Introspection, attention or awareness? The role of the frontal lobe in binocular rivalry

Bistable stimuli are one of the most popular approaches to studying the neural mechanism of conscious visual perception. Such stimuli contain conflicting information, which the visual system cannot integrate into a unified percept. This causes the perceptual state of the observer to change every few seconds between the two interpretations while the physical stimulus remains the same. Binocular rivalry is an example of such perceptual phenomena with ambiguity achieved by presenting one image to one eye and a different image to the other eye. Perceptual changes during binocular rivalry are particularly vivid, and closely resemble a physical image exchange. The study of neural mechanisms of bistable perception and binocular rivalry revealed the involvement of multiple areas across different levels of the visual hierarchy (Sterzer et al., 2009). While the activated stimulus-selective temporal lobe areas depend on the stimulus category that produces ambiguity, activity in the parietal and frontal lobe seems to be common to all stimuli and increases specifically during transition periods between the two percepts. The activation of the frontal lobe areas is particularly intriguing. It suggests that the mechanisms of conscious vision might involve typical higher-level frontal lobe functions such as attention, motivation and decision-making. Previous studies of bistable perception relied on participants’ explicit reports of their conscious state (most commonly button presses). Under certain conditions, however, perceptual states can be inferred objectively, without self-report. An example recent study by Frässle et al. (2014) took advantage of two ocular reflexes, optokinetic nystagmus and the pupillary light reflex, and designed binocular rivalry stimuli that selectively drive these reflexes. Simple eye tracking measures provided the authors with objective information about their subjects’ perceptual changes over time. The authors used fMRI to monitor brain activity when observers experienced either genuine binocular rivalry or a “replay” (a control condition which simulates rivalry-like perceptual alterations by physically switching the stimulus presented to both eyes). These conditions were performed while subjects either actively reported their perceptual state or just passively viewed the stimuli. Such experimental design allowed Frässle et al. to make an important observation. Comparison of rivalry with replay in the passive viewing condition showed less activation in the frontal cortex compared to active report condition. The most prominent decrease was observed in the left superior and bilateral middle frontal gyri. According to the authors, decrease of frontal activity implies that frontal lobe areas play a role in introspection and motor response generation, but not in perceptual changes per se. Frontal lobe takes about one third of the cortical volume, and is comprised of multiple architectonically and functionally distinct areas (Stuss, 2011). Given this diversity it is important to ask, which frontal lobe regions are typically active during perceptual transitions in bistable perception, and how they relate to the regions reported by Frässle et al. as showing reduced activation during passive viewing. Previous studies comparing perceptual changes in rivalry with replay frequently reported activation in the inferior frontal cortex (IFC), middle frontal gyrus (MFG) and superior frontal gyrus (SFG) (Lumer et al., 1998; Zaretskaya et al., 2010; Knapen et al., 2011; Frässle et al., 2014), located mostly in the right hemisphere (Figure 1, green). Frässle et al. on the other hand, report decreased activity around the bilateral MFG and bilateral SFG only (Figure 3 and Table 2 in Frässle et al., 2014, Figure 1, red). Moreover, their right superior frontal activation is relatively far from the locations reported previously. Thus, the two activation maps in the frontal lobe overlap only partially, namely around the right MFG, and perhaps also the left SFG. Activity of other rivalry-related frontal nodes, in particular the right superior frontal and the right inferior frontal ones, did not decrease significantly. The latter areas may therefore continue to play an important role in perceptual changes even without active motor report. Besides, passive viewing involves not only less self-monitoring, but also less attention. Attention, in turn, is linked to increased activity in frontal, but also