Is the frontal lobe involved in conscious perception?

Abstract

When studying the neural mechanisms underlying conscious perception we should be careful not to misinterpret evidence, and delineate these mechanisms from activity which could reflect the prerequisites or consequences of conscious experiences (Aru et al., 2012; de Graaf et al., 2012). However, at the same time, we need to be careful not to exclude any relevant evidence about the phenomenon. Recently, novel paradigms have attempted to dissociate activity related to conscious perception from activity reflecting its prerequisites and consequences. In particular, one of these studies focused on resolving the role of frontal lobe in conscious perception (Frassle et al., 2014). Through a clever experimental design that contrasted blood-oxygen-level-dependent (BOLD) activity elicited during binocular rivalry with and without behavioral reports, Frassle et al. (2014) suggested that frontal lobe, or a large part of it, may not be necessary for conscious perception per se. Rather frontal areas are involved in processing the consequences of conscious perception like monitoring the perceptual content in order to elicit the appropriate report of the subjective experience. In particular, Frässle et al. showed that behavioral reports of conscious experiences resulted in increased and more widespread activity of the frontal lobe compared to a condition without behavioral reports, where spontaneous transitions in the content of consciousness were estimated through the objective measures like optokinetic nystagmus (OKN) and pupil dilation. The authors of this study concluded that ldquo;frontal areas are associated with active report and introspection rather than with rivalry per serdquo;. Therefore activity in prefrontal regions could be considered as a consequence rather than a direct neural correlate of conscious experience. However, a previous study (Panagiotaropoulos et al., 2012) that measured directly neural activity in the macaque lateral prefrontal cortex (LPFC) using extracellular electrophysiological recordings could help to narrow down the role of frontal activity in conscious perception and exclude the contribution of cognitive or motor consequences in prefrontal neural activity during visual awareness. Specifically, the activity of feature selective neurons in the macaque LFPC was shown to be modulated in accordance with the content of subjective perception, without any confound from motor action (i.e. behavioral reports). Using binocular flash suppression (BFS), a paradigm of robust, externally induced perceptual suppression and without any requirement of behavioral reports, neurons in the LPFC were found to increase or decrease their discharge activity when their preferred stimulus was perceptually dominant or suppressed, respectively. Therefore, since neuronal discharges in the LPFC follow the content of conscious perception even without any motor action, the conclusion of Frassle et al. (2014) about the role of frontal lobe activity in rivalrous perception needs to be refined. Prefrontal activity can indeed reflect the content of conscious perception under conditions of rivalrous stimulation and this activity should not be necessarily considered as the result of a motor action or self-monitoring required for active report. Moreover, the results obtained by Frassle et al. (2014) do not anatomically preclude the entire prefrontal cortex from having a role in conscious perception. Specifically, the BOLD activity related to rivalry in their experiment is still present in the right inferior frontal lobe and right superior frontal lobe (Zaretskaya and Narinyan, 2014). Further, activation of dorso-lateral prefrontal cortex in conscious perception of Mooney images was also reported in a study that explicitly controlled for activity elicited by motor action (Imamoglu et al., 2012). It is true that the BFS-related prefrontal activity cannot conclude on a mechanistic, causal involvement of prefrontal activity in driving spontaneous transitions in conscious perception. This is because BFS is a paradigm of externally induced perceptual suppression and is therefore not directly informative about the role of recorded activity in spontaneous transitions. Therefore, the possibility remains open that the kind of prefrontal activity observed in the macaque LPFC during BFS is not a causal factor for conscious perception but rather reflects some other aspects of monitoring that are not directly related to motor action. For example, prefrontal activity could just reflect a read-out from other areas like the inferior temporal cortex (Sheinberg and Logothetis, 1997) that also reliably reflects the content of conscious perception. However, if this is the case, it triggers the question why this activity that closely follows the content of subjective perception is observed in the LPFC even in the absence of any behavioral report. Overall, it motivates further investigation to understand whether prefrontal activity has a mechanistic ro