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Crucial Role of the Prefrontal Cortex in Conscious Perception
Chapter 6
Crucial Role of the Prefrontal Cortex in Conscious Perception Seth Lew1 and Hakwan Lau1,2 1 2
Psychology Department, University of California Los Angeles, Los Angeles, CA, United States, Brain Research Institute, University of California Los Angeles, Los Angeles, CA, United States
EARLY NEUROIMAGING EVIDENCE OF PREFRONTAL CORTEX’S INVOLVEMENT IN CONSCIOUS PERCEPTION Functional magnetic resonance imaging (fMRI) studies since the late 1990s presented findings that areas in the prefrontal cortex (PFC) are associated with conscious perception (Dehaene & Naccache, 2001; Dehaene, Changeux, Naccache, Sackur, & Sergent, 2006; Lumer & Rees, 1999; Rees, Kreiman, & Koch, 2002). For example, one of the earlier studies by Lumer and Rees (1999) identified activity in the extrastriate cortex that correlated with perceptual switching in binocular rivalry and PFC activity that covaried with the activation of the extrastriate cortex. A review (Rees et al., 2002) pooled results from five different neuroimaging studies that identified neural correlates of consciousness and found an overlap of activity in the dorsolateral prefrontal cortex (DLPFC). Dehaene et al. (2006) further reasoned that the involvement of PFC is selective to conscious versus un- or preconscious perception. Specifically, they posited that conscious awareness requires both bottom-up stimulus processing and top-down attention in areas of higher cognition, such as the PFC (Dehaene & Naccache, 2001), a view that we will discuss at the end of this chapter. In this chapter, we evaluate the status of the claim that PFC is critically involved in conscious perception.
THE “NO-REPORT” ARGUMENT AGAINST PFC’S ROLE IN CONSCIOUSNESS One argument against PFC’s association with consciousness is that the activation of PFC may reflect processes used for self-report instead of conscious perception. Researchers usually make use of participants’ self-report Executive Functions in Health and Disease. DOI: http://dx.doi.org/10.1016/B978-0-12-803676-1.00006-4 © 2017 Elsevier Inc. All rights reserved.
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to assess their conscious experience of the presented stimuli. These reports are crucial to studies searching for differences in neural activity that track changes in perceptual states while the stimulus is being held constant (Ress, Backus, & Heeger, 2000; Super, Spekreijse, & Lamme, 2001; Tong, Meng, & Blake, 2006). The idea is that if a stimulus remains constant but a person’s perceptual experience of it has changed, then any difference in the person’s neural activities must be correlated with the difference in their conscious experience. In that way, the parts of the brain that show different levels of activity when a person has different conscious experiences of the same stimulus can be understood as neural correlates of consciousness. However, some authors have recently argued that the self-report itself can be a confounding factor (Tsuchiya, Wilke, Fr¨assle, & Lamme, 2015). The need to self-report requires employment of neural areas correlated with paying attention to the upcoming stimulus, self-monitoring after sensing the stimulus, accessing the sensory data, and generating and delivering a report, which are processes conceptually distinct from the phenomenon of conscious perception itself. Therefore, the brain areas reported to be neural correlates of consciousness could have wrongly included activity due to demands of self-report rather than conscious perception per se. To remove confounds associated with self-report, “no-report” paradigms have been developed and used as alternatives to those that require self-report (Tse, Martinez-Conde, Schlegel, & Macknik, 2005). As the name suggests, no-report paradigms remove the reliance on self-report from the participants to determine their perceptual state. Instead, researchers use neural recordings or physiological changes of the participant to infer their perceptual experience. For example, optokinetic nystagmus (i.e., eye movement to follow a moving object while the head remains stationary) and pupil size were used to accurately verify perceptual switching in binocular rivalry in the absence of self-report (Fr¨assle, Sommer, Jansen, Naber, & Einh¨auser, 2014). Neural correlates found in no-report paradigms are expected to be more refined than those from report-dependent paradigms because the regions of the brain that activates solely for aspects of self-report would be truncated from the results. Interestingly, findings from no-report paradigms have revealed consistent activity in the striate and extrastriate cortex but none in the PFC or the parietal cortex that correlated with consciousness (Brascamp, Blake, & Knapen, 2015; Fr¨assle et al., 2014; Kouider, Dehaene, Jobert, & Le Bihan, 2007; Tse et al., 2005). For instance, Tse et al. (2005) took advantage of the same perceptual content of monoptic and dichoptic visual masking to narrow down the areas that might be correlated to consciousness. In monoptic visual masking, the visual stimulus and mask were presented to both eyes, whereas in dichoptic masking, the visual stimulus was presented to one eye and the mask to the other eye. The masked pattern occupied most of the screen but was unattended to by the participant due to their focus on a fixation task. Although there was no need for the participants to report on the masked pattern, it is unlikely that they did not consciously see the pattern, considering
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it spanned almost the entire screen. The authors found that with monoptic visual masking, visibility of the pattern was correlated with activation throughout the visual pathway. In dichoptic masking, there was only activation beyond V2. Because the perceptual experience between monoptic and dichoptic masking did not change, they reasoned that these results narrowed down the potential brain regions responsible for conscious perception to only the regions activated in both masking conditions: occipital retinotopic areas beyond V2. A similar masking study using words (Kouider et al., 2007) broadened the scope of the results from Tse et al. (2005). The participants of the study were instructed to perform a semantic decision task on words shown on a screen. Just before the target word was shown, a different priming word was flashed very briefly. Similar to Tse’s study, the prime was irrelevant to the task and was unattended to by the participants. Whether they could consciously see the priming word was determined by if it was masked by a string of letters immediately after it was shown. In the subliminal masking condition, the string of letters made the priming word invisible, whereas in the supraliminal masking condition, the absence of the string of letters made the prime visible, although still unattended to by the participants. FMRI results showed that visibility of the prime word was correlated with activity only in occipital and temporal cortices. Extensive repetition enhancement and suppression (i.e., increase or decrease in neural activity) in frontal and parietal cortices suggested that these areas are responsible for conscious access and information processing rather than conscious perception. Fr¨assle et al. (2014) used the aforementioned correlation of optokinetic nystagmus and pupil size with perceptual switch in binocular rivalry to conduct a study comparing active brain regions in a report-dependent paradigm versus a no-report paradigm. The authors first instructed the participants to report switches in percept by holding down and switching between two buttons. They also kept track of the participants’ eye movements and pupil size to get an objective time point of the switch and continuous data of the dominance of the percept at any given time determined by the values of the physical measures. The fMRI data revealed a significant increase of activity in occipital, parietal, and frontal regions that correlated with subjective and objective perceptual switches in active report trials. When participants were no longer asked to respond on buttons, there was a similar activation pattern across the occipital and parietal regions, but there was no longer any significant activity in the frontal region that correlated with rivalry switching. Bilateral activity in the middle frontal gyrus was entirely eliminated. The authors interpreted this negative finding to mean that frontal cortex is not involved in switches in perceptual experience itself but rather in selfmonitoring for reporting any such switches. Another no-report binocular rivalry paradigm yielded negative results (Brascamp et al., 2015). The paradigm incorporated a method of binocular
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rivalry in which the viewer sees moving dots with each eye that move around randomly in such a way that the viewer cannot know if and when a perceptual switch occurs. To make the changes noticeable, the experimenters simply colored the dots differently in each eye. When viewers could determine when the percepts were changing due to the difference in color of the dots, activity in the PFC, along with other areas of the frontal cortex such as the frontal eye fields, and occipital and parietal cortices was correlated with perceptual switches. However, when the viewers could not know about and therefore could not report perceptual changes, there was no such correlated activity in the frontal cortex. Therefore, the authors reasoned that activity in the frontal cortex was not involved with changes in conscious perception.
RESPONSES TO THE NO-REPORT ARGUMENT Not being able to find any positive results in PFC after getting rid of subjective report could mean that those areas were correlated with selfreport, not consciousness per se. However, while such interpretation of negative findings is reasonable and popular, negative findings are limited in nature, especially when there are clear positive findings from other studies using no-report paradigms. For example, in Lumer and Rees (1999), the pioneering study that revealed a correlation between PFC activity and subjective visual perception, the subjects did not make any reports about perceptual switches during the viewing condition. Yet, they found prefrontal involvement in the absence of self-report that consistently covaried with activity in the extrastriate cortex. Another evidence for PFC’s association with consciousness comes from a study that successfully decoded unattended stimuli from neurons in the PFC (Mante, Sussillo, Shenoy, & Newsome, 2013). The study consisted of taking single- and multiunit recordings from monkeys trained to saccade to a visual target based on either the color or the direction of motion of the majority of moving dots on a display. The color of the fixation cue determined which of the two features—direction of movement or color—the monkeys needed to discriminate. Interestingly, even with no task demand to respond to one of the features, neuronal activity in the frontal eye field could be decoded to extract information about the task-irrelevant feature. Information that was not required to be discriminated on a particular block of trials was also found to be encoded in the PFC, undermining the interpretation of PFC’s activity in human conscious perception studies to be reflective of only the self-reports. Positive activity was revealed when electrocorticogram (ECoG) measurements on surgical epileptics during a no-report visual memory task displayed a late “glow” of late activity in the PFC (Noy et al., 2015). The task required the subjects to click whenever they see an image flash twice in a row on a laptop screen. Even when there was no need to respond because the consecutive images were different, there was activity in the PFC that overlapped in
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time with activation of higher order visual areas, similar to Lumer’s results. Rather than seeing this as evidence of PFC’s involvement in conscious perception, the authors interpreted the observed activity in the PFC to be associated with choosing not to make any motor responses. Similar to how making a motor response might need to recruit areas of the PFC, the need to refrain from doing so might have weakly activated the same areas for planning and decision-making. While this is a possible interpretation, it does not rule out the possibility that the PFC activity they found may simply reflect conscious perception even when no explicit response was required. The study by Mante et al. (2013) supports this latter interpretation. These positive results from no-report paradigms hint that there is an alternative explanation to the other negative findings that are currently seen as evidence against PFC’s involvement in consciousness. One such explanation is that the activity in the PFC correlated with conscious perception went unnoticed, perhaps because they are only weakly expressed in some imaging modalities when reporting demand or attention is removed. One way to maximize the sensitivity for the frontal regions in imaging studies would be to target a priori functionally defined regions of interest for each individual. The alternative method of spatially morphing each individual’s brain to a normalized template based on anatomical landmarks could introduce errors from potential distortions and mismatches of brain regions. Such errors could lead to a misinterpretation of activity in a certain region of an individual’s brain as an activity in a different region in the transformed brain. Incorporating multivoxel pattern analysis (MVPA), which has been shown to be able to detect and decode information from “silent” sustained activity in the PFC (Stokes, 2015), could also boost the visibility of PFC activity. Stokes found that there is dynamic activity in the PFC that may be hidden from detection methods that measure increases in activity at the population level, such as the fMRI BOLD signals. Recent advancements in MVPA techniques that measure response patterns between voxels instead of their average activity have enabled detection of maintained activity otherwise unrecognizable by fMRI alone. The view that conventional fMRI may just lack sensitivity is also compatible with the fact that Noy et al. (2015) was able to detect activity in the PFC by utilizing ECoG, a more sensitive, intracranial method of measuring brain activity.
THE ARGUMENT BASED ON LESION STUDIES It has long been argued that PFC lesions reveal no resulting impairment of conscious perception (Pollen, 1995). Even in 1940s and 1950s, bilateral frontal lobectomy, prefrontal topectomy, and lobotomy on humans have left consciousness intact, despite other consequential intellectual and behavioral impairments (Brickner, 1952; Fullton, 1949; Hebb & Penfield, 1940; Mettler, 1949). Although such statements are not the results of modern psychological
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scrutiny, it seems safe to say from their accounts that the patients were, at the very least, conscious. More recent cases of patients with PFC damage tell a similar story. In a case study (Markowitsch & Kessler, 2000) of a 27-year-old woman with widespread degeneration in her PFC, the woman performed poorly on tests that measure prefrontal abilities but normally or even superiorly on other memory tests. Her consciousness was left unimpaired despite her selective deficiencies in prefrontal abilities. A different case study (Mataro´ et al., 2001) of a 81-year-old man 60 years after a severe bilateral lesion in the orbital and dorsolateral frontal regions also recorded behavioral and intellectual disturbances believed to be involved with those regions, such as executive functioning, memory, and motor speed, as well as mood, emotion, and personality. However, his consciousness was still intact. Also, a “virtual lesion” of the DLPFC induced by transcranial magnetic stimulation (TMS) did not interrupt conscious perception (de Graaf, de Jong, Goebel, van Ee, & Sack, 2011). In this study, participants viewed a bistable display of dots moving in an ambiguous direction (either left or right). TMS to DLPFC had no effect on passive viewing of the bistable display and only affected voluntary perceptual switching. That is, participants could still experience two different percepts but had trouble trying to voluntarily switch from one to the other. These results indicate that disruption of DLPFC activity does not obstruct conscious perception.
RESPONSES TO THE “LESION” ARGUMENT In stark contrast, there are many reports that magnetic stimulations and lesions of relevant regions within PFC do in fact impair specific aspects of conscious perception (Chiang, Lu, Hsieh, Chang, & Yang, 2014; Del Cul, Dehaene, Reyes, Bravo, & Slachevsky, 2009; Fleming, Ryu, Golfinos, & Blackmon, 2014; Rounis, Maniscalco, Rothwell, Passingham, & Lau, 2010; Turatto, Sandrini, & Miniussi, 2004). Many of these studies report an impairment related to perceptual metacognition. Metacognition here refers to the subjective evaluation of one’s own perceptual process, which is usually measured by the correspondence between subjective report and perceptual task performance (Lau & Rosenthal, 2011). Mismatch between subjective confidence and objective performance indicates impaired metacognitive abilities. Relevance of metacognition in consciousness research is exemplified in blindsight (Weiskrantz, Barbur, & Sahraie, 1995). In blindsight, cortically blind patients perform above chance level at visual discrimination tasks despite their denial of consciously seeing the relevant visual stimuli (Ko & Lau, 2012). Studies with blindsight avoid performance confounds that may be prevalent in other conscious perception paradigms such as backward masking (Lau, 2008) because the performance between blindsight (unconscious perception) and normal vision (conscious perception) can be matched
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(Weiskrantz et al., 1995). Poor metacognition has been identified as the potential underlying mechanism responsible for the unconscious perception in blindsight (Ko & Lau, 2012; Persaud et al., 2011), which could be extended to say that impairment in metacognition is an impairment in conscious perception. TMS to DLPFC decreased metacognitive sensitivity—the correspondence between visibility ratings and task performance—demonstrating PFC’s role in metacognition of conscious perception (Rounis et al., 2010). Participants viewed a diamond and a square placed next to each other in either of the two possible orientations in each trial. They were asked to report the visibility of the figures (clear vs unclear) and their orientation (square left and diamond right vs vice versa). TMS induction decreased subjective visibility ratings when the orientation was correctly identified, similar to the discrepancy between poor visibility and high visual discrimination performance observed in blindsight (Ko & Lau, 2012). The mismatch between visibility and task performance caused by disruption of activity in DLPFC confirms previous attribution of poor metacognition in blindsight to PFC activity (Ko & Lau, 2012), ratifying the crucial role of the PFC in metacognitive accuracy of conscious perception. A different study found a decrease in subjective confidence ratings following repetitive transmagnetic stimulation (rTMS) of the DLPFC (Chiang et al., 2014). The participants were shown a display of dots in two different colors, which moved in different directions. Following the stimulus presentation, they were asked to correctly identify either the direction moved by one of the two groups of colored dots or the color of the dots that moved a certain direction. Also, they were asked to give a confidence rating (confident vs guessing) of their answer to the identification question. Compared to the number of confident and guessed responses of the control groups that did not receive rTMS or received a sham rTMS, the DLPFC rTMS group reported significantly more guesses, reflecting a drop in their confidence in response. Hence, the DLPFC seems to be engaged in determining the quality of metacognitive percepts. Turatto et al. (2004) also utilized rTMS to temporarily disable the right DLPFC during a visual change detection task, which impaired the ability to perceive changes in conscious visual perception. The study consisted of participants indicating with a key press whether any one of the four faces presented on a screen has changed between the first and second displays separated by a brief interval. Disrupting the right DLPFC significantly lowered the percentage of correct change detection, a clear indication of DLPFC’s role in conscious perception of change. A lesion study (Fleming et al., 2014) has revealed a drop in perceptual metacognitive accuracy upon damage to the PFC. The patients and controls had to decide which of the two circles on the screen contained more dots that briefly flashed inside them and rate their confidence in rating on a scale of 1 6. The patients with anterior PFC lesions had much lower correspondence between their confidence rating and perceptual task performance.
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Such lowered metacognitive accuracy was specific to perception tasks (rather than memory tasks) and was not observed in patients with temporal lobe lesions or healthy controls, suggesting a causal role of anterior PFC in perceptual metacognition. Furthermore, focal PFC lesions had a negative effect on subjective visibility of masked visual stimuli (Del Cul et al., 2009). A single digit was flashed on the screen and shortly after masked with four letters surrounding the target location. A subjective response (see vs did not see target digit) and an objective response (identifying the presented digit) were given verbally after each display. Patients had less accurate objective performance and subjective visibility than controls, conveying that the damaged area in those patients—specifically the left anterior PFC—plays a causal role in conscious perception of masked visual stimuli. Taken together, it is empirically unsound to deny the role the PFC plays in conscious perception. Such role may be specific, i.e., especially regarding subjective, metacognitive aspects of perception. But if we are concerned with subjective conscious awareness, rather than just perception, these results are clearly relevant.
WHY DO PFC LESIONS PRODUCE SUCH SUBTLE EFFECTS? Above data shows that disruption of activity within or damage to the PFC only partially impairs conscious perception rather than eliminating it as a whole (i.e., cortical blindness). Severe lesions to many areas of the brain result in near-complete degradation of its functions (Aldrich, Alessi, Beck, Gilman, 1987). If PFC causally contributes to conscious perception, why does not lesion completely remove conscious perception? Curiously, conscious perception is not the only PFC-dependent operation that does not get completely abolished from PFC damage. A recent finding (Mackey, Devinsky, Doyle, Meager, & Curtis, 2016) shows that even working memory, a classic PFC function, withstands severe damage to the PFC. Mackey et al. (2016) prepared a study with patients with lesions to either the DLPFC or the precentral sulcus (PCS). The patients performed a memoryguided saccade task, in which they were shown a dot on a screen and needed to remember and saccade to its location after a delay period. The average degree of saccade error for PCS lesion patients was significantly higher than that of healthy controls, whereas the patients with DLPFC lesions performed at the same level as the controls. These results highlight that even a reliable function of the DLPFC that has been studied and elucidated in many studies can remain intact after a lesion to the DLPFC. Therefore, the lack of data for a complete elimination of conscious perception following PFC damage should not be a reason to believe that PFC is not responsible for conscious perception; rather, the more appropriate question may be why damage to the PFC does not entirely extinguish at least some of its functions.
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To theorize how PFC functions are buffered from physical damage, perhaps it may be useful to consider how brain structures encode the underlying functions. Hebb (1949) famously hypothesized that mental phenomena are results of the networks between nodes (i.e., single neuron or group of neurons) in our brain. This well-accepted basic principle is reflected in many theories of cognitive processing, as in parallel distributed processing (PDP; Thomas & McClelland, 2008). PDP posits that neural networks process multiple pieces of information simultaneously and in parallel, as opposed to models of intelligence that process information serially in a rule-based fashion, such as in a Turing machine. An important consideration about PDP is how many nodes or neurons are activated to encode a piece of information or a cognitive process. In “sparse” coding, an item or process is coded as an activation of a small number of neurons, even down to a single neuron at an extreme (Olshausen & Field, 1997). Each neuron has a highly selective activation rule, and there is hardly any activational overlap among two different items. An example of sparse coding is seen in simple cells, which are located in the primary visual cortex and only respond to bars of particular orientations. Another example is the famous hypothetical case of a “grandmother” neuron, which responds to nothing but the face of one’s grandmother (Gross, 2002). However, in “dense” coding (as contra “sparse” coding; Rigotti et al., 2013), an object or concept is represented by ensemble activity of a large group of neurons, which also carry the shared duty of coding other representations. In some cases, dense coding provides a computational advantage over lower dimensional neural representations to allow for higher cognition of more potential informational states (Fusi, Miller, & Rigotti, 2016). Identifying the coding mechanism underlying neural networks is valuable because it could explain how “graceful degradation” might work in the PFC. Graceful degradation refers to the overall intact ability of a neural system to carry out its function although its component has been damaged (Rolls, 1994). Such protection of the functionality of the whole system can account for various mental phenomena, such as partial memory and only a partial impairment in relevant functions in patients with brain lesions (Baddeley, 1997). Even under sparse coding, graceful degradation has been believed to be possible (Rolls & Treves, 1990). Given that the PFC likely uses a “dense” coding scheme (Rigotti et al., 2013), meaning that a single representation spreads over many neurons distributed throughout the system, perhaps it is not surprising that damages to PFC often do not produce devastating effects (de Graaf et al., 2011; Mackey et al., 2016). In fact, Rigotti et al. (2013) reported that neurons in the PFC have heterogeneous, mixed selectivity for multiple task-related features and encode information about each feature they respond to. Importantly, they found that even after turning off single-cell selectivity to a feature, information could still be decoded at the population level in the PFC.
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Congruent with the foregoing speculations, indeed, bilateral lesion of the relatively sparsely coded primary visual cortex results in detrimental cortical blindness (Aldrich et al., 1987). In contrast, damage to the PFC has been much more lenient in hurting its functions (Mackey et al., 2016) as discussed before. PFC functions have also been shown to be able to recover from unilateral damage because the undamaged side compensates for any losses in functions normally carried out by the damaged side, revealing the flexibility of the PFC’s system as a whole (Voytek et al., 2010).
IMPLICATIONS FOR THEORIES OF CONSCIOUSNESS So far, we have defended PFC’s involvement in consciousness from opposing arguments. But such defense also helps us to characterize the extent to which PFC may contribute to conscious perception. From early on, evidence of PFC’s activity in conscious perception (Lumer & Rees, 1999) has been interpreted as part of a global workspace for conscious processing across regions of the cortex that provide top-down cognitive processing and attentional amplification necessary for conscious experience (Baars, 1988; Dehaene & Naccache, 2001; Dehaene et al., 2006). Theoretically, one would expect that information reaching the global workspace would lead to superior performance in perceptual and higher cognitive tasks, because the workspace would serve to “ignite” and “broadcast” to amplify such signals. However, it has recently been shown that induction of rTMS on DLPFC resulted in less metacognitive awareness of visual stimuli without lowered task performance (Chiang, Lu, Hsieh, Chang, & Yang, 2014). Because the disruption of PFC activity selectively reduced subjective awareness without lowering performance capacity, and that under no-report situations, PFC activity may be relatively local and weak rather than widespread (Noy et al., 2015), these results seem difficult to interpret in the light of global workspace theory. On the other end of the spectrum of theories on PFC’s importance in conscious perception, first-order theories hold that consciousness solely depends on early sensory activity without any higher levels of cognition. An example of such a view is the popular local recurrency theory (Lamme, 2006). An empirical prediction made by such views is that PFC activity does not play a part in conscious experience. But earlier we reviewed that PFC does play important and specific roles in conscious perception. The foregoing review suggests that the most plausible view reflecting PFC’s involvement may exist somewhere in between global workspace theory and first-order theories. Such model would explain correlated activation of the PFC with conscious perception without attributing too many other cognitive functions to the same mechanisms. Higher order theories of consciousness posit that consciousness is contingent on some higher level activity that makes oneself aware of being in a particular mental state, which makes that mental state conscious (Lau & Rosenthal, 2011). Relating the
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studies that identified the association between PFC activity and conscious awareness (Rees et al., 2002) to higher order theories, it is likely that such activity occurs in the PFC. A study (Maniscalco & Lau, 2016) that lends support to higher order theories analyzed the relationship between subjective visibility ratings and objective perceptual processing performance. The authors observed a clear dissociation between visibility rating and task performance, which is difficult to be captured by the most parsimonious computational models that hold task performance and visibility ratings to be based on the same underlying process. The model that fit their data the best was a hierarchical model in which early processing generates the objective perceptual judgment, whereas a later processing stream evaluates those early perceptual processes to generate the subjective judgments. This model predicts that altering the late processing stage would affect only the subjective reports and not the objective task capacity, as congruent with the TMS and lesion results reviewed earlier (Chiang et al., 2014; Del Cul et al., 2009; Fleming et al., 2014; Rounis et al., 2010). Findings that could uphold or challenge some major theories of consciousness are still emerging. Perhaps it is fair to say that at this point, there is no conclusive victor among the reviewed theories of consciousness. However, there are optimistic signs that one could eventually resolve these differences between the theories through careful consideration of empirical evidence collected using different methods. This review hopefully represents a modest exercise in this spirit.
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Olshausen, B. A., & Field, D. J. (1997). Sparse coding with an overcomplete basis set: A strategy employed by V1? Vision Research, 37(23), 3311 3325. Persaud, N., Davidson, M., Maniscalco, B., Mobbs, D., Passingham, R. E., Cowey, A., & Lau, H. (2011). Awareness-related activity in prefrontal and parietal cortices in blindsight reflects more than superior visual performance. Neuroimage, 58(2), 605 611. Pollen, D. A. (1995). Cortical areas in visual awareness. Nature, 377(6547), 293 295. Ress, D., Backus, B. T., & Heeger, D. J. (2000). Activity in primary visual cortex predicts performance in a visual detection task. Nature Neuroscience, 3(9), 940 945. Rees, G., Kreiman, G., & Koch, C. (2002). Neural correlates of consciousness in humans. Nature Reviews Neuroscience, 3(4), 261 270. Rigotti, M., Barak, O., Warden, M. R., Wang, X. J., Daw, N. D., Miller, E. K., & Fusi, S. (2013). The importance of mixed selectivity in complex cognitive tasks. Nature, 497(7451), 585 590. Rolls, E. T. (1994). Brain mechanisms for invariant visual recognition and learning. Behavioural Processes, 33(1-2), 113 138. Rolls, E. T., & Treves, A. (1990). The relative advantages of sparse versus distributed encoding for associative neuronal networks in the brain. Network: Computation in Neural Systems, 1(4), 407 421. Rounis, E., Maniscalco, B., Rothwell, J. C., Passingham, R. E., & Lau, H. (2010). Theta-burst transcranial magnetic stimulation to the prefrontal cortex impairs metacognitive visual awareness. Cognitive Neuroscience, 1(3), 165 175. Stokes, M. G. (2015). ‘Activity-silent’ working memory in prefrontal cortex: A dynamic coding framework. Trends in Cognitive Sciences, 19(7), 394 405. Super, H., Spekreijse, H., & Lamme, V. A. (2001). Two distinct modes of sensory processing observed in monkey primary visual cortex (V1). Nature Neuroscience, 4, 304 310. Thomas, M. S., & McClelland, J. L. (2008). Connectionist models of cognition. The Cambridge handbook of computational psychology. New York: Cambridge University Press. Tong, F., Meng, M., & Blake, R. (2006). Neural bases of binocular rivalry. Trends in Cognitive Sciences, 10(11), 502 511. Tse, P. U., Martinez-Conde, S., Schlegel, A. A., & Macknik, S. L. (2005). Visibility, visual awareness, and visual masking of simple unattended targets are confined to areas in the occipital cortex beyond human V1/V2. Proceedings of the National Academy of Sciences of the United States of America, 102(47), 17178 17183. Tsuchiya, N., Wilke, M., Fr¨assle, S., & Lamme, V. A. (2015). No-report paradigms: Extracting the true neural correlates of consciousness. Trends in Cognitive Sciences, 19(12), 757 770. Turatto, M., Sandrini, M., & Miniussi, C. (2004). The role of the right dorsolateral prefrontal cortex in visual change awareness. Neuroreport, 15(16), 2549 2552. Voytek, B., Davis, M., Yago, E., Barcelo´, F., Vogel, E. K., & Knight, R. T. (2010). Dynamic neuroplasticity after human prefrontal cortex damage. Neuron, 68(3), 401 408. Weiskrantz, L., Barbur, J. L., & Sahraie, A. (1995). Parameters affecting conscious versus unconscious visual discrimination with damage to the visual cortex (V1). Proceedings of the National Academy of Sciences of the United States of America, 92, 6122 6126.
Crucial Role of the Prefrontal Cortex in Conscious Perception Seth Lew1 and Hakwan Lau1,2 1 2
Psychology Department, University of California Los Angeles, Los Angeles, CA, United States, Brain Research Institute, University of California Los Angeles, Los Angeles, CA, United States
EARLY NEUROIMAGING EVIDENCE OF PREFRONTAL CORTEX’S INVOLVEMENT IN CONSCIOUS PERCEPTION Functional magnetic resonance imaging (fMRI) studies since the late 1990s presented findings that areas in the prefrontal cortex (PFC) are associated with conscious perception (Dehaene & Naccache, 2001; Dehaene, Changeux, Naccache, Sackur, & Sergent, 2006; Lumer & Rees, 1999; Rees, Kreiman, & Koch, 2002). For example, one of the earlier studies by Lumer and Rees (1999) identified activity in the extrastriate cortex that correlated with perceptual switching in binocular rivalry and PFC activity that covaried with the activation of the extrastriate cortex. A review (Rees et al., 2002) pooled results from five different neuroimaging studies that identified neural correlates of consciousness and found an overlap of activity in the dorsolateral prefrontal cortex (DLPFC). Dehaene et al. (2006) further reasoned that the involvement of PFC is selective to conscious versus un- or preconscious perception. Specifically, they posited that conscious awareness requires both bottom-up stimulus processing and top-down attention in areas of higher cognition, such as the PFC (Dehaene & Naccache, 2001), a view that we will discuss at the end of this chapter. In this chapter, we evaluate the status of the claim that PFC is critically involved in conscious perception.
THE “NO-REPORT” ARGUMENT AGAINST PFC’S ROLE IN CONSCIOUSNESS One argument against PFC’s association with consciousness is that the activation of PFC may reflect processes used for self-report instead of conscious perception. Researchers usually make use of participants’ self-report Executive Functions in Health and Disease. DOI: http://dx.doi.org/10.1016/B978-0-12-803676-1.00006-4 © 2017 Elsevier Inc. All rights reserved.
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to assess their conscious experience of the presented stimuli. These reports are crucial to studies searching for differences in neural activity that track changes in perceptual states while the stimulus is being held constant (Ress, Backus, & Heeger, 2000; Super, Spekreijse, & Lamme, 2001; Tong, Meng, & Blake, 2006). The idea is that if a stimulus remains constant but a person’s perceptual experience of it has changed, then any difference in the person’s neural activities must be correlated with the difference in their conscious experience. In that way, the parts of the brain that show different levels of activity when a person has different conscious experiences of the same stimulus can be understood as neural correlates of consciousness. However, some authors have recently argued that the self-report itself can be a confounding factor (Tsuchiya, Wilke, Fr¨assle, & Lamme, 2015). The need to self-report requires employment of neural areas correlated with paying attention to the upcoming stimulus, self-monitoring after sensing the stimulus, accessing the sensory data, and generating and delivering a report, which are processes conceptually distinct from the phenomenon of conscious perception itself. Therefore, the brain areas reported to be neural correlates of consciousness could have wrongly included activity due to demands of self-report rather than conscious perception per se. To remove confounds associated with self-report, “no-report” paradigms have been developed and used as alternatives to those that require self-report (Tse, Martinez-Conde, Schlegel, & Macknik, 2005). As the name suggests, no-report paradigms remove the reliance on self-report from the participants to determine their perceptual state. Instead, researchers use neural recordings or physiological changes of the participant to infer their perceptual experience. For example, optokinetic nystagmus (i.e., eye movement to follow a moving object while the head remains stationary) and pupil size were used to accurately verify perceptual switching in binocular rivalry in the absence of self-report (Fr¨assle, Sommer, Jansen, Naber, & Einh¨auser, 2014). Neural correlates found in no-report paradigms are expected to be more refined than those from report-dependent paradigms because the regions of the brain that activates solely for aspects of self-report would be truncated from the results. Interestingly, findings from no-report paradigms have revealed consistent activity in the striate and extrastriate cortex but none in the PFC or the parietal cortex that correlated with consciousness (Brascamp, Blake, & Knapen, 2015; Fr¨assle et al., 2014; Kouider, Dehaene, Jobert, & Le Bihan, 2007; Tse et al., 2005). For instance, Tse et al. (2005) took advantage of the same perceptual content of monoptic and dichoptic visual masking to narrow down the areas that might be correlated to consciousness. In monoptic visual masking, the visual stimulus and mask were presented to both eyes, whereas in dichoptic masking, the visual stimulus was presented to one eye and the mask to the other eye. The masked pattern occupied most of the screen but was unattended to by the participant due to their focus on a fixation task. Although there was no need for the participants to report on the masked pattern, it is unlikely that they did not consciously see the pattern, considering
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it spanned almost the entire screen. The authors found that with monoptic visual masking, visibility of the pattern was correlated with activation throughout the visual pathway. In dichoptic masking, there was only activation beyond V2. Because the perceptual experience between monoptic and dichoptic masking did not change, they reasoned that these results narrowed down the potential brain regions responsible for conscious perception to only the regions activated in both masking conditions: occipital retinotopic areas beyond V2. A similar masking study using words (Kouider et al., 2007) broadened the scope of the results from Tse et al. (2005). The participants of the study were instructed to perform a semantic decision task on words shown on a screen. Just before the target word was shown, a different priming word was flashed very briefly. Similar to Tse’s study, the prime was irrelevant to the task and was unattended to by the participants. Whether they could consciously see the priming word was determined by if it was masked by a string of letters immediately after it was shown. In the subliminal masking condition, the string of letters made the priming word invisible, whereas in the supraliminal masking condition, the absence of the string of letters made the prime visible, although still unattended to by the participants. FMRI results showed that visibility of the prime word was correlated with activity only in occipital and temporal cortices. Extensive repetition enhancement and suppression (i.e., increase or decrease in neural activity) in frontal and parietal cortices suggested that these areas are responsible for conscious access and information processing rather than conscious perception. Fr¨assle et al. (2014) used the aforementioned correlation of optokinetic nystagmus and pupil size with perceptual switch in binocular rivalry to conduct a study comparing active brain regions in a report-dependent paradigm versus a no-report paradigm. The authors first instructed the participants to report switches in percept by holding down and switching between two buttons. They also kept track of the participants’ eye movements and pupil size to get an objective time point of the switch and continuous data of the dominance of the percept at any given time determined by the values of the physical measures. The fMRI data revealed a significant increase of activity in occipital, parietal, and frontal regions that correlated with subjective and objective perceptual switches in active report trials. When participants were no longer asked to respond on buttons, there was a similar activation pattern across the occipital and parietal regions, but there was no longer any significant activity in the frontal region that correlated with rivalry switching. Bilateral activity in the middle frontal gyrus was entirely eliminated. The authors interpreted this negative finding to mean that frontal cortex is not involved in switches in perceptual experience itself but rather in selfmonitoring for reporting any such switches. Another no-report binocular rivalry paradigm yielded negative results (Brascamp et al., 2015). The paradigm incorporated a method of binocular
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rivalry in which the viewer sees moving dots with each eye that move around randomly in such a way that the viewer cannot know if and when a perceptual switch occurs. To make the changes noticeable, the experimenters simply colored the dots differently in each eye. When viewers could determine when the percepts were changing due to the difference in color of the dots, activity in the PFC, along with other areas of the frontal cortex such as the frontal eye fields, and occipital and parietal cortices was correlated with perceptual switches. However, when the viewers could not know about and therefore could not report perceptual changes, there was no such correlated activity in the frontal cortex. Therefore, the authors reasoned that activity in the frontal cortex was not involved with changes in conscious perception.
RESPONSES TO THE NO-REPORT ARGUMENT Not being able to find any positive results in PFC after getting rid of subjective report could mean that those areas were correlated with selfreport, not consciousness per se. However, while such interpretation of negative findings is reasonable and popular, negative findings are limited in nature, especially when there are clear positive findings from other studies using no-report paradigms. For example, in Lumer and Rees (1999), the pioneering study that revealed a correlation between PFC activity and subjective visual perception, the subjects did not make any reports about perceptual switches during the viewing condition. Yet, they found prefrontal involvement in the absence of self-report that consistently covaried with activity in the extrastriate cortex. Another evidence for PFC’s association with consciousness comes from a study that successfully decoded unattended stimuli from neurons in the PFC (Mante, Sussillo, Shenoy, & Newsome, 2013). The study consisted of taking single- and multiunit recordings from monkeys trained to saccade to a visual target based on either the color or the direction of motion of the majority of moving dots on a display. The color of the fixation cue determined which of the two features—direction of movement or color—the monkeys needed to discriminate. Interestingly, even with no task demand to respond to one of the features, neuronal activity in the frontal eye field could be decoded to extract information about the task-irrelevant feature. Information that was not required to be discriminated on a particular block of trials was also found to be encoded in the PFC, undermining the interpretation of PFC’s activity in human conscious perception studies to be reflective of only the self-reports. Positive activity was revealed when electrocorticogram (ECoG) measurements on surgical epileptics during a no-report visual memory task displayed a late “glow” of late activity in the PFC (Noy et al., 2015). The task required the subjects to click whenever they see an image flash twice in a row on a laptop screen. Even when there was no need to respond because the consecutive images were different, there was activity in the PFC that overlapped in
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time with activation of higher order visual areas, similar to Lumer’s results. Rather than seeing this as evidence of PFC’s involvement in conscious perception, the authors interpreted the observed activity in the PFC to be associated with choosing not to make any motor responses. Similar to how making a motor response might need to recruit areas of the PFC, the need to refrain from doing so might have weakly activated the same areas for planning and decision-making. While this is a possible interpretation, it does not rule out the possibility that the PFC activity they found may simply reflect conscious perception even when no explicit response was required. The study by Mante et al. (2013) supports this latter interpretation. These positive results from no-report paradigms hint that there is an alternative explanation to the other negative findings that are currently seen as evidence against PFC’s involvement in consciousness. One such explanation is that the activity in the PFC correlated with conscious perception went unnoticed, perhaps because they are only weakly expressed in some imaging modalities when reporting demand or attention is removed. One way to maximize the sensitivity for the frontal regions in imaging studies would be to target a priori functionally defined regions of interest for each individual. The alternative method of spatially morphing each individual’s brain to a normalized template based on anatomical landmarks could introduce errors from potential distortions and mismatches of brain regions. Such errors could lead to a misinterpretation of activity in a certain region of an individual’s brain as an activity in a different region in the transformed brain. Incorporating multivoxel pattern analysis (MVPA), which has been shown to be able to detect and decode information from “silent” sustained activity in the PFC (Stokes, 2015), could also boost the visibility of PFC activity. Stokes found that there is dynamic activity in the PFC that may be hidden from detection methods that measure increases in activity at the population level, such as the fMRI BOLD signals. Recent advancements in MVPA techniques that measure response patterns between voxels instead of their average activity have enabled detection of maintained activity otherwise unrecognizable by fMRI alone. The view that conventional fMRI may just lack sensitivity is also compatible with the fact that Noy et al. (2015) was able to detect activity in the PFC by utilizing ECoG, a more sensitive, intracranial method of measuring brain activity.
THE ARGUMENT BASED ON LESION STUDIES It has long been argued that PFC lesions reveal no resulting impairment of conscious perception (Pollen, 1995). Even in 1940s and 1950s, bilateral frontal lobectomy, prefrontal topectomy, and lobotomy on humans have left consciousness intact, despite other consequential intellectual and behavioral impairments (Brickner, 1952; Fullton, 1949; Hebb & Penfield, 1940; Mettler, 1949). Although such statements are not the results of modern psychological
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scrutiny, it seems safe to say from their accounts that the patients were, at the very least, conscious. More recent cases of patients with PFC damage tell a similar story. In a case study (Markowitsch & Kessler, 2000) of a 27-year-old woman with widespread degeneration in her PFC, the woman performed poorly on tests that measure prefrontal abilities but normally or even superiorly on other memory tests. Her consciousness was left unimpaired despite her selective deficiencies in prefrontal abilities. A different case study (Mataro´ et al., 2001) of a 81-year-old man 60 years after a severe bilateral lesion in the orbital and dorsolateral frontal regions also recorded behavioral and intellectual disturbances believed to be involved with those regions, such as executive functioning, memory, and motor speed, as well as mood, emotion, and personality. However, his consciousness was still intact. Also, a “virtual lesion” of the DLPFC induced by transcranial magnetic stimulation (TMS) did not interrupt conscious perception (de Graaf, de Jong, Goebel, van Ee, & Sack, 2011). In this study, participants viewed a bistable display of dots moving in an ambiguous direction (either left or right). TMS to DLPFC had no effect on passive viewing of the bistable display and only affected voluntary perceptual switching. That is, participants could still experience two different percepts but had trouble trying to voluntarily switch from one to the other. These results indicate that disruption of DLPFC activity does not obstruct conscious perception.
RESPONSES TO THE “LESION” ARGUMENT In stark contrast, there are many reports that magnetic stimulations and lesions of relevant regions within PFC do in fact impair specific aspects of conscious perception (Chiang, Lu, Hsieh, Chang, & Yang, 2014; Del Cul, Dehaene, Reyes, Bravo, & Slachevsky, 2009; Fleming, Ryu, Golfinos, & Blackmon, 2014; Rounis, Maniscalco, Rothwell, Passingham, & Lau, 2010; Turatto, Sandrini, & Miniussi, 2004). Many of these studies report an impairment related to perceptual metacognition. Metacognition here refers to the subjective evaluation of one’s own perceptual process, which is usually measured by the correspondence between subjective report and perceptual task performance (Lau & Rosenthal, 2011). Mismatch between subjective confidence and objective performance indicates impaired metacognitive abilities. Relevance of metacognition in consciousness research is exemplified in blindsight (Weiskrantz, Barbur, & Sahraie, 1995). In blindsight, cortically blind patients perform above chance level at visual discrimination tasks despite their denial of consciously seeing the relevant visual stimuli (Ko & Lau, 2012). Studies with blindsight avoid performance confounds that may be prevalent in other conscious perception paradigms such as backward masking (Lau, 2008) because the performance between blindsight (unconscious perception) and normal vision (conscious perception) can be matched
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(Weiskrantz et al., 1995). Poor metacognition has been identified as the potential underlying mechanism responsible for the unconscious perception in blindsight (Ko & Lau, 2012; Persaud et al., 2011), which could be extended to say that impairment in metacognition is an impairment in conscious perception. TMS to DLPFC decreased metacognitive sensitivity—the correspondence between visibility ratings and task performance—demonstrating PFC’s role in metacognition of conscious perception (Rounis et al., 2010). Participants viewed a diamond and a square placed next to each other in either of the two possible orientations in each trial. They were asked to report the visibility of the figures (clear vs unclear) and their orientation (square left and diamond right vs vice versa). TMS induction decreased subjective visibility ratings when the orientation was correctly identified, similar to the discrepancy between poor visibility and high visual discrimination performance observed in blindsight (Ko & Lau, 2012). The mismatch between visibility and task performance caused by disruption of activity in DLPFC confirms previous attribution of poor metacognition in blindsight to PFC activity (Ko & Lau, 2012), ratifying the crucial role of the PFC in metacognitive accuracy of conscious perception. A different study found a decrease in subjective confidence ratings following repetitive transmagnetic stimulation (rTMS) of the DLPFC (Chiang et al., 2014). The participants were shown a display of dots in two different colors, which moved in different directions. Following the stimulus presentation, they were asked to correctly identify either the direction moved by one of the two groups of colored dots or the color of the dots that moved a certain direction. Also, they were asked to give a confidence rating (confident vs guessing) of their answer to the identification question. Compared to the number of confident and guessed responses of the control groups that did not receive rTMS or received a sham rTMS, the DLPFC rTMS group reported significantly more guesses, reflecting a drop in their confidence in response. Hence, the DLPFC seems to be engaged in determining the quality of metacognitive percepts. Turatto et al. (2004) also utilized rTMS to temporarily disable the right DLPFC during a visual change detection task, which impaired the ability to perceive changes in conscious visual perception. The study consisted of participants indicating with a key press whether any one of the four faces presented on a screen has changed between the first and second displays separated by a brief interval. Disrupting the right DLPFC significantly lowered the percentage of correct change detection, a clear indication of DLPFC’s role in conscious perception of change. A lesion study (Fleming et al., 2014) has revealed a drop in perceptual metacognitive accuracy upon damage to the PFC. The patients and controls had to decide which of the two circles on the screen contained more dots that briefly flashed inside them and rate their confidence in rating on a scale of 1 6. The patients with anterior PFC lesions had much lower correspondence between their confidence rating and perceptual task performance.
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Such lowered metacognitive accuracy was specific to perception tasks (rather than memory tasks) and was not observed in patients with temporal lobe lesions or healthy controls, suggesting a causal role of anterior PFC in perceptual metacognition. Furthermore, focal PFC lesions had a negative effect on subjective visibility of masked visual stimuli (Del Cul et al., 2009). A single digit was flashed on the screen and shortly after masked with four letters surrounding the target location. A subjective response (see vs did not see target digit) and an objective response (identifying the presented digit) were given verbally after each display. Patients had less accurate objective performance and subjective visibility than controls, conveying that the damaged area in those patients—specifically the left anterior PFC—plays a causal role in conscious perception of masked visual stimuli. Taken together, it is empirically unsound to deny the role the PFC plays in conscious perception. Such role may be specific, i.e., especially regarding subjective, metacognitive aspects of perception. But if we are concerned with subjective conscious awareness, rather than just perception, these results are clearly relevant.
WHY DO PFC LESIONS PRODUCE SUCH SUBTLE EFFECTS? Above data shows that disruption of activity within or damage to the PFC only partially impairs conscious perception rather than eliminating it as a whole (i.e., cortical blindness). Severe lesions to many areas of the brain result in near-complete degradation of its functions (Aldrich, Alessi, Beck, Gilman, 1987). If PFC causally contributes to conscious perception, why does not lesion completely remove conscious perception? Curiously, conscious perception is not the only PFC-dependent operation that does not get completely abolished from PFC damage. A recent finding (Mackey, Devinsky, Doyle, Meager, & Curtis, 2016) shows that even working memory, a classic PFC function, withstands severe damage to the PFC. Mackey et al. (2016) prepared a study with patients with lesions to either the DLPFC or the precentral sulcus (PCS). The patients performed a memoryguided saccade task, in which they were shown a dot on a screen and needed to remember and saccade to its location after a delay period. The average degree of saccade error for PCS lesion patients was significantly higher than that of healthy controls, whereas the patients with DLPFC lesions performed at the same level as the controls. These results highlight that even a reliable function of the DLPFC that has been studied and elucidated in many studies can remain intact after a lesion to the DLPFC. Therefore, the lack of data for a complete elimination of conscious perception following PFC damage should not be a reason to believe that PFC is not responsible for conscious perception; rather, the more appropriate question may be why damage to the PFC does not entirely extinguish at least some of its functions.
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To theorize how PFC functions are buffered from physical damage, perhaps it may be useful to consider how brain structures encode the underlying functions. Hebb (1949) famously hypothesized that mental phenomena are results of the networks between nodes (i.e., single neuron or group of neurons) in our brain. This well-accepted basic principle is reflected in many theories of cognitive processing, as in parallel distributed processing (PDP; Thomas & McClelland, 2008). PDP posits that neural networks process multiple pieces of information simultaneously and in parallel, as opposed to models of intelligence that process information serially in a rule-based fashion, such as in a Turing machine. An important consideration about PDP is how many nodes or neurons are activated to encode a piece of information or a cognitive process. In “sparse” coding, an item or process is coded as an activation of a small number of neurons, even down to a single neuron at an extreme (Olshausen & Field, 1997). Each neuron has a highly selective activation rule, and there is hardly any activational overlap among two different items. An example of sparse coding is seen in simple cells, which are located in the primary visual cortex and only respond to bars of particular orientations. Another example is the famous hypothetical case of a “grandmother” neuron, which responds to nothing but the face of one’s grandmother (Gross, 2002). However, in “dense” coding (as contra “sparse” coding; Rigotti et al., 2013), an object or concept is represented by ensemble activity of a large group of neurons, which also carry the shared duty of coding other representations. In some cases, dense coding provides a computational advantage over lower dimensional neural representations to allow for higher cognition of more potential informational states (Fusi, Miller, & Rigotti, 2016). Identifying the coding mechanism underlying neural networks is valuable because it could explain how “graceful degradation” might work in the PFC. Graceful degradation refers to the overall intact ability of a neural system to carry out its function although its component has been damaged (Rolls, 1994). Such protection of the functionality of the whole system can account for various mental phenomena, such as partial memory and only a partial impairment in relevant functions in patients with brain lesions (Baddeley, 1997). Even under sparse coding, graceful degradation has been believed to be possible (Rolls & Treves, 1990). Given that the PFC likely uses a “dense” coding scheme (Rigotti et al., 2013), meaning that a single representation spreads over many neurons distributed throughout the system, perhaps it is not surprising that damages to PFC often do not produce devastating effects (de Graaf et al., 2011; Mackey et al., 2016). In fact, Rigotti et al. (2013) reported that neurons in the PFC have heterogeneous, mixed selectivity for multiple task-related features and encode information about each feature they respond to. Importantly, they found that even after turning off single-cell selectivity to a feature, information could still be decoded at the population level in the PFC.
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Congruent with the foregoing speculations, indeed, bilateral lesion of the relatively sparsely coded primary visual cortex results in detrimental cortical blindness (Aldrich et al., 1987). In contrast, damage to the PFC has been much more lenient in hurting its functions (Mackey et al., 2016) as discussed before. PFC functions have also been shown to be able to recover from unilateral damage because the undamaged side compensates for any losses in functions normally carried out by the damaged side, revealing the flexibility of the PFC’s system as a whole (Voytek et al., 2010).
IMPLICATIONS FOR THEORIES OF CONSCIOUSNESS So far, we have defended PFC’s involvement in consciousness from opposing arguments. But such defense also helps us to characterize the extent to which PFC may contribute to conscious perception. From early on, evidence of PFC’s activity in conscious perception (Lumer & Rees, 1999) has been interpreted as part of a global workspace for conscious processing across regions of the cortex that provide top-down cognitive processing and attentional amplification necessary for conscious experience (Baars, 1988; Dehaene & Naccache, 2001; Dehaene et al., 2006). Theoretically, one would expect that information reaching the global workspace would lead to superior performance in perceptual and higher cognitive tasks, because the workspace would serve to “ignite” and “broadcast” to amplify such signals. However, it has recently been shown that induction of rTMS on DLPFC resulted in less metacognitive awareness of visual stimuli without lowered task performance (Chiang, Lu, Hsieh, Chang, & Yang, 2014). Because the disruption of PFC activity selectively reduced subjective awareness without lowering performance capacity, and that under no-report situations, PFC activity may be relatively local and weak rather than widespread (Noy et al., 2015), these results seem difficult to interpret in the light of global workspace theory. On the other end of the spectrum of theories on PFC’s importance in conscious perception, first-order theories hold that consciousness solely depends on early sensory activity without any higher levels of cognition. An example of such a view is the popular local recurrency theory (Lamme, 2006). An empirical prediction made by such views is that PFC activity does not play a part in conscious experience. But earlier we reviewed that PFC does play important and specific roles in conscious perception. The foregoing review suggests that the most plausible view reflecting PFC’s involvement may exist somewhere in between global workspace theory and first-order theories. Such model would explain correlated activation of the PFC with conscious perception without attributing too many other cognitive functions to the same mechanisms. Higher order theories of consciousness posit that consciousness is contingent on some higher level activity that makes oneself aware of being in a particular mental state, which makes that mental state conscious (Lau & Rosenthal, 2011). Relating the
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studies that identified the association between PFC activity and conscious awareness (Rees et al., 2002) to higher order theories, it is likely that such activity occurs in the PFC. A study (Maniscalco & Lau, 2016) that lends support to higher order theories analyzed the relationship between subjective visibility ratings and objective perceptual processing performance. The authors observed a clear dissociation between visibility rating and task performance, which is difficult to be captured by the most parsimonious computational models that hold task performance and visibility ratings to be based on the same underlying process. The model that fit their data the best was a hierarchical model in which early processing generates the objective perceptual judgment, whereas a later processing stream evaluates those early perceptual processes to generate the subjective judgments. This model predicts that altering the late processing stage would affect only the subjective reports and not the objective task capacity, as congruent with the TMS and lesion results reviewed earlier (Chiang et al., 2014; Del Cul et al., 2009; Fleming et al., 2014; Rounis et al., 2010). Findings that could uphold or challenge some major theories of consciousness are still emerging. Perhaps it is fair to say that at this point, there is no conclusive victor among the reviewed theories of consciousness. However, there are optimistic signs that one could eventually resolve these differences between the theories through careful consideration of empirical evidence collected using different methods. This review hopefully represents a modest exercise in this spirit.
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