Review
Multistable phenomena: changing views in perception

https://doi.org/10.1016/S1364-6613(99)01332-7Get rights and content

Abstract

Traditional explanations of multistable visual phenomena (e.g. ambiguous figures, perceptual rivalry) suggest that the basis for spontaneous reversals in perception lies in antagonistic connectivity within the visual system. In this review, we suggest an alternative, albeit speculative, explanation for visual multistability – that spontaneous alternations reflect responses to active, programmed events initiated by brain areas that integrate sensory and non-sensory information to coordinate a diversity of behaviors. Much evidence suggests that perceptual reversals are themselves more closely related to the expression of a behavior than to passive sensory responses: (1) they are initiated spontaneously, often voluntarily, and are influenced by subjective variables such as attention and mood; (2) the alternation process is greatly facilitated with practice and compromised by lesions in non-visual cortical areas; (3) the alternation process has temporal dynamics similar to those of spontaneously initiated behaviors; (4) functional imaging reveals that brain areas associated with a variety of cognitive behaviors are specifically activated when vision becomes unstable. In this scheme, reorganizations of activity throughout the visual cortex, concurrent with perceptual reversals, are initiated by higher, largely non-sensory brain centers. Such direct intervention in the processing of the sensory input by brain structures associated with planning and motor programming might serve an important role in perceptual organization, particularly in aspects related to selective attention.

Section snippets

Activity in the brain during multistable vision

A number of recent neurophysiological and imaging experiments in monkeys and humans, respectively, have shed light on cortical activity during multistable perception. Most of these studies have used binocular rivalry, a psychophysical paradigm in which perception can be destabilized simply by showing sufficiently dissimilar images to the two eyes (see Fig. 1D; for reviews see 10, 12). During rivalry, perception is wholly dominated by one pattern while that presented to the other eye is rendered

Temporal dynamics

A strong line of evidence in support of the present hypothesis is the very similar temporal dynamics for perceptual reversals and a variety of spontaneously generated visuomotor behaviors. For example, periods of dominance and suppression in ambiguous vision are characterized by sequential stochastic independence8, 22, 23, 24. This empirical observation has presented difficulties for reciprocal-inhibition models of bistable perception in which fatigue initiates perceptual reversals, for such

Why might perception alternate?

The view of multistable perception presented here invites the question: Why does the brain continually reorganize an ambiguous sensory input? Although an observer can have significant voluntary control over dominance and suppression (as discussed above), it is clear that this influence is not the driving force for alternation, which continues in the absence of any particular intent on the part of the observer and can never be stopped entirely. By and large, any events leading to perceptual

Conclusions

The hypothesis presented in this article can be restated as follows: the complex analysis of sensory information ultimately leading to visual perception is continually steered and modified by sequences of planned interventions emerging from areas lying outside the visual system. Such intervention is most apparent when perception is unstable, as in ambiguous vision, but is likely to be a general property of active perception that is closely related to selective attention. If the brain's planning

Outstanding questions

  • What is the temporal relationship between neural responses in different cortical areas during subjective transitions? Would activity changes in the frontoparietal areas precede those in the extrastriate visual cortex as suggested by the present hypothesis?

  • What is the role of intra- and inter-areal synchrony between populations of neurons in multistable perception? Might competing neural stimulus representations alternate in their degree of coherence during the perceptual changes?

  • What is the

Acknowledgements

We would like to thank Drs Francis Crick and Christof Koch for useful comments on the manuscript, and Dr Jochen Braun for finding it interesting.

References (101)

  • R.I. Reynolds

    The role of object-hypotheses in the organization of fragmented figures

    Perception

    (1985)
  • R.H.S. Carpenter

    A neural mechanism that randomises behavior

    J. Conscious. Stud.

    (1999)
  • S.R. Ellis et al.

    Eye movements during the viewing of Necker cubes

    Perception

    (1978)
  • R.W. Ditchburn et al.

    Binocular vision with two stabilized retinal images

    Q. J. Exp. Psychol.

    (1960)
  • R.M. Pritchard et al.

    Visual perception approached by the method of stabilized images

    Can. J. Psychol.

    (1960)
  • K.H. Britten et al.

    A relationship between behavioral choice and the visual responses of neurons in macaque MT

    Visual Neurosci.

    (1996)
  • S. Celebrini et al.

    Neuronal and psychophysical sensitivity to motion signals in extrastriate area MST of the macaque monkey

    J. Neurosci.

    (1994)
  • L.A. Necker

    Observations on some remarkable optical phaenomena seen in Switzerland; and on an optical phaenomenon which occurs on viewing a figure of a crystal or geometical solid

    London and Edinburgh Philosophical Magazine and Journal of Science

    (1832)
  • V.S. Ramachandran et al.

    Perceptual organization in multistable apparent motion

    Perception

    (1985)
  • E. Rubin

    Figure and ground, in Readings in Perception

    (1958)
  • DuTour, M. (1760) Discussion d'une question d'optique (discussion on a question of optics) Academie des Sciences:...
  • I. Rock

    Perception

    (1995)
  • M.M. Taylor et al.

    Stochastic processes in reversing figure perception

    Percept. Psychophys.

    (1974)
  • S.R. Lehky

    An astable multivibrator model of binocular rivalry

    Perception

    (1988)
  • R.R. Blake

    A neural theory of binocular rivalry

    Psychol. Rev.

    (1989)
  • W. Koehler et al.

    Figural aftereffects; an investigation of visual processes

    Proc. Am. Philos. Soc.

    (1944)
  • N.K. Logothetis

    Single units and conscious vision

    Proc. R. Soc. London Ser. B

    (1998)
  • E.D. Lumer

    A neural model of binocular integration and rivalry based on the coordination of action-potential timing in primary visual cortex

    Cereb. Cortex

    (1998)
  • P. Fries et al.

    Synchronization of oscillatory reponses in visual cortex correlates with perception in interocular rivalry

    Proc. Natl. Acad. Sci. U. S. A.

    (1997)
  • C.M. Gray et al.

    Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex

    Proc. Natl. Acad. Sci. U. S. A.

    (1989)
  • D.A. Leopold et al.

    Microsaccades differentially modulate neural activity in the striate and extrastriate visual cortex

    Exp. Brain Res.

    (1998)
  • E.D. Lumer et al.

    Neural correlates of perceptual rivalry in the human brain

    Science

    (1998)
  • F. Tong et al.

    Binocular rivalry and visual awareness in human extrastriate cortex

    Neuron

    (1998)
  • A. Kleinschmidt et al.

    Human brain activity during spontaneously reversing perception of ambiguous figures

    Proc. R. Soc. London Ser. B

    (1998)
  • A. Borsellino et al.

    Reversal time distribution in the perception of visual ambiguous stimuli

    Kybernetik

    (1972)
  • R. Fox et al.

    Stochastic properties of binocular rivalry alternations

    Percept. Psychophys

    (1967)
  • P. Walker

    Stochastic properties of binocular rivalry alternations

    Percept. Psychophys.

    (1975)
  • R. Fox et al.

    Binocular rivalry and reciprocal inhibition

    Percept. Psychophys.

    (1969)
  • C.M. Harris et al.

    The distribution of fixation durations in infants and naive adults

    Vis. Res.

    (1988)
  • P. Suppes

    A procedural theory of eye movements in doing arithmetic

    J. Math. Psychol.

    (1983)
  • M. Heisenberg

    Initiale aktivitaet und willkuerverhalten bei tieren

    Naturwissenschaften

    (1983)
  • W.J. Levelt

    On Binocular Rivalry

    (1965)
  • A. DeMarco et al.

    Stochastic models and fluctuation in reversal time of ambiguous figures

    Perception

    (1977)
  • S.R. Lehky

    Binocular rivalry is not chaotic

    Proc. R. Soc. London Ser. B

    (1995)
  • J. Myerson et al.

    Binocular rivalry in macaque monkeys and humans: a comparative study in perception

    Behav. Analysis Lett.

    (1981)
  • D.A. Leopold et al.

    Activity changes in early visual cortex reflect monkeys' percepts during binocular rivalry

    Nature

    (1996)
  • C.M. Harris et al.

    The distribution of fixation durations in infants and naive adults

    Vis. Res.

    (1988)
  • P. Suppes

    A procedural theory of eye movements in doing arithmetic

    J. Math. Psychol.

    (1983)
  • J.E. Richards et al.

    Extended visual fixation in young infants: look distributions, heart rate changes, and attention

    Child Dev.

    (1997)
  • M. Wertheimer

    Experimentelle Studien ueber das Sehen von Bewegung

    Zeitschrift für Psychologie mit Zeitschrift fur angewandte Psychologie

    (1912)
  • Cited by (0)

    View full text