derrington, A.M., Krauskopf, J. & Lennie, P. (1984). Chromatic mechanisms in lateral geniculate nucleus of macaque. The Journal of Physiology 357, 241–265.CrossRefGoogle ScholarPubMed
Derrington, A.M. & Lennie, P. (1984). Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. The Journal of Physiology 357, 219–240.CrossRefGoogle ScholarPubMed
De Valois, R.L. & De Valois, K.K. (1988). Spatial Vision. New York: Oxford University Press.Google Scholar
Diamond, M.R., Ross, J. & Morrone, M.C. (2000). Extraretinal control of saccadic suppression. Journal of Neuroscience 20, 3449–3455.Google Scholar
Ellemberg, D., Hammarrenger, B., Lepore, F., Roy, M.S. & Guillemot, J.P. (2001). Contrast dependency of VEPs as a function of spatial frequency: The parvocellular and magnocellular contributions to human VEPs. Spatial Vision 15, 99–111.CrossRefGoogle ScholarPubMed
Eskew, R.T. Jr, Stromeyer, C.F. III & Kronauer, R.E. (1994). Temporal properties of the red-green chromatic mechanism. Vision Research 34, 3127–3137.CrossRefGoogle ScholarPubMed
Flitcroft, D.I. (1989). The interactions between chromatic aberration, defocus and stimulus chromaticity: Implications for visual physiology and colorimetry. Vision Research 29, 349–360.Google Scholar
Gegenfurtner, K.R. & Hawken, M.J. (1995). Temporal and chromatic properties of motion mechanisms. Vision Research 35, 1547–1563.CrossRefGoogle ScholarPubMed
Gegenfurtner, K.R. & Hawken, M.J. (1996). Interaction of motion and color in the visual pathways. Trends in Neurosciences 19, 394–401.Google Scholar
Hoekstra, J., van der Goot, D.P., van den Brink, G. & Bilsen, F.A. (1974). The influence of the number of cycles upon the visual contrast threshold for spatial sine wave patterns. Vision Research 14, 365–368.Google Scholar
Holt, E.B. (1903). Eye movements and central anaesthesia. Psychological Review 4, 3–45.Google Scholar
Howell, E.R. (1978). The functional area for summation to threshold for sinusoidal gratings. Vision Research 18, 369–374.Google Scholar
Hutton, S.B. & Tegally, D. (2005). The effects of dividing attention on smooth pursuit eye tracking. Experimental Brain Research 163, 306–313.Google Scholar
Ibbotson, M.R., Price, N.S., Crowder, N.A., Ono, S. & Mustari, M.J. (2007). Enhanced motion sensitivity follows saccadic suppression in the superior temporal sulcus of the macaque cortex. Cerebral Cortex 17, 1129–1138.Google Scholar
Ikeda, M. (1965). Temporal summation of positive and negative flashes in the visual system. Journal of the Optical Society of America 55, 1527–1534.Google Scholar
Kelly, D.H. (1975). Luminous and chromatic flickering patterns have opposite effects. Science 188, 371–372.Google Scholar
Kelly, D.H. (1977). Visual contrast sensitivity. Optica Acta 24, 107–129.CrossRefGoogle Scholar
Kelly, D.H. (1983). Spatiotemporal variation of chromatic and achromatic contrast thresholds. Journal of the Optical Society of America 73, 742–750.CrossRefGoogle ScholarPubMed
Kelly, D.H. (1984). Retinal inhomogeneity. I. Spatiotemporal contrast sensitivity. Journal of the Optical Society of America A 1, 107–113.Google Scholar
Kerzel, D., Souto, D. & Ziegler, N.E. (2008). Effects of attention shifts to stationary objects during steady-state smooth pursuit eye movements. Vision Research 48, 958–969.CrossRefGoogle ScholarPubMed
Kerzel, D. & Ziegler, N.E. (2005). Visual short-term memory during smooth pursuit eye movements. Journal of Experimental Psychology: Human Perception and Performance 31, 354–372.Google ScholarPubMed
Khurana, B. & Kowler, E. (1987). Shared attentional control of smooth eye movement and perception. Vision Research 27, 1603–1618.Google Scholar
King-Smith, P.E. & Kulikowski, J.J. (1975). Pattern and flicker detection analysed by subthreshold summation. The Journal of Physiology 249, 519–548.CrossRefGoogle ScholarPubMed
Koenderink, J.J. & Doorn, A.J.v. (1979). Spatiotemporal contrast detection threshold surface is bimodal. Optics Letters 4, 32–34.Google Scholar
Landy, M.S. & Oruc, I. (2002). Properties of second-order spatial frequency channels. Vision Research 42, 2311–2329.Google Scholar
Lee, B.B., Pokorny, J., Smith, V.C. & Kremers, J. (1994). Responses to pulses and sinusoids in macaque ganglion cells. Vision Research 34, 3081–3096.CrossRefGoogle ScholarPubMed
Legge, G.E. (1978). Sustained and transient mechanisms in human vision: Temporal and spatial properties. Vision Research 18, 69–81.Google Scholar
Leonova, A., Pokorny, J. & Smith, V.C. (2003). Spatial frequency processing in inferred PC- and MC-pathways. Vision Research 43, 2133–2139.CrossRefGoogle ScholarPubMed
Levitt, H. (1971). Transformed up-down methods in psychoacoustics. Journal of the Acoustical Society of America 49, 467–477.Google Scholar
Marimont, D.H. & Wandell, B.A. (1994). Matching color images: The effects of axial chromatic aberration. Journal of the Optical Society of America A 11, 3113–3122.CrossRefGoogle Scholar
Marrocco, R.T. & Li, R.H. (1977). Monkey superior colliculus: Properties of single cells and their afferent inputs. Journal of Neurophysiology 40, 844–860.Google Scholar
McAlonan, K., Cavanaugh, J. & Wurtz, R.H. (2008). Guarding the gateway to cortex with attention in visual thalamus. Nature 456, 391–394.CrossRefGoogle ScholarPubMed
Merigan, W.H. (1989). Chromatic and achromatic vision of macaques: Role of the P pathway. Journal of Neuroscience 9, 776–783.Google Scholar
Merigan, W.H. & Eskin, T.A. (1986). Spatio-temporal vision of macaques with severe loss of P beta retinal ganglion cells. Vision Research 26, 1751–1761.Google Scholar
Merigan, W.H. & Katz, L.M. (1990). Spatial resolution across the macaque retina. Vision Research 30, 985–991.Google Scholar
Merigan, W.H., Katz, L.M. & Maunsell, J.H. (1991). The effects of parvocellular lateral geniculate lesions on the acuity and contrast sensitivity of macaque monkeys. Journal of Neuroscience 11, 994–1001.CrossRefGoogle ScholarPubMed
Merigan, W.H. & Maunsell, J.H. (1990). Macaque vision after magnocellular lateral geniculate lesions. Visual Neuroscience 5, 347–352.Google Scholar
Mitrani, L., Yakimoff, N. & Mateeff, S. (1970). Dependence of visual suppression on the angular size of voluntary saccadic eye movements. Vision Research 10, 411–415.Google Scholar
Nishida, S., Watanabe, J., Kuriki, I. & Tokimoto, T. (2007). Human visual system integrates color signals along a motion trajectory. Current Biology 17, 366–372.Google Scholar
O’Connor, D.H., Fukui, M.M., Pinsk, M.A. & Kastner, S. (2002). Attention modulates responses in the human lateral geniculate nucleus. Nature Neuroscience 5, 1203–1209.Google Scholar
Olzak, L.A. & Thomas, J.P. (1986). Seeing spatial patterns. In Handbook of Perception and Human Performance, Vol. 7, ed. Boff, K.R., Kaufman, L. & Thomas, J.P., pp. 1–56. New York: Wiley.Google Scholar
Przybyszewski, A.W., Gaska, J.P., Foote, W. & Pollen, D.A. (2000). Striate cortex increases contrast gain of macaque LGN neurons. Visual Neuroscience 17, 485–494.CrossRefGoogle ScholarPubMed
Rashbass, C. (1970). The visibility of transient changes of luminance. The Journal of Physiology 210, 165–186.CrossRefGoogle ScholarPubMed
Reppas, J.B., Usrey, W.M. & Reid, R.C. (2002). Saccadic eye movements modulate visual responses in the lateral geniculate nucleus. Neuron 35, 961–974.Google Scholar
Ridder, W.H. III & Tomlinson, A. (1997). A comparison of saccadic and blink suppression in normal observers. Vision Research 37, 3171–3179.Google Scholar
Rizzolatti, G., Riggio, L., Dascola, I. & Umilta, C. (1987). Reorienting attention across the horizontal and vertical meridians: Evidence in favor of a premotor theory of attention. Neuropsychologia 25, 31–40.CrossRefGoogle ScholarPubMed
Robinson, D.L. & Wurtz, R.H. (1976). Use of an extraretinal signal by monkey superior colliculus neurons to distinguish real from self-induced stimulus movement. Journal of Neurophysiology 39, 852–870.Google Scholar
Ross, J., Burr, D. & Morrone, C. (1996). Suppression of the magnocellular pathway during saccades. Behavioral Brain Research 80, 1–8.Google Scholar
Ross, J., Morrone, M.C., Goldberg, M.E. & Burr, D.C. (2001). Changes in visual perception at the time of saccades. Trends in Neurosciences 24, 113–121.Google Scholar
Royal, D.W., Sary, G., Schall, J.D. & Casagrande, V.A. (2006). Correlates of motor planning and postsaccadic fixation in the macaque monkey lateral geniculate nucleus. Experimental Brain Research 168, 62–75.Google Scholar
Savoy, R.L. & McCann, J.J. (1975). Visibility of low-spatial-frequency sine-wave targets: Dependence on number of cycles. Journal of the Optical Society of America 65, 343–350.Google Scholar
Schiller, P.H. & Malpeli, J.G. (1977). Properties and tectal projections of monkey retinal ganglion cells. Journal of Neurophysiology 40, 428–445.Google Scholar
Schiller, P.H., Malpeli, J.G. & Schein, S.J. (1979). Composition of geniculostriate input ot superior colliculus of the rhesus monkey. Journal of Neurophysiology 42, 1124–1133.Google Scholar
Schütz, A.C., Braun, D.I. & Gegenfurtner, K.R. (2009). Chromatic contrast sensitivity during optokinetic nystagmus, visually-enhanced vestibulo-ocular reflex and smooth pursuit eye movements. Journal of Neurophysiology 101, 2317–2327.Google Scholar
Schütz, A.C., Braun, D.I., Kerzel, D. & Gegenfurtner, K.R. (2008). Improved visual sensitivity during smooth pursuit eye movements. Nature Neuroscience 11, 1211–1216.Google Scholar
Schütz, A.C., Delipetkos, E., Braun, D.I., Kerzel, D. & Gegenfurtner, K.R. (2007). Temporal contrast sensitivity during smooth pursuit eye movements. Journal of Vision 7, 1–15.Google Scholar
Schwarz, G. (1978). Estimating the dimension of a model. The Annals of Statistics 6, 461–464.Google Scholar
Solomon, S.G., White, A.J. & Martin, P.R. (2002). Extraclassical receptive field properties of parvocellular, magnocellular, and koniocellular cells in the primate lateral geniculate nucleus. Journal of Neuroscience 22, 338–349.Google Scholar
Sperry, R.W. (1950). Neural basis of the spontaneous optokinetic response produced by visual inversion. Journal of Comparative and Physiological Psychology 43, 482–489.CrossRefGoogle ScholarPubMed
Stevenson, S.B., Volkmann, F.C., Kelly, J.P. & Riggs, L.A. (1986). Dependence of visual suppression on the amplitudes of saccades and blinks. Vision Research 26, 1815–1824.Google Scholar
Terao, M., Watanabe, J., Yagi, A. & Nishida, S. (2008). Improvement of chromatic temporal resolution during smooth pursuit eye movement. Journal of Vision 8, 663a.Google Scholar
Thiele, A., Henning, P., Kubischik, M. & Hoffmann, K.P. (2002). Neural mechanisms of saccadic suppression. Science 295, 2460–2462.Google Scholar
Tong, J., Aydin, M. & Bedell, H.E. (2007). Direction and extent of perceived motion smear during pursuit eye movement. Vision Research 47, 1011–1019.Google Scholar
Tong, J., Patel, S.S. & Bedell, H.E. (2005). Asymmetry of perceived motion smear during head and eye movements: Evidence for a dichotomous neural categorization of retinal image motion. Vision Research 45, 1519–1524.CrossRefGoogle ScholarPubMed
Tong, J., Patel, S.S. & Bedell, H.E. (2006). Asymmetrical modulation of the temporal impulse response during smooth pursuit. Journal of Vision 6, 866a.Google Scholar
Tong, J., Stevenson, S.B. & Bedell, H.E. (2008). Signals of eye-muscle proprioception modulate perceived motion smear. Journal of Vision 8, 1–6.Google Scholar
Uchikawa, K. & Ikeda, M. (1986). Temporal integration of chromatic double pulses for detection of equal-luminance wavelength changes. Journal of the Optical Society of America A 3, 2109–2115.Google Scholar
Uchikawa, K. & Sato, M. (1995). Saccadic suppression of achromatic and chromatic responses measured by increment-threshold spectral sensitivity. Journal of the Optical Society of America A 12, 661–666.Google Scholar
von Holst, E. & Mittelstaedt, H. (1950). Das Reafferenzprinzip. Die Naturwissenschaften 37, 464–476.Google Scholar
Wang, X., Zhang, M., Cohen, I.S. & Goldberg, M.E. (2007). The proprioceptive representation of eye position in monkey primary somatosensory cortex. Nature Neuroscience 10, 640–646.CrossRefGoogle ScholarPubMed
Watanabe, J. & Nishida, S. (2007). Veridical perception of moving colors by trajectory integration of input signals. Journal of Vision 7, 1–16.Google Scholar
Watson, A.B. (1979). Probability summation over time. Vision Research 19, 515–522.Google Scholar
Watson, A.B. (1986). Temporal sensitivity. In Handbook of Perception and Human Performance, Vol. 6, ed. Boff, K.R., Kaufman, L. & Thomas, J.P., pp. 1–43. New York: Wiley.Google Scholar
Watson, A.B. & Ahumada, A.J. Jr. (2005). A standard model for foveal detection of spatial contrast. Journal of Vision 5, 717–740.Google Scholar
White, B.J., Boehnke, S.E., Marino, R.A., Itti, L. & Munoz, D.P. (2008). Color Signals in the Primate Superior Colliculus. Journal of Vision 8, 5a.Google Scholar
Wichmann, F.A. & Hill, N.J. (2001). The psychometric function: I. Fitting, sampling, and goodness of fit. Perception & Psychophysics 63, 1293–1313.Google Scholar
Wurtz, R.H. (1969 a). Comparison of effects of eye movements and stimulus movements on striate cortex neurons of the monkey. Journal of Neurophysiology 32, 987–994.Google Scholar
Wurtz, R.H. (1969 b). Response of striate cortex neurons to stimuli during rapid eye movements in the monkey. Journal of Neurophysiology 32, 975–986.Google Scholar
Wurtz, R.H. (2008). Neuronal mechanisms of visual stability. Vision Research 48, 2070–2089.Google Scholar
Wyatt, H.J. (1998). Detecting saccades with jerk. Vision Research 38, 2147–2153.CrossRefGoogle ScholarPubMed
Xing, J. & Heeger, D.J. (2000). Center-surround interactions in foveal and peripheral vision. Vision Research 40, 3065–3072.Google Scholar
Supplementary material: PDF

Schutz supplementary material

Tables and figures.pdf

Download Schutz supplementary material(PDF)
PDF 199 KB