Stable perception of visually ambiguous patterns
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1 Stle perception of visully miguous ptterns Dvid A. Leopold, Melnie Wilke, Alexnder Mier nd Nikos K. Logothetis Mx Plnck Institut für iologische Kyernetik, Spemnnstrβe 38, Tüingen, Germny Correspondence should e ddressed to D.A.L. (dvid.leopold@tueingen.mpg.de) Pulished online: 6 My 2002, DOI: /nn851 During the viewing of certin ptterns, widely known s miguous or puzzle figures, perception lpses into sequence of spontneous lterntions, switching every few seconds etween two or more visul interprettions of the stimulus. Although their nture nd origin remin topics of dete, these stochstic switches re generlly thought to e the utomtic nd inevitle consequence of viewing pttern without unique solution. We report here tht in humns such perceptul lterntions cn e slowed, nd even rought to stndstill, if the visul stimulus is periodiclly removed from view. We lso show, with visul illusion, tht this stilizing effect hinges on perceptul disppernce rther thn on ctul removl of the stimulus. These findings indicte tht uninterrupted sujective perception of n miguous pttern is required for the initition of the rin-stte chnges underlying multistle vision. Visul perception involves coordintion etween sensory smpling of the world nd ctive interprettion of the sensory dt. Humn perception of ojects nd scenes is normlly stle nd roust, ut it flters when one is presented with ptterns tht re inherently miguous or contrdictory. Under such conditions, vision lpses into chin of continully lternting percepts, wherey vile visul interprettion domintes for few seconds nd is then replced y rivl interprettion. This multistle vision, or multistility, is thought to result from destiliztion of fundmentl visul mechnisms, nd hs offered vlule insights into how sensory ptterns re ctively orgnized nd interpreted in the rin 1,2. Despite gret del of recent reserch nd interest in multistle perception, however, its neurophysiologicl underpinnings remin poorly understood. Physiologicl studies hve suggested tht dismigution of miguous ptterns drws on ctivity within the visul cortex 3 10, ut how this ctivity ultimtely contriutes to perceptul solution is not yet known. Even less cler is the nture of the perceptul lterntion process itself. Trditionl views hold tht it is n utomtic consequence of incomptile, ntgonistic stimulus representtions in the sensory visul cortex 11,12. Recent evidence chllenges this notion, suggesting insted tht perceptul lterntions re initited outside the primrily sensory res 13,14 (for review, see ref. 15). In the present study, we report tht the spontneous chnges of multistle perception cn e gretly slowed, nd even rought to stndstill, when the inducing ptterns re viewed intermittently rther thn continuously. Specificlly, when we introduced lnk periods of severl seconds into n extended period of continuous viewing, we consistently slowed the rte of lterntion y two orders of mgnitude. Individul periods of perceptul dominnce often exceeded 10 minutes. The stiliztion effect ws present for vriety of istle ptterns, nd could not e ttriuted to permnent perceptul is. In ddition, we used visul illusion clled motion-induced lindness 16 to show tht the stiliztion effect depended on intermittent sujective dis- ppernce of the pttern, not on intermittent disppernce of the sensory representtion itself. RESULTS The initil im of this study ws to exmine the influence of recent visul history on the perceptul orgniztion of n miguous pttern. To ddress this, we repetedly presented rotting sphere (RS) stimulus (Fig. 1), whose three-dimensionl structure is miguous 17, in trin of 3-s presenttions seprted y 5-s periods during which the screen ws lnk. Whenever the stimulus ws present, sujects reported whether it ppered to e rotting upwrd or downwrd round the horizontl xis. For intermittent viewing, perception tended to ecome stuck in prticulr configurtion, often for severl minutes t time (Fig. 2). As compred with the continuous viewing condition, phses of perceptul dominnce were mrkedly lengthened, nd some sujects sw no reversls in rottion for the durtion of the 10-min session. Stiliztion for the RS ws present in 22 of 23 sujects tested in different experiments throughout the study, with no consistent difference etween horizontl nd verticl rottion. This effect ws not the result of permnent perceptul is or reset mechnism following ech new stimulus presenttion, s there ws often sequentil stiliztion of oth possile percepts (sujects BL, AM, MW, HH & AH, Fig. 2). In generl, sujects with shorter men dominnce phses during continuous presenttion exhiited less stiliztion during the intermittent condition. As ech presenttion time ws fixed t 3 s for ll sujects, we ttriute this trend to n incresed proility for fst-switchers to experience perceptul reversl during single stimulus presenttion. Stiliztion incresed when the stimulus ws sent for longer periods of time (Fig. 3), indicting tht perceptul configurtion, once estlished, could survive even reltively long epochs in which the stimulus ws gone. There ws no pprent decline in the survivl of percept for lnk times s long s 40 s nture neuroscience volume 5 no 6 june
2 Fig. 1. Stimuli used in the study. () Rotting sphere (RS), which turned out either the verticl or horizontl xis; () qurtet dots (QD); (c) Necker cue (NC); (d) inoculr rivlry (BR); nd (e) rotting str (RSt) mid rndomly moving dots used to provoke the motion-induced lindness illusion. (f) Stimuli were presented either continuously or intermittently, with vrile on-times nd lnk-screen durtions. c e d f (Fig. 3). Notly, when lterntions did occur, the proility of configurtion persisting until the susequent presenttion ws highly dependent on how long it ws seen efore the stimulus ws removed. Only when perceptul configurtion ws seen consistently (without reversls) for 2 s or longer efore stimulus disppernce ws there high proility tht it would persist to the next stimulus presenttion (Fig. 3c). Given the relile persistence of perceptul configurtion cross lnk periods, could the incresed stiliztion with longer lnk times e ccounted for simply y the decresed overll time of exposure to the stimulus? This cnnot e the cse, ecuse the ctul reduction in totl lterntions fr exceeded tht expected from stimulus presenttion time lone (Fig. 3d). This lso ws true for the link condition, where sujects mimicked the disppernce nd reppernce of the stimulus y periodiclly shutting nd opening their eyes when they herd ppropritely timed tones. For linking, even higher stiliztion ws oserved. Finlly, lterntion rtes were mesured for 1-minute sliding window shifted y 1-s increments, pooled for ll sujects nd compiled into histogrm for ech condition (with lnks, Fig. 3e; with links, Fig. 3f). Note tht for oth conditions, very low reversl rtes dominted the inter- mittent/links presenttion, wheres mix of higher rtes ws seen during continuous presenttion. To exmine whether this stiliztion effect holds for multistle stimuli other thn the RS, we repeted the experiment with three other common, ut inherently different, istle ptterns (Fig. 1 d): the Necker cue 18 (NC, miguous sttic depth), qurtet dots 19 (QD, miguous motion correspondence) nd inoculr rivlry 20 (BR, introculr conflict). For ech stimulus, we first djusted the time the stimulus ws present (on-time) to e mrkedly shorter thn the men dominnce phse during continuous viewing. Sujects gin viewed ech pttern either continuously or intermittently, reporting which of the two perceptul configurtions they sw whenever the stimulus ws present. Results for these three dditionl stimuli were similr to those otined with the RS (Fig. 4). Finlly, we sked whether physicl removl of the stimulus ws necessry to chieve stiliztion, or whether its mere sujective disppernce would give similr results. To test this, we exploited the recently descried visul illusion of motion-induced lindness (MIB) 16 to provoke frequent illusory fding of n miguous rotting str (RSt) pttern (Fig. 1e). The RSt ws similr in mny respects to the RS: during continuous viewing, it produced perceptul reversls in the direction of rottion. Insted of compring continuous with intermittent presenttion s efore, we overlid the RSt with field of rndomly moving lck dots, which cused the str to periodiclly fde from perception (severl times per minute; Fig. 5). As with the RS, sujects were required to trck the rottionl direction of the moving str whenever it ws visile. These epochs of illusory fding hd the sme stilizing effect on the perceived direction of rottion s did the physicl lnking descried ove for the RS. This result indictes tht the sujective disppernce of the pttern, rther thn the ctul sensory representtion, ultimtely underlies this stiliztion phenomenon. Fig. 2. Effects of intermittent presenttion on perception of RS rotting round the horizontl xis (11 sujects). Alterntion in the perceived motion of the front surfce is shown here s fluctution etween the upper (gry) nd lower (lck) levels, corresponding to upwrd nd downwrd rottion, respectively. Ech row compres the condition when the stimulus ws continuously present (left) to tht when it ws only intermittently present (right). Intermittent viewing consisted of 3-s onperiods interleved with 5-s lnk periods, illustrted t the ottom. For ech suject, ordered from top to ottom ccording to their inherent switch rte during continuous viewing, the totl numer of perceptul reversls during ech stimulus condition is shown t the right. 606 nture neuroscience volume 5 no 6 june 2002
3 Fig. 3. Fctors contriuting to stiliztion of the RS. () Men phse durtion (± s.e.m.) for intermittent presenttion s function of lnk durtion (six sujects, ontime 5 s). () Proility tht given perceptul stte survived vrile-length lnking period (sme dt s in ). Arrows indicte the lnk durtions for the experiment shown in Fig. 2. (c) Proility tht spontneous perceptul reversl persists to the next stimulus presenttion, s function of post-reversl intervl (time etween the perceptul chnge nd stimulus lnking). The numer of instnces contriuting to ech in is shown ove the corresponding rs (sme dt s in ). (d) Reversl rte for intermittent condition, normlized to the reversl rte under continuous viewing, shown for periodic removl of the stimulus (, five sujects, ontime 2 s) nd timed eye closure (, six sujects, eyes open 2 s). The dotted line represents the rte decrese expected if the diminished overll presenttion time were the only fctor. (e) Distriution of reversl rtes for continuous versus intermittent (on-time 2 s, lnk 5 s) viewing of RS (five sujects), clculted using sliding window (see Results). Proility density plotted for continuous (light gry) nd intermittent (drk gry) conditions. (f) Sme s (e), ut with eye linking insted of stimulus lnking (six sujects, pooled). DISCUSSION The inevitility of perceptul lterntions during miguous vision hs often een tken s evidence for stimulus-induced ut utonomously mintined rection of the sensory processing pprtus to multistle ptterns, prompting models whose sis ws limited to the visul system 11,12,21. More recently, the switching mechnism hs een postulted to lie outside of exclusively visul res. Severl lines of evidence hve suggested tht frontoprietl res ssocited with selective visul ttention re centrlly involved in the initition of perceptul lterntions 13,15. Other evidence hs suggested tht lterntion in hemispheric dominnce, controlled y free-running oscilltor circuit in the rinstem, might underlie visul istility 14,22. Although the present results cnnot pinpoint specific structures responsile for perceptul reversl, they do offer new insights into the process itself. First, the stiliztion effect descried here is evidence ginst the notion tht perceptul c d e f reversl is governed y n utonomous oscilltor tht opertes independently of the visul stimulus 14. If tht were the cse, simple stimulus mnipultion proly would not ring perceptul lterntion to stndstill. Second, our results indicte tht continuous, prolonged viewing of n miguous stimulus is requirement for the initition of the fluctutions underlying multistle perception. Moreover, the MIB illusion experiment showed tht the continuous presence of the sensory stimulus does not utomticlly led to perceptul instility s predicted y models of ltertion sed on reciprocl sensory connectivity nd dption. Insted, the periodic sujective fding of the miguous stimulus hd pproximtely the sme stilizing effect s its physicl removl. Perceptul switching thus ppers to e governed y n ctive mechnism tht continuously monitors the conscious perceptul representtion of the stimulus itself. Perceptul chnges my involve the reorgniztion of neurl networks relted to sensory processing, ut they do not seem to e triggered y competition in such networks, nor do they reflect the workings of seprte, endogenous istle circuit whose impct is merely proed y n miguous pttern. The fct tht the gretest stiliztion ws otined when sujects mde the stimulus dispper y purposefully closing their eyes dds further support to the notion tht ctive, endogenous mechnisms ultimtely govern the occurrence of perceptul reversl. Finlly, miguous perception hs often een descried s memoryless ecuse of the lck of c d Fig. 4. Stiliztion of different istle ptterns. ( c) Effects of continuous (left) versus intermittent (right) presenttion on the perception of NC, QD nd BR stimuli (two sujects shown for ech stimulus). (d) Totl numer of reversls for continuous versus intermittent viewing (mens ± s.e.m. shown). Blnk durtions were 5 s in ll cses, nd on-times were RS, 3 s (eight sujects); NC, 1 s (seven sujects); QD, 5 s (eight sujects); BR, 1.2 s (eight sujects). nture neuroscience volume 5 no 6 june
4 sttisticl correltion etween successive reversl intervls 23,24. Nonetheless, we found tht once the miguous stimulus ws removed, recent perceptul history ws the dominnt fctor in determining how tht stimulus ws interpreted on susequent viewings. Thus, with ech presenttion, perceptul orgniztion seems to e guided y some sort of implicit perceptul memory tht does not decline over severl seconds. This memory, which my e importnt during norml vision, ws olished y the continuous presenttion of n miguous stimulus. Wheres numer of previous studies hve demonstrted tht externl stimuli cn ct to deterministiclly is the perception of n miguous pttern 25 28, the stiliztion oserved here depended entirely on the persistence of n internlly generted perceptul stte. Further experiments my revel whether the sme frontoprietl corticl res tht hve een implicted in perceptul lterntion during istle pttern viewing 13,29 lso contriute to perceptul stiliztion during intermittent viewing. METHODS Sujects. Thirty-nine sujects (19 femle, 20 mle) etween the ges of 15 nd 36 yers (medin 25) prticipted in the study. The experiments were done in ccordnce with guidelines of the locl uthorities (Regierungspresidium), nd ll sujects gve informed written consent. Ech suject hd norml or corrected-to-norml vision, nd most hd prior experience s psychophysicl suject. Aprt from two uthors (sujects MW nd AM), ech suject ws completely nïve to the hypotheses nd gols of the experiment, nd ws pid for prticiption. An interview fter ech session reveled tht most sujects (>80%) were unwre tht the perceptul chnges they experienced were entirely sujective. Fig. 5. Effect of sujective disppernce on perceptul reversl of the RSt. () Comprison of continuous visiility (left) versus intermittent visiility (right). Intermittent visiility ws chieved y motion-induced lindness (see Methods). In oth cses, the physicl stimulus ws continuously present. Dt is shown for two sujects (CW nd VM). The pttern of sujective ppernce nd disppernce is shown t the ottom for ech suject, with gry periods representing times when the stimulus ws visile. () Men reversl rte (± s.e.m.) with nd without epochs of perceptul disppernce (five sujects). Visul stimuli. Stimuli were generted on computer (Intergrph Zx10 PC, Huntsville, Alm; Intense3D Grphics, Sunnyvle, Cliforni) nd presented in color on two 21-inch monitors, presented seprtely to ech eye y mirror stereoscope. The sptil resolution of ech monitor ws 1, pixels, with n eye screen distnce of 123 cm nd refresh rte of 90 Hz. Unless otherwise mentioned, ll stimuli were drwn on the center of gry screen (5.50 cd/m 2 ) with no fixtion spot. Four white, rdilly protruding rs ( ), strting 2.8 from the center of the screen nd extending outwrd, were used to ensure proper inoculr vergence for ll conditions. The RS, QD nd NC stimuli were lue (CIE x = 0.250, y = 0.208, 7.30 cd/m 2 ) nd were presented monoculrly to the left eye while the right eye viewed lnk screen. Sujects verified tht under this condition the stimuli did not sujectively fde (indicting tht there ws no inoculr rivlry). The RS stimulus consisted of n orthogrphic projection of 450 lue dots (0.044 in dimeter) uniformly covering virtul sphere with dimeter of 1.72 in dimeter. The sphere rotted rigidly with period of 4.0 s, giving the ppernce of three-dimensionl structure. Becuse no size or perspective cues differentited the front from rer surfces, the direction of rottion ws miguous. The NC, contining miguous informtion out sttic depth, ws composed of lue lines (0.12 in thickness) nd covered n re of The QD consisted of solid lue circles (0.36 in dimeter) ppering in pirs on opposite corners of n imginry squre ( ) centered on the middle of the screen. At ech moment, only two circles were displyed. The stimulus lternted etween the two possile configurtions every 311 ms, generting the perception of pprent motion etween either verticlly or horizontlly corresponding points. The BR stimulus consisted of two dichopticlly presented Gor ptches (rdius, 2.25 ; sptil frequency, 2.7 cycles/ ), with the left eye viewing 45 leftwrd-tilted greenish ptch nd the right eye viewing 45 rightwrd-tilted pinkish ptch. The RSt ws similr to the RS in tht it ws miguous in its three-dimensionl structure from motion. It ws 1.15 in extent, composed of dots (0.044 in dimeter) tht were red (CIE x = 0.547, y = 0.319, 7.61 cd/m 2 ) nd rotted once every 1.3 s. In the MIB condition 16, the RSt ws presented mid lrge field of smll lck dots moving in rndom directions (dot dimeter, 0.072; density, 9.9 dots/ ; speed, 5.4 /s; lifetime, 330 ± 30 ms). While the RSt ws presented monoculrly to the left eye, the dots were shown inoculrly in correspondence. Pilot experiments showed tht inoculr presenttion of the dots nerly douled the disppernce time of the str, n effect tht my e fcilitted, in prt, y inoculr rivlry. The eccentricity of presenttion rnged from nd ws determined initilly for ech suject sed on the position providing the highest frequency of stimulus disppernce. Experimentl tsk. Prticipnts rested their chins on pdded r nd were instructed to inspect the stimulus without specil regrd to fixtion, except for the MIB experiment, where they were instructed to mintin fixtion on smll cross. For ech istle stimulus, uttons were ssigned eforehnd to ech of the two potentil percepts. Sujects were required to press the utton corresponding to the perceived configurtion of ech pttern when it ppered, nd to relese the utton when it disppered. In the cse of BR, where percepts could e mixed, they were instructed to respond ccording to the dominnt pttern, even if its dominnce ws incomplete. All relevnt events, including stimulus presenttions nd suject responses, were recorded on computer for nlysis. Acknowledgments The uthors would like to thnk M. Sereno for suggestions nd help with the structure from motion stimuli, A. Gil for discussion regrding the inoculr rivlry experiment nd J. Werner for technicl ssistnce. This work ws supported y the Mx Plnck Society. Competing interests sttement The uthors declre tht they hve no competing finncil interests. RECEIVED 7 FEBRUARY; ACCEPTED 9 APRIL Rock, I. Perception (Scientific Americn Lirry, New York, 1984). 2. Gregory, R. Eye nd Brin: The Psychology of Seeing 5th edn. (Princeton Univ. Press, Princeton, NJ, 1997). 3. Logothetis, N. K. & Schll, J. D. Neuronl correltes of sujective visul perception. Science 245, (1989). 4. Leopold, D. A. & Logothetis, N. K. Activity chnges in erly visul cortex 608 nture neuroscience volume 5 no 6 june 2002
5 reflect monkeys percepts during inoculr rivlry. Nture 379, (1996). 5. Sheinerg, D. L. & Logothetis, N. K. The role of temporl corticl res in perceptul orgniztion. Proc. Ntl. Acd. Sci. USA 94, (1997). 6. Brdley, D. C., Chng, G. C. & Andersen, R. A. Encoding of threedimensionl structure-from-motion y primte re MT neurons. Nture 392, (1998). 7. Dodd, J. V., Krug, K., Cumming, B. G. & Prker, A. J. Perceptully istle three-dimensionl figures evoke high choice proilities in corticl re MT. J. Neurosci. 21, (2001). 8. Polonsky, A., Blke, R., Brun, J. & Heeger, D. J. Neuronl ctivity in humn primry visul cortex correltes with perception during inoculr rivlry. Nt. Neurosci. 3, (2000). 9. Tononi, G., Srinivsn, R., Russell, D. P. & Edelmn, G. M. Investigting neurl correltes of conscious perception y frequency-tgged neuromgnetic responses. Proc. Ntl. Acd. Sci. USA 95, (1998). 10. Brown, R. J. & Norci, A. M. A method for investigting inoculr rivlry in rel-time with the stedy-stte VEP. Vision Res. 37, (1997). 11. Attneve, F. Multistility in perception. Sci. Am. 225, (1971). 12. Mueller, T. J. A physiologicl model of inoculr rivlry. Vis. Neurosci. 4, (1990). 13. Lumer, E. D., Friston, K. J. & Rees, G. Neurl correltes of perceptul rivlry in the humn rin. Science 280, (1998). 14. Pettigrew, J. D. Serching for the switch: neurl ses for perceptul rivlry lterntions. Brin Mind 2, (2001). 15. Leopold, D. A. & Logothetis, N. K. Multistle phenomen: chnging views in perception. Trends Cogn. Sci. 3, (1999). 16. Bonneh, Y. S., Coopermn, A. & Sgi, D. Motion-induced lindness in norml oservers. Nture 411, (2001). 17. Wllch, H. & O Connell, D. N. The kinetic depth effect. J. Exp. Psychol. 45, (1953). 18. Necker, L. A. Oservtions on some remrkle opticl phenomen seen in Switzerlnd; nd on n opticl phenomenon which occurs on viewing figure of crystl or geometricl solid. Lond. Edinurgh Phil. Mgzine J. Sci. 1, (1832). 19. von Schiller, P. Strooskopische Alterntivversuche. Psychol. Forsch. 17, (1933). 20. Dutour, E. F. Discussion d une question d optique [Discussion on question of optics]. l Acdemie des Sciences. Memoires de Mthemtique et de physique presentes pr Divers Svnts 3, (1760). 21. Lehky, S. R. An stle multivirtor model of inoculr rivlry. Perception 17, (1988). 22. Miller, S. M. et l. Interhemispheric switching medites perceptul rivlry. Curr. Biol. 10, (2000). 23. Borsellino, A., De Mrco, A., Allzett, A., Rinesi, S. & Brtolini, B. Reversl time distriution in the perception of visully miguous stimuli. Kyernetik 10, (1972). 24. Fox, R. & Herrmnn, J. Stochstic properties of inoculr rivlry lterntions. Percept. Psychophys. 2, (1967). 25. Crlson, V. R. Stition in reversile perspective figure. J. Exp. Psychol. 45, (1953). 26. Wolfe, J. M. Reversing oculr dominnce nd suppression in single flsh. Vision Res. 24, (1984). 27. Nwrot, M. & Blke, R. Neurl integrtion of informtion specifying structure from stereopsis nd motion. Science 244, (1989). 28. Blke, R., Westendorf, D. & Fox, R. Temporl perturtions of inoculr rivlry. Percept. Psychophys. 48, (1990). 29. Lumer, E. D. & Rees, G. Covrition of ctivity in visul nd prefrontl cortex ssocited with sujective visul perception. Proc. Ntl. Acd. Sci. USA 96, (1999). nture neuroscience volume 5 no 6 june
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