Perceptual entrainment of individually unambiguous motions

Abstract

When two bistable spheres defined by dots oscillating around a common axis (coaxial condition) are placed near each other, their motions become entrained such that they appear to rotate in the same direction. When the dots in the two spheres oscillate around parallel axes (non-coaxial condition), entrainment is much reduced, suggesting that this phenomenon is driven by interactions between the global stimulus representations rather than between the locally ambiguous motion signals. In order to examine where these interactions may be arising, we created highly unambiguous spheres by introducing size and contrast cues on the dots. We find that coupling is strong for the two nearly unambiguous spheres rotating in opposite directions of motion in the coaxial condition but, importantly, that this effect is subject to attentional control. Forcing observers to withdraw their attention from the rotating spheres by performing a demanding task at fixation significantly reduces the amount of coupling, arguing against mediation by low-level interactions between the spheres. These results reveal a disjunct between the local motion signals that are unambiguous and the global percept, implicating a process that requires active suppression of reliable visual information. We propose that this is a dynamic process that requires feedback from higher levels to bind opposite motions into a unified directional percept.

Introduction

In bistable displays, the perception of a stimulus alternates between two competing perceptual interpretations even though its physical properties remain unchanged. A common example is structure from motion (SFM) where the oscillation of dots around a single axis yields the perception of a three-dimensional rotating sphere. The motion of this stimulus is inherently ambiguous and the perceived direction of rotation switches frequently between the two alternatives (Bradley, Chang, & Andersen, 1998; Nawrot & Blake, 1989; Treue, Husain, & Andersen, 1991). The neural processes underlying bistability have been proposed to result both from low-level adaptation mechanisms as well as high-level grouping and attentional processes. Support for the idea that adaptation underlies the bistability comes from evidence that the rate of switches between the two alternative percepts can be decreased or abolished by presenting the stimulus in ways that minimize adaptation. This has been achieved either by producing a wobble in the axis of rotation (Blake, Sobel, & Gilroy, 2003), by perceptually removing the object from view (Leopold, Wilke, Maier, & Logothetis, 2002), or by adapting out one of the directions of rotation with an unambiguously rotating sphere (Nawrot & Blake, 1989). 

Evidence for higher level influences on the alternation rate comes from experiments showing that the duration of a dominant percept can be increased by attentional manipulations. Nakatani and van Leeuwen (2005) find that an observer's level of attention can account for individual differences in switch rates for the Necker cube, and Brouwer and van Ee (2006) report that the duration of perception of the direction of the SFM is under attentional control. Using a quartet of dots whose direction of motion can be perceived as either horizontal or vertical, Kohler, Haddad, Singer, and Muckli (2008) report that observers can switch the direction of motion by attention. There is, however, some debate as to the overall role of attention in bistable perception with Pastukhov and Braun (2007) reporting that some phenomenal switches occur without any prompting by attention. 

High-level perceptual grouping also influences the interpretation of ambiguous visual stimuli (e.g., Gillam, 1972, 1976; Ramachandran & Anstis, 1983). In binocular rivalry, it has been shown that the brain reassembles patches of images presented in different eyes into coherent percepts (Kovacs, Papathomas, Yang, & Feher, 1996). Using bistable stimuli like the SFM, Grossman and Dobbins (2003) find that coupling between the two spheres is strong when both spheres are ambiguous but reduced when one is made unambiguous. They argue that the lack of coupling between the ambiguous and unambiguous stimuli is not due to the dissimilarity between the stimuli but rather due to global feedback, which is proportional to the amount of ambiguity. Freeman and Driver (2006) replicate this result when the unambiguity is determined by opacity. However, when luminance and depth cues are introduced, they report strong coupling between stimuli that differ in the strength of the directional ambiguity of their motion. 

A critical factor in elucidating the nature of the underlying mechanisms of bistability is whether high-level cues are relevant even in cases where low-level cues are sufficient to disambiguate the stimuli. By some computational accounts, visual competition is a feedforward, hierarchical process in which the higher levels are engaged only when resolution is not possible at the previous level (Freeman, 2005; Wilson, 2003). However, alternative frameworks emphasize the top-down influence of prior knowledge in a more complex interplay of feedforward and feedback signals (Hohwy, Roepstorff, & Friston, 2008; Watson, Pearson, & Clifford, 2004). In order to determine if high-level effects influence the perception of bistable stimuli when low-level signals are disambiguated, we examined coupling using two highly unambiguous spheres. Since the direction of either sphere presented in isolation is stable, any coupling that arises between the two spheres presented together will not simply be the passive result of random, single sphere dynamics but represent an active process of the visual system to override the physical characteristics of one of the spheres. Given that higher level grouping principles are believed to exert their influence on the visual competition process through attentionally modulated feedback (Carmel, Walsh, Lavie, & Rees, 2010; Kanai, Bahrami, & Rees, 2010; Kanai, Carmel, Bahrami, & Rees, 2011), we also postulated that coupling would be reduced when attention is diverted from the SFM stimulus. 

Methods

Observers

One of the authors and 5 naive observers served as subjects. All wore optical correction as necessary. 

Apparatus and stimuli

A Dell Optiplex computer running MATLAB (MathWorks) was used for stimulus generation, experiment control, and recording subjects' responses. The programs controlling the experiment incorporated elements of the PsychToolbox (Brainard, 1997). Stimuli were displayed on a Diamond Digital monitor (resolution = 1024 * 768 pixels, refresh rate = 85 Hz, background luminance = 50 cd/m²) driven by the computer's built-in Radeon graphics card. The display was calibrated using a photometer and linearized using look-up tables in software. At the viewing distance of 57 cm, 1 pixel subtended 2.1 arcmin. 

Stimulus

A set of 200 dots whose position oscillates around either a vertical (for left/right motion) or a horizontal axis (for Up/Down motion) was used to create the illusion of a spherical object rotating in space. When the dots are equal in size and contrast, the motion is ambiguous and flips between the two alternative percepts with durations in either direction following a gamma distribution (Leopold & Logothetis, 1999). We created highly unambiguous directional spheres by introducing size and contrast cues into the stimulus resulting in an “imposed” direction of motion. This was achieved by making the dots in one trajectory (e.g., “up” if the imposed direction was upward) more visible/salient by increasing their size and contrast compared to those in the other trajectory (e.g., “down”). The larger dots were black and had a diameter of 7 arcmin, while the smaller dots had a diameter of 3 arcmin and a luminance of 32 cd/m². The dots followed simple harmonic motion with a peak speed of 2.1 deg/s. Each illusory sphere subtended 4.2 deg in diameter and its center was separated from the fixation cross by 3.3 deg. 

Procedure

Experiment 1: No attentional load—Constant monitoring of two directions of motion

Schematic example of one frame of the stimulus is shown in Figure 1a. Observers fixated a cross that was present throughout the stimulus duration and were required to monitor the direction of motion of two nearly unambiguous spheres presented on either side of fixation that always rotated in opposite directions. Two conditions were tested: a coaxial condition, whereby the spheres rotated either upward or downward and shared a common axis of motion (though the motions were always in opposite directions), and a non-coaxial condition, whereby the spheres rotated either to the left or right of a vertical axis and had parallel axes of motion. Observers completed a minimum of 10 blocks, each lasting 240 s. During a block, 8 regular directional switches were imposed on the stimulus every 30 s (plus a temporal jitter of ±400 ms) to ensure a balanced representation of the two motions on either side of fixation, resulting in eight full cycles of dual motion. The observer had to indicate the direction of motion using response keys (“a” and “s” in the coaxial condition or “a” and “z” in the non-coaxial condition) for the stimulus on the left of fixation and (“k” and “l” (coaxial) or “k” and “m” (non-coaxial)) for the stimulus on the right of fixation (Figure 1a). Data from the 8 cycles of a block were pooled together and averaged across blocks (for a duration of 29.6 s because of the temporal jitter). We were not interested in biases due to spatial location and combined the four “up” (or “right”) conditions on the left of fixation with the four “up” (or “right”) conditions on the right of fixation. Only Observer IM ran the conditions interleaved. 

Figure 1

 

SFM stimulus procedure and data for one observer. (a) Schematic of one frame in Experiment 1. Fixation is a cross that is present throughout the stimulus duration. Dashed line and arrows illustrate the directions of motion but were not present in the experiment. Observers were tested in blocks that lasted 240 s consisting of eight 30-s periods of unambiguous motion (only 2 periods shown). In each period, the stimuli on the left and right of fixation rotated in opposite directions (illustrated by arrows) while observers reported both directions of motion with two key presses. (b) The perceived direction of motion (red lines) of the spheres did not always match their physical directions, leading to coupling (shaded gray areas). (c) Directional data in coaxial and non-coaxial conditions for Observer IM. The leftmost column plots the two directions of motion separately in the (top) coaxial and (bottom) non-coaxial conditions. The blue curve plots the proportion of times the observer said “up” (or “right”) for an upward (or rightward) rotating sphere over the 30-s time period. The red curve is the proportion of times the observer classified a downward (or leftward) motion as going “up” (or “right”). Error bars contain ±1 standard error. The middle column plots data in the same format for single sphere stimuli. The rightmost column plots in green the proportion of coupling as a function of time. The black curves represent the proportion of random coupling predicted from the single sphere dynamics. Error bars are 95% confidence intervals.

A single sphere condition was also run on each observer to measure a “baseline” level from which to calculate the amount of coupling that would be predicted from switches based on the single sphere dynamics. Observers completed a minimum of 4 blocks in two conditions: (a) when the direction of rotation of the single sphere was around a horizontal axis (termed “coaxial,” as the single sphere motion is the same as one of the spheres in the coaxial condition) and (b) when the direction of rotation was around a vertical axis (termed non-coaxial). In half the blocks, the sphere was on the left side of fixation, and in the other half, it was on the right side of fixation to account for any biases due to spatial location. The proportion of coupling predicted from the single sphere dynamics was calculated as 

$\mathrm{P}\mathrm{r}\mathrm{e}\mathrm{d}\mathrm{i}\mathrm{c}\mathrm{t}\mathrm{e}\mathrm{d}\mathrm{p}\mathrm{r}\mathrm{o}\mathrm{p}\mathrm{o}\mathrm{r}\mathrm{t}\mathrm{i}\mathrm{o}\mathrm{n}\mathrm{c}\mathrm{o}\mathrm{u}\mathrm{p}\mathrm{l}\mathrm{i}\mathrm{n}\mathrm{g}=(1-p)*q+(1-q)*p,$

(1)

where each sphere in isolation had the probability of being seen to rotate in its imposed direction of motion, p (e.g., “up”) and q (e.g., “down”). 

In the few instances where no keys were pressed or the two keys for the same sphere were pressed (between 0.01% and 0.5% of all frames), responses for the corresponding frames were coded as not indicating the correct direction of motion. 

Experiment 2: Attentional load—Regular sampling of two directions of motion in the coaxial condition

High attentional load task: The stimuli were similar to those in Experiment 1, except that a string of numbers was presented at fixation and observers were required to count the number of times a white “2” appeared over the 240-s period. The nine distracter numbers (4 white and 5 black) and the one target had an equal probability of appearing in the string. While observers performed the counting task at fixation, they were also required to do a directional task on both spheres at regular intervals throughout the trial. Starting from 3 s after the stimulus onset, and occurring every 5 s thereafter, a cross would appear at fixation instead of a number. This cued observers to report the direction of motion of the two spheres within a response window using the same response keys as in Experiment 1. The durations of the response window, the fixation cross, and the target and non-target numbers were always equal and were individually set for each observer based on practice runs to ensure performance above 70% (between 300 and 500 ms). At the end of each of the eight cycles, the two spheres would disappear and a number would appear at fixation corresponding to the total number of times the target was present in the cycle. Using a key press, observers indicated whether this total was correct or not, where an incorrect total was produced by adding 1 to the final count on 50% of the trials. The total was present for 5 s, followed by a gray screen for 2 s before the next cycle commenced. Observers practiced on the task prior to data collection and performed a minimum of 10 blocks of 240 s each. 

Low attentional load task: The stimulus presentation was the same to avoid any potential confounds caused by the string of numbers and observers were instructed to only perform the directional task. At the end of each 240-ms period, the sum answer that subjects were instructed to ignore was presented for 2 s followed by a blank screen for 2 s. Observers performed a minimum of 10 blocks. 

Results

Experiment 1

Observers monitored the perceived directions of two spheres over time. Although the spheres were always rotating in opposite directions (Figure 1a depicting coaxial condition), observers would often perceive them as rotating in the same direction (shaded areas in Figure 1b). Figure 1c plots the proportion of time Observer IM reported that the spheres were moving in one of the imposed directions as a function of time (top shows coaxial condition, whereas bottom shows non-coaxial). If neither sphere had appeared to switch from its imposed direction of motion, this value should always equal 1 for one of the directions and 0 for the other. In both conditions, the curves start to converge toward the center (0.5), slightly earlier in the coaxial condition than the non-coaxial condition. 

In the single sphere data, fluctuations in the directions of motion do not start to appear until after approximately 13 s. The rightmost column plots coupling that reflects the proportion of times in each frame the observer indicated that the two spheres were rotating in the same direction. Note that for Observer IM coupling diverges significantly from the prediction based on the single sphere data (Equation 1) after roughly 2 s in the coaxial condition. In the non-coaxial condition, the coupling is weaker and only diverges from the single sphere prediction after approximately 22 s. 

Figure 2 plots coupling in the coaxial and non-coaxial conditions for the five naive observers. Although there is some intersubject variability regarding the onset and strength of coupling, all observers display significant departures from the single sphere dynamics in the coaxial condition. The non-coaxial condition leads to more intersubject variability with LB perceiving the veridical directions of the two spheres throughout the trials, whereas the other observers display various degrees of coupling in the non-coaxial condition. 

Figure 2

 

Coupling in (left) coaxial and (right) non-coaxial conditions for five naive observers. The black curves represent the proportion of coupling predicted from the single sphere dynamics. Error bars are 95% confidence intervals. Bottom right plots are the proportion of measured coupling (dual sphere conditions) and predicted coupling (single sphere conditions) averaged across time in the coaxial arrangement (left) and in the non-coaxial arrangement (right). Error bars are 95% confidence intervals and solid line depicts equal proportions of actual and predicted coupling.

The time-averaged proportion of coupling in the two dual sphere conditions is plotted against the predicted coupling in the single sphere conditions for the six observers, in the bottom right of Figure 2. The left-hand plot shows data in the coaxial condition with all data points well above the unity line: The coupling in the dual axis condition is significantly different from that predicted from the single sphere dynamics (within-subjects ANOVA, F _1,20 = 41.7, p < 0.0001). The right-hand plot shows data in the non-coaxial condition with the data points clustering above the line of equality and the amount of coupling also significantly different from the single sphere condition (F _1,20 = 10.1, p = 0.0049). There is also a significant interaction (F _1,20 = 12.5, p = 0.0021) between the condition (coaxial or non-coaxial) and the configuration (dual or single) indicating that coupling is significant in the dual coaxial condition. 

Experiment 2

In order to determine if diverting attention away from the spheres would reduce coupling, observers performed a counting task at fixation while reporting the direction of motion of the spheres only when cued. Figure 3 plots the effects of attention on the amount of coupling between the rotating spheres in the coaxial condition. When observers performed the high attentional load task at fixation (gray symbols), there was a significant decrease in the proportion of coupling compared to the low attentional load task (t ₅ = 3.35, p < 0.05), most markedly for AA, IM, and LB. For all observers, the amount of coupling measured in Experiment 2 with the low attentional load task (respond upon presentation of fixation cross only: black symbols) was similar to the constant monitoring technique in Experiment 1 (as can be seen by comparing black symbols in Figure 3 with the green curves from Figures 1 and 2). 

Figure 3

 

Proportion of coupling in the dual sphere conditions sampled at 6 discrete points within the 30-s period. Gray symbols represent the high attentional load condition; black symbols are the low load condition. Error bars are ±1 standard errors. Percent correct scores represent performance on the secondary task.

Discussion

We find rapid and reliable coupling between two unambiguous spheres when they rotate around a common axis, supporting the perceptual construct of a single, unidirectional, object. When attention is diverted from the structure-from-motion stimuli, we find that the perceptual grouping of their directions of rotation is significantly reduced. This study differs fundamentally from previous experiments using bistable stimuli where the visual system received conflicting or ambiguous information from the same spatial location. Here, we have the opposite situation: Faced with locally unambiguous signals, the visual system overrides reliable information to generate a percept that is inconsistent with one-half of the stimulus. 

It has been reported previously that the alignment of local and global cues can enhance performance on many basic, low-level tasks. Using a contour detection task, Field, Hayes, and Hess (1993) report that performance decreases as the degree of collinearity between the local Gabor patches and the global contour axis is reduced. A similar dependence on the coalignment between the local Gabor patches and the global axis of the stimulus underlies contrast facilitation and discrimination tasks (e.g., Bonneh & Sagi, 1998; Cannon & Fullenkamp, 1991; Kapadia, Ito, Gilbert, & Westheimer, 1995). More recently, the relative importance of both local and global cues has been examined in more higher level processes such as binocular rivalry. Silver and Logothetis (2004) found that the perceptual grouping of dot arrays without any change in low-level stimulus features could alter dominance periods in rivalry. Using biological motion to induce perceptual grouping, Watson et al. (2004) report rivalry between point-light walkers that occurs due to high-level perceptual grouping rather than low-level cues, since at the local level these stimuli would fail to initiate rivalry. Consistent with this finding of global dominance, Andrews and Lotto (2004) report that rivalry can occur between physically identical monocular stimuli if they elicit different higher level percepts. They also show that physically different stimuli that would otherwise cause rivalry fail to do so if they are perceived as belonging to the same object. However, Carlson and He (2004) examined this issue using bar and grating stimuli and report that rivalry was due to the local interactions, not global percepts. Our results using bistable stimuli support the former findings whereby global cues in the stimulus alter the stability of one sphere's direction of rotation. In order to achieve a unidirectional motion percept, the visual system overrules local motion signals in half of the stimulus. 

The ability of the visual system to impose coupling on the rotating spheres is severely hampered when attention is diverted away from them. Attention is known to modulate the size of visual phenomena such as the motion aftereffect (Chaudhuri, 1990; Lankheet & Verstraten, 1995; Rees, Frith, & Lavie, 1997), the tilt aftereffect (Spivey & Spirn, 2000), and contrast facilitation (Freeman, Driver, Sagi, & Zhaoping, 2003), as well as the amount of adaptation to illusory contours (Montaser-Kouhsari & Rajimer, 2004). Our results are consistent with these reports and we find that observers must attend to the coaxial spheres for coupling to occur. We suggest that coupling is the result of a feedback mechanism that suppresses local motion signals and that attention modulates the strength of this feedback. 

There is growing interest in determining the anatomical areas involved in the perception of bistable stimuli (Carmel et al., 2010; Kanai et al., 2010, 2011). In their most recent paper, Kanai et al. (2011) report a structural and functional segmentation of the superior parietal lobule (SPL) that receives feedback from higher cortical areas to modulate bistable perception. Given that our behavioral result implicates higher level mechanisms, it would be of interest to determine whether the SPL might also regulate the entrainment of highly unambiguous stimuli. 

Acknowledgments

C.W.G. Clifford was funded by an Australian Research Council Future Fellowship. 

Commercial relationships: none. 

Corresponding author: Isabelle Mareschal. 

Email: [e-mail]. 

Address: School of Psychology, The University of Sydney, Room 508, Griffith Taylor Building, NSW 2006, Australia.