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Journal of Experimental Psychology: Human Perception and Performance 2011, Vol. 00, No. 00, 000 – 000

© 2011 American Psychological Association 0096-1523/11/$12.00 DOI: 10.1037/a0026963

Perceptual Fading Without Retinal Adaptation Po-Jang Hsieh

Jaron T. Colas

Duke-NUS Graduate Medical School Singapore, Singapore

California Institute of Technology, Pasadena, California

A retinally stabilized object readily undergoes perceptual fading and disappears from consciousness. This startling phenomenon is commonly believed to arise from local bottom-up sensory adaptation to edge information that occurs early in the visual pathway, such as in the lateral geniculate nucleus of the thalamus or retinal ganglion cells. Here we use random dot stereograms to generate perceivable contours or shapes that are not present on the retina and ask whether perceptual fading occurs for such “cortical” contours. Our results show that perceptual fading occurs for “cortical” contours and that the time a contour requires to fade increases as a function of its size, suggesting that retinal adaptation is not necessary for the phenomenon and that perceptual fading may be based in the cortex. Keywords: perceptual fading, adaptation

sented red to one eye and green to the other through a stereoscope, indicating that feature mixing may result from cortical processing because streams of information from the two eyes are processed separately before reaching cortex. Moreover, functional magnetic resonance imaging results have indicated the presence of mixed feature information as far downstream in the visual pathway as cortical area V1 (Hsieh & Tse, 2010). All of these findings attest to the existence of a cortical component in the feature mixing stage of perceptual fading. In the current study, we inquire whether perceptual fading can occur in the absence of retinal adaptation. Here we use random dot stereograms to create perceivable contours or shapes that are not represented by the retina and ask whether perceptual fading still occurs for these “cortical” contours. Our results show that perceptual fading does occur for “cortical” contours and that the time a contour requires to fade increases as a function of its size. These findings suggest that retinal adaptation is not necessary for perceptual fading to occur.

Perceptual fading (Troxler, 1804; Kanai & Kamitani, 2003) in most cases occurs optimally when a visual stimulus is located peripherally, has indistinct edges and a low luminance level relative to that of the background, and has been stabilized on the retina, as happens under conditions of visual fixation (Livingstone & Hubel, 1987, but see Pessoa & De Weerd, 2003, for some exceptions). Perceptual fading is commonly thought to arise because of local bottom-up sensory adaptation to edge information (Ramachandran, 1992). Although previous studies have suggested that perceptual fading occurs early in the visual pathway, such as in the lateral geniculate nucleus of the thalamus or retinal ganglion cells (Clarke & Belcher, 1962; Kotulak & Schor, 1986; Millodot, 1967), whether later cortical areas also play a role in the phenomenon remains an open question. Because perceptual fading is characterized by both inhibition of signals that indicate the presence of an object (the stage of neuronal adaptation) and amplification of signals that “fill in” the background in place of the object (the stage of feature replacement or mixing), it is possible that the effect includes both retinal and cortical components. Recently, we (Hsieh & Tse, 2006, 2009) demonstrated that the “filling-in” signal is approximately the areaand magnitude-weighted average of the background and foreground features. In light of these data, we hypothesized that information within the boundary of the perceptually vanished figure is not lost or replaced by features from outside the boundary during perceptual “filling-in”; rather, “filling-in” involves perceptual “feature mixing,” whereby information on either side of a perceptually faded boundary merges. Our data (Hsieh & Tse, 2006) further showed that feature mixing occurred when we pre-

Experiment 1: Stereoscopic Perceptual Fading for Static Contours Method Participants. Nine healthy adult volunteers with normal or corrected-to-normal visual acuity and depth perception participated in Experiment 1. All subjects for both experiments provided informed consent within a protocol approved by either the Massachusetts Institute of Technology or the Duke-NUS Graduate Medical School and were paid $5 for their participation. Stimuli and procedures. The stimulus configuration used in Experiments 1 and 2 are shown in Figure 1. Subjects viewed dichoptic images through a mirror stereoscope in a dark room. A white frame subtending 15.7 ! 15.7 degrees of visual angle delineated the visual field in the center of a black screen. A red fixation spot subtending 0.4 ! 0.4 degrees was located 6 degrees below the center of the frame. The visual stimuli used for both experiments included randomly generated black-and-white dot patterns that consisted of pixels

Po-Jang Hsieh, Neuroscience and Behavioral Disorders Program, DukeNUS Graduate Medical School Singapore, Singapore; and Jaron T. Colas, Computation and Neural Systems Program, California Institute of Technology, Pasadena, California. Correspondence concerning this article should be addressed to Po-Jang Hsieh, Neuroscience and Behavioral Disorders Program, Duke-NUS Graduate Medical School, 8 College Road, Singapore 169857. E-mail: [email protected] 1

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Figure 1. Stimuli. Subjects viewed dichoptic images through a mirror stereoscope in a dark room. A randomly generated pair of identical blackand-white dot patterns was presented binocularly to serve as a background. They were partially covered by another pair of smaller identical dot patterns in the center. A slight horizontal disparity between the smaller dot patterns produced a stereogram, which can be observed in this figure by crossing one’s eyes. The subject was required to fixate on the red spot and indicate if and when each stereogram faded perceptually.

each subtending 0.2 ! 0.2 degrees. After 2 s of fixation at the beginning of each trial, a new dot pattern subtending 15.7 ! 15.7 degrees (the extent of the frame) was presented binocularly to serve as a background. Another unique dot pattern with variable

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size (3, 4, 5, 6, 7, or 8 degrees) was simultaneously presented over the center of the display. The smaller dot pattern was also presented binocularly, but in this case a stereogram was produced with a horizontal disparity of 0.2 degrees between the images presented to the two eyes. Each subject was required to fixate and eventually press a button to report if and when each peripherally presented stereogram faded completely from perception within 20 s of presentation. The six sizes of the stereograms and the two conditions (experimental and control) were randomly counterbalanced across the 42 trials. For the control condition, which was implemented for 12 of those trials, the horizontal disparity between the two images was removed after 1 s of presentation, so that the stereogram actually disappeared before perceptual fading could occur. Subjects placed their chins on a chin rest for visual stabilization. The visual stimulator ran on a Dell workstation running Windows XP. The stimuli were presented with Vision Egg (Straw, 2008) on a 20-in. Sony CRT gamma-corrected monitor with a resolution of 1024 ! 768 pixels and a frame rate of 100 Hz. Data analysis. We recorded the durations of subjects’ percepts as a function of the sizes of the stereograms for each condition. A one-way repeated-measures analysis of variance (ANOVA) was performed for data from the experimental con-

Figure 2. Results of Experiment 1. Data from nine subjects show perceptual durations as a function of static stereogram size for Experiment 1. In the experimental condition, we measured the time until subjects reported that perceptual fading occurred (solid line with squares); in the control condition, the stimulus was removed after 1 s (dotted line with circles) (a). Data averaged across subjects (b). Error bars indicate standard errors of the means.

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PERCEPTUAL FADING OF NONRETINAL CONTOURS

dition to test for significant differences in perceptual duration across stimulus size. Additionally, a two-way repeatedmeasures ANOVA (Size ! Condition) was performed for all data to test for a significant interaction between size and condition.

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retinal image and a blurry “cortical” contour. To further rule out the possibility that the perceptual fading observed in Experiment 1 is partially due to retinal adaptation to the random dot textures, we presented dynamic patterns in Experiment 2.

Method

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Results in Figures 2a show mean perceptual durations as a function of stereogram size for each subject in Experiment 1. Data averaged across all nine subjects are shown in Figure 2b. Analysis by means of one-way ANOVA for the experimental condition (solid line with squares in Figure 2) demonstrated that perceptual duration differed significantly across the six stimulus sizes in Experiment 1, F(5, 40) " 11.69, p # 10$5. A two-way omnibus ANOVA over all data indicated the existence of a significant interaction between size and condition, F(5, 40) " 10.15, p # 10$5.

Experiment 2: Stereoscopic Perceptual Fading for Dynamic Contours One might argue that there is still retinal adaptation in response to the random dot pattern itself, which could result in both a blurry

Participants. Six of the participants from Experiment 1 and three additional healthy adult volunteers with normal or correctedto-normal visual acuity and depth perception participated in Experiment 2. Stimuli and procedures. The stimulus configuration, experimental procedures, and data analysis for Experiment 2 were identical to those of Experiment 1, except as follows. In Experiment 2, all random dot patterns were constantly generated and refreshed at a rate of 1 Hz.

Results Results in Figures 3a show mean perceptual durations as a function of stereogram size for each subject in Experiment 2. Data averaged across all nine subjects are shown in Figure 3b. Analysis by means of two-way ANOVA for the experimental condition (solid line with squares in Figure 3) demonstrated that

Figure 3. Results of Experiment 2. Data from nine subjects show perceptual durations as a function of dynamic stereogram size for Experiment 2 (a). Data averaged across subjects (b).

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perceptual duration differed significantly across the six stimulus sizes in Experiment 2, F(5, 40) " 11.28, p # 10$5. A two-way omnibus ANOVA over all data indicated the existence of a significant interaction between size and condition, F(5, 40) " 8.06, p # 10$4.

General Discussion

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Our results showed that perceptual fading occurs for “cortical” (i.e., nonretinal) contours or shapes and that the time a contour requires to fade increases as a function of its size. This finding is consistent with previously reported stereoscopic tilt and size aftereffects (Tyler, 1975), indicating that retinal adaptation is not necessary for perceptual fading or aftereffects. Our result is also consistent with a previous finding that perceptual fading can occur for a stabilized “cortical” image (Blakemore, Muncey, & Ridley, 1971). In that study, the authors demonstrated that perceptual fading is not entirely retinal— but rather is partly cortical— because an image viewed freely (i.e., without fixation) also becomes less distinct. Similar nonretinal fading phenomena have been shown in previous studies using artificial scotomas presented over a dynamic noise background (Ramachandran & Gregory, 1991; Spillmann & Kurtenbach, 1992). The fading of such artificial scotomas cannot easily be accounted for by local retinal adaptation to luminance edges because the dynamic background continually refreshes the edges of the fading stimulus on the retina. However, because there were still texture-defined contours on the retina, such fading may occur because of edge perturbation at the pixel level and/or the increase in increment threshold caused by an oscillating surround (Mackay, 1970; Kruger & Fisher, 1973; Breitmeyer, Valberg, Kurtenbach, & Neumeyer, 1980; Hammond & Mackay, 1981; Hammond & Smith, 1984; Spillmann & Kurtenbach, 1992). Our result differs from these previous findings in that the image we used included no edges or contours on the retina at all and therefore completely rules out the possibility of retinal adaptation. Perceptual fading over “cortical” contours may be a manifestation of a kind of cortical neuronal adaptation, which usually occurs after prolonged representation of a stimulus or feature by spiking activity. Whether cortical adaptation also plays a role in perceptual fading when retinal adaptation does occur remains to be determined with future research. It has been shown that adaptation and its aftereffects can occur for a number of low-level visual features, such as motion or orientation when they are presented with or without conscious perception (Blake & Fox, 1974; Lehmkuhle & Fox, 1975). Such aftereffects have also been observed for highlevel visual features, such as the sex, ethnicity, gaze direction, and expression of a face (Leopold, O’Toole, Vetter, & Blanz, 2001; Webster et al., 2004), and have been reported to be transferrable across different retinal positions, stimulus sizes, and identities of the adapting stimulus (Afraz & Cavanagh, 2009; Afraz & Cavanagh, 2008; Fox & Barton, 2007; Leopold et al., 2001; Zhao & Chubb, 2001). Our finding suggests that, with proper manipulation, cortical adaptation can lead to a nearly total cessation of neural representation and a complete absence of conscious perception of the adapted stimuli.

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Received August 18, 2011 Revision received November 30, 2011 Accepted December 2, 2011 !