Age Related Changes to Perceptual Surround Suppression of Moving Stimuli

In: Seeing and Perceiving
View More View Less
  • 1 Department of Optometry and Vision Sciences, University of Melbourne, Parkville 3010, Australia

Purchase instant access (PDF download and unlimited online access):

Perceptual analogues of centre–surround suppression have been applied as indirect measures of cortical inhibitory function in several clinical disorders. Two tasks have been used: a centre–surround contrast perception task and a motion direction discrimination task, where the stimulus size and contrast is varied to measure surround suppression effects. The tasks are markedly different, yet previous literature implies that both measures indirectly assess inhibitory function and that results will be complementary. This is not the case for age-related effects on surround suppression, however, as previous reports using the different measures are conflicting. Here we use a low-spatial frequency, drifting grating version of the centre–surround contrast perception task, and compare results to those obtained with the motion direction task in a single group of older observers. Older adults demonstrate significantly increased perceptual surround suppression of contrast for drifting, high contrast stimuli. Using the motion discrimination task, older observers showed similar amounts of surround suppression for the largest stimulus. This study confirms that visual surround suppression is altered by ageing. The complexity of neuronal systems involved in centre–surround interactions makes it unlikely that a single perceptual task will be sufficient to describe the effects of clinical disorders on surround suppression.

  • Angelucci A., Bressloff P. C. (2006). Contribution of feedforward, lateral and feedback connections to the classical receptive field center and extra-classical receptive field surround of primate V1 neurons, in: Progress in Brain Research, Martinez-Conde S., Macknik S. L., Martinez L. M., Alonso J. M., Tse P. U. (Eds), Vol. 154, pp.  93120. Elsevier, Dordrecht.

    • Search Google Scholar
    • Export Citation
  • Bair W., Cavanaugh J. R., Movshon J. A. (2003). Time course and time–distance relationships for surround suppression in Macaque V1 neurons, J. Neurosci. 23, 76907701.

    • Search Google Scholar
    • Export Citation
  • Battista J., Badcock D. R., McKendrick A. M. (2010). Center–surround visual motion processing in migraine, Invest. Ophthalmol. Vis. Sci. 51, 60706076.

    • Search Google Scholar
    • Export Citation
  • Battista J., Badcock D. R., McKendrick A. M. (2011). Migraine increases centre–surround suppression for drifting visual stimuli, PLoS One 6, e18211.

    • Search Google Scholar
    • Export Citation
  • Betts L. R., Taylor C. P., Sekuler A. B., Bennett P. J. (2005). Aging reduces center–surround antagonism in visual motion processing, Neuron 45, 361366.

    • Search Google Scholar
    • Export Citation
  • Bonin V., Mante V., Carandini M. (2005). The suppressive field of neurons in lateral geniculate nucleus, J. Neurosci. 25, 1084410856.

  • Cannon M. W., Fullenkamp S. C. (1991). Spatial interactions in apparent contrast: inhibitory effects among grating patterns of different spatial frequencies, spatial positions and orientations, Vision Res. 31, 19851998.

    • Search Google Scholar
    • Export Citation
  • Cavanaugh J. R., Bair W., Movshon J. A. (2002a). Nature and interaction of signals from the receptive field center and surround in Macaque V1 neurons, J. Neurophysiol. 88, 25302546.

    • Search Google Scholar
    • Export Citation
  • Cavanaugh J. R., Bair W., Movshon J. A. (2002b). Selectivity and spatial distribution of signals from the receptive field surround in Macaque V1 neurons, J. Neurophysiol. 88, 25472556.

    • Search Google Scholar
    • Export Citation
  • Chubb C., Sperling G., Solomon J. A. (1989). Texture interactions determine perceived contrast, Proc. Natl. Acad. Sci. USA 86, 96319635.

  • Churan J., Khawaja F. A., Tsui J. M. G., Pack C. C. (2008). Brief motion stimuli preferentially activate surround-suppressed neurons in macaque visual area MT, Curr. Biol. 18, R1051R1052.

    • Search Google Scholar
    • Export Citation
  • Croner L. J., Kaplan E. (1995). Receptive fields of P and M ganglion cells across the primate retina, Vision Res. 35, 724.

  • Dakin S., Carlin P., Hemsley D. (2005). Weak suppression of visual context in chronic schizophrenia, Curr. Biol. 15, R822R824.

  • Ditchfield J. A., McKendrick A. M., Badcock D. R. (2006). Processing of global form and motion in migraineurs, Vision Res. 46, 141148.

  • Ejima Y., Takahashi S. (1985). Apparent contrast of a sinusoidal grating in the simultaneous presence of peripheral gratings, Vision Res. 25, 12231232.

    • Search Google Scholar
    • Export Citation
  • Glasser D. M., Tadin D. (2010). Low-level mechanisms do not explain paradoxical motion percepts, J. Vision 10, 19.

  • Golomb J. D., McDavitt J. R. B., Ruf B. M., Chen J. I., Saricicek A., Maloney K. H., Hu J., Chun M. M., Bhagwagar Z. (2009). Enhanced visual motion perception in major depressive disorder, J. Neurosci. 29, 90729077.

    • Search Google Scholar
    • Export Citation
  • Henson D. B., Chaudry S., Artes P. H., Faragher E. B., Ansons A. (2000). Response variability in the visual field: comparison of optic neuritis, glaucoma, ocular hypertension and normal eyes, Investigat. Ophthalmol. Vis. Sci. 41, 417421.

    • Search Google Scholar
    • Export Citation
  • Huang W., Jiao L., Jia J. (2008a). Modeling contextual modulation in the primary visual cortex, Neural Networks (2008 Special Issue) 21, 11821196.

    • Search Google Scholar
    • Export Citation
  • Huang X., Albright T. D., Stoner G. R. (2008b). Stimulus dependency and mechanisms of surround modulation in cortical area MT, J. Neurosci. 28, 1388913906.

    • Search Google Scholar
    • Export Citation
  • Jones H. E., Grieve K. L., Wang W., Sillito A. M. (2001). Surround suppression in Primate V1, J. Neurophysiol. 86, 20112028.

  • Karas R., McKendrick A. M. (2009). Aging alters surround modulation of perceived contrast, J. Vision 9, 19.

  • Kilpeläinen M., Donner K., Laurinen P. (2007). Time course of suppression by surround gratings: highly contrast-dependent, but consistently fast, Vision Res. 47, 32983306.

    • Search Google Scholar
    • Export Citation
  • Leventhal A. G., Wang Y., Pu M., Zhou Y., Ma Y. (2003). GABA and its agonists improved visual cortical function in senescent monkeys, Science 300, 812.

    • Search Google Scholar
    • Export Citation
  • Levitt J. B., Lund J. S. (1997). Contrast dependence of contextual effects in primate visual cortex, Nature 387, 7376.

  • Pack C. C., Hunter J. N., Born R. T. (2005). Contrast dependence of suppressive influences in cortical area MT of alert Macaque, J. Neurophysiol. 93, 18091815.

    • Search Google Scholar
    • Export Citation
  • Petrov Y., McKee S. P. (2006). The effect of spatial configuration on surround suppression of contrast sensitivity, J. Vision 6, 15.

  • Petrov Y., McKee S. P. (2009). The time course of contrast masking reveals two distinct mechanisms of human surround suppression, J. Vision 9, 111.

    • Search Google Scholar
    • Export Citation
  • Sceniak M. P., Ringach D. L., Hawken M. J., Shapley R. (1999). Contrast’s effect on spatial summation by macaque V1 neurons, Nature Neurosci. 2, 733.

    • Search Google Scholar
    • Export Citation
  • Schmolesky M. T., Wang Y., Pu M., Leventhal A. G. (2000). Degradation of stimulus selectivity of visual cortical cells in senescent rhesus monkeys, Nature Neurosci. 3, 384.

    • Search Google Scholar
    • Export Citation
  • Schwabe L., Ichida J. M., Shushruth S., Mangapathy P., Angelucci A. (2010). Contrast-dependence of surround suppression in Macaque V1: experimental testing of a recurrent network model, Neuroimage 52, 777792.

    • Search Google Scholar
    • Export Citation
  • Solomon S. G., White A. J. R., Martin P. R. (2002). Extraclassical receptive field properties of parvocellular, magnocellular and koniocellular cells in the primate lateral geniculate nucleus, J. Neurosci. 22, 338349.

    • Search Google Scholar
    • Export Citation
  • Tadin D., Kim J., Doop M. L., Gibson C., Lappin J. S., Blake R., Park S. (2006). Weakened center–surround interactions in visual motion processing in schizophrenia, J. Neurosci. 26, 1140311412.

    • Search Google Scholar
    • Export Citation
  • Tadin D., Lappin J. S. (2005). Optimal size for perceiving motion decreases with contrast, Vision Res. 45, 20592064.

  • Tadin D., Lappin J. S., Gilroy L. A., Blake R. (2003). Perceptual consequences of centre–surround antagonism in visual motion processing, Nature 424, 312315.

    • Search Google Scholar
    • Export Citation
  • Tailby C., Solomon S. G., Peirce J. W., Metha A. B. (2007). Two expressions of in V1 that arise independent of cortical mechanisms of suppression, Vis. Neurosci. 24, 99109.

    • Search Google Scholar
    • Export Citation
  • Wall M., Maw R. J., Stanek K. E., Chauhan B. C. (1996). The psychometric function and reaction times of automated perimetry in normal and abnormal areas of the visual field in patients with glaucoma, Investigat. Ophthalmol. Vis. Sci. 37, 878885.

    • Search Google Scholar
    • Export Citation
  • Wetherill G., Levitt H. (1965). Sequential estimation of points on a psychometric function, Brit. J. Math. Stat. Psychol. 18, 110.

  • Wichmann F. A., Hill N. J. (2001). The psychometric function: I. Fitting, sampling and goodness of fit, Percept. Psychophys. 63, 12931313.

    • Search Google Scholar
    • Export Citation
  • Xing J., Heeger D. J. (2000). Center–surround interactions in foveal and peripheral vision, Vision Res. 40, 30653072.

  • Xing J., Heeger D. J. (2001). Measurement and modeling of center-surround suppression and enhancement, Vision Res. 41, 571583.

  • Yang Y., Liang Z., Li G., Wang Y., Zhou Y. (2009). Aging affects response variability of V1 and MT neurons in rhesus monkeys, Brain Res. 1274, 2127.

    • Search Google Scholar
    • Export Citation
  • Yu C., Klein S. A., Levi D. M. (2001). Surround modulation of perceived contrast and the role of brightness induction, J. Vision 1, 1831.

    • Search Google Scholar
    • Export Citation
  • Zenger-Landolt B., Heeger D. J. (2003). Response suppression in V1 agrees with psychophysics of surround masking, J. Neurosci. 23, 68846893.

    • Search Google Scholar
    • Export Citation

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 270 65 4
Full Text Views 163 13 0
PDF Downloads 25 5 0