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Identifying Separate Components of Surround Suppression Journal of Vision (2016) 16(1):2, 1–12 1 Identifying separate components of surround suppression Department of Psychology, University of Washington, # Michael-Paul Schallmo Seattle, WA $ Department of Psychology, University of Washington, # Scott O. Murray Seattle, WA $ Surround suppression is a well-known phenomenon in Hammett, 1998; Xing & Heeger, 2000, 2001; Yu, Klein, which the response to a visual stimulus is diminished by & Levi, 2001). Studies in animal models have shown the presence of neighboring stimuli. This effect is that neurons in primary visual cortex (V1) typically observed in neural responses in areas such as primary show reduced spike rates in response to a stimulus visual cortex, and also manifests in visual contrast presented with a surround, compared to when a perception. Studies in animal models have identified at stimulus appears in the receptive field alone (Bair, least two separate mechanisms that may contribute to Cavanaugh, & Movshon, 2003; Cavanaugh, Bair, & surround suppression: one that is monocular and Movshon, 2002a, 2002b; DeAngelis, Freeman, & resistant to contrast adaptation, and another that is Ohzawa, 1994; Ichida, Schwabe, Bressloff, & Ange- binocular and strongly diminished by adaptation. The lucci, 2007; Shushruth, Ichida, Levitt, & Angelucci, current study was designed to investigate whether these 2009; Shushruth et al., 2013; Walker, Ohzawa, & two mechanisms exist in humans and if they can be identified psychophysically using eye-of-origin and Freeman, 1999). Similar results have been observed in contrast adaptation manipulations. In addition, we human V1 using functional magnetic resonance imag- examined the prediction that the monocular suppression ing (Chen, 2014; Flevaris & Murray, 2015; Joo, component is broadly tuned for orientation, while Boynton, & Murray, 2012; Nurminen, Kilpelainen, suppression between eyes is narrowly tuned. Our results Laurinen, & Vanni, 2009; Pihlaja, Henriksson, James, confirmed that when center and surrounding stimuli & Vanni, 2008; Williams, Singh, & Smith, 2003; were presented dichoptically (in opposite eyes), Zenger-Landolt & Heeger, 2003), suggesting that a suppression was orientation-tuned. Following reduction in the V1 response may underlie the adaptation in the surrounding region, no dichoptic reduction in perceived contrast observed with surround suppression was observed, and monoptic suppression no suppression. longer showed orientation selectivity. These results are Using electrophysiology in macaques, Webb, Dhruv, consistent with a model of surround suppression that Solomon, Tailby, and Lennie (2005) suggested that two depends on both low-level and higher level components. neural mechanisms may give rise to surround suppres- This work provides a method to assess the separate sion in V1. They showed that the first is monocular, contributions of these components during spatial broadly tuned for stimulus features (e.g., spatial and context processing in human vision. temporal frequency), resistant to contrast adaptation, and likely operates at the level of the lateral geniculate nucleus (LGN) or the input layers of V1. We will henceforth refer to this first mechanism as ‘‘low-level,’’ Introduction given the functional properties and the putative anatomical substrates of this suppression. The second Perception of a visual stimulus depends on its proposed mechanism (‘‘higher level’’ hereafter) is surrounding context; a well-known example of con- binocular, narrowly feature-tuned, diminished by textual modulation is surround suppression, wherein contrast adaptation, and most likely occurs at a cortical the perceived contrast of a stimulus is reduced by the level beyond the input layers of V1. More recent presence of surrounding stimuli, compared to when it is psychophysical studies in humans have suggested that viewed in isolation (Cannon & Fullenkamp, 1991; perceptual surround suppression may also depend on Chubb, Sperling, & Solomon, 1989; Ejima & Takaha- both monocular and binocular processes (Cai, Zhou, & shi, 1985; Petrov & McKee, 2006; Snowden & Chen, 2008; Petrov & McKee, 2009). However, it is not Citation: Schallmo, M.-P., & Murray, S. O. (2016). Identifying separate components of surround suppression. Journal of Vision, 16(1):2, 1–12, doi:10.1167/16.1.2. doi: 10.1167/16.1.2 Received September 30, 2015; published January 12, 2016 ISSN 1534-7362 This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License. Journal of Vision (2016) 16(1):2, 1–12 Schallmo & Murray 2 yet clear to what extent these components are selective The stereoscope was calibrated for each subject for stimulus features such as orientation, or whether before the experiment in order to achieve stable fusion they are influenced by contrast adaptation. Thus, the of the images presented to each eye. Subjects were relationship between surround suppression in human instructed to adjust the relative horizontal position of vision and the two constituent mechanisms proposed in test images using the stereoscope, to align the images in animals has not been fully established. each eye (a circle within a ring, two collinear vertical The current study was designed to test whether lines). Finally, subjects completed a brief task designed surround suppression during visual contrast perception to measure sensitivity to horizontal disparity in the in humans may be subdivided into distinct components alignment of the images presented to each eye. Fixation on the basis of feature (orientation) selectivity, marks (width ¼ 0.18, length ¼ 0.58) were presented sensitivity to contrast adaptation, and the degree of centrally in both eyes (left mark oriented vertically, interocular transfer. Indeed, using a contrast adapta- right horizontally). When aligned, these fixation marks tion paradigm along with stereoscopic image presen- form the percept of a plus sign. Subjects were asked to tation, we show that two distinct suppression detect whether or not there was a 0.258 horizontal offset components may be identified that contribute to human between the fixation marks (50% probability). Across contrast perception, which are well matched to the 16 trials, subjects averaged 84% accuracy on this task functional properties of the low- and higher level (SD ¼ 5%), indicating that they were sensitive to suppression mechanisms described in nonhuman pri- horizontal disparity between the images in each eye on mates (Angelucci & Bressloff, 2006; Webb et al., 2005). a fine scale. Methods Stimuli Stimuli consisted of sinusoidal luminance modula- tion gratings presented on a gray background (Figure Participants 1). Fixation marks were presented centrally in each eye, as described above. Two gratings (target and reference) Six people (four male and two female, mean age 31 were presented at 5.38 eccentricity. These stimuli years) completed both experiments after providing appeared 18 below the horizontal meridian (relative to written informed consent. Two additional subjects fixation) in order to facilitate future experiments using failed to complete the experiments due to difficulty in electroencephalography, for which such an offset is achieving stable binocular fusion using a stereoscope; advantageous. Gratings were presented within a data from these subjects were excluded. The experi- circular mask (radius ¼ 0.758) blurred with a Gaussian mental protocol was approved by the University of envelope (SD ¼ 0.058). Gratings were oriented either Washington Institutional Review Board, and con- vertically or horizontally, and had a spatial frequency formed to the ethical guidelines for research on human of 1.5 cycles/8. In a subset of stimulus conditions (see subjects provided in the Declaration of Helsinki. All below), an array of eight circular gratings was participants had normal or corrected-to-normal bin- presented surrounding the target grating. These sur- ocular vision. All of the subjects were experienced rounding gratings were arranged in a square grid psychophysical observers, and two of the subjects were around the target (18 center-to-center distance). Target the authors. and surrounding gratings were the same size and spatial frequency, were spatially in-phase, and were all presented at 77% Michelson contrast. This relatively Visual display high stimulus contrast was used because previous work suggests that the putative low-level suppression com- Stimuli were presented on a ViewSonic G90fB CRT ponent may dominate at lower contrasts (Cavanaugh et monitor, and were generated on a PC running al., 2002b; Webb et al., 2005). The reference grating Windows XP using MATLAB (MathWorks, Natick, had the same spatial phase as the target, was always MA) and Psychtoolbox (Brainard, 1997; Pelli, 1997). presented without surrounding stimuli, and varied in Subjects viewed the stimuli through a mirror stereo- contrast across trials (see below). scope at a distance of 50 cm. This allowed us to present Five different stimulus conditions were used to images to each eye independently (e.g., images on the examine the feature specificity and binocularity of left half of the screen were seen only in the left eye). surround suppression during contrast perception. When viewed through the stereoscope, the maximum Conditions were defined by the presence and configu- luminance of the monitor was reduced from 95 cd/m2 ration of the surrounding gratings. Surrounding to 40 cd/m2. gratings were not presented in the No Surround Journal of Vision (2016) 16(1):2, 1–12 Schallmo & Murray 3 Figure 1. Stimuli
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