When two dissimilar stimuli are presented to the eyes, perception alternates between multiple interpretations, a phenomenon dubbed binocular rivalry. Numerous recent imaging studies have attempted to unveil neural substrates underlying multistable perception. However, these studies had a conceptual constraint: access to observers' perceptual state relied on their introspection and active report. Here, we investigated to what extent neural correlates of binocular rivalry in healthy humans are confounded by this subjective measure and by action. We used the optokinetic nystagmus and pupil size to objectively and continuously map perceptual alternations for binocular-rivalry stimuli. Combining these two measures with fMRI allowed us to assess the neural correlates of binocular rivalry time locked to the perceptual alternations in the absence of active report. When observers were asked to actively report their percept, our objective measures matched the report. In this active condition, objective measures and subjective reporting revealed that occipital, parietal, and frontal areas underlie the processing of binocular rivalry, replicating earlier findings. Furthermore, objective measures provided additional statistical power due to their continuous nature. Importantly, when observers passively experienced rivalry without reporting perceptual alternations, a different picture emerged: differential neural activity in frontal areas was absent, whereas activation in occipital and parietal regions persisted. Our results question the popular view of a driving role of frontal areas in the initiation of perceptual alternations during binocular rivalry. Instead, we conclude that frontal areas are associated with active report and introspection rather than with rivalry per se.

Humans move their eyes while looking at scenes and pictures. Eye movements correlate with shifts in attention and are thought to be a consequence of optimal resource allocation for high-level tasks such as visual recognition. Models of attention, such as “saliency maps,” are often built on the assumption that “early” features (color, contrast, orientation, motion, and so forth) drive attention directly. We explore an alternative hypothesis: Observers attend to “interesting” objects. To test this hypothesis, we measure the eye position of human observers while they inspect photographs of common natural scenes. Our observers perform different tasks: artistic evaluation, analysis of content, and search. Immediately after each presentation, our observers are asked to name objects they saw. Weighted with recall frequency, these objects predict fixations in individual images better than early saliency, irrespective of task. Also, saliency combined with object positions predicts which objects are frequently named. This suggests that early saliency has only an indirect effect on attention, acting through recognized objects. Consequently, rather than treating attention as mere preprocessing step for object recognition, models of both need to be integrated.

During sustained viewing of an ambiguous stimulus, an individual's perceptual experience will generally switch between the different possible alternatives rather than stay fixed on one interpretation (perceptual rivalry). Here, we measured pupil diameter while subjects viewed different ambiguous visual and auditory stimuli. For all stimuli tested, pupil diameter increased just before the reported perceptual switch and the relative amount of dilation before this switch was a significant predictor of the subsequent duration of perceptual stability. These results could not be explained by blink or eye-movement effects, the motor response or stimulus driven changes in retinal input. Because pupil dilation reflects levels of norepinephrine (NE) released from the locus coeruleus (LC), we interpret these results as suggestive that the LC–NE complex may play the same role in perceptual selection as in behavioral decision making.

In natural vision both stimulus features and task-demands affect an observer's attention. However, the relationship between sensory-driven (“bottom-up”) and task-dependent (“top-down”) factors remains controversial: Can task-demands counteract strong sensory signals fully, quickly, and irrespective of bottom-up features? To measure attention under naturalistic conditions, we recorded eye-movements in human observers, while they viewed photographs of outdoor scenes. In the first experiment, smooth modulations of contrast biased the stimuli's sensory-driven saliency towards one side. In free-viewing, observers' eye-positions were immediately biased toward the high-contrast, i.e., high-saliency, side. However, this sensory-driven bias disappeared entirely when observers searched for a bull's-eye target embedded with equal probability to either side of the stimulus. When the target always occurred in the low-contrast side, observers' eye-positions were immediately biased towards this low-saliency side, i.e., the sensory-driven bias reversed. Hence, task-demands do not only override sensory-driven saliency but also actively countermand it. In a second experiment, a 5-Hz flicker replaced the contrast gradient. Whereas the bias was less persistent in free viewing, the overriding and reversal took longer to deploy. Hence, insufficient sensory-driven saliency cannot account for the bias reversal. In a third experiment, subjects searched for a spot of locally increased contrast (“oddity”) instead of the bull's-eye (“template”). In contrast to the other conditions, a slight sensory-driven free-viewing bias prevails in this condition. In a fourth experiment, we demonstrate that at known locations template targets are detected faster than oddity targets, suggesting that the former induce a stronger top-down drive when used as search targets. Taken together, task-demands can override sensory-driven saliency in complex visual stimuli almost immediately, and the extent of overriding depends on the search target and the overridden feature, but not on the latter's free-viewing saliency.