Master thesis, 18 December 2009

Neuroscience & Cognition, Utrecht University

Connecting Consciousness:
The role of large scale brain networks in consciousness

Jeanette Mostert1*, Rob van Gerwen2 and Martijn van den Heuvel3
1. Neuroscience and Cognition – Cognitive Neuroscience, Graduate School of Life Sciences, Utrecht
University, Utrecht, The Netherlands. 2. Philosophy department, Faculty of Humanities, Utrecht
University, Utrecht, The Netherlands. 3. Department of Psychiatry, Rudolf Magnus Institute of
Neuroscience, University Medical Center Utrecht, The Netherlands,

Abstract

Conscious awareness is the unitary experience we have of knowing what is happening

around us and what we think and feel about that. Although stimulus information is
initially processed in unimodal sensory areas, our experiences are multimodal. This
requires the integration of information between various specialised brain areas. Such
integration is facilitated in a dynamic network in which distant specialised areas are
functionally connected. The global workspace model incorporates such a dynamic
network and predicts that conscious awareness arises when different pieces of
information are united in a single workspace. This model is supported by other
theories of information integration. Additionally, the architecture of the brain, with
long-range axonal bundles, is well equipped to sustain such a global workspace.
Furthermore, the synchronised firing of neural populations that has been found to be
related to visual consciousness suggests a way of how different features can be
integrated into one percept. When we bring all of this together, there is considerable
evidence for a global network in the brain that comprises of long-distance interactions
between unimodal and multimodal, as well as between frontal and parietal areas. This
suggests that when information is integrated in a global workspace, conscious
awareness can arise from this.

Keywords: Consciousness; global workspace; information integration; synchronisation

* Corresponding author. Email-address: j.c.mostert@students.uu.nl.

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The requirement that science be objective does not prevent us from getting an

epistemically objective science of a domain that is ontologically subjective.

(Searle, 1998, p.1937).

1. Introduction

For a long time, consciousness has been a subject that was only discussed by

philosophers. However, recent discoveries in the neurosciences have resulted in a

strong belief that it is indeed possible to discover the neural correlates of

consciousness with scientific methods (Crick & Koch, 1990). These neuroscientific

investigations differ from philosophical discussions in that philosophers want to know

what consciousness is, while neuroscience mainly focuses on what is required for

consciousness. Although a clear definition of consciousness is lacking, the fact that

everyone seems to have a rough idea of what consciousness is, is enough to study

what neural mechanisms are related to this idea of consciousness (Crick & Koch,

1998). Furthermore, as we are gaining a better understanding of cognitive processes

such as working memory, attention, novelty detection and body schema,

investigations on consciousness are becoming more relevant (Dehaene & Naccache,

2001). A better understanding of how conscious experiences are brought about can aid

in the understanding of many cognitive processes that fall within the realm of

conscious experiences. In the last two decades many new, competing models of

consciousness have been proposed that contain testable hypotheses to scientifically

investigate the subjective phenomenon that consciousness is.

One such model is the global workspace model. This model is interesting because it

shows many similarities with several other heuristic theories in cognitive sciences. All

these models concern the integration of information within a network. The global

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workspace theory proposes that there is not one area responsible for creating a

conscious experience, but that the integration of information occurs within a network,

or workspace (Dehaene & Naccache, 2001). It is hypothesised that this process of

information integration is required for conscious experiences. Several studies have

shown that the way the brain is built and organised corresponds to what is necessary

for a global workspace. By reviewing several theories and models of information

integration as well as evidence for neural structures and neural functioning that

support such integration, we will argue that the integration of information via long-

distance connections that support global functional connectivity and synchronisation

is a requirement for conscious experiences.

2. Defining Consciousness

In order to investigate the neural requirements for a conscious experience, we first

have to narrow down what we mean by consciousness, because this term is used for a

wide variety of states and experiences. First of all, we can say that we are conscious,

meaning that we are not asleep or in coma. This can be termed as state consciousness,

indicating that a person resides in a state of being conscious. Being in such a state is

necessary in order to have any type of conscious experience (Dehaene et al., 2006;

Rees et al. 2002). However, even when you are in a conscious state, you can still be

unconscious of many things happening around you. You are consciously aware of

particular things that occur in the environment, or in your mind (i.e. thoughts). If

someone asks you if you saw the dog running away and you affirm, this means that

you had a conscious experience of seeing a dog running and that you can reflect upon

that experience and report about it. This can be termed as content consciousness,

because you are aware of a particular content that has become conscious to you (Rees

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et al., 2002). Thirdly, between being in a general state of consciousness and being

conscious of a particular content or experience, there is also a grey area of experiences

that contribute to your feeling of being conscious, but that you are not consciously

aware of. The smell of grass, the feeling of sitting on a chair, the sound of cars coming

by, all contribute to the conscious experience of where you are and the feeling of

‘what it is like’ to be you.

This last description of consciousness is so vague and difficult to determine that it is

hardly ever included in scientific research. At the most it is regarded as pre-

consciousness, to which we will come back later on. State consciousness on the other

hand is much more straightforward, as in most cases it is relatively simple to

determine if someone is consciously awake or not. We know that being in a conscious,

vigilant state is correlated with increased blood flow in the cerebral cortex, brainstem

and thalamus and a high baseline activity, even during rest, in the thalamocortical

network (Dehaene et al., 2006; Rees et al., 2002). The method used most to discover

the neural requirements for content consciousness is to compare brain activity when

someone perceives a stimulus to when the person did not perceive the stimulus. In

carefully designed tasks the presentation of stimuli is manipulated in such a way that

with equal presentation length and strength subjects sometimes report to have seen the

stimuli, and sometimes report not to have seen them (Gazzaniga et al., 2002).

However, are we only conscious of a stimulus when we can report to have seen the

stimulus? Or are we also conscious of a stimulus if we act in a certain way that shows

that we have seen the stimulus, even though we might now be able to report about it?

The way content consciousness was defined above is that you are aware of a certain

‘content’, or a stimulus in an experimental setting. Although reportability is not a

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requirement for content consciousness, this criterion is often used in an experimental

setting, because it is assumed that healthy, adult individuals can always report about

the stimuli they were consciously aware of perceiving (Dehaene & Naccache, 2001).

To stress the reportable aspect of content consciousness, some call it access to

consciousness or access consciousness. Here access does not mean that a person has

access to the inner workings of the brain that bring about consciousness, but instead

has access to the environment that is consciously perceived (McDowell, 1994) as well

as to first person data such as our thoughts, emotions and memories (Chalmers, 2004).

It is our awareness of what we experience, think, feel, remember, know, plan etcetera

(Block, 2005).

Not everyone agrees with this however; some argue that content consciousness can

also include a non-reportable aspect. This phenomenal consciousness is the minimum

content of an experience, or the experience of ‘what it is like’ to experience something

(Block, 1990, Nagel, 1974). This content is that what is different between the

experience of seeing ‘red’ and of seeing ‘green’. Philosophers have widely discussed

this problem of qualia (i.e. what is the quality of red that makes me see red), while

neuroscientists have investigated the differences in neural activation when a person

did or did not consciously see a visual stimulus. In certain tasks or under certain

conditions stimuli can influence behaviour even when subjects report not to have seen

the stimulus. In such cases neural activation in the visual areas is found that is less

widespread than when a stimulus is consciously perceived, but larger than when a

stimulus goes by completely unnoticed (Fahrenfort et al., 2007). Based on this

evidence, some argue that phenomenal consciousness is an ‘in between’ form of

consciousness that is independent of attention and reportability, but that is conscious

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nonetheless and that can be influenced by our motivations and other forms of

cognitive control (Block 2005; Irvine, 2009). However, it seems counterintuitive to

investigate consciousness processes that we ourselves do not experience as conscious

Box 1: Phenomenal consciousness, access consciousness and the global

workspace, an analogy:
The difference between phenomenal and access consciousness and the global
workspace can be explained with an analogy. We can see the global workspace as
the manufacturing of a car. The raw materials are first combined into different parts
of the car, such as the wheels, the steering wheel, the doors, the chairs and the
windows. These parts are manufactured in specialised factories that then send their
produced wheels to the factories that build the cars. These different parts, such as
wheels and windows, can be compared to phenomenal consciousness: raw materials
are integrated into individual parts in specialised areas or factories. However, these
parts themselves do not make a car. For this, all parts need to be integrated and put
together. That occurs in the car making factory, which receives input from all other
specialised units. What the car will look like depends on the orders that have been
placed at the factory, but also on what materials are being delivered. The building of
the car can be compared to the global workspace, with the end result, a complete
car, as access consciousness.
This analogy of course does not completely encompass what phenomenal and
access consciousness and the global workspace are. However, it does illustrate how
the global workspace (the manufacturing of a car) is the process that results in a
product (conscious awareness) which is a unitary experience composed from
different parts. The question ‘what is driving?’, which can be compared to asking
‘what is consciousness?’, does not demand immediate answering when we want to
understand the requirements for the product. This analogy also shows how
phenomenal consciousness is very different from access consciousness, but not
completely unrelated from it. Although a wheel is very much related to a car, the
meaning and experience of a wheel is very different than that of a car. We therefore
do not consider phenomenal experiences as consciousness.

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processes. Access consciousness is therefore generally considered as conscious

awareness, while phenomenal consciousness is termed pre-consciousness (see box 1).

Most people agree  that when we are consciously aware of something,  we have a

single unitary experience that includes internal and external information and that we

can   report   about.   Such   an   experience   seems   to   require   the   integration   of   many

different pieces of information into a coherent whole. In order to discover the neural

processes   that  underlie   this   experience   of  consciousness,  we  can   study  models  of

information integration and compare these to scientific evidence that supports these

models. 

3. The Global Workspace Theory

Traditionally, research on conscious awareness has focused on the functioning of

single areas. The visual areas for example have been so thoroughly researched that we

know of many different functions that are localized within specific areas of the visual

cortex. However, for consciousness this does not seem to be the right approach, as

consciousness is unlikely to be centred in a specific area in the brain. Brain lesions

can occur without a loss of consciousness, and when consciousness is lost then other

brain functions are lost as well. There is not a single, particular area that, when

lesioned or lost, results in the specific loss of consciousness while other functions

remain intact. Therefore, the idea has emerged that consciousness is not localized to

one specific area which controls what becomes conscious and what does not. Instead,

consciousness requires the integration of information within a global network.

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The global workspace theory posits that for a conscious, reportable experience,

various cortical areas should be integrated in a dynamic network that comprises long-

distance connections (Baars, 1988, 2005; Dehaene & Naccache, 2001). For a

conscious visual experience for example, three conditions should be met. First of all,

the visual areas should be activated when a stimulus is presented. Secondly, this

activation should be of sufficient strength to trigger wide-spread activation in several

other regions, especially higher-order parietal and frontal cortices. Finally, activation

to and from the lower sensory and higher parietal and frontal areas should result in a

reverberant state of coherent activity within a wide network of functionally connected

areas (Gaillard et al., 2009). This means that mere activation in the visual areas is not

enough for conscious vision (see box 1). Instead, the visual information needs to be

integrated with other information in frontal and parietal areas. According to this

theory, there is no single area in the brain that needs to be activated for consciousness,

but a workspace in which various areas with coherent activity are integrated. There

are five neural systems that are thought to be essential for a conscious experience and

that should therefore always participate in the workspace. These are perceptual

circuits, motor circuits, evaluation circuits, long-term memory circuits and attentional

circuits (Dehaene & Naccache, 2001). Furthermore, information is not automatically

integrated, but depends on highly dynamic processes. Such dynamic integration is

thought to be accomplished by large scale synchronised activity that is influenced by

feedback and feedforward processing between the areas.

What determines what is included into the workspace and what is not? In the original

global workspace theory a metaphor was used to explain this (Baars, 1998, 2005).

According to this metaphor, the brain is compared to a theatre and working memory is

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the stage on which the play is played. You are only consciously aware of what occurs

in the spotlight, which is the attended part of working memory. This conscious

‘content’ that is in the spotlight can also influence the ‘content’ that is outside of

conscious awareness. Thus, what is in the spotlight is determined by attention and

working memory, but also by consciousness itself. Although this metaphor is quite

crude, it does describe how attention is thought to be intimately linked to conscious

awareness. This metaphor of the global workspace theory has been implemented into

a neurocomputational workspace model (Dehaene & Naccache, 2001; Dehaene et al.,

2006). According to this model, top-down attentional control influences what is

incorporated into the global workspace. Within separate modular networks

information is processed in parallel and does not reach conscious awareness. When

these networks are integrated into a workspace under the influence of attention,

information becomes globally available. This global availability of integrated

information is thought to result in a conscious experience (Gaillard et al., 2009). A

very important aspect of this theory is that although many brain areas contain

workspace neurons that have long-distance and widespread connections (see section

4), only a fraction of these neurons constitute the ‘actual’ workspace at any given time

(Dehaene & Naccache, 2001). In other words, what is conscious at a certain time

depends on which neurons and brain areas are functionally connected at that moment.

3.1 The role of attention

Attention, as well as working memory, is often thought to require a workspace of

interconnected brain areas. According to the global workspace model, conscious

awareness is not possible without attention (Dehaene & Naccache, 2001; Dehaene et

al., 2006). When a stimulus is not attended, then this stimulus will be processed

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subliminally or pre-consciously, but it will never be consciously perceived (see fig. 1).

Whether or not the presentation of a stimulus results in conscious awareness therefore

depends on two factors: the bottom-up stimulus strength (i.e. the loudness of a sound)

and whether or not top-down attention is directed towards the stimulus.

Figure 1: The relation between attention and consciousness. According to Dehaene et al. (2006),

there are three levels of processing: subliminal, preconscious and conscious. At what level a stimulus is

processed depends on the the bottom-up stimulus strength (on the vertical axis at the left) and the

amount of top-down attention (on the horizontal axis). Coloured circles indicate the amount of

activation in local areas. Interactions between local areas are depicted by the small arrows. Top-down

attentional control, either towards the stimulus or away from it, is illustrated with the large arrows.

Some states lie on a continuum, as depicted by the dashed curves. The thick lines with separators

indicate that there is a sharp transition between the states. See text for details about subliminal,

preconscious and conscious processing. Adapted from: Dehaene et al., 2006.

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When a stimulus is of sufficient strength and attention is focussed towards the

stimulus, then this stimulus will be consciously perceived. For this to occur, bottom-

up activation in the early visual areas should exceed a dynamical threshold in order

for a self-amplifying system to get into action. This means that as soon as the

activation exceeds the threshold, feedforward activity is propagated towards higher

order areas (fig. 1, bottom right). This then triggers large-scale activation in many

brain areas within the global network, including the frontal and parietal areas. These

higher order areas also send back recurrent activation towards the lower areas which

keeps the information active within the entire network. It is the coherent activity in all

these areas that results in a conscious, unitary and reportable experience of the

stimulus. This experience can last longer than the presence of the stimulus that

triggered the experience, as the information is maintained in the network and thus in

working memory.

When presented stimuli are not attended and they elicit little bottom-up activation,

then the stimuli are processed subliminally. In this case the stimulus is of insufficient

strength to exceed the threshold and activate the self-amplifying system (fig. 1, top

left). Thus activation quickly dies out, does not enter working memory and the

stimulus is unnoticed. However, subliminal processing can also occur when stimuli

are attended. In this case, despite top-down attention, bottom-up activation is too low

to exceed the threshold that results in widespread activation (fig. 1, top right). Pre-

conscious processing occurs when there is potentially enough bottom-up activation

for a conscious experience, but there is a lack of top-down attentional activation (fig.

1, bottom left). Due to this, feedforward and feedback processing only occurs in the

lower sensory areas, but does not result in widespread activation to the frontal and

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parietal areas and long-distance synchrony. The difference between subliminal and

pre-conscious processing is that preconscious activation has the potential to result in

conscious awareness, once attention is directed towards the stimulus, while subliminal

activation can not. Pre-conscious information is kept active for a few hundred

milliseconds in a sensory buffer. If during this brief period attention is directed

towards this information in the sensory buffer, then the activation caused by the

stimulus can still be enhanced by attentional activation, thereby exceeding the

activation threshold and resulting in conscious perception.

The difference between attention and consciousness is a widely discussed topic. From

the above description it follows that attention does not automatically result in

conscious awareness. On the other hand, an important aspect of the global workspace

model is that there cannot be conscious awareness without attention (Dehaene et al.,

2006). Attention and consciousness are therefore two intimately linked, but

nonetheless distinct processes. Some however, argue that conscious awareness can

occur without attention (Lamme, 2004; Koch & Tsuchiya, 2008). Arguments in favour

of this are generally in line with arguments in favour of regarding phenomenal

experiences as consciousness, as described above (Block, 2005). Such experiences are

never reportable and are therefore not considered as conscious. In chapter 4, evidence

of recurrent processing and synchronisation will be discussed, that some regard as

proof that pre-conscious experiences are conscious.

One way to circumvent the discussion of whether attention is required for conscious

awareness is to argue that cognitive control, attention, working memory and

consciousness are fundamentally the same processes (Maia & Cleeremans, 2005).

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Information is not processed in separate modules (on a local scale), but instead on a

more global scale. Under the influence of prefrontal processes some of this global

information is enhanced (biased) and becomes conscious. This information is then

sustained in working memory and is attended. Consciousness, working memory,

attention and cognitive control are all mere dynamics of this global competition. This

idea is not so different from the global workspace model. In both cases consciousness

arises from the dynamic global integration of information. By looking into other

theories of information integration we can investigate if the global workspace model

is a suitable model to explain the neural processes that are required for conscious

experiences.

4. Theories of information integration

To investigate if the global workspace theory is a suitable model to study

consciousness we can look into several other theories of information integration and

compare these to the global workspace model. The Integrated Information Theory is a

theoretical analysis of information integration and proposes that conscious awareness

is related to a high degree of functional integration. Furthermore, the small-world

model can be used to investigate if the cerebral cortex is organised in such a way that

information can be integrated efficiently. On a more local level the Dynamic

Association Network model elucidates how information from different sensory

modalities can be integrated into a multimodal concept.

4.1 The Integrated Information Theory

The empirical evidence for the neural requirements for conscious awareness comes

from a wide range of different studies, often not even aimed to study conscious

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awareness, and this evidence is at certain points very contradictory. A theoretical

analysis that complements this evidence can therefore be very useful. For this reason

the Integrated Information Theory (IIT) was proposed (Tononi, 2004). According to

this theory, consciousness fundamentally is the same thing as integrated information.

Consciousness is not specified as being state or content consciousness, but is treated

as a general concept in this theory. The IIT proposes that many different elements

need to causally interact, so that the integration of all the bits of information from

different parts results in an experience that is bigger than the sum of its parts (Tononi,

2008). The amount of integrated information that is generated by a complex of

elements is depicted as Φ. The corticothalamic system (the cerebral cortex and

thalamus together) has a high Φ, as functionally specialised areas are also functionally

integrated. The cerebellum on the other hand has low Φ, as it consists of many small,

quasi-independent modules (Tononi, 2008). When a system has a high Φ it can be

conscious and when it has a low Φ it cannot be conscious. However, it is unclear how

much Φ is needed for consciousness. According to the IIT, consciousness is a graded

phenomenon, ranging from minimal consciousness to maximal consciousness

depending on how much information is integrated. We often experience a state of

being ‘half conscious’, for example when we are between waking up and falling

asleep. This is an important difference from the global workspace theory, because in

that theory only conscious awareness is taken into account. Conscious awareness is

regarded as an all-or-none phenomenon that depends on whether bottom-up and top-

down activation together result in activation that can cross a certain threshold. This

means that there is a sharp transition pre-consciousness and conscious awareness (see

figure 1) (Dehaene et al., 2006). This is related to the argument of reportability,

because we can either report about an experience, or we cannot, in which case it is not

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considered as a conscious experience. On the other hand, the global workspace theory

is comparable the IIT in that when information is not integrated, this does not result in

conscious awareness. From the IIT is also follows that phenomenal experiences

cannot be conscious, because they are not integrated into the global workspace.

While the IIT is very theoretical, it does fit with our observations about the

architecture of the brain and conscious awareness. As the IIT requires a mix of

functional specialization and integration, the model predicts that this is most likely

brought about by a network of neurons that form complexes that are connected by

long-range neuronal interactions and that interact in a fast and dynamic manner

(Tononi, 2008). Furthermore, the IIT requires a very special kind of complexity with

causal interactions between specialised networks, to which the small-world

architecture of the cerebral cortex seems very well adapt.

4.2 Small-world networks

Similar to the IIT, the concept of small-world networks is a mathematical model that

can be used to investigate a wide variety of phenomena with. This type of network is

often found in biology, technology and society and is an intermediate form between a

completely random and a completely orderly network (Watts & Strogatz, 1998, see

figure 2). A small-world network comprises of nodes that are highly connected to

neighbouring nodes over short distances but with a few long-distance links (Watts &

Strogatz, 1998; Gomez Portillo & Gleiser, 2009). This is thought to be the optimal

type of network to combine highly specialised areas with global functional integration

(Gomez Portillo & Gleiser, 2009). Dynamical systems that show small-world

organisations are known to have a high computational power and synchronisability, as

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well as that they allow for fast signal propagation (Watts & Strogatz, 1998). Evidence

that the brain is structured in such a small-world organisation comes from several

fMRI studies (reviewed by Sporns et al., 2004). In the brain, highly clustered sub-

networks are functionally integrated via global connections. Furthermore, the network

organisation of the brain is also scale-free. This entails that there is not an equal

distribution in how many connections each node in the network has, but that some

nodes in the network have very many connections, while the majority of nodes only

has a few connections. Such an organisation creates so-called hubs, which are widely

connected to many other nodes in the network. This small-world and scale-free

organisation of the brain seems to be very suitable for information integration

(Tononi, 2008).

Investigating if a global workspace model shows small-world characteristics would be

an interesting topic for future research on understanding the neural processes that

bring about consciousness. Thus far this has already been done for higher cognitive

functions such as intelligence. In a recent study it was shown that intelligence is

correlated with a high degree of efficiency in the neural network (Van den Heuvel et

al., 2009).

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Figure 2: The difference between a regular, a small-world and a random network. In a regular

network, individual nodes (circles) are connected to, in this case 4 of, its direct neighbors. P is the

probability that a node is connected randomly to another node. In a random network p = 1, so all

connections are random. In a small-world network, only a couple nodes are not connected directly to

their neighbors but instead to more distant nodes. This combines the clustering of information in

specialised nodes with long-range integration. (From Watts & Strogatz, 1998. Figure 1).

4.3 The Dynamic Association Network

A third model of information integration is concerned with the integration on a more

local level. The Dynamic Association Network (DAN) theory tackles the question

how information from different sensory modalities is integrated into a multimodal

percept (Pennartz, 2009). This is called the Modality Identification (MI) problem.

This roughly translates to the question: what is the neural basis of experiencing one

type of input to the central nervous system as ‘visual’ and another type as ‘auditory’?

(Pennartz, 2009 p.719). The DAN theory therefore focuses on the neural correlates of

phenomenal experiences.

The DAN model comprises of the following: unimodal sensory areas, such as those

for vision, audition or touch (somatosensation) are anatomically segregated. The

visual areas reside in the occipital cortex, the auditory areas in the temporal cortex and

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the somatosensory areas in the anterior part of the parietal cortex. Despite this

segregation, these areas are highly functionally connected. This integration is needed

for conscious multimodal experiences. We never experience just seeing something in

the absence of auditory, tactile, vestibular or olfactory sensations. Our perceptions are

constantly influenced by all our senses. This is termed the ‘topological uniqueness of

sensory modalities’, which means that each sensory modality is unique in the way it is

integrated with other sensory modalities (Pennartz, 2009). Information about a single

object feature such as colour is therefore not spatiotemporally invariant (Pennartz,

2009). This means that other features of the same object influence the representation

of this single feature. When a feature is removed or added to the object, this therefore

also alters the spatiotemporal representations of other features in other modalities. For

example, the experience of seeing a red ball will be completely different when this

ball starts to move, and this will again change when a sound accompanies the moving

ball. Although all these pieces of information are initially processed in different

unimodal areas, we do have a single, multimodal experience (Dehaene & Naccache,

2001).

According to the global workspace model, the integration of unimodal information

into a multimodal concept is not yet equal to a conscious experience. For that to arise

this multimodal concept needs to be integrated with other networks such as that of

attention and long-term memory (Dehaene & Naccache, 2001). The processes that the

DAN is concerned with are therefore more related to pre-consciousness, also

considered as phenomenal consciousness by some (Block, 2005). The transition from

unconscious, to pre-conscious, to conscious awareness can be seen as a hierarchical

structure (fig. 3). At the bottom of the hierarchy are the sensory areas that process

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unimodal information. This information is then integrated at the next level of the

hierarchy as explained by the DAN model and this results in pre-conscious

experiences. When information moves another level up, it is integrated with global

information and becomes part of the global workspace. The integrated information

then reaches conscious awareness.

Figure 3: The hierarchical structure of information integration. At the lowest level unimodal

information is processed within specialised sensory areas. Content at this level is unconscious. When

unimodal content is integrated with information from other modalities, a multimodal content is created.

The Dynamic Association Network is a model that describes this process. When multimodal content

from higher-order perceptual systems is integrated with content from attentional, long-term memory,

evaluative and motor networks, a conscious experience arises. This last step of global integration is

described by the global workspace model.

5. Neural evidence for the global workspace and long-distance connectivity

We have seen that the global workspace model is supported by other theories of

information integration. The next question is if this model can also be validated with

scientific research.

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5.1 Evidence for structural integration

A key aspect of the global workspace theory is that many brain areas contain so-called

workspace neurons that have long-distance and widespread connections. When a

person is at rest and is not engaged in any particular task, several brain regions show

high functional connectivity. Analyses of such resting-state networks have shown that

the thalamus, precuneus and anterior cingulate cortex (ACC) are regions that have

many functional connections to other regions (Van den Heuvel et al., 2008). Such

highly connected areas can be seen as hubs within the scale-free network of the brain.

These regions are therefore expected to have a high density of ‘workspace neurons’

that play a major role in forming the dynamic connections of the global workspace

(Dehaene & Naccache, 2001). Neurons that fit the description of workspace neurons

have been found in the ACC. This region is known to have a large collection of

spindle cells. These neurons are much larger than pyramidal cells and have long-

distance projections to many different areas in the brain. Additionally, such spindle-

cells have only been found in humans and great apes, suggesting a special role in

higher cognitive functions (Allman et al., 2001). This fits with the functions that are

generally linked to the ACC: emotional self-control, focused problem solving, error

recognition and adaptation to changing situations (Allman et al., 2001).

While in other areas besides the ACC and frontoinsular cortex such spindle cells have

not been found, other evidence of long-distance connections between various regions

is available. Already in 1988 it was found that a dense network of long-distance

reciprocal connections exists between the dorsolateral prefrontal cortex (PFC), the

premotor area, the superior temporal, inferior parietal and anterior and posterior

cingulate cortices and with the neostriatum, parahippocampal formation and the

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thalamus (Goldman-Rakic, 1988). A recent study has shown that this network is very

important for access to consciousness in humans (Reuter et al., 2009). In patients who

suffer from the autoimmune disease multiple sclerosis (MS) the threshold for

conscious perception of a masked stimulus was found to be higher than in healthy

controls. MS is characterised by diffuse white matter damage in the central nervous

system, which especially affects long-distance connectivity in the brain (Reuter et al.,

2009). Accordingly, in this study significant negative correlations were found between

damage in prefrontal areas and in associative fibre tracts between frontal and occipital

areas, and the threshold for conscious access. In other words, the more white matter

damage, the longer the delay between the stimulus and the mask needed to be for a

conscious perception of the stimulus. This evidence fits with the global workspace

model that consciousness requires a network of long axon bundles that connect

perceptual areas with prefrontal, cingulate and parietal cortices (Dehaene et al., 1998).

The diffuse white matter damage in MS patients might disturb this connectivity,

thereby resulting in impaired conscious access (Reuter et al., 2009).

Besides the thalamus, precuneus and ACC, the PFC is often linked to conscious

awareness and is thought to contain many workspace neurons (Dehaene & Naccache,

2001, Gaillard et al., 2009). The role of the PFC in attention (Posner, 1994), the

explicit learning of motor sequences (Destrebecqz et al., 2005) and conscious

perception (Feinstein et al., 2004) is often taken as evidence that the PFC is very

important for conscious awareness. This should however be considered carefully as

the PFC is known to play a major role in many cognitive functions such as working

memory, reasoning and planning (Dehaene & Naccache, 2001). As discussed above,

these functions are highly related to access consciousness. However, this does not

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mean that the PFC is a neural correlate for consciousness, neither is this evidence that

this is the place where all integration takes place. The dynamic mobilization of

neurons into a workspace is thought to be the result of spontaneous activity of these

workspace neurons and does not require any ‘supervision’. Activity within regions of

the PFC is likely to be important for conscious experiences, which is supposedly why

these regions are often connected into the global workspace.

Although evidence of long-distance axon fibres and workspace neurons indicates that

neural regions can connect to each other, this is not sufficient for the global

workspace. Conscious experiences are very dynamic, so the integration of information

into a workspace should also be dynamic. For the global workspace model it is

therefore important that areas are functionally connected. Which areas are integrated

at a particular moment determines what becomes conscious at that moment. Such

functional connectivity is thought to arise from recurrent processing, synchronisation

and phase coding.

5.2 Evidence for functional integration

From what has been discussed until now we can see that there is considerable

evidence, from other theories and models as well as from neurological studies, that a

global workspace can exist in the brain in which information is integrated. The next

question is how the functional integration of information takes place.

5.2.1 Recurrent processing

The terms ‘feedback projections’ and ‘recurrent processing’ have already been

mentioned as being important in the global workspace theory (see fig. 1).

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Bidirectional communication is important for the integration of information. When

two areas can communicate in a bidirectional way, they can influence each other’s

activity and thereby integrate their information by acting as one. As can be seen from

figure 3, information is not only projected from lower to higher areas, but higher-

order areas also send back information towards the lower areas. Evidence that such

recurrent processing is important for conscious perception comes from studies in

which a stimulus was masked in such a way that it was not consciously perceived.

When a stimulus is briefly flashed in front of a participant’s eyes, rapid feedforward

processing occurs from early to higher order visual areas. This feedforward

processing is then followed by feedback processing from the higher to the lower

visual areas and feedforward and feedback connections between frontal, parietal and

occipital areas (Fahrenfort et al., 2007). In this case the subject will report to have

seen the stimulus. However, when the stimulus is immediately masked by another

stimulus, this interferes with the feedback processing from the higher to the lower

areas. The subject will then report not to have seen the stimulus. This clearly shows

that activity in the early sensory areas is not enough for conscious perception, but that

this visual information needs to be sent to higher order areas. Furthermore, recurrent

processing between lower and higher visual areas is thought to occur pre-consciously

(Fahrenfort et al., 2007). This fits with the hierarchical structure depicted in figure 3.

When information is integrated within the sensory areas, a pre-conscious or

phenomenal experience arises. For a conscious experience this information then needs

to be integrated with information from frontal and parietal structures. Interestingly, in

the study with MS patients it was found that despite the damage to long-distance axon

fibres, feedforward processing and subliminal priming were not impaired in these

patients (Reuter et al., 2007). This is further evidence that local processing results in

23
pre-conscious experiences and that recurrent and self-amplifying signals are required

for conscious access and reportability.

5.2.2 Neural synchronisation

When areas can communicate with each other in a reciprocal way, they can also

synchronise. The coherent firing of neuronal populations is thought to be a

mechanism of neuronal communication (Fries, 2005). As explained above, such

bidirectional communication is necessary for the integration of information. While

many researchers focus on the activity of certain areas, also in relation to

consciousness, this focus has recently shifted towards the extent to which areas

exhibit synchronous activity. This research is interesting, because changes in the firing

synchrony do not influence the firing activity that is usually measured (i.e. metabolic

activity with fMRI) (Gaillard et al., 2009). With the same firing rate, neural

populations can fire in or out of phase with each other. While this is of great

importance for the integration of information, such effects are often missed with

neuroimaging techniques. In the last years many studies have shown that conscious

vision is related to widespread synchronisation and phase-locking between the

occipital, frontal and parietal areas (Rees et al., 2002; Uhlhaas et al., 2009, Gaillard et

al., 2009).

According to the Dynamic Association Network model, information from a particular

sensory area is integrated with unimodal information from other sensory areas

(Pennartz, 2009). This is not only integrated into a multimodal content, but

information from one modality can also influence the information in another modality.

Hence besides feedforward projections towards higher order sensory areas, recurrent

24
projections back to the lower sensory areas are also needed (Fahrenfort et al., 2007).

One way through which this integration may occur is via gamma oscillations, in

which neuronal populations communicate with each other by firing in synchrony. The

early, unconscious and pre-conscious processing of visual information that involves

feedforward and local recurrent activity is characterised by local high frequency

oscillations, called gamma oscillations (30-100Hz) (Gaillard et al., 2009). However,

when this local activation does not exceed the threshold to ignite global activation and

synchronisation, then this does not result in a conscious experience (Dehaene et al.,

2006). This can occur because the bottom-up activation caused by the stimulus is too

low (i.e. the stimulus was too weak in intensity, too briefly shown or immediately

masked by another stimulus) or because of a lack in top-down attention (i.e. when

attention is directed away from the stimulus or during an attentional blink) (fig. 1 and

3). The long-range global integration of information that is necessary for a conscious

experience is characterised by lower frequency beta oscillations (12-30 Hz) (Fries,

2005). Such oscillations have a slower period and are therefore thought to be more

suitable to be sustained across large cortical distances (Gaillard et al., 2009). When a

visual stimulus is consciously experienced, synchronous firing at the beta frequency

can be seen in many cortical areas. This fits with the global workspace model that

information is ‘broadcasted’ into the workspace network of the cortex (Gaillard et al.,

2009). Furthermore, these synchronised areas are causally related, indicating that they

can influence each other’s activity. The dominant direction of these causal relations is

from posterior areas towards anterior areas (Gaillard et al., 2009), which is also in line

with the integration of posterior sensory information with that from frontal and

parietal areas.

25
According to the global workspace theory, information is first integrated locally and

then globally (fig. 3). This distinction also follows from ERP and intracranial EEG

studies (Uhlhaas et al., 2009; Gaillard et al., 2009).

The transient and dynamic synchronisation of a widely distributed neural network is

hypothesised to be a neural mechanism that is required for conscious experiences

(Gaillard et al., 2009). This however does not mean that such synchronisation only

allows for access consciousness. Instead, this mechanism might underlie many

processes such perceptual stabilisation, maintenance in working memory and the

generation of expectations (Uhlhaas et al., 2009). As these processes are all intimately

related with consciousness it is not so strange that such patterns of synchronisation

have been found in relation to a wide variety of cognitive processes.

Besides gamma oscillations, a low-frequency potential was recently discovered to be

also related to the integration of information and consciousness (He & Raichle, 2009).

The slow cortical potential (SCP) is a slow wave fluctuation in the cortical signal of

less than 4 Hz. Conscious experiences of visual and somatosensory stimuli, as well as

attentional control, were related to recordings of the SCP over the parietal cortex (He

& Raichle, 2009). Furthermore, this SCP is recorded over the superficial layers of the

cortex in which most cortico-cortical feedback connections and thalamic inputs

terminate. As fluctuations in the SCP are also highly correlated with the fMRI signal,

this is a very interesting fluctuation that should be investigated further. The specific

function of the SCP is not yet known, as well as the functional difference between

beta oscillations and the SCP. However, from what is known now a potential

26
contribution of this fluctuation in the integration of information is quite likely to be

found in the future.

6. Discussion

In this paper we have overviewed the global workspace model and affiliated theories.

According to these models the integration of information is a requirement for

conscious awareness. Information from different specialised areas needs to be

integrated into a unitary, multimodal concept for conscious experiences. This

integration does not occur in a single area, but instead in a global workspace that

connects many different brain areas. Due to this, perceptual information is integrated

with information from memory, evaluative circuits, motor circuits, cognitive control

and attentional systems. The synchronisation of these networks also creates a

reverberating state in which the integrated information is kept active, even though

initial activation within the sensory areas may long have subsided (Gaillard et al.,

2009).

When investigating conscious awareness it is important to distinguish between

phenomenal and access consciousness. The global workspace model explains why

phenomenal experiences cannot be conscious. Local processing of information does

not result in a conscious experience, because this does not trigger the widespread

functional integration within a workspace that is required for a reportable experience.

Nonetheless, investigating how information is integrated on a local scale can aid in

our understanding of how this may occur on a more global scale. Recurrent

processing and synchronised firing are thought to enable the integration of

information on a local level, but perhaps also on a more global scale.

27
Access consciousness designates the conscious experiences that we can report about

(Dehaene & Naccache, 2001). Through these experiences we have conscious access to

our environment (McDowell, 1994) as well as to our thoughts and memories. This

requires the involvement of language and motor circuits, as well as attention and

memory. The recurrent processing from frontal and parietal areas towards sensory

areas that is observed when a stimulus is consciously perceived, as well as the

widespread synchronisation of many cortical areas, indicates that such global

integration is indeed required (Gaillard et al., 2009). Some areas have been especially

linked to consciousness, because they show enhanced activity when a stimulus is

perceived consciously. These areas are the prefrontal cortex, the anterior cingulate

cortex and the precuneus in the parietal cortex (Dehaene & Naccache, 2001).

However, this does not mean that consciousness arises merely from activity within

these areas. Instead, as these regions are very important for higher cognitive functions

such as cognitive control, long-term memory and attention, they are often part of the

global workspace and therefore associated with consciousness. This is support by

findings that these areas show high functional connectivity during resting conditions

and contain many workspace neurons that have long-distance projections to other

regions. Further evidence that the global workspace model is suitable to study

consciousness comes from theoretical models of information integration. The

integrated information theory predicts that a consciousness is generated by the

functional integration of information from specialised areas (Tononi, 2008).The small-

world characteristics of the cerebral cortex and the scale-free organisation of hubs that

are globally connected fits in the model of information integration within a global

28
network. This indicates that the global workspace model is supported by theories of

information integration and network formation.

However, despite the fact that there is a considerable body of evidence that shows that

information integration can occur in the brain within a global workspace network, the

picture is far from complete. Many explanatory gaps still remain, especially

concerning how information is integrated in such a network and what determines what

is integrated. Future research should be aimed at investigating dynamic interactions

between brain areas and how alterations in these dynamic interactions affect

conscious awareness. Combining research techniques form different fields will be of

great value for this. For example, combining functional connectivity data with that

from neural synchronisation studies can provide for more insight in how distant areas

integrate information. Additionally analyses should be focussed on the entire brain, as

well as on conscious behaviour and subjective reports. Just as observing a single

herring will not explain how a group of herring produces its complex, unitary

behaviour, observing single neurons or neuronal populations will not contribute a

great deal in understanding how consciousness is brought about.

There is however one limitation to this type of research, and that is the emphasis on

reportability. As was stressed before, access consciousness requires that a subject can

report about his (or her) experiences. Although this is very useful in an experimental

setting, it should be stressed that conscious awareness does not require reportability.

Instead, the neural requirements for reportable conscious awareness are studied in

healthy individuals, who we assume can report about their conscious experiences,

because we can do so as well. From the knowledge that we gain from these

29
observations, for example that global synchronisation and recurrent activity is related

to consciousness, we gain a better understanding of what is required for

consciousness. Such knowledge can then be used to study for example patients who

reside in a vegetative state. These patients do not show any signs of awareness of

themselves or the environment even though they are awake (Laureys et al., 2007).

However, if it can be established that the global integration of information is still

intact, this can indicate that they are fully aware of what is happening around them.

Three years ago such a patient was found who had been conscious, but locked-in a

paralysed body and unable to communicate. Better knowledge of neural mechanisms

that are required for conscious experiences can also aid in such difficult diagnoses.

To conclude, the way that the brain is organised, with specialised areas that are highly

integrated and that can influence each other’s activity and firing patterns, fits with the

prediction of several models that conscious awareness requires the integration of

information. Local specialisation, long-distance connectivity, synchronisability and

recurrent processing all seem to be very important aspects for the formation of a

global workspace from which conscious awareness may arise.

30
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