Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-10T06:41:18.609Z Has data issue: false hasContentIssue false

A common contrast pooling rule for suppression within and between the eyes

Published online by Cambridge University Press:  01 July 2008

TIM S. MEESE*
Affiliation:
School of Life and Health Sciences, Aston University, Birmingham, UK
KIRSTEN L. CHALLINOR
Affiliation:
School of Life and Health Sciences, Aston University, Birmingham, UK
ROBERT J. SUMMERS
Affiliation:
School of Life and Health Sciences, Aston University, Birmingham, UK
*
*Address correspondence and reprint requests to: Tim S. Meese, School of Life and Health Sciences, Aston University, Birmingham B47ET, UK. E-mail: t.s.meese@aston.ac.uk

Abstract

Recent work has revealed multiple pathways for cross-orientation suppression in cat and human vision. In particular, ipsiocular and interocular pathways appear to assert their influence before binocular summation in human but have different (1) spatial tuning, (2) temporal dependencies, and (3) adaptation after-effects. Here we use mask components that fall outside the excitatory passband of the detecting mechanism to investigate the rules for pooling multiple mask components within these pathways. We measured psychophysical contrast masking functions for vertical 1 cycle/deg sine-wave gratings in the presence of left or right oblique (±45 deg) 3 cycles/deg mask gratings with contrast C%, or a plaid made from their sum, where each component (i) had contrast 0.5Ci%. Masks and targets were presented to two eyes (binocular), one eye (monoptic), or different eyes (dichoptic). Binocular-masking functions superimposed when plotted against C, but in the monoptic and dichoptic conditions, the grating produced slightly more suppression than the plaid when Ci ≥ 16%. We tested contrast gain control models involving two types of contrast combination on the denominator: (1) spatial pooling of the mask after a local nonlinearity (to calculate either root mean square contrast or energy) and (2) “linear suppression” (Holmes & Meese, 2004, Journal of Vision4, 1080–1089), involving the linear sum of the mask component contrasts. Monoptic and dichoptic masking were typically better fit by the spatial pooling models, but binocular masking was not: it demanded strict linear summation of the Michelson contrast across mask orientation. Another scheme, in which suppressive pooling followed compressive contrast responses to the mask components (e.g., oriented cortical cells), was ruled out by all of our data. We conclude that the different processes that underlie monoptic and dichoptic masking use the same type of contrast pooling within their respective suppressive fields, but the effects do not sum to predict the binocular case.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 2008

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

Adelson, E.H. & Bergen, J.R. (1985). Spatiotemporal energy models for the perception of motion. Journal of the Optical Society of America A 2, 284299.Google Scholar
Albrecht, D.G. & Geisler, W.S. (1991). Motion selectivity and the contrast-response function of simple cells in the visual cortex. Visual Neuroscience 7, 531546.CrossRefGoogle ScholarPubMed
Baker, D.H. & Meese, T.S. (2007). Binocular contrast interactions: Dichoptic masking is not a single process. Vision Research 47, 30963107.Google Scholar
Baker, D.H., Meese, T.S. & Georgeson, M.A. (2007 a). Binocular interaction: Contrast matching and contrast discrimination are predicted by the same model. Spatial Vision 20, 397413.Google Scholar
Baker, D.H., Meese, T.S. & Summers, R.J. (2007 b). Psychophysical evidence for two routes to suppression before binocular summation of signals in human vision. Neuroscience 146, 435448.CrossRefGoogle ScholarPubMed
Bird, C.M., Henning, G.B. & Wichmann, F.A. (2002). Contrast discrimination with sinusoidal gratings of different spatial frequency. Journal of the Optical Society of America A 19, 12671273.Google Scholar
Bonds, A.B. (1989). Role of inhibition in the specification of orientation selectivity of cells in the cat striate cortex. Visual Neuroscience 2, 4155.Google Scholar
Bonin, V., Mante, V. & Carandini, M. (2005). The suppressive field of neurons in lateral geniculate nucleus. Journal of Neuroscience 25, 1084410856.Google Scholar
Bonin, V., Mante, V. & Carandini, M. (2006). The statistical computation underlying contrast gain control. Journal of Neuroscience 26, 63466353.Google Scholar
Büchert, M., Greenlee, M.W., Rutschmann, R.M., Kraemer, F.M., Luo, F. & Hennig, J. (2002). Functional magnetic resonance imaging evidence for binocular interactions in human visual cortex. Experimental Brain Research 145, 334339.CrossRefGoogle ScholarPubMed
Burton, G.J. (1981). Contrast discrimination by the human visual system. Biol Cybern 40, 2738.Google Scholar
Challinor, K.L., Meese, T.S. & Holmes, D.J. (2008). A two-stage process for masking: Linear suppression is more broadly tuned than super-suppression. Perception 37, 313.Google Scholar
Challinor, K.L., Meese, T.S. & Summers, R.J. (2007). Surround suppression saturates, cross-orientation suppression does not. Perception 36, suppl. 38. (ECVP Abstract).Google Scholar
Chen, C.-C. & Tyler, C.W. (2001). Lateral sensitivity modulation explains the flanker effect in contrast DISCRIMINATION. Proceedings of the Royal Society B 268, 509516.CrossRefGoogle ScholarPubMed
Chirimuuta, M. & Tolhurst, D.J. (2005). Does a Bayesian model of V1 contrast coding offer a neurophysiological account of human contrast discrimination? Vision Research 45, 29432959.Google Scholar
Clatworthy, P.L., Chirimuuta, M., Lauritzen, J.S. & Tolhurst, D.J. (2001). Coding of the contrasts in natural images by populations of neurons in primary visual cortex (V1). Vision Research 43, 19832001.Google Scholar
Derrington, A.M. & Henning, G.B. (1989). Some observations on the masking effects of two-dimensional stimuli. Vision Research 29, 241246.Google ScholarPubMed
Derrington, A.M. & Lennie, P. (1984). Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. Journal of Physiology 357, 219240.Google Scholar
Ding, J. & Sperling, G. (2006). A gain-control theory of binocular combination. Proceedings of the National Academy of Sciences of the United States of America 103, 11411146.CrossRefGoogle ScholarPubMed
Durand, S., Freeman, T.C.B. & Carandini, M. (2007). Temporal properties of surround suppression in cat primary visual cortex. Visual Neuroscience 24, 679690.CrossRefGoogle ScholarPubMed
Felisberti, F. & Derrington, A.M. (1999). Long-range interactions modulate the contrast gain in the lateral geniculate nucleus of cats. Visual Neuroscience 16, 943956.Google Scholar
Felisberti, F. & Derrington, A.M. (2001). Long-range interactions in the lateral geniculate nucleus of the New-World monkey, Callithrix jacchus. Visual Neuroscience 18, 209218.CrossRefGoogle ScholarPubMed
Foley, J.M. (1994). Human luminance pattern-vision mechanisms: Masking experiments require a new model. Journal of the Optical Society of America A 11, 17101719.Google Scholar
Foley, J.M. & Legge, G.E. (1981). Contrast detection and near-threshold discrimination in human-vision. Vision Research 21, 10411053.Google Scholar
Freeman, T.C.B., Durand, S., Kiper, D.C. & Carandini, M. (2002). Suppression without inhibition in visual cortex. Neuron 35, 759771.Google Scholar
García-Pérez, M.A. & Alcalá-Quintana, R. (2007). The transducer model for contrast detection and discrimination: Formal relations, implications, and an empirical test. Spatial Vision 20, 543.CrossRefGoogle Scholar
Georgeson, M.A. & Meese, T.S. (2006). Fixed or variable noise in contrast discrimination? The jury's still out… Vision Research 46, 42944303.Google Scholar
Georgeson, M.A. & Meese, T.S. (2007). Binocular combination at threshold: Temporal filtering and summation of signals in separate ON and OFF channels. Perception 36 suppl. 60. (ECVP).Google Scholar
Georgeson, M.A. & Scott-Samuel, N.E. (1999). Motion contrast: A new metric for direction discrimination. Vision Research 39, 43934402.Google Scholar
Graham, N. & Sutter, A. (1998). Spatial summation in simple (Fourier) and complex (non-Fourier) texture channels. Vision Research 38, 231257.Google ScholarPubMed
Graham, N. & Sutter, A. (2000). Normalization: Contrast-gain control in simple (Fourier) and complex (non-Fourier) pathways of pattern vision. Vision Research 40, 27372761.Google Scholar
Heeger, D.J. (1992). Normalization of cell responses in cat striate cortex. Visual Neuroscience 9, 181197.Google Scholar
Hirsch, J.A., Martinez, L.M., Pillai, C., Alonso, J.M., Wang, Q. & Sommer, F.T. (2003). Functionally distinct inhibitory neurons at the first stage of visual cortical processing. Nature Neuroscience 6, 13001308.Google Scholar
Holmes, D.J. & Meese, T.S. (2004). Grating and plaid masks indicate linear summation in a contrast gain pool. Journal of Vision 4, 10801089.CrossRefGoogle Scholar
Itti, L., Koch, C. & Braun, J. (2000). Revisiting spatial vision: Toward a unifying model. Journal of the Optical Society of America A 17, 18991917.Google Scholar
Katkov, M., Tsodyks, M. & Sagi, D. (2006). Singularities in the inverse modelling of 2AFC contrast discrimination data. Vision Research 46, 259266.Google Scholar
Katkov, M., Tsodyks, M. & Sagi, D. (2007). Inverse modelling of human contrast response. Vision Research 47, 28552867.Google Scholar
Klein, S.A. (2006). Separating transducer non-linearities and multiplicative noise in contrast discrimination. Vision Research 46, 42794293.CrossRefGoogle ScholarPubMed
Kontsevich, L.L., Chen, C.-C. & Tyler, C.W. (2002). Separating the effects of response nonlinearity and internal noise psychophysical. Vision Research 42, 17711784.Google Scholar
Kontsevich, L.L. & Tyler, C.W. (1999) Nonlinearities of near-threshold contrast transduction. Vision Research 39, 18691880.CrossRefGoogle ScholarPubMed
Legge, G. & Foley, J. (1980). Contrast masking in human vision. Journal of the Optical Society of America A 70, 14581471.CrossRefGoogle ScholarPubMed
Li, B., Peterson, M.R., Thompson, J.K., Duong, T. & Freeman, R.D. (2005). Cross-orientation suppression: Monoptic and dichoptic mechanisms are different. Journal of Neurophysiology 94, 16451650.CrossRefGoogle ScholarPubMed
Li, B., Thompson, J.K., Duong, T., Peterson, M.R. & Freeman, R.D. (2006). Origins of cross-orientation suppression in the visual cortex. Journal of Neurophysiology 96, 17551764.Google Scholar
Lu, Z.L. & Dosher, B.A. (1999). Characterizing human perceptual inefficiencies with equivalent internal noise. Journal of the Optical Society of America A 16, 764778.Google Scholar
McIlhagga, W. & Peterson, R. (2006). Sinusoid = light bar plus dark bar? Vision Research 46, 19341945.Google Scholar
McKee, S.P., Klein, S.A. & Teller, D.Y. (1985). Statistical properties of forced-choice psychometric functions—Implications of probit analysis. Perception & Psychophysics 37, 286298.Google Scholar
Macknik, S.L. & Martinez-Conde, S. (2004) Dichoptic visual masking reveals that early binocular neurons exhibit weak interocular suppression: Implications for binocular vision and visual awareness. Journal of Cognitive Neuroscience 16, 10491059.CrossRefGoogle ScholarPubMed
Maehara, G. & Goryo, K. (2005). Binocular, monocular and dichoptic pattern masking. Optical Review 12, 7682.Google Scholar
Manahilov, V., Simpson, W.A. & McCulloch, D.L. (2001). Spatial summation of peripheral Gabor patches. Journal of the Optical Society of America A 18, 273282.CrossRefGoogle ScholarPubMed
Mante, V. & Carandini, M. (2005). Mapping of stimulus energy in primary visual cortex. Journal of Neurophysiology 94, 788798.Google Scholar
Martinez, L.M., Wang, Q.B., Reid, R.C., Pillai, C., Alonso, J.M., Sommer, F.T. & Hirsch, J.A. (2005). Receptive field structure varies with layer in the primary visual cortex. Nature Neuroscience 8, 372379.Google Scholar
Medina, J., Meese, T.S. & Mullen, K. (2007). Cross-orientation masking in the red-green isoluminant and luminance systems. Journal of Vision 7, 257a, Abstract 257 (VSS).Google Scholar
Meese, T.S. (2004). Area summation and masking. Journal of Vision 4, 930943.Google Scholar
Meese, T.S., Georgeson, M.A. & Baker, D.H. (2006). Binocular contrast vision at and above threshold. Journal of Vision 6, 12241243.CrossRefGoogle ScholarPubMed
Meese, T.S. & Hess, R.F. (2004). Low spatial frequencies are suppressively masked across spatial scale, orientation, field position, and eye of origin. Journal of Vision 4, 843859.Google Scholar
Meese, T.S. & Hess, R.F. (2005). Interocular suppression is gated by interocular feature matching. Vision Research 45, 915.CrossRefGoogle ScholarPubMed
Meese, T.S., Hess, R.F. & Williams, C.B.W. (2005). Size matters, but not for everyone: Individual differences for contrast discrimination. Journal of Vision 5, 928947.CrossRefGoogle Scholar
Meese, T.S. & Holmes, D.J. (2002). Adaptation and gain pool summation: alternative models and masking data. Vision Research 42, 11131125.Google Scholar
Meese, T.S. & Holmes, D.J. (2003). Orientation-masking: suppression and mechanism bandwidth. Perception 32, 388388. (AVA Christmas Abstract).Google Scholar
Meese, T.S. & Holmes, D.J. (2007). Spatial and temporal dependencies of cross-orientation suppression. Proceedings of the Royal Society B 274, 127136.Google Scholar
Meese, T.S., Holmes, D.J. & Challinor, K.L. (2007). Remote facilitation in the Fourier domain. Vision Research 47, 11121119.Google Scholar
Meese, T.S. & Summers, R.J. (2007). Area summation in human vision at and above detection threshold. Proceedings of the Royal Society 274, 28912900.Google Scholar
Meese, T.S., Summers, R.J., Holmes, D.J. & Wallis, S.A. (2007). Contextual modulation involves suppression and facilitation form the centre and the surround. Journal of Vision 7, 121.Google Scholar
Morrone, M.C., Burr, D.C. & Maffei, L. (1982). Functional implications of cross-orientation inhibition of cortical visual cells. 1. Neurophysiological evidence. Proceedings of the Royal Society B 216, 335354.Google Scholar
Naito, T., Sadakane, M., Okamoto, M. & Sato, H. (2007). Orientation tuning of surround suppression in lateral geniculate nucleus and primary visual cortex of cat. Neuroscience 149, 962975.Google Scholar
Nolt, M.J., Kumbhani, R.D. & Palmer, L.A. (2007). Suppression at high spatial frequencies in the lateral geniculate nucleus of the cat. Journal of Neurophysiology 98, 11671180.Google Scholar
Ohzawa, I., Sclar, G. & Freeman, R.D. (1985). Contrast gain-control in the cats visual-system. Journal of Neurophysiology 54, 651667.Google Scholar
Olzak, L.A. & Thomas, J.P. (1999). Neural recoding in human pattern vision: Model and mechanisms. Vision Research 39, 231256.Google Scholar
Olzak, L.A. & Thomas, J.P. (2003). Dual nonlinearities regulate contrast sensitivity in pattern discrimination tasks. Vision Research 43, 14331442.Google Scholar
Parraga, C.A., Troscianko, T. & Tolhurst, D.J. (2005). The effects of amplitude-spectrum statistics on foveal and peripheral discrimination of changes in natural images, and a multi-resolution model. Vision Research 45, 31453168.Google Scholar
Pelli, D.G. (1985). Uncertainty explains many aspects of visual contrast detection and discrimination. Journal of the Optical Society of America A 2, 15081532.Google Scholar
Pelli, D.G. (1987). On the relation between summation and facilitation. Vision Research 27, 119123.CrossRefGoogle ScholarPubMed
Petrov, Y., Carandini, M. & McKee, S. (2005). Two distinct mechanisms of suppression in human vision. Journal of Neuroscience 25, 87048707.Google Scholar
Priebe, N.J. & Ferster, D. (2006). Mechanisms underlying cross-orientation suppression in cat visual cortex. Nature Neuroscience 9, 552561.Google Scholar
Ringach, D.L., Bredfeldt, C.E., Shapley, R.M. & Hawken, M.J. (2002 a). Orientation selectivity in macaque V1: Diversity and laminar dependence. Journal of Neuroscience 22, 56395651.Google Scholar
Ringach, D.L., Bredfeldt, C.E., Shapley, R.M. & Hawken, M.J. (2002 b). Suppression of neural responses to nonoptimal stimuli correlates with tuning selectivity in macaque V1. Journal of Neurophysiology 87, 10181027.Google Scholar
Ross, J. & Speed, H.D. (1991). Contrast adaptation and contrast masking in human vision. Proceedings of the Royal Society B 246, 6169.Google Scholar
Schwartz, O. & Simoncelli, P. (2001). Natural image statistics and sensory gain control. Nature Neuroscience 4, 819825.Google Scholar
Sclar, G., Maunsell, J.H.R. & Lennie, P. (1990). Coding of image-contrast in central visual pathways of the macaque monkey. Vision Research 30, 110.Google Scholar
Sengpiel, F. & Vorobyov, V. (2005). Intracortical origins of interocular suppression in the visual cortex. Journal of Neuroscience 25, 63946400.Google Scholar
Shapley, R.M. & Victor, J.D. (1978). The effect of contrast on the transfer properties of cat retinal ganglion cells. Journal of Physiology (London) 318, 161179.Google Scholar
Shapley, R.M. & Victor, J.D. (1981). How the contrast gain modifies the frequency responses of cat ganglion cells. Journal of Physiology (London) 285, 275298.CrossRefGoogle Scholar
Smith, M.A., Bair, W. & Movshon, J.A. (2006). Dynamics of suppression in macaque primary visual cortex. Journal of Neuroscience 25, 1084410856.Google Scholar
Snowden, R.J. & Hammett, S.T. (1998). The effects of surround contrast on contrast thresholds, perceived contrast and contrast discrimination. Vision Research 38, 19351945.Google Scholar
Solomon, J.A. (2007 a). Contrast discrimination: Second responses reveal the relationship between the mean and variance of visual signals. Vision Research 47, 32473258.Google Scholar
Solomon, J.A. (2007 b). Intrinsic uncertainty explains second responses. Spatial Vision 20, 4560.CrossRefGoogle ScholarPubMed
Solomon, S.G., Lee, B.B. & Sun, H. (2006). Suppressive surrounds and contrast gain in magnocellular-pathway retinal ganglion cells of macaque. Journal of Neuroscience 26, 87158726.Google Scholar
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. Journal of Neuroscience 22, 338349.CrossRefGoogle ScholarPubMed
Stromeyer, C.F. & Klein, S. (1974). Spatial frequency channels in human vision as asymmetric (edge) mechanisms. Vision Research 14, 14091420.Google Scholar
Summers, R.J. & Meese, T.S. (2007). Area summation is linear but the contrast transducer is nonlinear: Models of summation and uncertainty and evidence from the psychometric function. Perception 36 suppl. 5. (ECVP)Google Scholar
Tolhurst, D.J., Movshon, J.A. & Dean, A.F. (1983). The statistical reliability of signals in single neurons in cat and monkey visual cortex. Vision Research 23, 775785.Google Scholar
Truchard, A.M., Ohzawa, I. & Freeman, R.D. (2000). Contrast gain control in the visual cortex: Monocular versus binocular mechanisms. Journal of Neuroscience 20, 30173032.Google Scholar
Tse, P.U., Martinez-Conde, S., Schlegel, A.A. & Macknik, S.L. (2005). Visibility, visual awareness, and visual masking of simple unattended targets are confined to areas in the occipital cortex beyond human V1/V2. Proceedings of the National Academy of Sciences of the United States of America 102, 1717817183.Google Scholar
Tsuchiya, N., Koch, C., Gilroy, L.A. & Blake, R. (2006). Depth of interocular suppression associated with continuous flash suppression, flash suppression and binocular rivalry. Journal of Vision 6, 10681078.Google Scholar
Tyler, C.W. & Chen, C.C. (2000). Signal detection theory in the 2AFC paradigm: Attention, channel uncertainty and probability summation. Vision Research 40, 31213144.Google Scholar
Walker, G.A., Ohzawa, I. & Freeman, R.D. (1998). Binocular cross-orientation suppression in the cat's striate cortex. Journal of Neurophysiology 79, 227239.CrossRefGoogle ScholarPubMed
Wallis, S.A., Georgeson, M.A. & Mehta, P. (2008). Seeing light vs dark lines: Psychophysical performance is based on separate channels, limited by noise and uncertainty. Perception 37 315.Google Scholar
Watson, A.B. (2000). Visual detection of spatial contrast patterns: Evaluation of five simple models. Optics Express 6, 1233.Google Scholar
Watson, A.B., Barlow, H.B. & Robson, J.G. (1983). What does the eye see best. Nature 302, 419422.Google Scholar
Watson, A.B. & Solomon, J.A. (1997). Model of visual contrast gain control and pattern masking. Journal of the Optical Society of America A-Optics Image Science and Vision 14, 23792391.Google Scholar
Webb, B.S., Dhruv, N.T., Solomon, S.G., Tailby, C. & Lennie, P. (2005). Early and late mechanisms of surround suppression in striate cortex of Macaque. Journal of Neuroscience 25, 1166611675.Google Scholar
Weiler, J.A., Maxwell, J.S. & Schor, C.M. (2007). Illusory contrast-induced shifts in binocular visual direction bias saccadic eye movements toward the perceived target position. Journal of Vision 7, 118.Google Scholar
Wetherill, G.B. & Levitt, H. (1965). Sequential estimation of points on a psychometric function. Journal of Experimental Psychology 15, 485492.Google Scholar
Wilson, H.R. (1980). A transducer function for threshold and suprathreshold human-vision. Biological Cybernetics 38, 171178.Google Scholar
Wilson, H.R. & Humanski, R. (1993). Spatial-frequency adaptation and contrast gain-control. Vision Research 33, 11331149.Google Scholar
Wilson, H.R., McFarlane, D.K. & Phillips, G.C. (1983). Spatial-frequency tuning of orientation selective units estimated by oblique masking. Vision Research 23, 873882.Google Scholar
Yu, C., Klein, S.A. & Levi, D.M. (2003). Cross- and iso-oriented surrounds modulate the contrast response function: The effect of surround contrast. Journal of Vision 3, 527540.Google Scholar
Zenger-Landolt, B. & Heeger, D.J. (2003). Response suppression in V1 agrees with psychophysics of surround masking. Journal of Neuroscience 23, 68846893.CrossRefGoogle ScholarPubMed