The Conscious Brain

Empirical investigations of the neural correlates of perceptual awareness

Umeå Studies in Cognitive Science 4

Copyright © 2007 Johan ErikssonISBN: 978-91-7264-457-1ISSN: 1654-2568Printed by Arkitektkopia, Umeå, 2007

ABSTRACT

Eriksson, J. (2007). The conscious brain: Empirical investigations of the neural correlates of perceptual awareness. Doctoral dissertation from the Department of Psychology, Umeå University, S-901 87 Umeå, Sweden.ISBN: 978-91-7264-457-1

Although consciousness has been studied since ancient time, how the brain implements consciousness is still considered a great mystery by most. This thesis investigates the neural correlates of consciousness by measuring brain activity with functional magnetic resonance imaging (fMRI) while specific contents of consciousness are defined and maintained in various experimental settings. Study 1 showed that the brain works differently when creating a new conscious percept compared to when maintaining the same percept over time. Specifically, sensory and fronto-parietal regions were activated for both conditions but with different activation patterns within these regions. This distinction between creating and maintaining a conscious percept was further supported by Study 2, which in addition showed that there are both differences and similarities in how the brain works when defining a visual compared to an auditory percept. In particular, frontal cortex was commonly activated while posterior cortical activity was modality specific. Study 3 showed that task difficulty influenced the degree of frontal and parietal cortex involvement, such that fronto-parietal activity decreased as a function of ease of identification. This is interpreted as evidence of the non-necessity of these regions for conscious perception in situations where the stimuli are distinct and apparent. Based on these results a model is proposed where sensory regions interact with controlling regions to enable conscious perception. The amount and type of required interaction depend on stimuli and task characteristics, to the extent that higher-order cortical involvement may not be required at all for easily recognizable stimuli.

Keywords: consciousness, visual perception, object identification, functional neuroimaging, top-down processing, prefrontal cortex, auditory perception

ACKNOWLEDGEMENTS

I want to thank my supervisor Lars Nyberg for being the quintessence of what a supervisor should be. Thank you Anne Larsson and Micael Andersson for valuable help with various fMRI issues. Thank you Arne Börjesson, Bert Jonsson, Björn Andersson, and Martin Ingvar for comments on earlier versions of this thesis. I would also like to thank all colleagues at the Department of Psychology, Umeå University, for creating a pleasant working environment. Special thanks to my wife Pernilla and my two sons Edvin and Adrian, and to the rest of my family and friends.

Umeå, November, 2007Johan Eriksson

LIST OF PAPERS

This thesis for the doctorate degree is based on the following studies:

I Eriksson, J., Larsson, A., Riklund Åhlström, K., & Nyberg, L. (2004). Visual consciousness: Dissociating the neural correlates of perceptual transitions from sustained perception with fMRI. Consciousness and Cognition, 13, 61-72.

II Eriksson, J., Larsson, A., Riklund Åhlström, K., & Nyberg, L. (2007). Similar frontal and distinct posterior cortical regions mediate visual and auditory perceptual awareness. Cerebral Cortex, 17, 760-765.

III Eriksson, J., Larsson, A., & Nyberg, L. (2007). Item-specific training reduces prefrontal cortical involvement in perceptual awareness. Manuscript submitted for publication.

TABLE OF CONTENTS

INTRODUCTION .............................................................................................1BACKGROUND ...............................................................................................2

WHY BOTHER? ...................................................................................................... 2THE SUBJECT MATTER ......................................................................................... 3

Phenomenal consciousness .............................................................................. 4Access consciousness ...................................................................................... 5

THE PRESENT EMPIRICAL APPROACH ................................................................ 7CONSCIOUSNESS AND COGNITION .................................................................... 9

Unconscious cognition ...................................................................................... 9Attention and consciousness ..........................................................................12Working memory and consciousness .............................................................14The global workspace theory ..........................................................................15Long-term memory and consciousness ..........................................................16

A BRIEF REVIEW OF SOME NEURAL CORRELATES OF CONSCIOUSNESS ................................................................................................16

OBJECTIVES ................................................................................................20EMPIRICAL STUDIES ...................................................................................21

STUDY I - VISUAL CONSCIOUSNESS: DISOCIATING THE NEURAL CORRELATES OF PERCEPTUAL TRANSITIONS FROM SUSTAINED PERCEPTION WITH fMRI .....................................................................................21STUDY II - SIMILAR FRONTAL AND DISTINCT POSTERIOR CORTICAL REGIONS MEDIATE VISUAL AND AUDITORY PERCEPTUAL AWARENESS ......23STUDY III - ITEM-SPECIFIC TRANING REDUCES PREFRONTAL CORTICAL INVOLVEMENT IN PERCEPTUAL AWARENESS ..................................................26

GENERAL DISCUSSION ..............................................................................29HAVE I STUDIED WHAT I SAID I WOULD? ..........................................................30

Is it really neural correlates of consciousness? ...............................................30Is identification of a fragmented object really a visual experience? ................32

CONSCIOUSNESS AND COGNITION RECONSIDERED ......................................32Reconsidering the neglect syndrome .............................................................33Reconsidering previous neuroimaging research .............................................34Studies showing no fronto-parietal activity correlation ...................................35An alternative explanation ...............................................................................36Other considerations .......................................................................................37Implications .....................................................................................................38

A SYNTHESIS .......................................................................................................39LIMITATIONS AND FUTURE DIRECTIONS ..........................................................41CONCLUSIONS ....................................................................................................43

REFERENCES ...............................................................................................45

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INTRODUCTION

Our mental world is made up of (at least) two different kinds of processes: conscious and unconscious ones. As you read these words you are conscious of them, in the sense that you have a phenomenal experience of “seeing” them as black markings on a white background. You are also conscious of the meaning implied by these markings, as they are meant to convey information on a more abstract level (they are not pictures). However, you are probably not conscious of the mental processing taking place to transform the black markings into meaningful words (i.e. the process of reading). This process of identifying the various markings as letters, composing them into words and associating semantic content to them, is a highly trained skill that you most likely had to spend a significant amount of time to learn. But now you do it automatically and unconsciously. (You are of course conscious of the act of reading, just not the workings behind it). There is in fact a large amount of processing taking place in your brain right now that you have no experience of and which you could not describe or report if asked to do so (Kihlstrom, 1987). But what is the difference between conscious and unconscious processes, besides the obvious fact that you have a phenomenal experience of the former but not the latter? It is intuitively appealing to think that the parts of our minds that are conscious are largely what matters to us on a personal plane. It seems that if all my brain processes were unconscious I would lead a duller life, to say the least. Granted that there is a difference, how is this difference reflected in terms of brain processes? Is there some unique defining quality associated with conscious processing, or is it perhaps only a matter of quantity (would unconscious neural activity become conscious by being more vigorous)? This thesis intends to explore the relation between consciousness and the brain. This is done through three fMRI (functional magnetic resonance imaging) studies that explore what parts of the brain are activated when specific contents of consciousness are defined and maintained in various experimental settings.

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BACKGROUND

Why bother?

Consciousness has been a focus for studies on and off during the history of psychology (Leahey, 2000). Although studies of consciousness was an initial driving force for defining psychology as an independent discipline from philosophy, later trends such as behaviourism completely shunted the subject. Even though behaviourism had a strong negative effect on the acceptance of the study of consciousness there has been relevant empirical work done throughout the past century, although it was not always obvious that it was related to consciousness as such (Baars, 1988). However, the last decades have shown a strong escalation in the number of published scientific papers directly related to the subject, and a science of consciousness can now be said to be fair game (Baars, Banks, & Newman, 2003; Koch, 2004; Revonsuo, 2006).

“After almost a century of neglect, consciousness has become a major focus for research. Each month new findings appear in leading journals. In the coming century this new ferment is likely to reshape our understanding of mind and brain in the most basic way.”

(Baars & Banks, 2003, p. ix)

But how is our understanding going to be reshaped? What is it that we will find as we explore consciousness? Some say that consciousness is not important, that it is only an epiphenomenon and that studying it is a waste of time. But if we do not yet know its role in our psyche (and we don’t), these pessimists have nothing on their feet. Therefore, the perhaps most compelling reason to study consciousness is that unless we do, there will be a huge gap in our knowledge of the human mind. Furthermore, it is quite possible that other psychological concepts such as perception, memory, attention, etc, can never be completely understood without explaining their conscious features as well (Baars, 1988). There is also evidence indicating that we can do different things with conscious and unconscious information. For instance, conscious information is said to be more flexible and apt to be incorporated into a larger context (Dehaene & Naccache, 2001). Understanding the mechanisms behind conscious and

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unconscious information is vital to understand the different influences each kind of information can have on our behaviour.

The subject matter

The term “consciousness” can be used in a number of different ways that have different meanings. However, there are about as many ways to slice that pie as there are people writing about consciousness. This section is therefore not intended as a comprehensive account of the various uses of the word, but is only intended to explain the term enough for the purposes of this thesis. Here are the different meanings that I find relevant to distinguish:

i) Phenomenal consciousness means that a mental state is conscious if (and only if ) it is accompanied by phenomenal characteristics, if it is “something it is like” to have the state (Nagel, 1974). It is this sense of the word that will be relevant in this thesis and it will be further explored below.

ii) In reference to the global state of mind, being conscious simply means that you are awake as opposed to asleep or in a coma.

There is a double dissociation between phenomenal consciousness and wakefulness. First, you can have phenomenal experiences while asleep (dreams). Second, you can be awake but unconsciously process information. The distinction is sometimes also expressed as “state” vs. “content” consciousness, where the state kind is the degree of wakefulness and the content kind is phenomenal consciousness, since it always has content: you are conscious of x. However, I will use “state” more liberally, e.g. as in “a mental state is (phenomenally) conscious if…” or “to create a conscious state” (see e.g. Van Gulick, 2004, for a similar use of “state”).

Some have found it useful to create separate terms for self-consciousness (an egocentric perspective that contrasts you from other environmental entities, e.g. Zeman, 2001) and also meta-cognitive notions of consciousness (where the content of consciousness is another mental state, “a thought about a thought”,

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e.g. reflective consciousness, Revonsuo, 2006; extended consciousness, Damasio, 1999). Personally, I prefer not to treat self- and meta-consciousness as special kinds, but rather as forms of phenomenal consciousness. That is, when reflecting upon something we have a phenomenal experience of doing so and when “appreciating oneself ” we have a phenomenal experience of doing that. Hence, that kind of sub-division would to me be similar to separating visual consciousness from auditory consciousness and from somatosensory etc. The key difference between them is, as I see it, content and nothing else. While I am sure that there are certain brain regions specifically important for these kinds of phenomenal contents, I believe that when the mechanisms for any form of phenomenal consciousness is found they will apply to all forms. This is not a denial of potentially different cognitive functions related to the different terms, or of the usefulness of such differentiations in other theoretical contexts (i.e. different content can make a big difference for cognitive processing, Zelazo, 2004). It is only a statement that I find these distinctions irrelevant for present purposes, since self- and metacognitive notions can be considered as forms of phenomenal consciousness in all senses relevant to this thesis (see Figure 1).

Phenomenal consciousness

It is commonly agreed that phenomenal consciousness cannot be defined, although this of course depends on what you are willing to call “definition”. At the present state of knowledge I feel it safe to say that at least it cannot be defined analytically (Searle, 1998) or non-circularly (Block, 1995). Therefore, it may be more appropriate to call it a description rather than definition. As stated in i) above, phenomenal consciousness is the “what it is like”-ness of things. I do not consider this to be confined to raw sensory experiences but would also include thoughts, dreams, hallucinations, and feelings, including diffuse feelings such as anxiety or excitement. In short, anything that we have a phenomenal experience of. Throughout the thesis I will restrict the use of consciousness to mean only the phenomenal aspect and not the global state of mind or other possible connotations, unless specifically stated. I will also use the notion of awareness interchangeably with the notion of phenomenal

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consciousness. That is, when we become aware of something the content of consciousness has changed and a new conscious experience is instantiated (see Crick, 1994, and Koch, 2004, for a similar use). In the experiments presented below the participants become perceptually aware of an object at the moment they manage to identify it against a noisy background, thereby manifesting a new conscious mental state1.

There is a terminological issue not yet mentioned that has had an increasing impact on the consciousness literature: access consciousness. While my opinion is that this should not be treated as a separate kind of consciousness, this theoretical statement should be justified.

Access consciousness

Some (foremost the philosopher Ned Block) claim that we need to make a distinction between phenomenal consciousness and access consciousness. The latter sense is here restricted to certain aspects of consciousness, namely “reasoning and rationally guiding speech and action” (Block, 1995, p. 227). The reason for doing this split of terms is that Block wants to avoid the common association between consciousness and higher forms of “thinking”. I am sympathetic with this line of reasoning, but I do not feel that it is motivated to create a separate concept because of this. I do believe that parts of access consciousness are a kind of consciousness, but in my view these are subsumed by the concept of phenomenal consciousness. That is, I believe that higher order thoughts such as reasoning and planning can be accompanied by phenomenal characteristics and therefore be part of phenomenal consciousness. The major breaking point (for me) is that while Block argues that we can have access consciousness without phenomenal consciousness (Block, 2002), I do not. A state of mind that is completely devoid of phenomenal content does not count as a conscious state in my book (metaphorically and literally).

For some people the relation between consciousness and the cognitive components that Block reserves to access consciousness is so tight that � Hence,perceptualawareness,visualandauditoryawareness,visualandauditoryconsciousness,consciousexperience,consciousperception,andconsciousawarenessalldenotethesamething:phenomenalconsciousness.InthestudiesbelowIhaveusedthesenotionssynonymously.

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you cannot, according to them, have consciousness at all without access consciousness (Baars, 1988; Dehaene & Naccache, 2001; Naccache, 2006). Block, on the other hand, goes so far as to drop the connotation of “consciousness” all together and states that just “phenomenology” is adequate (Block, In Press). That is, while he acknowledges the link between access consciousness and higher order cognitive processes, his view of phenomenal consciousness is extreme in the opposite direction. The suggested switch in terminology (phenomenology instead of phenomenal consciousness) is, as I understand it, only a matter of emphasis and I find it agreeable because it makes less (implicit) assumptions about what phenomenal consciousness is and what it is for. When describing consciousness (e.g. as in the previous paragraph), one generally does not describe it in terms of functions but rather in terms of phenomenology, which is at the heart of the concept. However,

“phenomenology” is far from an all accepted terminology so I will stick with the traditional use throughout the thesis. I would also like to note that higher

Self- Meta- Global state(wakefulness)

AccessPhenomenal

Figure 1. Diagram showing my take on the relation among the different conceptions of consciousness. Phenomenal consciousness and consciousness as the global state of mind are different in the sense analogous to the difference between a mouse in the woods and a mouse used to navigate a computer: different things with the same label. Self-consciousness and meta-cognitive notions of consciousness are parts of phenomenal consciousness. Access consciousness is partially overlapping with phenomenal consciousness and the disjunctive part (dotted line) is viewed as unconscious.

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order cognitive processes may well turn out to be important or even essential for consciousness, but I do not think that this should be assumed by default.

In sum, I prefer to reduce the various connotations of consciousness into two separate meanings: phenomenal consciousness and consciousness as a global state of mind (Figure 1). I am reluctant to make further distinctions within phenomenal consciousness because those distinctions often involve commitment to one or several cognitive functions. At present I wish to avoid the prior assumptions this would involve.

The present empirical approach

If you look back at the description of consciousness above, you will see that it depends on the knowledge and imagination of the reader (you). This is because it refers to a subjective view-point that is inaccessible to others (Nagel, 1974). Hence, when I describe phenomenal consciousness as the experiences we have when we see, hear, feel, etc., you will not know what I’m talking about unless you are able to have these experiences yourself. Try telling a man born blind what green looks like… The dependence on subjective view-points does not, however, prevent us from studying consciousness empirically and scientifically (Searle, 1998), though it does make us dependent on the reporting of such experiences, verbal or otherwise (Dennett, 2005). That is, unless you tell me what you are conscious of I will not know. To ensure myself that you are conscious of what I think you are conscious of, I can use two “comforters”: similarities in behaviour and similarities in physiology (Palmer, 1999). I can be fairly sure that you are in pain if you stub your toe, scream “gosh, that hurts!” and jump around, because that’s the behaviour that I would have displayed if I were in pain from stubbing my toe. This confidence is increased by my knowledge that you and I have similar nervous systems that wires pain receptors in the toe to relevant areas in the brain. I must of course submit to the fact that no one can know for sure what another person is conscious of2. However, to conclude from this that consciousness � Atleastnotwithoutaccesstotheperson’sbrainstate.Ithasinfactbeendemonstratedrepeatedlythatthecontentofconsciousnesscanbe“readout”frombrainactivity(Brown&Norcia,�99�;Haynes&Rees,�00�;Kamitani&Tong,�00�,�00�;Kreiman,Koch,&Fried,�000;O’Craven&Kanwisher,�000).

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cannot be studied is for most practical purposes just silly. In the experiments presented below I will assume that a participant is conscious of x when he/she tells me so (verbally or through agreed upon signals such as button presses). It is hence relatively easy to establish that a subject is conscious of x. It is harder to establish that the subject is unconsciously perceiving x (Merikle, Smilek, & Eastwood, 2001), but that will not be of major concern in this thesis.

If one wants to describe consciousness in terms of brain activity, it seems reasonable to consider consciousness to be completely determined by the physiology of the brain. This “astonishing hypothesis” (Crick, 1994) means that there is no need for anything extraphysical to explain the phenomenon of consciousness. Consciousness is hence determined by its physical implementation, and there cannot be a change in a conscious state without a corresponding change in the physical system implementing that conscious state. While a causal explanation of consciousness is the ultimate goal of its empirical investigations, we are still far from achieving it. To get a science of consciousness off the ground, it has been suggested that we look for the neural correlates of consciousness (NCC) and use this as a framework (Crick & Koch, 2003; Frith, Perry, & Lumer, 1999). Therefore, while describing what brain activity that is correlated with a conscious percept wouldn’t necessarily explain consciousness, it is a good starting point. Indeed, it is the best starting point I can think of.

Brain activity can be described at many different levels. Crick and Koch (2003) are pushing for a description of the NCC at the neuronal level, but there are a few difficulties related to measuring brain activity in this detail. One is that we are mainly interested in the consciousness of human beings, and while single-cell recordings can be made on humans in relation to certain rare neurosurgical procedures, they are mostly done on experimental animals. Personally, I am willing to assume that primates are conscious and that our nervous systems are similar enough to be comparable in terms of perceptual awareness. However, using human subjects is preferable because it avoids the problem of animal consciousness (Dennett, 1999). Another problem is that while single-cell recordings have an extremely high spatial and temporal resolution, it is limited to measuring a very restricted area of the brain at any given time. It is quite possible that consciousness depends on the cooperation between different brain areas (Lumer & Rees, 1999), a scenario that single-

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cell recordings will have trouble detecting. Based on these arguments, it seems reasonable to parallel the search for the NCC with an instrument that measures brain activity at a global level. While fMRI (functional magnetic resonance imaging) does not have spatial resolution matching single-cell recordings, it is the best non-invasive alternative with a possible resolution of a few millimetres. Moreover, it has the capacity to measure the whole brain simultaneously, and is preferably done on human subjects. The temporal resolution is fairly limited however, and fMRI is therefore unable to measure neural synchronization and oscillation (or at least to identify it as such), aspects of neural activity that has been hypothesized to be important for consciousness (Singer, 2000, but see Rolls, In Press, for an opposing view). Nevertheless, fMRI seems like an excellent measuring device to characterize what parts of the brain that are important for consciousness, and also how these parts interact. This is the empirical method used in the present thesis.

Consciousness and cognition

As the attempt to specify what consciousness is may imply, we do not yet know what function, if any, consciousness has within the cognitive architecture of our brains. However, contrasting conscious and unconscious processing may give suggestions to what conscious processing is for. I will here also briefly discuss other cognitive constructs that are frequently associated with consciousness.

Unconscious cognition

We appear to be able to process information to a great extent even if it is unconscious. The degree of unconscious perceptual processing has been rather controversial over the years (see Kouider & Dehaene, 2007, for a recent review), but it seems that new object representations can be created (Mitroff & Scholl, 2005) and processed to the extent that its emotional (Morris, Ohman, & Dolan, 1998; Naccache, Gaillard et al., 2005; Williams, Morris, McGlone, Abbott, & Mattingley, 2004) and semantic (Dehaene & Naccache, 1998;

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Gaillard et al., 2006; Luck, Vogel, & Shapiro, 1996) content is extracted without awareness of the stimulus. Unconscious processing is not confined to perception, but also includes motivational incitement (Pessiglione et al., 2007), planning and execution of actions (Binsted, Brownell, Vorontsova, Heath, & Saucier, 2007; Dehaene & Naccache, 1998), and even cognitive control (Lau & Passingham, 2007). Indeed, it has been argued that almost all cognitive processes can proceed unconsciously, with the exception of willed action (Kihlstrom, 1987). Conscious information may thus be used in deliberate behaviour, while unconscious information is limited to routine behaviour: “…information perceived without awareness leads to more automatic reactions that cannot be controlled by the perceiver.” (Merikle et al., 2001, p. 126). This implies that conscious information can be used more flexibly, possibly by taking more information into consideration. Consider for example the exclusion task, where the participant is instructed to complete a partial word, e.g. “tab__”, with anything but a prime, e.g. “table” (Debner & Jacoby, 1994). If the participant is aware of the prime the task is simple. But if the prime is presented too fast to support conscious perception of it, it is likely that the prime is used to complete the word despite the explicit instructions not to do so. That is, unless the participant has consciously perceived the prime, he/she is unable to adjust the behaviour appropriately.

Another suggestion of differences between conscious and unconscious information is that only conscious information can be sustained over a longer period of time (Dehaene & Naccache, 2001). This is supported by work showing that unconscious priming decays rapidly (Greenwald, Draine, & Abrams, 1996), and that behaviour based on previously acquired information almost exclusively uses information that have been processed consciously (Gentilucci, Chieffi, Daprati, Saetti, & Toni, 1996; Hu & Goodale, 2000). While there have been reports of long-lasting memory of information presented during anesthesia (Merikle & Daneman, 1996), this has been criticized due to uncontrollable variations in the depth of anesthesia (Baars, 2002). Direct empirical investigations of the longevity of unconscious information is sparse, and although at least 2 reports claim to have found long-lasting effects, the evidence is as of yet unconvincing (e.g., not peer-reviewed, Merikle & Smith, 2005, or using crude methods to establish the absence of conscious perception, Sohlberg & Birgegard, 2003). This does not need to imply that unconscious

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processes cannot have a significant impact on behaviour beyond the immediate present. But it indicates that information must have been conscious at some point in time for it to be of behavioural significance beyond the here and now. This view is, however, probably too simplistic. Take again the example of reading. At first, you are painfully aware of each letter, how it is pronounced and how they connect to form a word. As your reading skills progress you become increasingly less aware of the details behind it all, and by the time you graduate from school it is all done automatically. This is not how you learn to see, hear, or move etc. You were never conscious of the processes leading up to a visual percept and you can never ever become aware of these processes. So, there must be some other feature(s) than sustainability per se that differs between conscious and unconscious information. We may then modify the statement, stating instead that active information must have been conscious at some point in time for it to be of behavioural significance beyond present time. That is, we need to acknowledge that vast amounts of information are latently present in the hardwiring of the brain and that this information is inaccessible to consciousness, although it clearly affects our behaviour.

It is interesting to note that the former two suggestions of the effect of having had a conscious experience of a stimulus, i.e. willed/deliberate action and flexibility in use of information, may depend on and in some sense be reduced to the last one: sustainability. That is, the flexibility and deliberation of behaviour (and thought) may be the result of being able to sustain information over time (see Courtney, 2004, for a similar view). All in all, it is still unclear what the defining characteristic of conscious information processing is, although the above discussion is suggestive.

It should be noted that differences between conscious and unconscious cognition do not necessarily give us any information on what makes a state conscious. While theories have been (at least partially) built upon the differences discussed above (Baars, 1988; Dehaene & Naccache, 2001), it does not follow logically that the functions implied by the conscious/unconscious contrasts is relevant for the creation of consciousness. It may be that these functions depend on consciousness, but not vice versa. For example, it is possible that consciousness is a prerequisite for global accessibility (see below), but this does not necessarily mean that the mechanisms of global accessibility are the mechanisms of consciousness. It should perhaps also be stated that

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some theories equates consciousness with a certain function (e.g. Dennett, 2001). That is, global accessibility is consciousness. However, while admittedly possibly correct, this does not seem to explain consciousness to a satisfactory extent. The limitations of functionalistic descriptions of consciousness has been elaborated on extensively (e.g. Block, 1995; Nagel, 1974; Revonsuo, 2006), and I refrain from doing this here. My personal view, in short, is that it can be of great value to consider different functions of consciousness to make theoretical progress, but at the end of the day it seems slightly inadequate. This may of course be because no proposition has yet quite “hit the spot”. I know of no convincing formal reasons why functionalism could not explain consciousness, only intuitive ones. Furthermore, finding out what function consciousness effectuates is one of the major driving forces for studying it. However, I am inclined to think that we need a biological/mechanistic explanation before we can evaluate a functionalistic one properly.

Attention and consciousness

There is compelling evidence that attention and consciousness are closely interrelated. For example, attention can enhance the phenomenal aspects of vision (Carrasco, Ling, & Read, 2004; Fuller & Carrasco, 2006; Gobell & Carrasco, 2005; Tse, 2005). That is, it seems that when your attention is drawn to an object, you will see the object clearer, with more contrast, and in more vivid colours. Moreover, several behavioural studies indicate that attention may be an important constituent for conscious awareness. For example, patients with a right-sided lesion in parietal cortex have trouble using information on their left side of the world, a condition called unilateral neglect (see Driver & Mattingley, 1998, for review). Illustratively, when asked to copy a drawing they tend to ignore the left part. The affliction is not sensory related: the patient can sometimes “discover” the left side world by turning around (i.e. making what was their left side their right, Sacks, 1992) or by having someone explicitly pointing at the left side of a drawing. Usually the affliction is explained as a deficit in spatial attention, meaning that the patient cannot aim the “attentional spotlight” to the left and therefore cannot become aware of that side of the world. Other examples of the importance

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of attention for awareness are attentional blindness (Mack & Rock, 1998), where a stimulus that is not attended during a challenging task seems to be unable to reach awareness, and the attentional blink (e.g. Luck et al., 1996). In the attentional blink paradigm a fast series of items are presented to a subject. The task is to detect a first target item and then, within different time periods, detect a second target. If the second target is presented within a window of 100 - 500 ms after target 1, its detection will be severely reduced, presumably because attention is serial and has limited capacity. That is, if attentional recourses are temporarily busy, awareness is reduced.

Although the link between attention and consciousness is tight, it is important to remember that these concepts are distinct (Baars, 1997; Koch & Tsuchiya, 2007; Lamme, 2003; Lamme, 2004). Empirical support for this is that there can be attentional effects on unconscious stimuli (Jiang, Costello, Fang, Huang, & He, 2006; Melcher, Papathomas, & Vidnyanszky, 2005; Melcher & Vidnyanszky, 2006; Montaser-Kouhsari & Rajimehr, 2004; Naccache, Blandin, & Dehaene, 2002; Sumner, Tsai, Yu, & Nachev, 2006; Woodman & Luck, 2003). For instance, attention can be directed toward a specific location and modulate processing of invisible objects at that location (He, Cavanagh, & Intriligator, 1996). There have also been demonstrations of separable and independent electrophysiological correlates of attention and consciousness (Koivisto & Revonsuo, 2007; Koivisto, Revonsuo, & Lehtonen, 2006; Koivisto, Revonsuo, & Salminen, 2005).

It is also important to note that attention is not a unitary concept. It is therefore possible that the relation between consciousness and attention differs depending on what form of attention one is talking about. While attention is generally thought of as a selection mechanism that promotes certain processes over others, this can be achieved in a bottom-up manner (extrinsic, stimulus driven attention) or in a top-down manner (intrinsic, willed, controlled attention). The effect attention has on the very phenomenal character of things (see above) has mostly been demonstrated for extrinsic attention, and attempts at similar effects from intrinsic attention has generally been fruitless (Prinzmetal, Nwachuku, Bodanski, Blumenfeld, & Shimizu, 1997), except when using very specific types of stimuli (Tse, 2005). There is also a division of attention regarding what feature that it is supposed to work on: locations in space or objects. It seems that spatial attention can be affected by unconscious

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stimuli in a bottom-up manner (Jiang et al., 2006; Woodman & Luck, 2003), but can only be directed top-down towards consciously perceived stimuli (Kanai, Tsuchiya, & Verstraten, 2006). Object-based attention seems to be controlled by both bottom-up and top-down processes, regardless of whether stimuli is consciously perceived or not (Kanai et al., 2006; Soto & Humphreys, 2006). It is unclear why different aspects of attention should have different effects on conscious vs. unconscious information, but it is an interesting discrepancy that may in the future contribute with a better understanding of consciousness as such.

Working memory and consciousness

While it is clear that at least a subset of the content of working memory (WM) is conscious (Baars & Franklin, 2003), the exact relation between consciousness and WM is often left unspecified (Shah & Miyake, 1999). However, the proposal that only conscious information can be sustained over a longer period of time suggests that WM and consciousness are interrelated, since this is a hallmark of WM. “The theoretical concept of working memory assumes that a limited capacity system, which temporarily maintains and stores information, supports human thought processes by providing an interface between perception, long-term memory and action.” (Baddeley, 2003, p.829). It may be, of course, that the often assumed association is due to this sustainability factor, but since it does not infer a necessary or directional link it often evades an explicit formulation. It is usually simply stated that the active component of WM is conscious, period.

There are, however, exceptions to this bypass. For example, Baddeley and Andrade (2000) proposes that not only is the (total) content of WM conscious, WM is essential for consciousness (see also Baddeley, 2003). While the formulations are somewhat fleeting, I take this to mean that WM is a requirement for consciousness. This contrasts with Baars and Franklin (2003), stating instead that only a subset of the processes related to WM are conscious. However, these parts are fully dependent on consciousness as this is meant to work as the medium through which these processes are instantiated. That is, consciousness is a requirement for WM functions. In

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this theory consciousness creates a global workspace that, among other things, can accomplish the functions of WM. While these two views of WM and consciousness seem to diverge, it is worth noting that the episodic buffer, a component of WM that is meant to work as an integrator of various kinds of information, has been suggested to be identical with the global workspace (Baddeley, 2003).

The global workspace theory

The global workspace (GW) is a relatively recent psychological construct that is meant to be specifically related to consciousness (Baars, 1988; Baars, 2002). In its most general form, the GW is a system for information distribution where local and specialized processing units can share their information through a common element, the global workspace. This information distribution is instantiated by consciousness. Hence, the primary function of consciousness, according to this theory, is to broadcast information to the system as a whole.

While Baars has focused more on the functionalistic description of the GW, others have elaborated on its possible neural implementation (Dehaene & Changeux, 2004; Dehaene & Naccache, 2001). The global neuronal workspace (GNW) theory is based on two major system divisions: the network of processors and the GNW. This translates directly to Baars conception of parallel, distributed modules that specialize in specific kinds of information and that work unconsciously (the network of processors), and the GW that connects these modules through the medium of consciousness (the GNW). The GNW consists of long-distance connected neurons that, while linking basically all cortical processors, are more densely packed in dorsolateral prefrontal, inferior parietal, and cingulate cortices (Dehaene & Changeux, 2004). Moreover, the GNW explicitly states that no consciousness can occur without attention. Attention is hypothesised to be the prime constituent for the creation of a conscious state, because it “ignites” and sustains neural activity in the local processors to the required level. Hence, GNW makes specific predictions about relevant localized neural activity in relation to consciousness which I will return to in the general discussion.

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Long-term memory and consciousness

Long-term memory (LTM) can be crudely divided into explicit (or declarative) and implicit (non-declarative) memory, based on whether or not the retrieval phase involve conscious recollection. This categorization says nothing, however, about the nature of the encoding phase, nor about the storage phase. Given the previous discussion on the limitations in durability of unconscious information processing, it may be assumed that encoding is always conscious. By contrast, LTM storage can be seen as a paradigm example of unconscious cognitive content (Baars et al., 2003). Hence, consciousness always interacts with LTM at the input stage and, depending on the type of memory, at the output stage. Moreover, it has been suggested that the nature of the content of consciousness dictates what type of memory a person can have (Perner & Ruffman, 1995; Wheeler, 1999; Zelazo, 2004). For example, young children that lack the capacity to be aware of and reflect upon themselves as “I in relation to the world” (i.e. autonoetic consciousness, Tulving, 1985) are unable to form episodic memories. The episodic buffer component of working-memory has been suggested to be the (conceptual) structure of interaction between consciousness and LTM (Baddeley, 2000), where the memory content is made conscious by being “cached” in to the buffer (Baddeley, 2003).

While information from LTM may assist in various perceptual processes (Bar et al., 2006), it is unlikely that LTM is a necessary constituent for consciousness (unless, of course, the content of consciousness is a memory) since there is no reason to believe that novel stimuli cannot be consciously perceived (but perhaps not categorised).

A brief review of some neural correlates of consciousness

There are several strategies available to investigate the neural correlates of consciousness. The goal is to ensure that the brain activity found to correlate with conscious awareness cannot be accounted for by changes in stimulation or changes in behaviour. A common way to accomplish this is to create a condition where the same stimulus parameters can yield both conscious and non-conscious perception. For example, if you present a different picture to

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each eye the percept will not be a blend of the two. Instead, it will fluctuate, with one picture dominating for a period and then changing into the other picture and so on, a phenomenon called binocular rivalry (Lumer, Friston, & Rees, 1998; Tong, Nakayama, Vaughan, & Kanwisher, 1998). A similar but less striking effect can be achieved with ambiguous stimuli like the Necker cube or the old woman/young lady picture (Kleinschmidt, Buchel, Zeki, & Frackowiak, 1998; Sterzer, Russ, Preibisch, & Kleinschmidt, 2002). Alternatively, stimulus presentation can be close to perceptual threshold, e.g. by using short durations and/or masking, and thus make the stimulus visible on some trials and invisible on others (Bar et al., 2001; Dehaene et al., 2001; Grill-Spector, Kushnir, Hendler, & Malach, 2000).

A second strategy is to divert attention away from the target object and thereby render it invisible (see previous descriptions of attentional blindness and the attentional blink). Since this manipulation is not 100 % effective it can be adjusted to produce successful identification on about half the trials, thereby creating suitable comparison conditions (Marois, Yi, & Chun, 2004; Sergent, Baillet, & Dehaene, 2005). A third option is to use illusions. Here the stimulus parameters are not producing the percept that would be predicted from its low-level features. By changing these features in a way that spoils the illusion but keeps the features comparable, it is possible to separate brain activity related to conscious perception apart from stimulus presentation (Blankenburg, Ruff, Deichmann, Rees, & Driver, 2006; Watkins, Shams, Tanaka, Haynes, & Rees, 2006). It is also possible to use various after-effects (Barnes et al., 1999; Taylor et al., 2000). For example, if you look at a revolving spiral pattern for a while and then look at a stationary pattern, it will seem as if the pattern “comes alive” and you perceive motion even though nothing is actually moving. In addition to these strategies, information can also be obtained from investigating various neuropsychological disorders (see Rees, 2001, for review), such as unilateral neglect (see description above). The most consistent finding across all previous research is that sensory cortices are activated for conscious perception (all references, with no exceptions, from previous paragraph). Furthermore, the specific content of consciousness is reflected in subparts of sensory cortex devoted to that specific feature. For example, perception of faces during binocular rivalry activates face-specific parts of the fusiform gyrus (Lumer et al., 1998; Tong

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et al., 1998), while perception of the rivalrous stimuli (moving gratings in Lumer et al. and houses in Tong et al.) activates motion-related and place-related parts respectively. Additional evidence of the involvement of sensory cortices comes from studies of neural activity during hallucinations and imagery, which also activates content specific regions (ffytche et al., 1998; Kosslyn, Ganis, & Thompson, 2001; Shergill et al., 2001). That is, if you imagine or hallucinate hearing something, auditory cortex will be activated, etc.

While few, if anyone, questions the importance of sensory cortex for conscious sensory content, the involvement of primary sensory regions has been more controversial (see Rees, 2007; Tong, 2003, for reviews). The early investigations using binocular rivalry etc. did not find that conscious perception correlated with primary visual cortex (V1) activity (Lumer et al., 1998; Sheinberg & Logothetis, 1997; Tong et al., 1998). However, later research has demonstrated that this may have been due to the nature of the stimulus used (Polonsky, Blake, Braun, & Heeger, 2000; see also Lee, Blake, & Heeger, 2005; Meng, Remus, & Tong, 2005; Muckli, Kohler, Kriegeskorte, & Singer, 2005; Murray, Boyaci, & Kersten, 2006; Tong & Engel, 2001). Indeed, there have now even been demonstrations of activity in the lateral geniculate nucleus (thalamus) correlating specifically with conscious perception (Haynes, Deichmann, & Rees, 2005; Wunderlich, Schneider, & Kastner, 2005). While the possibility of correlated activity in early sensory regions is now established, it is still unclear if activity in these regions is necessary for conscious perception. A recent TMS (transcranial magnetic stimulation) study indicates that this is so. Silvanto and colleagues (Silvanto, Lavie, & Walsh, 2005) showed that if V1 activity is disrupted by TMS either before or after the time-window where V5 is activated by a moving stimulus, motion perception is disrupted. Importantly, if V1 is disrupted during this time-window perception is unaffected. Hence, V1 is not only important as a

“cable” leading information from the eyes to higher brain regions. Feedback from V5 back to V1 is evidently also necessary (see also Pascual-Leone & Walsh, 2001; Silvanto, Cowey, Lavie, & Walsh, 2005). However, it is unclear to what extent this generalizes to other stimuli, situations, and modalities. For example, it has been suggested that the fact that damage to V1 does not lead to a total cessation of visual dreaming implies that V1 cannot be necessary for

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visual consciousness per se (Revonsuo, 2006). The systematic study of the neural correlates of consciousness is obviously

central, but it is also important to find out how these differ from other kinds of neural activity (Frith et al., 1999). For example, it is relevant to compare neural correlates of consciousness with those of unconscious processing. It has been demonstrated that basically all parts of the visual cortex can be activated by unconsciously perceived stimuli (Dehaene et al., 2001; Fang & He, 2005; Haynes, Driver, & Rees, 2005; Marois et al., 2004; Moutoussis & Zeki, 2002; Moutoussis & Zeki, 2006; Rees et al., 2000). Therefore, neural activity in these regions cannot by itself be sufficient to produce conscious visual perception. However, Zeki has proposed that awareness of each perceptual feature (e.g. motion, colour, shape, etc.) is created within the dedicated perceptual architecture (Zeki, 2001, 2003). When conscious, these features constitutes “micro-consciousness” that are independent of each other and of higher cortical regions. The difference between conscious and unconscious activity, according to this theory, is quantity. That is, if activity reaches a certain threshold level it becomes conscious. This is supported by several fMRI studies showing that the level of activity for unconsciously processed stimuli is weaker than activity for consciously processed stimuli (Dehaene et al., 2001; Lee, Blake, & Heeger, 2007; Marois et al., 2004; Moutoussis & Zeki, 2002; Moutoussis & Zeki, 2006; Vuilleumier et al., 2001; Zeki & Ffytche, 1998). However, it has been suggested that results from event-related potential (ERP) studies presents opposing evidence (Dehaene, Changeux, Naccache, Sackur, & Sergent, 2006). While at least two studies have demonstrated equal levels of activity for specific ERP components (Sergent et al., 2005; Vuilleumier et al., 2001), it is unclear how these components relate to consciousness. Specifically, it was the early components that had similar amplitude while later components diverged, again showing larger amplitude for consciously perceived stimuli. It is far from clear at what point in time conscious awareness is instantiated, and if this were to be at a late stage (e.g. Bachmann, 2000; Del Cul, Baillet, & Dehaene, 2007; Libet, 1965; Sergent et al., 2005), demonstrations of equal level of activity at earlier stages would constitute no evidence against the hypothesis. Indeed, using the time of differential amplitude is the most straightforward way to infer when in time consciousness occurs. The only direct evidence against the level of activity hypothesis comes from an fMRI

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case study of unilateral neglect, where activity level in extrastriate cortex of patient G.K. was comparable for extinguished and seen stimuli (Rees et al., 2000). How generalizable this is to other individuals with neglect and to normal individuals needs to be further explored. Also, it is interesting to note that while there was no statistically significant difference, the trend in the data point in the direction predicted by the level of activity hypothesis (see Figure 3 in Rees et al., 2000).

It has been noted that the majority of research papers reporting whole brain imaging results have reported frontal and parietal cortex activity in addition to sensory related activity (see Naghavi & Nyberg, 2005; Rees, 2007; Rees, Kreiman, & Koch, 2002, for reviews). Based on this observation it has been suggested that the addition of fronto-parietal activity may be what differs between conscious and unconscious brain activity, rather than level of activity. There are, however, exceptions to this pattern, which I will return to in the general discussion. The fact that a vast array of empirical work has demonstrated consciousness-correlated activity in higher order cortical regions has also fuelled the interest in access consciousness, as described above, and also models that integrate this finding such as the global workspace theory and its physiologically elaborated version (the global neuronal workspace).

OBJECTIVES

A general aim of all three studies in this thesis was to further elucidate the relation between consciousness and the neurophysiology of the brain. The specific objective of Study 1 was to investigate the possible distinction in how the brain implements different temporal aspects of consciousness. The objective of Study 2 was to see how generic previously described activation patterns are in relation to consciousness in different sensory modalities. Finally, the objective of Study 3 was to further investigate the nature of the prefrontal cortical activity found to be common across modalities in Study 2.

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EMPIRICAL STUDIES

Study 1

Whereas the majority of studies of the neural correlates of consciousness has focused on the generation of perceptual awareness (i.e., activity correlated with perceptual shifts), a few others have investigated whether different brain activity is required to sustain a particular percept in mind. The separation of different temporal profiles of brain activity has proven beneficial by providing additional information on what kinds of processes that are related to various cognitive tasks (Donaldson, 2004). Portas and colleagues (Portas, Strange, Friston, Dolan, & Frith, 2000) used random dot stereograms (RDS) as stimuli in an object identification task. Unlike most other perceptually unstable stimuli, the RDS percept can be sustained for a relatively long period of time. Therefore, brain activity specifically related to identification and sustained perception could be separated analytically within trials.

The results from Portas et al. associated perceptual identification with frontal, parietal, and occipito-temporal (ventral visual) regions, whereas sustained perception engaged a distinct dorsolateral prefrontal region as well as the hippocampus. Kleinschmidt and colleagues (Kleinschmidt, Buchel, Hutton, Friston, & Frackowiak, 2002) used a phenomenon called perceptual hysteresis, where identification of an object in a low-contrast stimulus allowed the participant to sustain perception below the initial identification contrast level (i.e., once you see it you can tolerate a more degraded stimulus). By comparing the condition before and after identification, Kleinschmidt et al. could control for stimulus parameters and characterize brain activity specifically related to perceptual shifts and sustained perception. In line with Portas et al., medial temporal lobe (MTL) activity was found to correlate with sustained perception rather than identification. However, unlike Portas et al. there was also pronounced similarities in activity between identification and sustained perception in fronto-parietal and ventral visual regions. Moreover, MTL activity has also been implicated in relation to perceptual identification (Kreiman, Fried, & Koch, 2002). Earlier research is hence inconclusive of which regions should be attributed to what temporal aspect of perception.

To further investigate this issue we used fragmented pictures in an object

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identification task (Figure 2a). The participants were asked to view the fragmented pictures and press a button upon identification3. A brief tone appeared when the button was pressed, and reappeared 10 s later. Participants were instructed to make a second button press when the tone reappeared, thereby creating a unique activation profile for the motor response, identification, and also sustained perception following identification (Figure 2b). This paradigm makes it possible to correlate brain activity with each activation profile and find regions specifically activated for each effect.

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Figure 2. a) An example fragmented picture, where a small bird is made out of a subset of green lines. b) Stimulus onset and identification is separated by a delay created by the difficulty in identifying a fragmented object. Each effect of interest can be dissociated by modelling unique activation profiles and then correlating brain activity with each profile: M = motor response, I = identification, SP = sustained perception.

Identification was related to increased activity in ventral visual, frontal, and parietal regions (Figure 3), and also MTL. Although the specific loci were separate, sustained perception also activated ventral visual and fronto-parietal regions. There was also significant activity increase in cingulate cortex and posterior temporal cortex. Results from previous research on sustained perception (Kleinschmidt et al., 2002; Portas et al., 2000) motivated a closer look at MTL, and a more liberal statistical criterion revealed additional activity in a MTL region, slightly posterior to the one seen during identification.

3 In the original article (Eriksson, Larsson, Riklund Åhlström, & Nyberg, 2004), we used the term ”pop-out” to denote the moment of identification. The reason for this was mainly to be consistent with the terminology of Portas et al. and Kleinschmidt et al. It simply refers to the subjective characteristics of the sudden Aha! feeling often experienced at the moment of identification and did not intend to imply that the underlying processes were automatic, bottom-up etc.

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Identification Sustained Sensorimotor

Figure 3. Lateral view of the brain showing activity for the three effects of interest in Study 1.

The results provide further evidence for a difference in how the brain implements perceptual identification compared to how it sustains a particular percept over time. However, there was also considerable overlap between conditions in ventral visual and fronto-parietal regions. Possibly, activity in some of the regions engaged during identification must be maintained to enable sustained perception. Study 1 thus provides additional evidence for fronto-parietal involvement in visual awareness by showing that it is also associated with sustained perception. It also adds a category of stimuli that can be used to probe the neural correlates of consciousness. The generality of the fronto-parietal activation pattern was further investigated in Study 2.

Study 2

Fronto-parietal activity is related to awareness of a number of different visual stimuli; objects: (Portas et al., 2000); words: (Dehaene et al., 2001; Kjaer, Nowak, Kjaer, Lou, & Lou, 2001); motion: (Williams, Elfar, Eskandar, Toth, & Assad, 2003); flicker: (Carmel, Lavie, & Rees, 2006). It is therefore reasonable to think that the fronto-parietal regions are related to more general cognitive processes than processes in the stimulus specific regions (e.g. specific parts of the fusiform gyrus for face processing). To see if this supposed

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generality would hold for other sensory modalities, we used auditory stimuli in a paradigm that is otherwise very similar to the one used in Study 1. Neural correlates of auditory awareness is a new area of investigation where no systematic studies have been done previously. The stimuli consisted of animal sounds that were initially drowned in noise. The noise level was then successively lowered until identification occurred, i.e. until the participant came to insight of what he/she was listening to. Noise level was then held constant during sustained perception. As in Study 1, two button presses were also executed: one signifying identification and the other working as a motor control. This again created unique activation profiles that could be separated analytically. A switch in background screen colour was used to indicate when the second button press should occur, analogous to the tone in Study 1. A colour switch also occurred at the first button press to make response conditions similar.

The results showed that auditory cortex and frontal regions were activated for auditory identification. However, no parietal cortex or MTL activity was found. At a more liberal statistical threshold some parietal activity appeared. To further investigate the difference between visual and auditory awareness, a second experiment was conducted with both auditory and visual trials, thereby replicating both Study 1 and experiment 1 of Study 2. The results from experiment 2 showed that whereas fronto-parietal and ventral visual regions were again activated for visual awareness, only superior temporal (auditory) cortex and frontal regions were activated for auditory awareness (Figure 4). A conjunction analysis, which formally characterized similarities between modalities, showed exclusively frontal regions jointly activated for perceptual identification. A similar analysis for sustained perception revealed a more distributed network of brain regions, including parietal cortex. MTL activity was significant for both identification and sustained perception, for both modalities.

It seems that perceptual identification engages common frontal regions that interact with modality specific posterior regions to produce awareness. An amodal network of fronto-parietal regions is then activated to maintain the specific percept over time. The results from previous research indicating parietal cortex as important for conscious awareness may hence be restricted to visual stimuli. Parietal cortex has been implicated in a number of cognitive

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functions, e.g. attention (Kanwisher & Vojciulik, 2000), working memory (Baddeley, 2003), and spatial processing (Colby & Goldberg, 1999), and it is unclear what function would be differently involved in auditory and visual awareness. Possibly, parietal activity for identification of visual targets reflects a redistribution of spatial attention, something that is not needed for auditory stimuli since they lack spatial features in the present setup. The prefrontal cortical activity at identification could be reflecting integration of information sent by posterior regions (Baddeley, 2000; Frith & Dolan,

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Figure 4. Lateral view (top right) of left and right hemispheres with auditory (red) and visual (green) activations from experiment 2 in Study 2. Blue regions designate results from the conjunction analysis, showing common activity across modalities. Diagrams show group mean effect size in selected regions. The left part of the figure shows activations projected on flat maps. Comparison of brain activity related to identification of auditory and visual stimuli showed that ACC (A) and lateral PFC (B) were similarly activated for both modalities, whereas parietal (C) and occipitotemporal regions were exclusively activated for visual awareness and superior temporal cortex (D) exclusively for auditory awareness.

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1996), or it could involve attentional or other cognitive control processes (Miller & Cohen, 2001). The specific nature of prefrontal activity was further investigated in Study 3.

Study 3

Given that a large number of empirical reports have noted frontal and parietal cortical activity related to consciousness (see above), and the results from Study 2 showing that frontal regions are more generally involved in the creation of a conscious percept than parietal regions, a logical next step was to ask how the prefrontal regions are related to this process. To this end we again used the fragmented pictures, but this time asked participants to practice on identifying a subset of these pictures before entering the scanner. Specifically, some items were presented 12 times (T12) and some were presented 60 times (T60) during training. We did not include sustained perception in the design since that would have taken up too much time. If the training manipulation did not change the activity level in prefrontal cortex (PFC), it would imply that PFC works mainly as a receiver of information that is created in posterior, sensory related regions (Baddeley, 2000; Frith & Dolan, 1996). If on the other hand PFC activity level decreases for previously trained items, this would suggest that PFC has a more active role in defining the contents of consciousness, since the trained items would require less work in the identification process.

While a general trend in the data was that the effect of training was more pronounced for T60 than for T12 items, the difference was not formally significant for either behaviour (time to identification) or for brain activity level. To simplify, I will therefore treat them together throughout the rest of the summary. Identification of novel items (compared to a low-level baseline) increased activity in a number of brain regions, including occipitotemporal, parietal, lateral and medial PFC (Figure 5). Hence, this activation pattern was replicated for the third time (in Study 1, 2, and now 3), demonstrating great stability in these results. Trained items showed a strong reduction of brain activity extent. Overall, brain activity was reduced to about 23 % of that for novel items. In the PFC, activity extent was reduced to about 12 %. Moreover,

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these results were specific for the moment of identification as practically no activity decrease was evident for the period preceding identification. While brain activity changes due to previous exposure has been extensively documented before (see e.g. Cabeza & Nyberg, 2000; Henson, 2003, for reviews), this is the first empirical investigation that demonstrates training effects specifically related to conscious awareness of object identity.

To further investigate the amplitude of the activity change we performed a region of interest (ROI) analysis based on results from Study 2. This showed a strong reduction of activity in all frontal ROIs as a result of training. Together these results indicate that the interplay between the PFC and posterior regions is reduced for trained compared to novel items. To formally investigate this we also performed an analysis of their functional connectivity, which is a way to measure how different brain regions interact to cooperatively solve a cognitive task (Friston et al., 1997). This revealed a significant change in connectivity between right dorsolateral PFC and bilateral occipital and inferotemporal cortices. Specifically, the functional connectivity was reduced

Figure 5. a) Compared to a low-level baseline identification of untrained items (red) activated extensive regions in frontal, parietal, and occipitotemporal regions, thereby replicating previous research using the same stimulus material. Activation level was markedly reduced in prefrontal cortex and several other regions for T12 (green) and T60 (blue) items. The lower part shows the activations projected on flat maps. b) The effect of training was not apparent for the period preceding identification. Hence, the training effect was specifically associated with conscious awareness of object identity.

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Identification Pre-identificationa) b)

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for trained items, indicating that posterior regions needed less PFC assistance to solve the identification task for easy compared to difficult items.

A study by Holm et al. (Holm, Eriksson, & Andersson, 2007, see also Holm, 2007) showed that implicit processing, possibly at a semantic level, predated identification by several seconds in a set of fragmented pictures similar to those used in the present studies. In the present study, brain activity indicative of implicit recognition processes prior to identification was evident in parietal and inferotemporal regions (Figure 6). While these results were too inconsistent to be reported in the paper (i.e. no significant overlap in a conjunction analysis), they suggest that weak activity related to unconscious processing of the target object is there and may be detected with more sensitive analysis procedures, e.g. pattern classification algorithms. This would imply that the fragmented pictures used in the studies not only controls for stimulus parameters and behaviour, but also for unconscious processing of the target.

Figure 6. Rendering of brain activity before identification in Study 3. Regions showing more activity for T12- (red) and T60-items (blue) than for untrained items indicates unconscious recognition processes. p < 0.001, uncorrected for multiple comparisons, k =5. Surface depth set to 20 mm for illustrative purposes. Note that this is the reverse contrast to that previously reported for pre-identification.

The reduction in PFC activity level and functional connectivity with sensory regions indicates that PFC plays an active role in the creation of conscious perception. The nature of this role can be of several kinds. For example, it is possible that the PFC is controlling attentional resources that selects and enhances certain posterior perceptual processes. Alternatively, the PFC might generate information that helps in the identification process by providing hypotheses about possible identities based on previous knowledge

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(Bar, 2003; Bar et al., 2006). Either way, the present results indicate that these processes are not needed to the same extent for trained compared to novel items. In fact, only visual, and to a smaller extent also ventral PFC, had a significantly different activity level compared to baseline for trained items. The residual ventral PFC activity is likely caused by the fact that even trained items may still not be completely obvious due to their fragmented nature. This indicates that the PFC might not be needed at all in conditions where perception is easy. If confirmed by future research, this would change the interpretation of a large amount of previous data and go against several theories of consciousness.

GENERAL DISCUSSION

While the number of man-hours spent on thinking and researching on the subject of consciousness throughout history is truly huge, consciousness has as of yet evaded any satisfactory explanation. Most people working in the field recognises the relation between brain and mind as paramount, which is evident when you for example consider the various afflictions and changes of mental states that are caused by damaged brains or chemically altered brain states; change the brain and you change the mind. A fruitful approach to investigate consciousness would then seem to be to study this relation empirically. The strategy in the 3 studies presented in this thesis has been to follow the brain activation profile of perceptual awareness that cannot be explained by stimulus properties or behaviour.

The results from all three studies corroborate previous research results in that activity in sensory regions correlates with perceptual awareness. These regions were also activated during sustained perception, indicating that they are continuously needed for perceptual awareness. It is unclear if forms of consciousness that do not have any sensory content even exist4. If not, sensory cortex activity can be seen as a necessary requirement for consciousness in general. � Considerforexample”thinking”.Ifconfinedtothekindofthinkingthatyouhaveaphenomenalexperienceof,itmostlikelyinvolvessomeformof”innerspeech”(auditorycontent)orimagery(visualand/orpossiblytactileandothersensorymodalities).However,thisisclearlydebatable(seee.g.Mangan,�00�).

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A sub-goal of Study 1 was to further investigate the role of the medial temporal lobe (MTL) for identification vs. sustained perception. Previous fMRI research has linked MTL activity to sustained perception (Kleinschmidt et al., 2002; Portas et al., 2000), whereas intracranial recordings have demonstrated MTL activity for identification as well (Kreiman et al., 2002). Study 1 and 2 showed that MTL activity increased for both identification and sustained perception, and Study 2 showed that this was true for both auditory and visual stimuli. MTL has been hypothesized to serve as a source of top-down information in situations where the stimulus is degraded but knowledge of identity has already been gained (Kleinschmidt et al., 2002). This condition is prevalent in both studies during sustained perception. It is possible that MTL also serves a similar role for the process of identification, but it may also instantiate other functions given that the function of the MTL is diverse (e.g. Andersen, Morris, Amaral, Bliss, & O’Keefe, 2006). More research is needed to fully understand how MTL is involved in conscious perception.

The results from Study 3 showing a distributed activity pattern in visual, frontal, and parietal cortices at identification are very similar to the corresponding results in Study 1 and 2. This is interesting to note because in Study 3 we did not try to separate activity related to different temporal profiles (i.e. identification vs. sustained perception). It is therefore likely that the results of no parietal cortex activity in Study 2 at identification would have been the same regardless of the exact experimental design. That is, this result is probably not a “hidden” effect that can only be detected by separating sustained and transient activity, which thereby increases the generality of this result. It is also noteworthy that the results from Study 1 are so well replicated in Study 2, and also in Study 3 for identification. The power in Study 1 was low, which could have been a concern without these replications.

Have I studied what I said I would?

Is it really neural correlates of consciousness?

In the experiments presented in this thesis the participants are conscious of something all the time. It is just that the content of their consciousness shifts

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and activity related to this creation of a new conscious percept is what is analysed. It may then be argued that what is studied is not consciousness with the big C, but rather some aspect of this that has limited implications. However, I fail to see how one can dissociate the process of creating a new conscious percept from the process of creating consciousness in general. In view of the distinction made in the beginning of this thesis between consciousness as a global state of mind and phenomenal consciousness, phenomenal consciousness “in general” does not even make sense to me. One possible reason for my inability to submit to this critique may stem from my opinion that we cannot have a (phenomenally) conscious state without content. Others, I suspect, may disagree on this. However, it might be that what is meant here is what can be referred to as “enabling factors” for consciousness, such as brainstem nuclei that determines global brain state levels, and a functioning heart for that matter (see e.g. Crick & Koch, 2003, or chapter 5 in Koch, 2004, for a more detailed description). While I recognize the obvious need for these enabling factors, I do not believe that this is what most people mean when they are talking about the neural correlates of consciousness (Chalmers, 2000).

It may be relevant in this context to mention some neurophysiological work where large parts of the non-visual cortex were removed, notably the frontal lobes, whereupon the subjects appeared to become “blind” (Nakamura & Mishkin, 1986; Sperry, Myers, & Schrier, 1960). This work can be interpreted as indicating that activity restricted to sensory regions cannot be sufficient for consciousness. However, as Nakamura and Mishkin note themselves, this use of “blindness” is only applicable in a most restricted way. “We wish to note at this point that we here use the term ‘blind’ simply as a verbal shorthand to describe animals that were totally unresponsive to visual stimulation … , without necessarily implying that they were totally lacking in visual sensation or perception.” (Nakamura & Mishkin, 1986, p. 173). Hence, the work says nothing about whether the subjects’ conscious visual perception was changed as a result of the lesions. Therefore, it would not be fair to say that even if fronto-parietal regions are not necessarily parts of the neural correlates of consciousness as indicated by Study 3, they could be needed as enabling factors. They may be, but the ablation work adds no information on this.

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Is identification of a fragmented object really a visual experience?

One might argue that identification of the fragmented objects is more similar to conceptual insight rather than “seeing”. I disagree for two reasons. First, my personal experience (introspection) is that there is a strong visual component of the phenomenal experience of identifying these objects, and people I have talked to concur. (You can see for yourself in figure 2a and on the cover.) Second, the fMRI results clearly show increased visual cortex activity associated with identification. Moreover, this activity was not confined to late stages of visual processing, as both figure 4 and 5 show. To some extent this can probably be explained as attentional effects, but the results from Study 3 show that visual cortex activity is still significantly increased at identification even though top-down related cortical activity has largely been reduced to non-significant levels. These results would unlikely occur if the identification process was merely conceptual or related to categorisation.

Consciousness and cognition reconsidered

The results from Study 3 indicate that prefrontal regions may not be as necessary for conscious perception as previous research has indicated. The prefrontal and parietal activity in previous neuroimaging studies is generally associated with the behavioural demonstration of lack of perceptual awareness when attentional resources are occupied, e.g. inattentional blindness (IB) and the attentional blink (AB). A widespread conclusion from this is that attention therefore is a necessary requirement for any sensory content to become conscious, and that attentional processing is reflected in the fronto-parietal activity. However, it is possible that the evidence supporting the principal role of attention for consciousness simply is the result of attention overriding what would otherwise be conscious representations. That is, since attention is a competitive selection process (Desimone & Duncan, 1995), it selects some stimuli over others, pushing the others out of consciousness. Hence, the paradigms implicating attention as necessary for consciousness may have induced “unconsciousness” where consciousness would otherwise be! This is consistent with the results from studies showing that performance

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in an AB paradigm improved by having the participants withdraw attention from the primary task (Olivers & Nieuwenhuis, 2005, 2006). Moreover, electrophysiological measures have demonstrated less attention-related brain activity for trials where the AB is weak (Kranczioch, Debener, Maye, & Engel, 2007; Shapiro, Schmitz, Martens, Hommel, & Schnitzler, 2006) and after training that resulted in better AB task performance (Slagter et al., 2007). Also, a recent transcranial magnetic stimulation (TMS) study showed that when the presentation of the first target in the series is accompanied with a magnetic pulse over parietal cortex, the AB is ameliorated (Kihara et al., 2007). That is, the attentional resources deployed by the parietal cortex are hindered by the magnetic pulse and therefore the blink of the second target is less severe. Hence, if attentional processes are decreased, by experimental manipulations, during trial to trial fluctuations, training, or TMS, the

“unconsciousness” induced by it is less severe.

Reconsidering the neglect syndrome

Neglect (see above), a neuropsychological disorder that supports the theory that attention is necessary for consciousness, may not provide as compelling evidence as one might think. The effect can be explained as a faulty attentional system that promotes one side of the world over the other. Similar to the argumentation above, it therefore seems that what happens in neglect is that attention constantly suppresses information from the contralateral side. This is supported by the “Sprague effect”, where effects of initial lesions to the parietal cortex can be partially amended by additional lesions in the brainstem (see Merker, 2007, for more detail). Specifically, the parietal cortical lesions seem to create an imbalance in inhibitory effects from the basal ganglia, which can be partially lessened by severing the connections between the substantia nigra and the colliculus. It is hence conceivable that neglect is caused by an

“unleashing” of inhibitory activity as a result of parietal cortex damage. Further support for this interpretation comes from recent work with neglect patients that, when holding a target matching item in working memory, experiences an amelioration of the neglect symptoms (Soto & Humphreys, 2006). That is, top-down processes from working memory help to override the defective attentional override.

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Reconsidering previous neuroimaging research

As described above, the major strategies for studying the neural correlates of consciousness involve tasks where the percept is difficult or ambiguous and therefore may require attentional or other top-down resources to be resolved. This would apply to binocular rivalry (Lumer et al., 1998; Lumer & Rees, 1999; Srinivasan & Petrovic, 2006), ambiguous stimuli (Kleinschmidt et al., 1998; Sterzer et al., 2002), threshold stimuli (Bar et al., 2001; Carmel et al., 2006; de Lafuente & Romo, 2005; Dehaene et al., 2001; Sahraie et al., 1997; Stephan et al., 2002), attentional blink paradigms (Feinstein, Stein, Castillo, & Paulus, 2004; Kjaer et al., 2001; Kranczioch, Debener, Schwarzbach, Goebel, & Engel, 2005; Marois et al., 2004; Sergent et al., 2005), change blindness paradigms (Beck, Muggleton, Walsh, & Lavie, 2006; Beck, Rees, Frith, & Lavie, 2001; Turatto, Sandrini, & Miniussi, 2004), and also the fragmented pictures and noisy sounds used in the present studies.

The frequent use of challenging tasks could explain the widespread finding of fronto-parietal activity in relation to conscious perception. It is therefore possible that if one were to use paradigms that did not rely on competing or highly demanding stimuli, the fronto-parietal correlation would vanish. This is supported by recent work showing that only competitive stimuli elicit selective attention mechanisms (Beck & Kastner, 2005). Also, in the work by Lumer et al. (1998) they used a control condition in relation to binocular rivalry that consisted of replaying the perceptual experience without rivalry. That is, the visual experience was identical to that during binocular rivalry, but since the same stimulus was presented to both eyes in one condition they could separate brain activity specific for rivalry related processing. Only fronto-parietal regions showed greater activity for rivalry compared to non-rivalrous stimuli, in line with the present argumentation. Similarly, in the study by Kleinschmidt et al. (2002) the activity time course for frontal and parietal regions showed an M shaped pattern whereas visual cortex showed an inverted V shape pattern. Hence, visual cortical activity followed the intensity of the percept, whereas fronto-parietal activity peaked at the border of perceptual pop-out and drop-out and decreased in between when the percept was clearly visible. Also, in a study by Bar et al. (Bar et al., 2001), objects were presented at threshold by being forward and backward masked and presented for only

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26 ms. Visibility was correlated with visual and frontal regions. Importantly, some items were presented for a longer duration and without the masks. For these items frontal cortex but not visual cortex activity was reduced, again supporting the present suggestion. Moreover, Moutoussis and Zeki (2006) demonstrated parietal cortex activity for invisible motion. By the same logic that indicates that visual cortex activity per se is insufficient for visual consciousness, this result indicates that parietal cortex is also insufficient. It may be noted, though, that the parietal cortex is large and is most likely related to several cognitive functions. It is therefore possible that other parts of parietal cortex than that reported by Moutoussis et al. is sufficient.

Studies showing no fronto-parietal activity correlation

Exceptions to the general pattern of fronto-parietal activity correlating with conscious perception are few. Watkins et al. demonstrated V1 activity correlating with the illusory perception of two flashes (one illusory and one veridical) accompanying two auditory bleeps (Watkins et al., 2006). It is unclear why this particular illusion does not elicit fronto-parietal cortex activity when other sensory illusions do (Blankenburg et al., 2006). Possibly, this is due to recently found direct connections between auditory and visual cortex (Clavagnier, Falchier, & Kennedy, 2004; Mishra, Martinez, Sejnowski, & Hillyard, 2007).

Tse et al. showed that when attention was diverted by a demanding central fixation task (detecting a slight colour change), activity related to visibility of a simple target was confined to early visual regions (Tse, Martinez-Conde, Schlegel, & Macknik, 2005). However, this result has been criticized because of the way visibility was assessed (Kouider, Dehaene, Jobert, & Le Bihan, 2007). Specifically, visibility was only measured in a separate condition that did not involve the demanding colour detection task. Since attention has been demonstrated to be able to make even salient perceptual events invisible (i.e. inattentional blindness), Koudier et al. argued that the target was in fact invisible in the Tse et al. report.

A third report of deviating results is the Kouider et al. paper it self. By using masking procedures they created conditions where a prime was invisible

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(masked) or visible (unmasked). They also varied the relation between prime and target to investigate priming effects. Prime and target could be orthographically related, phonologically related, or unrelated. A contrast between visible vs. invisible prime trials revealed only activity increase in visual cortical regions for visible trials. When confining this contrast to unrelated prime-target trials, prefrontal cortex activity was also evident. While the reason for this discrepancy among prime-target relations is unclear, the authors own suggestion is that the prime, when visible, created competition with the target only when they were unrelated and that this competition caused the prefrontal cortex activity increase. This would hence also be in line with the argumentation above. It should be noted, however, that Kouider et al. do not consider this to be neural correlates of consciousness, but rather of pre-consciousness (see below). They argue that the instructions to attend only to the target and to ignore the prime and masks could have induced inattentional blindness of the prime. This is theoretically possible since the visibility of the prime was tested after the main experiment in a separate session, where the instructions were to attend to the prime and not the target. Personally, I am sceptical and would take the results from Kouider et al. as a demonstration of visual awareness without fronto-parietal cortex activity. If one is to be strict, however, neither of the Tse et al. and Kouider et al. papers provide compelling evidence of conscious, preconscious, or unconscious neural activity, since visibility was evaluated under slightly different conditions.

An alternative explanation

It has recently been suggested that a new taxonomy of mental states could unite the seemingly opposing views of local sensory cortex vs. additional higher order structures as necessary and sufficient conditions for consciousness (Dehaene et al., 2006). It is argued that mental states could be of three kinds: conscious, preconscious, and subliminal, where the last two are supposed to be unconscious. Subliminal states are too weak to support consciousness, but can still be modified by attentional or other top-down mechanisms. Preconscious states have sufficient strength to reach consciousness, but fail to do so because they lack the support from attention. Conscious states are

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conscious because they have been “ignited” into a globally accessible state by attention (see also the description of the GNW above). This would explain why the neuroimaging results from Tse et al. (2005) and Kouider et al. (2007) are confined to sensory cortex: they are only preconscious. As stated previously, this is a theoretical possibility. However, it is not fair to claim that the results from Watkins et al. (Watkins et al., 2006) or from Study 3 are related to preconscious processes because there is no doubt that those mental states are fully conscious, despite the lack of fronto-parietal activity. Hence, the suggested explanation of misattributed fronto-parietal activity explains a larger portion of the data, is more parsimonious than the taxonomy of Dehaene et al. and is therefore preferable.

Other considerations

Attention may have been excessively portrayed as an inducer of unconsciousness rather than a creator of consciousness in the above discussion. In spite of this I do not mean to imply that attention or other top-down mechanisms are not necessary for consciousness in certain situations, such as when there is great need for attentional resources (Lavie, 2006), or when the input signals are ambiguous. Moreover, PFC activity may be a prerequisite for some types of conscious content, such as inner speech and imagery, even in low-load situations. While these mental events may require sensory regions (see previous discussion), it is possible that the trigger of activity is the PFC.

Given the subdivision of attention into spatial and object-based attention, the results from Study 3 may be limited to object-based attention. Hence, it is possible that spatial attention is required for consciousness to occur. However, this seems unlikely based on results from studies showing that gist perception is practically independent of spatial attention (Li, VanRullen, Koch, & Perona, 2002; Mack & Rock, 1998). Since spatial attention is a selection of certain locations over others and gist perception depends on information from the whole picture, it is unclear what function spatial attention could have in these situations (Koch & Tsuchiya, 2007). Moreover, recent research by Koivisto and colleagues (Koivisto & Revonsuo, 2007; Koivisto et al., 2006) has demonstrated that electrophysiological correlates of consciousness can be

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dissociated from both spatial and non-spatial attention. Finally, attention can cause the attended object to fade out of consciousness.

This seems to be applicable to both top-down attention (De Weerd, Smith, & Greenberg, 2006; Lou, 1999) and transient, stimulus driven effects (Kanai & Kamitani, 2003). The perceptual fading of attended objects demonstrates that attention can have the opposite effect on consciousness than that assumed by several theories.

Implications

If the above argumentation is correct, this would imply that we need to reinterpret a large amount of previous neuroimaging data, as well as the role of higher order cognitive functions such as attention in relation to conscious perception. Specifically, frontal and parietal regions may not need to be involved in conscious perception if the stimulus is clearly perceptible and/or presented in a low-load cognitive context. This would in turn suggest that aspects of the global neuronal workspace theory are incorrect. For example, it is clear that attention plays a key role in the model: “Top-down attentional selection and amplification are necessary for a representation to become available to consciousness.” (Dehaene & Changeux, 2004, p. 1148). The need for top-down attention also indicates that fronto-parietal regions are necessary according to the theory. While these aspects of the theory are at odds with the above discussion, the general gist of the workspace theory need not be questioned. It is possible that other mechanisms can make local information globally available that do not produce increased activity in fronto-parietal regions.

If future research supports the notion of sensory cortex as sufficient for consciousness, this may not change the view of hard core access consciousness supporters. For instance, if you believe that there can be pure access conscious states, the above argumentation will have little impact on that opinion. However, I do believe that such a change of focus regarding neural correlates of consciousness would make a difference in how the cognitive neuroscience community in general thinks of the concepts of phenomenal and access consciousness. Specifically, if prefrontal and parietal regions are not necessary

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participants in creating consciousness, the appeal of access consciousness will most likely diminish.

As described above, it has been hypothesised that the crucial difference between conscious and unconscious brain processes is the level of intensity (Moutoussis & Zeki, 2002; Zeki, 2003). This is consistent with the results from Study 3, although more research needs to be done to fully settle this issue. All in all, the hypothesis may seem unsatisfactory since it does not add all that much information about the neural correlates of consciousness, although it does suggest important constraints. The theory of fronto-parietal involvement may be seen as more progressive in that it would suggest the involvement of certain cognitive functions, which for example the GNW has incorporated. If the level of activity hypothesis turns out to be true this would most likely lead to more focus on process-theories of consciousness that are less specific about certain brain regions, such as the information integration theory (Tononi, 2004), or the theory of recurrent activity (Lamme, 2004; see also ffytche, 2002, for a similar view). This would probably also be the case if both the fronto-parietal hypothesis and the level of activity hypothesis turns out to be wrong.

A synthesis

A tentative model is proposed based on the results from Study 1, 2 and on the previous research results indicating sensory plus frontal and parietal cortex activity as important for conscious perception (initial and sustained), as well as the results from Study 3 showing that the frontal and parietal activity is modulated by stimulus difficulty (Figure 7). To simplify, I will designate the frontal and parietal activity as “controlling”, leaving unspecified the details of this process. This simplification includes leaving the differential parietal cortex involvement between sensory modalities untreated.

When stimulus parameters or task characteristics makes conscious perception difficult (Figure 7, top row), there is initially extensive interaction between sensory and controlling processes. At the moment of conscious perception activity in several control process-related regions peak (see Figure 3 in Eriksson, Larsson, & Nyberg, 2007), possibly reflecting top-down regulatory

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mechanisms. During sustained perception other controlling mechanisms are activated, likely linked to the goal-driven desire to continue selecting the present percept over others. The difference between control mechanisms for the moment of identification and sustained perception is supported by Study 1 and previous research (Kleinschmidt et al., 2002; Portas et al., 2000), but is perhaps most obvious in Study 2.

When the stimulus is clearly accessible and demands for attentional resources are low (Figure 7, bottom row), input signals travel to both sensory and controlling regions although their interaction is minimal (Bar et al., 2006). Local sensory processing is sufficient to produce conscious perception, although this does not preclude the possible importance of feedback mechanisms between local levels of processing (Hochstein & Ahissar, 2002). Sustained perception may still require some control processing to prevent

Hard

Easy

Pre-ID ID Sustained

sc

unconscious

conscious

c1

c2

c2

?

Figure 7. A model of different stages of processing for conscious perception (left to right) and under different cognitive demands (top vs. bottom). For simplicity, frontal and parietal processes are treated as a singular “control” module (c). Different control processes are designated by indexed arrows (c1 and c2). Sensory processing (s) is not meant to be confined to the visual modality, even though its location in the schematic brain may suggest this. The locations of s and c are stationary and are omitted in all but the top left brain for clarity. Note. Pre-ID = time before conscious perception; ID = moment of identification; sustained = sustained perception.

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shifts of attention, although empirical data for this remains to be collected. The present model gives a plausible explanation of a large amount of data,

but leaves much of the details unspecified. More research is needed to explain both local sensory processing and the control processes involved during difficult conditions.

Given the assignment of frontal and parietal cortical processes as controlling, I take consciousness to be located in sensory regions within the present empirical context. This is why only the circle denoting sensory cortex is solid (conscious) in Figure 7. However, as the requirement of sensory processing for all kinds of (phenomenal) consciousness is unclear (see footnote on page 29), it is possible that consciousness can be located within e.g. frontal cortex for other contents of consciousness, such as the feeling of mental effort (Naccache, Dehaene et al., 2005). In such a context frontal cortex activity would not be (exclusively) labelled controlling, but content generating.

Limitations and future directions

The fragmented pictures used in the studies were created for the purpose of separating stimulus parameters from conscious awareness of the target object. Since they are not very similar to any stimuli one might encounter in the “real” world (perhaps with the exception of a chameleon), brain activity related to conscious perception in more natural pictures might be different from that reported here. However, paradigms using threshold stimuli or manipulations of attention have reported very similar activation patterns using “natural” stimuli (see above), thereby indicating that the present results are applicable to other situations. Nevertheless, the results from Study 3 indicates that the difficulty of the identification task has significant impact on how the brain responds and a challenge for future studies will be to come up with other paradigms that can control for stimulus parameters, behaviour, and stimulus/task difficulty. Further research on the impact of task and stimulus difficulty is vital to fully understand how consciousness is implemented in the human brain. Furthermore, if future research supports the involvement of frontal and parietal regions specifically during difficult perception, the precise role played by these regions needs to be further investigated. This might involve varying

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attentional load, or varying the amount or type of information that can be used by the brain to limit the identity search space. Alternatively, other top-down mechanisms than those proposed in Study 3 may prove important.

In Study 1 and 2 there is a difference in how the two motor responses are initiated. The first response is initiated by the participant whereas the second response is a reaction to an external event. This may then confound brain activity that is supposed to be unique to conscious object identification. For example, it may be argued that the internally initiated response requires more frontal cortex involvement due to decision processes than the reactive, second response, and thus produces more frontal cortex activity coinciding with object identification. “Am I certain enough that I see/hear the target to give a response?” Moreover, this activity could be reduced as a consequence of training since it may be that participants are more confident of the identity of trained items. Hence, the results from Study 3 cannot rule out this possibility. However, while frontal cortex activity may well be related to decision processes (Binder, Liebenthal, Possing, Medler, & Ward, 2004), it is unclear how this process can be specifically related to response selection rather than being part of perceptually relevant processes (Bar, 2003; Bar et al., 2006). The degree of decision process related activity may be researched by for example collecting confidence ratings of target identity while participants perform the task in the scanner, which can then be correlated with brain activity. One would also need an independent measure of item difficulty to avoid this possible confounding effect, which for example is present in the work by Binder et al.

In consonance with the previous paragraph it is also relevant to consider possible variations in response criteria among participants. It is possible that different people have different criteria for claiming to have identified the target object. This could affect the results in that the first motor response would be a better indicator for object identification for some participants than others. In the case where the response is a bad indicator the power to detect neural correlates of object identification (and hence consciousness) would be attenuated. Since the visual stimuli do have a rather distinguished feeling of Aha! associated with identification, this may be of more concern for the auditory stimuli. However, the bar graphs in Figure 4 above displays the mean effect size in two frontal regions for visual and auditory stimuli, showing that these are very similar. Moreover, the fact that we do get significant results

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indicates that this may be of limited concern. Collecting confidence ratings, as suggested above, could be a way of gaining more detailed knowledge of how variations in response criteria may affect the results.

It is also important to acknowledge the limitations of using fMRI to study the neural correlates of consciousness. fMRI is an excellent tool for localizing brain activity, but knowing what parts of the brain that are relevant for consciousness is only one piece of the puzzle. As exemplified by the connectivity analysis in Study 3, fMRI can also provide information on how various parts of the brain interact. However, neuroimaging tools with higher temporal resolution (e.g. ERP, MEG) can be more precise regarding temporal shifts of neural activity. These tools can also be used to study other aspects of the neuronal code than spike frequency, such as synchronized and/or oscillating firing patterns. This may prove increasingly important if localized sensory cortex activity turns out to be feasible as a necessary and sufficient neural correlate of consciousness. Also, a chronometric analysis of the neural events leading up to conscious perception will obviously benefit from high temporal resolution, but also requires development of temporally precise behavioural measures of consciousness. That is, even though one can measure both spatially and temporally localized brain activity with the right equipment, one also needs information on when consciousness occurs and this information needs to have similar temporal resolution as the brain activity measures. A possible option could be to combine the behavioural measures introduced by Libet and colleagues (Libet, Wright Jr, & Gleason, 1982) with high temporal resolution neuroimaging of perceptual events. This is to my knowledge uncharted territory.

Conclusions

Consciousness has eluded a biological explanation despite massive research efforts. The empirical work presented in this thesis has not provided the final solution to this “deepest of biological mysteries” (Kandel, Schwartz, & Jessell, 2000), but it has revealed several novel findings as well as indicated important directions for future research. Taken together, the studies support a model where the neural correlates of consciousness depend non-trivially on

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stimulus and task characteristics. Specifically, Study 1 and 2 demonstrated that sustained perception requires support from different control processes than those needed during initial conscious perception, and Study 3 showed that the amount of necessary control processing support vary with stimulus difficulty. Thus, these results have implications for how to think of concepts such as access consciousness and theories that build on the association between consciousness and higher order cognitive functions. These findings are important to consider for future empirical and theoretical work on consciousness.

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