Conscious and unconscious processes in vision and homeostasis

Binocular rivalry--the alternations in perception that occur when different images are presented to the two eyes--has been the subject of intensive investigation for more than 160 years. The psychophysical properties of binocular rivalry have been well described, but newer imaging and electrophysiological techniques have not resolved the issue of where in the brain rivalry occurs. The most recent evidence supports a view of rivalry as a series of processes, each of which is implemented by neural mechanisms at different levels of the visual hierarchy. Although unanswered questions remain, this view of rivalry might allow us to resolve some of the controversies and apparent contradictions that have emerged from its study.

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.

Figures that can be seen in more than one way are invaluable tools for the study of the neural basis of visual awareness, because such stimuli permit the dissociation of the neural responses that underlie what we perceive at any given time from those forming the sensory representation of a visual pattern. To study the former type of responses, monkeys were subjected to binocular rivalry, and the response of neurons in a number of different visual areas was studied while the animals reported their alternating percepts by pulling levers. Perception-related modulations of neural activity were found to occur to different extents in different cortical visual areas. The cells that were affected by suppression were almost exclusively binocular, and their proportion was found to increase in the higher processing stages of the visual system. The strongest correlations between neural activity and perception were observed in the visual areas of the temporal lobe. A strikingly large number of neurons in the early visual areas remained active during the perceptual suppression of the stimulus, a finding suggesting that conscious visual perception might be mediated by only a subset of the cells exhibiting stimulus selective responses. These physiological findings, together with a number of recent psychophysical studies, offer a new explanation of the phenomenon of binocular rivalry. Indeed, rivalry has long been considered to be closely linked with binocular fusion and stereopsis, and the sequences of dominance and suppression have been viewed as the result of competition between the two monocular channels. The physiological data presented here are incompatible with this interpretation. Rather than reflecting interocular competition, the rivalry is most probably between the two different central neural representations generated by the dichoptically presented stimuli. The mechanisms of rivalry are probably the same as, or very similar to, those underlying multistable perception in general, and further physiological studies might reveal much about the neural mechanisms of our perceptual organization.