- Email: [email protected]
Perceptual reversal of bi-stable figures in microgravity and hypergravity during parabolic flight
Neuroscience Letters 507 (2012) 143–146
Contents lists available at SciVerse ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Perceptual reversal of bi-stable figures in microgravity and hypergravity during parabolic flight Gilles Clément ∗ , Michael Demel International Space University, Parc d’Innovation, 1 rue Jean-Dominique Cassini, Illkirch-Graffenstaden F-67400, France
a r t i c l e
i n f o
Article history: Received 17 October 2011 Received in revised form 2 December 2011 Accepted 2 December 2011 Keywords: Gravity Visual illusions Human visual perception Ambiguous figures Perspective
a b s t r a c t This experiment investigated whether the perception of depth-reversible figures is altered when the observer is in microgravity or hypergravity. A set of five bi-stable ambiguous figures was presented to ten participants in 1 g, 0 g, and 1.8 g during parabolic flight. The figures included static images such as the Necker cube; kinetic depth displays such as a moving plaid and a sphere cluster of moving dots appearing to rotate in one of two directions; and a silhouette photograph. For each stimulus figure, subjects reported which of the two possible perceptual configurations they saw first and then continuously indicated when perceptual reversals occurred for durations ranging from 20 to 30 s. The same first percept was reported in 1 g, 0 g, and 1.8 g. The time delay for the first reversal between the two possible image interpretations was longer and the number of reversals was fewer in 0 g as compared to 1 g for four of the five figures. The opposite effects were seen when going from 0 g to 1.8 g. These findings confirm that, consistent with a multisensory approach to three-dimensional form perception, gravity has a clear effect on the interpretation of depth-based stimuli and this gravity-based component interferes with visual perception stability. © 2011 Elsevier Ireland Ltd. All rights reserved.
Mach [27] pointed out that the perception of solid objects could switch back and forth between two (or more) possible interpretations. A well-known example of a reversible figure is the Necker cube (Fig. 1, inset, left). This simple line drawing can represent a cube in either of two possible orientations, facing upward and to the left or downward and to the right. Other examples of bi-stable figures are shown in Fig. 1. These images are planar images that are alternately identifiable as one of two disparate three-dimensional percepts. Researchers have used these bi-stable figures to study the dynamics of perceptual alternations by asking observers to continually report which of the two possible interpretations are perceived at every moment. In these experiments, observers typically watch a static or moving figure for several seconds on a laptop monitor and report their percept continually by pressing down one of keyboard keys. Results from these studies have been used to distinguish elementary sensory features of the physical image from the top-down processes involved in constructing either of its visuo-spatial interpretations [18,26]. Under prolonged observation of a bi-stable figure, even naive subjects experience reversals spontaneously. On the other hand, if perspective or other cues are added the figure reverses less frequently and there comes a point when it is no longer ambiguous [32]. For example, when holding a Necker cube constructed
∗ Corresponding author. Tel.: +33 388 65 5444; fax: +33 388 65 5447. E-mail address: [email protected] (G. Clément). 0304-3940/$ – see front matter © 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2011.12.006
from wire, the reversals happen less often and for shorter periods than for just seeing a line drawing of a Necker cube [16]. Therefore, haptic information stabilizes to some extent visual perception of the image. There is ample evidence that visual perception is influenced by multimodal integration of retinal, tactile, and gravitational inputs [17]. In the case of a visually bi-stable ambiguous figure, it is therefore possible that gravitational information interferes with perception, as do haptic cues. The perception of upright is a result of integrating the orientation of the ambient visual world, the direction of gravity, and an internal representation of the body’s longitudinal axis [29]. Previous studies have shown that ambiguous figures reversed less frequently [11,35,37], geometrical visual illusions were less frequent [7,23,34], and the face-inversion effect even disappeared [25] during large body tilt, i.e., when retinal and gravitational frames of reference deviate substantially. In microgravity, the perception of upright becomes relatively more body-defined [8,15] and the influence of vision in determining upright is significantly reduced [12], which also reduces visual illusions and character recognition [13,20,24,36]. Therefore, it was hypothesized that the absence of gravitational information in microgravity would reduce the frequency of reversals of visually ambiguous figures. Ten subjects (4 women, 6 men, aged 24–52, mean 30) participated in this experiment performed during two campaigns of parabolic flights onboard the Airbus A300 Zero-G. This aircraft is capable of flying parabolic trajectories during which the entire cabin is in microgravity (less than 10−2 g) for about 22 s. This period
144
G. Clément, M. Demel / Neuroscience Letters 507 (2012) 143–146
Fig. 1. Inset: all the ambiguous figures used in these studies were drawn on a planar surface. They were bi-stable, seeming to appear in either of two orientations or to move in either of two directions. The five figures included (from left to right): (1) the classical perspective-reversible Necker cube drawn with white lines over a black background; (2) a shaded cube that may become the corner of a room; (3) a plaid moving upwards at 1◦ /s [17] [see demonstration at http://www.cns.nyu.edu/home/hupe/arvo01demo/demo plaids.html]; (4) an ambiguous sphere made of random blue dots over a black background rotating about a horizontal axis at approximately 30◦ /s [2] [see demonstration at http://www.uq.edu.au/nuq/jack/rivalry.html]; (5) a photograph of the Space Shuttle (credit NASA) where the bay doors may look convex or concave. Top: mean + standard error of time to first reversal for each figure averaged across 3 trials and 10 subjects in normal gravity prior to the flight (1 g), in microgravity (0 g), hypergravity (1.8 g), and in normal gravity under the influence of the motion sickness medication (1 g med) during parabolic flight. *p < 0.05. Bottom: mean + standard error of the number of reversals per minute for the same conditions.
of microgravity is preceded and followed by periods of hypergravity (1.8 g) for about 20 s each. Subjects had given their informed consent to participate in this study in accordance with the guidelines of the local ethics committee, and had passed the equivalent of an Air Force Class III medical examination. All subjects reported that they had normal or corrected-to-normal vision with no known visual deficits. Only two subjects had previous parabolic flight experience. All the subjects took prophylactic medication (a combination of promethazine and dexedrine) before boarding the plane, and only one of them showed symptoms of motion sickness during the flight. Data were collected with this experiment in normal gravity prior to taking the medication (1 g), and on board the airplane in both microgravity (0 g), hypergravity following the 0 g phase (1.8 g) and normal gravity under the influence of the medication (1 g med). The latter condition was obtained when the aircraft was flying straight and level between two series of parabolas or during the flight back to the base. It was used to assess if the medication could be held responsible for the differences observed between the two gravity conditions. In microgravity, the observers were tested in the dark while free-floating to eliminate orientation-related cues. The freefloating condition is illustrated in a previous paper [8]. Each of the five figures shown in Fig. 1 was presented to the subjects in a headmounted display (Z800 3DVisor, eMagin Corporation, Bellevue, WA) using a macro-enhanced Microsoft PowerPoint presentation
running on a laptop computer. For the ambiguous static depth figures (the two cubes and the photograph), we asked the subjects to identify which configuration they saw first, and then to indicate when they saw the second configuration by pressing down either of the two buttons of a mini trackball finger mouse. For the ambiguous kinetic depth structures, subjects reported whether the plaid appeared to be moving upwards or interweaving horizontally, and whether the sphere made of blue dots appeared to be rolling toward them or away from them. The figures were presented on a black background and all external visual references were blocked by a fabric cover placed over the head-mounted display. The figures subtended a viewing angle of 30◦ at a perceived distance of approximately 50 cm. The sample rate of the trackball was 40 Hz and the refresh rate of the visual display was 60 Hz. Participants were instructed to focus on the center of the images and to limit scanning eye movements. The order of figures was randomized across subjects and parabolas. Each ambiguous figure was presented during 3 parabolas, i.e., a total of 15 parabolas per subject. This corresponded to a presentation duration totaling 61.3 ± 4.2 s and 40.4 ± 2.9 s per figure in 0 g and 1.8 g, respectively, across all subjects. In the 1 g and 1 g med conditions, the figures were also presented during 3 trials, but for 30 s each, i.e., a total presentation duration of 90 s per figure. The subjects were familiarized with the ambiguous figures used in this study prior to the first baseline data collection. The subjects were first allowed to practice with the figures and the experimental protocol during three trials in normal gravity on the morning of the flight, and the data was then collected in this order: 1 g, 0 g, 1.8 g, and 1 g med. The macro controlled the flow of the figures presented, recorded the subject inputs from the finger mouse buttons, and saved all of the relevant data into an external text file. The macro also made note of the times that the figures were first displayed, when the subject indicated the occurrence of the first percept, and the times for all subsequent perceptual reversals. For each figure, the measurements included: (a) the time from stimulus onset to the first percept report; (b) the first percept; (c) the time from the first percept report to the first reversal; (d) and the number of reversals. The number of reversals per minute was calculated for the period from the first percept report to the end of the trial. There was no significant difference between the measurements obtained in 1 g and 1 g med, thus ruling out an effect of the motion sickness medication on these results. The subjects reported the same first percept in 1 g and 1 g med in 93.2% of the responses. The same first percept was also reported in 1 g and 0 g in 89.5% of the responses, and in 1.8 g in 87.2% of the responses. That is, compared to 1 g (10 subjects × 5 figures × 3 trials = 150 responses), the first percept was different in 0 g in 16 responses, and in 1.8 g in 19 responses. The probability to view each percept was close to 50% and did not change significantly across gravity conditions. A within subjects (repeated measures) ANOVA was conducted to compare the effect of gravity on the time to first reversal and the number or reversals in 0 g, 1 g, and 1.8 g. When responses were pooled across figures, there was a significant effect of gravity on the time to first reversal [F(2,18) = 7.12, p < 0.001] and number of reversals [F(2,18) = 5.54, p < 0.001]. Paired samples t-tests were used to make post hoc comparisons between gravity conditions. The time to first reversal was longer in 0 g than in 1 g for all subjects (Fig. 1, top). This difference was statistically significant for the Necker’s cube [t(9) = −1.89, p = 0.04], the shaded cube [t(9) = −3.62, p = 0.002], the moving plaid [t(9) = −2.77, p = 0.01], and the silhouette photograph [t(9) = −2.09, p = 0.03]. The time to first reversal was significantly shorter in 1.8 g than in 1 g for the moving plaid only [t(9) = 2.05, p = 0.03]. However, the time to first reversal was significantly shorter in 1.8 g than in 0 g for all the figures: Necker’s
G. Clément, M. Demel / Neuroscience Letters 507 (2012) 143–146
Fig. 2. Time to first reversal as a function of number of reversals (mean of 3 trials, 10 subjects × 5 figures) in 1 g, 0 g, and 1.8 g. Both dependent variables seem to be linearly related. R2 = 0.430.
cube [t(9) = 1.93, p = 0.04], shaded cube [t(9) = 2.17, p = 0.03], moving plaid [t(9) = 5.24, p < 0.001], rolling sphere [t(9) = 2.27, p = 0.02], silhouette photograph [t(9) = 3.35, p = 0.004]. The frequency of changes in appearance of the figures was smaller in 0 g than in 1 g (Fig. 1, bottom) for 9 subjects out of 10. This decrease in the number of reversals was significant for the Necker’s cube [t(9) = 1.87, p = 0.04], the shaded cube [t(9) = 3.04, p = 0.006], the moving plaid [t(9) = 2.26, p = 0.02], and the silhouette photograph [t(9) = 2.02, p = 0.03]. Eight subjects had more reversals per minute in 1.8 g than in 1 g, but this increase was only significant for the moving plaid [t(9) = −2.62, p = 0.01]. Finally, the number of reversals was significantly larger (p < 0.006) in 1.8 g than in 0 g for all the five figures. When responses were pooled together between subjects and within subjects, the variances of the subjects’ judgments were stable in 1 g and 1.8 g for both the time to first reversal (14.1 and 11.8, respectively) and the number of reversals (21.6 and 28.9, respectively). In 0 g, the variance was larger than in 1 g for the time to first reversal (26.5) and smaller than in 0 g for the number of reversal (13.8). The number of reversals per minute measured in this study is consistent with earlier studies using long periods of exploration [1,32]. The steady-state probability of seeing each view, i.e., the cumulative time spent reporting each percept over a given observation time, was rather balanced for these stimuli (approximately 50%). In agreement with previous studies [18], there was an inverse correlation between the time to see the first reversal and the number of reversals. This correlation was present in all gravity conditions (Fig. 2). These results indicate that for four figures (the Necker’s cube, the shaded cube, the moving plaids, and the silhouette photograph), the percept reversal occurred less frequently in 0 g than in 1 g. How might the absence of gravitational information affect observers’ visual judgments of these ambiguous figures? Threedimensional ambiguous figures are ideal experimental model to investigate multisensory processes. The results of recent studies on visual illusions suggest that the visual system is relatively unreliable for 3D perception, and that observers give greater weight to the more reliable source, whether it is the visual, haptic, or gravitational input, so as to optimize overall reliability [14,28]. One prevalent theory of visual perception is the notion that one of the two views of the ambiguous figure “wins”, promoting models that embed a mechanism to choose between the two possible interpretations of the stimulus [32]. Transferring this approach to the role of gravity in visual perception would suggest an architecture where the neural representations of the visual and body-oriented interpretations of the stimulus continually compete for dominance. There is ample evidence that the frame of reference is more body-oriented
145
in microgravity [6,8,10,15,19,20]. In 0 g, the direction of upright would become more strongly driven by and aligned with the body vector, resulting in a proportionally weaker influence of the retinal reference [13]. Perception instability generated by visual illusions would then be reduced, leading to less reversal of ambiguous figures in 0 g. This explanation is supported by experiments showing that the orientation of the visual background is significantly less influential in determining the perceptual upright during the microgravity phase of parabolic flight than it is under normal gravity [13,20,23,24,36]. Similar results were obtained during the prolonged microgravity of orbital flight. For example, astronauts manifest a strong bias toward the body (idiotropic) vector when ask to point to the perceived “ceiling” of the spacecraft with their eyes closed [15]. The astronauts’ ability to recognize complex figures and interpret shapes based on shading (e.g., “the light comes from above”) is altered during orbital flight [see review in 6], which also suggests reduced visual effects in microgravity. Another interpretation is that the decrease in perceptual reversal seen in 0 g is related to a decrease in the geometric (linear) perspective and shading cues for depth when the gravitational input is absent. Previous research using visual illusions suggests that the reliance on geometric perspective and shading cues decreases when subjects are tilted relative to gravity [7,37] and in microgravity during parabolic [10,36] or orbital [6,31] flight. The interpretation for this decrease is that perspective and shading are well defined when the head is upright relative to gravity, but more ambiguous when the head is tilted or when gravity is virtually absent. In 0 g the gravitational reference is absent and the direction of gaze and perceived straight-ahead are also altered due to changes in the otolith signals [4]. Therefore, geometric perspective and shading would become less reliable as depth cues, and depth-reversible figures such as those in the present study would be less ambiguous. It is interesting to note that vestibular patients suffering from otolith vertigo also exhibit less geometric perspective effects when presented with visual illusions [9]. During hypergravity, a gravitational reference is present but its scale is altered relative to 1 g, possibly creating more perceptual instability and reversals [30]. In the case of the ambiguous rotating sphere, the depth effect is obtained from the motion of random dots. Because no size or perspective cues differentiate the front from rear surfaces, the direction of rotation is ambiguous. This figure would be less sensitive to gravity conditions that the other figures, as indicated by our results, because it does not include depth cues such as geometric lines or shading. One could argue that the difference in the number of reversals between 1 g and 0 g is due to an indirect effect on attention. It has been suggested that subjects may adopt different attention sets to deal with the task in different postures [33]. For example, it was found that subjects solve anagrams significantly faster when supine than when standing, and this difference was attributed to less locus coeruleus-noradrenergic system activity when lying down [22]. However, the absence of any reliable increase in our observers’ response variance during flight, and the opposite effects seen in 0 g and 1.8 g, suggests that the changes seen in our study were not related to the stress or unusual nature of parabolic flight itself. Also, even though subjects were instructed to fixate the center of the images, eye movements could have occurred during the experiment. The transition from hypergravity to microgravity during parabolic flight is known to generate nystagmus [5], changes in torsional eye position [3] and vertical misalignment of the eyes [21]. These induced eye movements could degrade the retinal image and indirectly cause a decrease in the visual effects.
146
G. Clément, M. Demel / Neuroscience Letters 507 (2012) 143–146
In conclusion, the absence of gravitational information increased the time for the first reversal and cut down the number of reversals in four of the five ambiguous figures. These perceptual changes are consistent with an increase in the use of the body as a reference frame when gravity is changed. These effects were seen for depth-reversible ambiguous figures. Such figures were chosen because previous results indicated that illusions based on perspective and shading were altered in normal subjects placed in microgravity [36] and in patients with otolithic vertigo on Earth [9]. Other complex visual stimuli that were not depth-based did not induce such changes [9,36]. Whether the effect seen in the present experiment also applies for other ambiguous figures that are more two-dimensional, such as the Rubin’s vase, will have to be the subject of future studies. The shortcomings described above for this pilot study should be eliminated in a planned experiment designed to investigate the effects of prolonged microgravity on board the International Space Station. Acknowledgements This research was supported by a CNES grant and CNRS. We thank the people at CEV, CNES, ESA, MEDES, and NOVESPACE, and in particular P. Denise, F. Gai, T. Gharib, C. Mora, V. Pletser, and P. Rosier. We are also grateful to our test subjects for participating in this experiment. References [1] J. Beer, Correlations among ambiguous figures, curiosity, and spatial ability, Percept. Mot. Skills 71 (1990) 1188–1190. [2] Y. Bonneh, A. Cooperman, D. Sagi, Motion induced blindness in normal observers, Nature 411 (2001) 798–801. [3] A.H. Clarke, Listing’s plane and the otolith-mediated gravity vector, Prog. Brain Res. 171 (2008) 291–294. [4] G. Clément, Alteration of eye movements and motion perception in microgravity, Brain Res. Rev. 28 (1998) 161–172. [5] G. Clément, C. André-Deshays, C.E. Lathan, Effects of gravitoinertial force variations on vertical gaze direction during oculomotor reflexes and visual fixation, Aviat. Space Environ. Med. 60 (1989) 1194–1198. [6] G. Clément, M.F. Reschke, Neuroscience in Space, Springer, New York, 2008. [7] G. Clément, J. Eckardt, Influence of the gravitational vertical on geometric visual illusions, Acta Astronaut. 56 (2005) 911–917. [8] G. Clément, T.N. Arnesen, M.H. Olsen, B. Sylvestre, Perception of longitudinal body axis in microgravity during parabolic flight, Neurosci. Lett. 413 (2007) 150–153. [9] G. Clément, M.J. Frayss, O. Deguine, Mental representation of space in vestibular patients with otolithic or rotatory vertigo, Neuroreport 20 (2009) 457–461. [10] G. Clément, A. Bukley, Mach’s square-or-diamond phenomenon in microgravity during parabolic flight, Neurosci. Lett. 447 (2008) 179–182.
[11] M.C. Corballis, N.J. Zbrodoff, L.I. Shetzer, P.B. Butler, Decisions about identity and orientation of rotated letters and digits, Mem. Cognit. 6 (1978) 98–107. [12] R.T. Dyde, M.R. Jenkin, L.R. Harris, The subjective visual vertical and the perceptual upright, Exp. Brain Res. 173 (2006) 612–622. [13] R.T. Dyde, M.R. Jenkin, H.L. Jenkin, J.E. Zacher, L.R. Harris, The effect of altered gravity states on the perception of orientation, Exp. Brain Res. 194 (2009) 647–660. [14] M.O. Ernst, M.S. Banks, Humans integrate visual and haptic information in a statistically optimal fashion, Nature 415 (2002) 429–432. [15] S. Glasauer, H. Mittelstaedt, Perception of spatial orientation in microgravity, Brain Res. Rev. 28 (1998) 185–193. [16] Y.-X. Ho, S. Serwe, J. Trommershäuser, L.T. Maloney, M.S. Landy, The role of visuo-haptic experience in visually perceived depth, J. Neurophysiol. 101 (2009) 2789–2801. [17] I.P. Howard, Human Visual Orientation, Wiley, Chichester, 1982. [18] J.-M. Hupé, N. Rubin, The dynamics of bi-stable alternation in ambiguous motion displays: a fresh look at plaids, Vision Res. 43 (2003) 531–548. [19] H.L. Jenkin, M. Jenkin, R.T. Dyde, L.R. Harris, Shape-from shading depends on visual, gravitational, and body-orientation cues, Perception 33 (2004) 1453–1461. [20] H.L. Jenkin, R.T. Dyde, J.E. Zacher, D.C. Zikovitz, M.R. Jenkin, R.S. Allison, I.P. Howard, L.R. Harris, Relative role of visual and non-visual cues determining the direction of ‘up’: experiments in parabolic flight, Acta Astronaut. 56 (2005) 1025–1032. [21] F. Karmali, S. Ramat, M. Shelhamer, Vertical skew due to changes in gravitoinertial force: a possible consequence of otolith asymmetry, J. Vestib. Res. 16 (2006) 117–125. [22] D.M. Lipnicki, D.G. Byrne, Thinking on your back: solving anagrams faster when supine than when standing, Cognit. Brain Res. 24 (2005) 719–722. [23] M.I. Lipshits, J. McIntyre, Gravity affects the preferred vertical and horizontal in visual perception of orientation, Neuroreport 10 (1999) 1085–1089. [24] M.I. Lipshits, A. Bengoetxea, G. Cheron, J. McIntyre, Two reference frames for visual perception in two gravity conditions, Perception 34 (2005) 545–555. [25] J.S. Lobmaier, F.W. Mast, The Thatcher illusion: rotating the viewer instead of the picture, Perception 36 (2007) 537–546. [26] G.M. Long, T.C. Toppino, Enduring interest in perceptual ambiguity: alternating views of reversible figures, Psychol. Bull. 130 (2004) 748–768. [27] E. Mach, The Analysis of Sensations, Dover, New York, 1959 (Original work published in 1897). [28] P.J. McAdie, M.J. Steinbach, Visually induced tilt affects form perception, Perception 10 (1981) 525–530. [29] H. Mittelstaedt, A new solution to the problem of the subjective vertical, Naturwissenschaften 70 (1983) 272–281. [30] I. Negishi, H. Kaneko, H. Mizushina, K. Ogata, Effects of tilt of the visual stimuli on the perception of gravitational vertical under normal- and hyper-gravity conditions, Opt. Rev. 16 (2009) 290–295. [31] C.M. Oman, Human visual orientation in weightlessness, in: L. Harris, W. Jenkin (Eds.), Levels of Perception, Springer Verlag, New York, 2003, pp. 375–398. [32] S.E. Palmer, Vision Science: Photons to Phenomenology, MIT Press, Cambridge, MA, 1999. [33] A. Peru, J.S. Morgant, When supine is better than upright: evidence from postural effects in extinction patients, Brain Res. 1110 (2006) 175–181. [34] W. Prinzmetal, D.M. Beck, The tilt-constancy theory of visual illusions, J. Exp. Psychol. Hum. Percept. Perform. 27 (2001) 206–217. [35] I. Rock, Orientation and Form, Academic Press, New York, 1973. [36] E. Villard, F. Tintó Garcia-Moreno, N. Peter, G. Clément, Geometric visual illusions in microgravity during parabolic flight, Neuroreport 16 (2005) 1395–1398. [37] S. Yamamoto, M. Yamamoto, Effects of the gravitational vertical on the visual perception of reversible figures, Neurosci. Res. 55 (2006) 218–221.
Contents lists available at SciVerse ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Perceptual reversal of bi-stable figures in microgravity and hypergravity during parabolic flight Gilles Clément ∗ , Michael Demel International Space University, Parc d’Innovation, 1 rue Jean-Dominique Cassini, Illkirch-Graffenstaden F-67400, France
a r t i c l e
i n f o
Article history: Received 17 October 2011 Received in revised form 2 December 2011 Accepted 2 December 2011 Keywords: Gravity Visual illusions Human visual perception Ambiguous figures Perspective
a b s t r a c t This experiment investigated whether the perception of depth-reversible figures is altered when the observer is in microgravity or hypergravity. A set of five bi-stable ambiguous figures was presented to ten participants in 1 g, 0 g, and 1.8 g during parabolic flight. The figures included static images such as the Necker cube; kinetic depth displays such as a moving plaid and a sphere cluster of moving dots appearing to rotate in one of two directions; and a silhouette photograph. For each stimulus figure, subjects reported which of the two possible perceptual configurations they saw first and then continuously indicated when perceptual reversals occurred for durations ranging from 20 to 30 s. The same first percept was reported in 1 g, 0 g, and 1.8 g. The time delay for the first reversal between the two possible image interpretations was longer and the number of reversals was fewer in 0 g as compared to 1 g for four of the five figures. The opposite effects were seen when going from 0 g to 1.8 g. These findings confirm that, consistent with a multisensory approach to three-dimensional form perception, gravity has a clear effect on the interpretation of depth-based stimuli and this gravity-based component interferes with visual perception stability. © 2011 Elsevier Ireland Ltd. All rights reserved.
Mach [27] pointed out that the perception of solid objects could switch back and forth between two (or more) possible interpretations. A well-known example of a reversible figure is the Necker cube (Fig. 1, inset, left). This simple line drawing can represent a cube in either of two possible orientations, facing upward and to the left or downward and to the right. Other examples of bi-stable figures are shown in Fig. 1. These images are planar images that are alternately identifiable as one of two disparate three-dimensional percepts. Researchers have used these bi-stable figures to study the dynamics of perceptual alternations by asking observers to continually report which of the two possible interpretations are perceived at every moment. In these experiments, observers typically watch a static or moving figure for several seconds on a laptop monitor and report their percept continually by pressing down one of keyboard keys. Results from these studies have been used to distinguish elementary sensory features of the physical image from the top-down processes involved in constructing either of its visuo-spatial interpretations [18,26]. Under prolonged observation of a bi-stable figure, even naive subjects experience reversals spontaneously. On the other hand, if perspective or other cues are added the figure reverses less frequently and there comes a point when it is no longer ambiguous [32]. For example, when holding a Necker cube constructed
∗ Corresponding author. Tel.: +33 388 65 5444; fax: +33 388 65 5447. E-mail address: [email protected] (G. Clément). 0304-3940/$ – see front matter © 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2011.12.006
from wire, the reversals happen less often and for shorter periods than for just seeing a line drawing of a Necker cube [16]. Therefore, haptic information stabilizes to some extent visual perception of the image. There is ample evidence that visual perception is influenced by multimodal integration of retinal, tactile, and gravitational inputs [17]. In the case of a visually bi-stable ambiguous figure, it is therefore possible that gravitational information interferes with perception, as do haptic cues. The perception of upright is a result of integrating the orientation of the ambient visual world, the direction of gravity, and an internal representation of the body’s longitudinal axis [29]. Previous studies have shown that ambiguous figures reversed less frequently [11,35,37], geometrical visual illusions were less frequent [7,23,34], and the face-inversion effect even disappeared [25] during large body tilt, i.e., when retinal and gravitational frames of reference deviate substantially. In microgravity, the perception of upright becomes relatively more body-defined [8,15] and the influence of vision in determining upright is significantly reduced [12], which also reduces visual illusions and character recognition [13,20,24,36]. Therefore, it was hypothesized that the absence of gravitational information in microgravity would reduce the frequency of reversals of visually ambiguous figures. Ten subjects (4 women, 6 men, aged 24–52, mean 30) participated in this experiment performed during two campaigns of parabolic flights onboard the Airbus A300 Zero-G. This aircraft is capable of flying parabolic trajectories during which the entire cabin is in microgravity (less than 10−2 g) for about 22 s. This period
144
G. Clément, M. Demel / Neuroscience Letters 507 (2012) 143–146
Fig. 1. Inset: all the ambiguous figures used in these studies were drawn on a planar surface. They were bi-stable, seeming to appear in either of two orientations or to move in either of two directions. The five figures included (from left to right): (1) the classical perspective-reversible Necker cube drawn with white lines over a black background; (2) a shaded cube that may become the corner of a room; (3) a plaid moving upwards at 1◦ /s [17] [see demonstration at http://www.cns.nyu.edu/home/hupe/arvo01demo/demo plaids.html]; (4) an ambiguous sphere made of random blue dots over a black background rotating about a horizontal axis at approximately 30◦ /s [2] [see demonstration at http://www.uq.edu.au/nuq/jack/rivalry.html]; (5) a photograph of the Space Shuttle (credit NASA) where the bay doors may look convex or concave. Top: mean + standard error of time to first reversal for each figure averaged across 3 trials and 10 subjects in normal gravity prior to the flight (1 g), in microgravity (0 g), hypergravity (1.8 g), and in normal gravity under the influence of the motion sickness medication (1 g med) during parabolic flight. *p < 0.05. Bottom: mean + standard error of the number of reversals per minute for the same conditions.
of microgravity is preceded and followed by periods of hypergravity (1.8 g) for about 20 s each. Subjects had given their informed consent to participate in this study in accordance with the guidelines of the local ethics committee, and had passed the equivalent of an Air Force Class III medical examination. All subjects reported that they had normal or corrected-to-normal vision with no known visual deficits. Only two subjects had previous parabolic flight experience. All the subjects took prophylactic medication (a combination of promethazine and dexedrine) before boarding the plane, and only one of them showed symptoms of motion sickness during the flight. Data were collected with this experiment in normal gravity prior to taking the medication (1 g), and on board the airplane in both microgravity (0 g), hypergravity following the 0 g phase (1.8 g) and normal gravity under the influence of the medication (1 g med). The latter condition was obtained when the aircraft was flying straight and level between two series of parabolas or during the flight back to the base. It was used to assess if the medication could be held responsible for the differences observed between the two gravity conditions. In microgravity, the observers were tested in the dark while free-floating to eliminate orientation-related cues. The freefloating condition is illustrated in a previous paper [8]. Each of the five figures shown in Fig. 1 was presented to the subjects in a headmounted display (Z800 3DVisor, eMagin Corporation, Bellevue, WA) using a macro-enhanced Microsoft PowerPoint presentation
running on a laptop computer. For the ambiguous static depth figures (the two cubes and the photograph), we asked the subjects to identify which configuration they saw first, and then to indicate when they saw the second configuration by pressing down either of the two buttons of a mini trackball finger mouse. For the ambiguous kinetic depth structures, subjects reported whether the plaid appeared to be moving upwards or interweaving horizontally, and whether the sphere made of blue dots appeared to be rolling toward them or away from them. The figures were presented on a black background and all external visual references were blocked by a fabric cover placed over the head-mounted display. The figures subtended a viewing angle of 30◦ at a perceived distance of approximately 50 cm. The sample rate of the trackball was 40 Hz and the refresh rate of the visual display was 60 Hz. Participants were instructed to focus on the center of the images and to limit scanning eye movements. The order of figures was randomized across subjects and parabolas. Each ambiguous figure was presented during 3 parabolas, i.e., a total of 15 parabolas per subject. This corresponded to a presentation duration totaling 61.3 ± 4.2 s and 40.4 ± 2.9 s per figure in 0 g and 1.8 g, respectively, across all subjects. In the 1 g and 1 g med conditions, the figures were also presented during 3 trials, but for 30 s each, i.e., a total presentation duration of 90 s per figure. The subjects were familiarized with the ambiguous figures used in this study prior to the first baseline data collection. The subjects were first allowed to practice with the figures and the experimental protocol during three trials in normal gravity on the morning of the flight, and the data was then collected in this order: 1 g, 0 g, 1.8 g, and 1 g med. The macro controlled the flow of the figures presented, recorded the subject inputs from the finger mouse buttons, and saved all of the relevant data into an external text file. The macro also made note of the times that the figures were first displayed, when the subject indicated the occurrence of the first percept, and the times for all subsequent perceptual reversals. For each figure, the measurements included: (a) the time from stimulus onset to the first percept report; (b) the first percept; (c) the time from the first percept report to the first reversal; (d) and the number of reversals. The number of reversals per minute was calculated for the period from the first percept report to the end of the trial. There was no significant difference between the measurements obtained in 1 g and 1 g med, thus ruling out an effect of the motion sickness medication on these results. The subjects reported the same first percept in 1 g and 1 g med in 93.2% of the responses. The same first percept was also reported in 1 g and 0 g in 89.5% of the responses, and in 1.8 g in 87.2% of the responses. That is, compared to 1 g (10 subjects × 5 figures × 3 trials = 150 responses), the first percept was different in 0 g in 16 responses, and in 1.8 g in 19 responses. The probability to view each percept was close to 50% and did not change significantly across gravity conditions. A within subjects (repeated measures) ANOVA was conducted to compare the effect of gravity on the time to first reversal and the number or reversals in 0 g, 1 g, and 1.8 g. When responses were pooled across figures, there was a significant effect of gravity on the time to first reversal [F(2,18) = 7.12, p < 0.001] and number of reversals [F(2,18) = 5.54, p < 0.001]. Paired samples t-tests were used to make post hoc comparisons between gravity conditions. The time to first reversal was longer in 0 g than in 1 g for all subjects (Fig. 1, top). This difference was statistically significant for the Necker’s cube [t(9) = −1.89, p = 0.04], the shaded cube [t(9) = −3.62, p = 0.002], the moving plaid [t(9) = −2.77, p = 0.01], and the silhouette photograph [t(9) = −2.09, p = 0.03]. The time to first reversal was significantly shorter in 1.8 g than in 1 g for the moving plaid only [t(9) = 2.05, p = 0.03]. However, the time to first reversal was significantly shorter in 1.8 g than in 0 g for all the figures: Necker’s
G. Clément, M. Demel / Neuroscience Letters 507 (2012) 143–146
Fig. 2. Time to first reversal as a function of number of reversals (mean of 3 trials, 10 subjects × 5 figures) in 1 g, 0 g, and 1.8 g. Both dependent variables seem to be linearly related. R2 = 0.430.
cube [t(9) = 1.93, p = 0.04], shaded cube [t(9) = 2.17, p = 0.03], moving plaid [t(9) = 5.24, p < 0.001], rolling sphere [t(9) = 2.27, p = 0.02], silhouette photograph [t(9) = 3.35, p = 0.004]. The frequency of changes in appearance of the figures was smaller in 0 g than in 1 g (Fig. 1, bottom) for 9 subjects out of 10. This decrease in the number of reversals was significant for the Necker’s cube [t(9) = 1.87, p = 0.04], the shaded cube [t(9) = 3.04, p = 0.006], the moving plaid [t(9) = 2.26, p = 0.02], and the silhouette photograph [t(9) = 2.02, p = 0.03]. Eight subjects had more reversals per minute in 1.8 g than in 1 g, but this increase was only significant for the moving plaid [t(9) = −2.62, p = 0.01]. Finally, the number of reversals was significantly larger (p < 0.006) in 1.8 g than in 0 g for all the five figures. When responses were pooled together between subjects and within subjects, the variances of the subjects’ judgments were stable in 1 g and 1.8 g for both the time to first reversal (14.1 and 11.8, respectively) and the number of reversals (21.6 and 28.9, respectively). In 0 g, the variance was larger than in 1 g for the time to first reversal (26.5) and smaller than in 0 g for the number of reversal (13.8). The number of reversals per minute measured in this study is consistent with earlier studies using long periods of exploration [1,32]. The steady-state probability of seeing each view, i.e., the cumulative time spent reporting each percept over a given observation time, was rather balanced for these stimuli (approximately 50%). In agreement with previous studies [18], there was an inverse correlation between the time to see the first reversal and the number of reversals. This correlation was present in all gravity conditions (Fig. 2). These results indicate that for four figures (the Necker’s cube, the shaded cube, the moving plaids, and the silhouette photograph), the percept reversal occurred less frequently in 0 g than in 1 g. How might the absence of gravitational information affect observers’ visual judgments of these ambiguous figures? Threedimensional ambiguous figures are ideal experimental model to investigate multisensory processes. The results of recent studies on visual illusions suggest that the visual system is relatively unreliable for 3D perception, and that observers give greater weight to the more reliable source, whether it is the visual, haptic, or gravitational input, so as to optimize overall reliability [14,28]. One prevalent theory of visual perception is the notion that one of the two views of the ambiguous figure “wins”, promoting models that embed a mechanism to choose between the two possible interpretations of the stimulus [32]. Transferring this approach to the role of gravity in visual perception would suggest an architecture where the neural representations of the visual and body-oriented interpretations of the stimulus continually compete for dominance. There is ample evidence that the frame of reference is more body-oriented
145
in microgravity [6,8,10,15,19,20]. In 0 g, the direction of upright would become more strongly driven by and aligned with the body vector, resulting in a proportionally weaker influence of the retinal reference [13]. Perception instability generated by visual illusions would then be reduced, leading to less reversal of ambiguous figures in 0 g. This explanation is supported by experiments showing that the orientation of the visual background is significantly less influential in determining the perceptual upright during the microgravity phase of parabolic flight than it is under normal gravity [13,20,23,24,36]. Similar results were obtained during the prolonged microgravity of orbital flight. For example, astronauts manifest a strong bias toward the body (idiotropic) vector when ask to point to the perceived “ceiling” of the spacecraft with their eyes closed [15]. The astronauts’ ability to recognize complex figures and interpret shapes based on shading (e.g., “the light comes from above”) is altered during orbital flight [see review in 6], which also suggests reduced visual effects in microgravity. Another interpretation is that the decrease in perceptual reversal seen in 0 g is related to a decrease in the geometric (linear) perspective and shading cues for depth when the gravitational input is absent. Previous research using visual illusions suggests that the reliance on geometric perspective and shading cues decreases when subjects are tilted relative to gravity [7,37] and in microgravity during parabolic [10,36] or orbital [6,31] flight. The interpretation for this decrease is that perspective and shading are well defined when the head is upright relative to gravity, but more ambiguous when the head is tilted or when gravity is virtually absent. In 0 g the gravitational reference is absent and the direction of gaze and perceived straight-ahead are also altered due to changes in the otolith signals [4]. Therefore, geometric perspective and shading would become less reliable as depth cues, and depth-reversible figures such as those in the present study would be less ambiguous. It is interesting to note that vestibular patients suffering from otolith vertigo also exhibit less geometric perspective effects when presented with visual illusions [9]. During hypergravity, a gravitational reference is present but its scale is altered relative to 1 g, possibly creating more perceptual instability and reversals [30]. In the case of the ambiguous rotating sphere, the depth effect is obtained from the motion of random dots. Because no size or perspective cues differentiate the front from rear surfaces, the direction of rotation is ambiguous. This figure would be less sensitive to gravity conditions that the other figures, as indicated by our results, because it does not include depth cues such as geometric lines or shading. One could argue that the difference in the number of reversals between 1 g and 0 g is due to an indirect effect on attention. It has been suggested that subjects may adopt different attention sets to deal with the task in different postures [33]. For example, it was found that subjects solve anagrams significantly faster when supine than when standing, and this difference was attributed to less locus coeruleus-noradrenergic system activity when lying down [22]. However, the absence of any reliable increase in our observers’ response variance during flight, and the opposite effects seen in 0 g and 1.8 g, suggests that the changes seen in our study were not related to the stress or unusual nature of parabolic flight itself. Also, even though subjects were instructed to fixate the center of the images, eye movements could have occurred during the experiment. The transition from hypergravity to microgravity during parabolic flight is known to generate nystagmus [5], changes in torsional eye position [3] and vertical misalignment of the eyes [21]. These induced eye movements could degrade the retinal image and indirectly cause a decrease in the visual effects.
146
G. Clément, M. Demel / Neuroscience Letters 507 (2012) 143–146
In conclusion, the absence of gravitational information increased the time for the first reversal and cut down the number of reversals in four of the five ambiguous figures. These perceptual changes are consistent with an increase in the use of the body as a reference frame when gravity is changed. These effects were seen for depth-reversible ambiguous figures. Such figures were chosen because previous results indicated that illusions based on perspective and shading were altered in normal subjects placed in microgravity [36] and in patients with otolithic vertigo on Earth [9]. Other complex visual stimuli that were not depth-based did not induce such changes [9,36]. Whether the effect seen in the present experiment also applies for other ambiguous figures that are more two-dimensional, such as the Rubin’s vase, will have to be the subject of future studies. The shortcomings described above for this pilot study should be eliminated in a planned experiment designed to investigate the effects of prolonged microgravity on board the International Space Station. Acknowledgements This research was supported by a CNES grant and CNRS. We thank the people at CEV, CNES, ESA, MEDES, and NOVESPACE, and in particular P. Denise, F. Gai, T. Gharib, C. Mora, V. Pletser, and P. Rosier. We are also grateful to our test subjects for participating in this experiment. References [1] J. Beer, Correlations among ambiguous figures, curiosity, and spatial ability, Percept. Mot. Skills 71 (1990) 1188–1190. [2] Y. Bonneh, A. Cooperman, D. Sagi, Motion induced blindness in normal observers, Nature 411 (2001) 798–801. [3] A.H. Clarke, Listing’s plane and the otolith-mediated gravity vector, Prog. Brain Res. 171 (2008) 291–294. [4] G. Clément, Alteration of eye movements and motion perception in microgravity, Brain Res. Rev. 28 (1998) 161–172. [5] G. Clément, C. André-Deshays, C.E. Lathan, Effects of gravitoinertial force variations on vertical gaze direction during oculomotor reflexes and visual fixation, Aviat. Space Environ. Med. 60 (1989) 1194–1198. [6] G. Clément, M.F. Reschke, Neuroscience in Space, Springer, New York, 2008. [7] G. Clément, J. Eckardt, Influence of the gravitational vertical on geometric visual illusions, Acta Astronaut. 56 (2005) 911–917. [8] G. Clément, T.N. Arnesen, M.H. Olsen, B. Sylvestre, Perception of longitudinal body axis in microgravity during parabolic flight, Neurosci. Lett. 413 (2007) 150–153. [9] G. Clément, M.J. Frayss, O. Deguine, Mental representation of space in vestibular patients with otolithic or rotatory vertigo, Neuroreport 20 (2009) 457–461. [10] G. Clément, A. Bukley, Mach’s square-or-diamond phenomenon in microgravity during parabolic flight, Neurosci. Lett. 447 (2008) 179–182.
[11] M.C. Corballis, N.J. Zbrodoff, L.I. Shetzer, P.B. Butler, Decisions about identity and orientation of rotated letters and digits, Mem. Cognit. 6 (1978) 98–107. [12] R.T. Dyde, M.R. Jenkin, L.R. Harris, The subjective visual vertical and the perceptual upright, Exp. Brain Res. 173 (2006) 612–622. [13] R.T. Dyde, M.R. Jenkin, H.L. Jenkin, J.E. Zacher, L.R. Harris, The effect of altered gravity states on the perception of orientation, Exp. Brain Res. 194 (2009) 647–660. [14] M.O. Ernst, M.S. Banks, Humans integrate visual and haptic information in a statistically optimal fashion, Nature 415 (2002) 429–432. [15] S. Glasauer, H. Mittelstaedt, Perception of spatial orientation in microgravity, Brain Res. Rev. 28 (1998) 185–193. [16] Y.-X. Ho, S. Serwe, J. Trommershäuser, L.T. Maloney, M.S. Landy, The role of visuo-haptic experience in visually perceived depth, J. Neurophysiol. 101 (2009) 2789–2801. [17] I.P. Howard, Human Visual Orientation, Wiley, Chichester, 1982. [18] J.-M. Hupé, N. Rubin, The dynamics of bi-stable alternation in ambiguous motion displays: a fresh look at plaids, Vision Res. 43 (2003) 531–548. [19] H.L. Jenkin, M. Jenkin, R.T. Dyde, L.R. Harris, Shape-from shading depends on visual, gravitational, and body-orientation cues, Perception 33 (2004) 1453–1461. [20] H.L. Jenkin, R.T. Dyde, J.E. Zacher, D.C. Zikovitz, M.R. Jenkin, R.S. Allison, I.P. Howard, L.R. Harris, Relative role of visual and non-visual cues determining the direction of ‘up’: experiments in parabolic flight, Acta Astronaut. 56 (2005) 1025–1032. [21] F. Karmali, S. Ramat, M. Shelhamer, Vertical skew due to changes in gravitoinertial force: a possible consequence of otolith asymmetry, J. Vestib. Res. 16 (2006) 117–125. [22] D.M. Lipnicki, D.G. Byrne, Thinking on your back: solving anagrams faster when supine than when standing, Cognit. Brain Res. 24 (2005) 719–722. [23] M.I. Lipshits, J. McIntyre, Gravity affects the preferred vertical and horizontal in visual perception of orientation, Neuroreport 10 (1999) 1085–1089. [24] M.I. Lipshits, A. Bengoetxea, G. Cheron, J. McIntyre, Two reference frames for visual perception in two gravity conditions, Perception 34 (2005) 545–555. [25] J.S. Lobmaier, F.W. Mast, The Thatcher illusion: rotating the viewer instead of the picture, Perception 36 (2007) 537–546. [26] G.M. Long, T.C. Toppino, Enduring interest in perceptual ambiguity: alternating views of reversible figures, Psychol. Bull. 130 (2004) 748–768. [27] E. Mach, The Analysis of Sensations, Dover, New York, 1959 (Original work published in 1897). [28] P.J. McAdie, M.J. Steinbach, Visually induced tilt affects form perception, Perception 10 (1981) 525–530. [29] H. Mittelstaedt, A new solution to the problem of the subjective vertical, Naturwissenschaften 70 (1983) 272–281. [30] I. Negishi, H. Kaneko, H. Mizushina, K. Ogata, Effects of tilt of the visual stimuli on the perception of gravitational vertical under normal- and hyper-gravity conditions, Opt. Rev. 16 (2009) 290–295. [31] C.M. Oman, Human visual orientation in weightlessness, in: L. Harris, W. Jenkin (Eds.), Levels of Perception, Springer Verlag, New York, 2003, pp. 375–398. [32] S.E. Palmer, Vision Science: Photons to Phenomenology, MIT Press, Cambridge, MA, 1999. [33] A. Peru, J.S. Morgant, When supine is better than upright: evidence from postural effects in extinction patients, Brain Res. 1110 (2006) 175–181. [34] W. Prinzmetal, D.M. Beck, The tilt-constancy theory of visual illusions, J. Exp. Psychol. Hum. Percept. Perform. 27 (2001) 206–217. [35] I. Rock, Orientation and Form, Academic Press, New York, 1973. [36] E. Villard, F. Tintó Garcia-Moreno, N. Peter, G. Clément, Geometric visual illusions in microgravity during parabolic flight, Neuroreport 16 (2005) 1395–1398. [37] S. Yamamoto, M. Yamamoto, Effects of the gravitational vertical on the visual perception of reversible figures, Neurosci. Res. 55 (2006) 218–221.