Neural bases of binocular rivalry

During binocular rivalry, conflicting monocular images compete for access to consciousness in a stochastic, dynamical fashion. Recent human neuroimaging and psychophysical studies suggest that rivalry entails competitive interactions at multiple neural sites, including sites that retain eye-selective information. Rivalry greatly suppresses activity in the ventral pathway and attenuates visual adaptation to form and motion; nonetheless, some information about the suppressed stimulus reaches higher brain areas. Although rivalry depends on low-level inhibitory interactions, high-level excitatory influences promoting perceptual grouping and selective attention can extend the local dominance of a stimulus over space and time. Inhibitory and excitatory circuits considered within a hybrid model might account for the paradoxical properties of binocular rivalry and provide insights into the neural bases of visual awareness itself.

Introduction

Something fascinating happens when conflicting monocular images are presented to each of the two eyes. Rather than forming a stable composite, the two images rival for exclusive dominance, with perceptual awareness spontaneously alternating every few seconds between one image and the other (Figure 1). Called binocular rivalry, this remarkable phenomenon provides an effective means for investigating neural circuits involved in visual competition, perceptual grouping and selective attention. Moreover, because the observer's conscious state is continually in flux while the visual stimulus remains invariant, binocular rivalry might ultimately shed light on the dynamical properties of visual awareness and its underlying neural bases 1, 2, 3, 4.

Vigorous debate about binocular rivalry has centered on three main issues: the potential sites of neural competition, the types of visual representations that compete at these sites, and the integrative mechanisms that coordinate competitive interactions between large-scale neuronal populations. According to one view, binocular rivalry arises from low-level interocular competition between monocular neurons in the primary visual cortex (V1) 5, 6 or in the lateral geniculate nucleus (LGN) of the thalamus [7]. According to another view, binocular rivalry transpires later in visual processing and reflects competition between incompatible patterns rather than competition between the eyes 8, 9. In recent years, a coherent picture incorporating elements of both views has emerged [1], built around the idea that rivalry involves neural competition at multiple levels of the visual pathway 10, 11.

Here, we review recent human neuroimaging and psychophysical studies that reveal the paradoxical nature of rivalry. Results from some of these studies indicate that binocular rivalry involves neural competition at remarkably early sites of the visual pathway, and that the instigation of rivalry depends on local, low-level competition. Other results, however, indicate that information about a suppressed stimulus reaches higher brain areas, and that perceptual grouping and top-down influences of selective attention can promote the dominance of a stimulus during rivalry. To make sense of these seemingly paradoxical results, we first describe a plausible hybrid framework to account for both low- and high-level properties of binocular rivalry.

It should be emphasized that this review focuses on recent evidence obtained from human observers. Reviews of neurophysiological [12] and earlier psychophysical studies [5] of rivalry can be found elsewhere, as can discussions of pattern rivalry 1, 9, 13, 14. In this review, we favor the notion that binocular rivalry is unlikely to result from a single process but, rather, from an assembly of perceptual processes underlying instigation of rivalry, promotion of dominance and implementation of suppression.