The neural bases of multistable perception

Multistable perception is the spontaneous alternation between two or more perceptual states that occurs when sensory information is ambiguous. Multistable phenomena permit dissociation of neural activity related to conscious perception from that related to sensory stimulation, and therefore have been used extensively to study the neural correlates of consciousness. Here, we review recent work on the neural mechanisms underlying multistable perception and how such work has contributed to understanding the neural correlates of consciousness. Particular emphasis is put on the role of high-level brain mechanisms that are involved in actively selecting and interpreting sensory information, and their interactions with lower-level processes that are more directly concerned with the processing of sensory stimulus properties.

Introduction

Multistable perception occurs when sensory information is ambiguous and consistent with two or more mutually exclusive interpretations. When no additional cues are available that allow perceptual synthesis to converge on one unique interpretation, perception alternates spontaneously every few seconds between two (‘bistable’) or more (‘multistable’) interpretations of the same sensory input. Well-known examples include the Necker cube, Rubin's face-vase illusion, bistable apparent motion and binocular rivalry (Figure 1). Interest in studying multistable perception in human observers has increased with the advent of modern non-invasive brain imaging techniques such as functional magnetic resonance imaging (fMRI) because multistable stimuli allow neural activity related to conscious perception to be distinguished from that related to physical stimulus properties. Moreover, multistable perception can help us understand the constructive neural processes that generate a unified and coherent subjective experience of the world even though the information available is often fragmentary, conflicting or even ambiguous.

A decade ago, a thought-provoking article on the neural basis of multistable perception was published in this journal [1]. Inspired by the first fMRI studies of bistable perception, (see Refs 1, 2 for reviews) and contrasting with the traditional view that spontaneous perceptual reversals are a consequence of antagonistic activity within the visual system (e.g. Refs 3, 4), the authors proposed that ‘reorganizations of activity throughout the visual cortex, concurrent with perceptual reversals, are initiated by higher, largely non-sensory brain centers’ [1]. Since then, hybrid theoretical proposals have emerged, on the basis of behavioural evidence, which conceptualise multistable perception as arising from interactions between low-level (sensory) and high-level (cognitive) processes [5]. In the last decade, the neural mechanisms of binocular rivalry, a special case of perceptual multistability, have been under intense investigation. Similar hybrid models of binocular rivalry that involve different visual processing levels have been proposed 6, 7, 8. Finally, converging evidence from several recent lines of empirical neuroscience suggests a causal role of frontal and parietal cortex in generating perceptual switches in multistability, as previously proposed [1].

Here, we review recent findings addressing the neural mechanisms of different types of multistable perception, including but not limited to binocular rivalry. We incorporate these findings into an integrated view of how different neural processing levels, ranging from early sensory brain structures to non-sensory associative cortices, might interact to give rise to multistable perception, and how these processes are related to conscious perception in general. As most work has studied visual multistability, we focus on the visual system. However, there are striking behavioural similarities with comparable phenomena in other sensory domains (e.g. auditory 9, 10 and tactile multistability [11]). The same or similar mechanisms involved in visual multistable perception might thus also have a role in other sensory domains (Box 1). Our review is structured according to the traditional hierarchical view of visual information processing, starting with subcortical and low-level cortical visual processing. After discussing intermediate processing stages at the level of extrastriate visual areas, we will focus on recent insights into higher-order mechanisms involving frontal and parietal cortices, and their interactions with lower-level sensory brain regions.