Neuroscience and Biobehavioral Reviews 36 (2012) 191–197

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Neuroscience and Biobehavioral Reviews

journal homepage: www.elsevier.com/locate/neubiorev

Review

The ‘correlates’ in neural correlates of consciousness

Tom A. de Graaf a,b,∗ , Po-Jang Hsieh c,d , Alexander T. Sack a,b
a
Department of Cognitive Neuroscience, Faculty of Psychology and Neuroscience, Maastricht University, Maastricht, the Netherlands
b
Maastricht Brain Imaging Center, Maastricht, the Netherlands
c
Department of Brain and Cognitive Sciences, McGovern Institute, Massachusetts Institute of Technology, Cambridge, MA 02139, USA
d
Duke-NUS Graduate Medical School, Singapore 169857, Singapore

a r t i c l e i n f o a b s t r a c t

Article history: In the search for neural correlates of consciousness (NCC), the concept of ‘consciousness’ remains prob-
Received 29 November 2010 lematic. We suggest that not only the ‘consciousness’ in neural correlates of consciousness is a confused
Received in revised form 16 May 2011 term, but ‘correlates’ is as well. When brain events are found to covary with conscious experience, these
Accepted 23 May 2011
brain events can be the neural substrates of the experience, as is often (implicitly) suggested, but they can
also be neural prerequisites or neural consequences of the experience. We here disentangle these different
Keywords:
sorts of brain processes conceptually. But we also propose a concrete multi-pronged research program
Consciousness
that may, in near-future consciousness research, distinguish these brain processes empirically.
Awareness
Correlates © 2011 Elsevier Ltd. All rights reserved.
Attention
Substrates
Prerequisites
Consequences
Sufficient
Necessary

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 191
1.1. Multiple possible roles of NCCs. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 192
2. The ‘consciousness’ in neural correlates of consciousness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 192
3. The ‘correlates’ in neural correlates of consciousness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 192
3.1. Neural prerequisites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 193
3.2. Neural consequences . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 193
3.3. Neural substrates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 194
4. How to untangle the entanglement: empirically distinguishing the correlates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 194
4.1. Cross-literature integration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 194
4.2. Brain interference methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 194
4.3. Temporal information, effective connectivity, and pre-stimulus brain states . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 195
4.4. Unconscious perception paradigms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 195
4.5. Orthogonal attention, performance, and consciousness modulations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 195
5. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 195
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 196
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 196

1. Introduction

∗ Corresponding author at: Maastricht University, Faculty of Psychology & Neuro-

The cognitive neuroscience of consciousness is blossoming.
science, Department of Cognitive Neuroscience, P.O. Box 616, 6200 MD, Maastricht,
Age-old questions about where our experiences come from,
the Netherlands, Tel.: +31 43 3881461. centuries-old questions about what distinguishes conscious from
E-mail address: tom.degraaf@maastrichtuniversity.nl (T.A. de Graaf). unconscious processing, or recent questions about which exact

0149-7634/$ – see front matter © 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.neubiorev.2011.05.012
192 T.A. de Graaf et al. / Neuroscience and Biobehavioral Reviews 36 (2012) 191–197

brain regions are involved in these conscious or unconscious pro- ally three. We will distinguish them conceptually, but also proceed
cesses, today we can address all these questions. The search for to suggest a program that may in future studies distinguish them
‘Neural Correlates of Consciousness’ (NCC: Koch, 2004) has given empirically.
rise to many theoretical proposals and debate (e.g. Cleeremans,
2006; Noë and Thompson, 2004) and has taken flight especially
2. The ‘consciousness’ in neural correlates of consciousness
since science has been able to look directly into brains to both
see and manipulate what happens there. Using a variety of exper-
There are many classifications that can be made when it comes
imental paradigms, conscious experience can be manipulated
to ‘types’, ‘kinds’, or ‘definitions’ of consciousness. Consciousness
independently of stimulus parameters. This is important, because
remains, after all, one of the most ill-defined concepts in sci-
changes in our conscious experience are generally confounded by
ence and philosophy. In our view, one can distinguish between
changes in external input. To isolate changes in conscious experi-
self-awareness, higher-order awareness, medical awareness, and
ence for study, these changes must be separated from changes in
consciousness as experience. Self-awareness, or self-consciousness,
stimulation conditions.
refers to all the aspects of our mind that create our perception
One example is the multistable paradigm, in which a constant
of being some ‘one’ in a world consisting of ‘others’ and ‘things’.
stimulus gives rise to alternating conscious experiences over time
We perceive continuity in our being, personality, body, and per-
(e.g. Blake, 2001; Fox, 1991; Howard and Rogers, 1995; Kim and
haps even possessions and so on. Higher-order awareness is likely
Blake, 2005; Kleinschmidt et al., 1998; Levelt, 1965; Wheatstone,
a form of consciousness that separates us from most animals. It
1838). While a participant engages in multistable perception, brain
involves those aspects of our minds that allow us to reflect on
imaging methods such as functional magnetic resonance imaging
things, such as past, present, and future that form the founda-
(fMRI) and electroencephalography (EEG) can be used to look at
tion of (or perhaps are founded by) language. Medical awareness, or
activity throughout the brain, to evaluate in which areas the activ-
state-consciousness (e.g. Hohwy, 2009), is the state of being con-
ity covaries with conscious experience. Whereas the sequence of
scious, as compared to not being conscious. Medical awareness is
conditions in an fMRI experiment (the protocol) is usually defined
the type of consciousness studied by researchers comparing sleep-
by experimenters beforehand, in these kinds of studies the pro-
ing versus awake (Massimini et al., 2005), healthy versus comatose
tocol is defined by the subject. He or she generally uses button
(Owen et al., 2006), drugged versus sober subjects (Ferrarelli et al.,
presses to indicate which conscious percept is currently experi-
2010). But being in a conscious state is really more of a precondition
enced. This subjective report then defines the timing and duration
for the kind of consciousness we are interested in here. Conscious-
of conditions that are later contrasted in statistical analyses. In
ness as experience, or sometimes called content-consciousness (e.g.
a set of binocular rivalry experiments, one form of multistable
Hohwy, 2009), is the actual phenomenal quality that is, at any
paradigm, one eye was continually presented with one image (e.g.
given point in time, in the mind of a conscious person. Over time
a grating, or house), and the other eye with a second image (e.g. a
these contents of consciousness change, such as in a multistable
face). The conscious experience alternated between the two images
paradigm, which means that a subject experiences different things
despite constant visual input, and the subjects indicated with but-
(but is all the time conscious in the sense of ‘medically aware’).
ton presses when, for example, a face or house was perceived.
The experiences we collectively refer to have previously been
Activity related to these switches (Lumer et al., 1998; Lumer and
dubbed ‘phenomenal awareness’ (Chalmers, 1996), or ‘qualia’. The
Rees, 1999) or activity in house- and face-specific regions (Tong
information ‘presented’ in experiences is probably, in most cases,
et al., 1998) were then evaluated to see which regions modu-
globally available to the information processing system that is the
lated their activation in response to subjective experience changes,
brain (Dehaene and Naccache, 2001; Tononi, 2004); meaning it
rather than objective visual input. We will discuss the results of
has reached ‘access consciousness’ (Block, 2005). Such experiences,
these experiments below, but it should be clear that brain areas thus
‘qualia’, items in ‘content-consciousness’, phenomenal pieces of
revealed were related to consciousness. Since their activity corre-
information, are the kind of consciousness we focus on in this arti-
lated to conscious experience, such areas are commonly referred
cle.
to as NCCs.
A short way of saying this is that the NCC research we are con-
sidering here is the type of research that evaluates what happens in
1.1. Multiple possible roles of NCCs
the brain when we consciously experience one thing, rather than
another thing. Often, as in our example above, this comes down
These studies were as important as they were interesting, since
to contrasting the conscious experience of one visual image with
they offered early insights into brain mechanisms to do with
the conscious experience of a second visual image (such as a house
consciousness-related processes. But in this writing, we would
versus a face).
like to draw attention to a largely neglected conceptual problem
within the cognitive neuroscience of consciousness. To look ahead,
the problem is that several sorts of brain processes can correlate 3. The ‘correlates’ in neural correlates of consciousness
to consciousness and are therefore often lumped together. How-
ever, these processes can have rather different roles or meanings. We have now distinguished different ‘types’, or ‘kinds’, or ‘def-
In other words, there is not one consciousness-related process, initions’ of ‘consciousness’. We also constrained our discussion
there are probably several. And these consciousness-related pro- to the type of consciousness that is ‘experience’, or ‘qualia’, also
cesses are generally all grouped together under the banner of ‘NCC’. referred to as the ‘contents of consciousness’. To make such clear
We suggest that this is no longer appropriate, or necessary. But distinctions and demarcations constitutes one step forward. How-
before we can outline this issue in more detail, we will first need ever, even within the NCC program as restricted to experiences,
to make clear what we mean exactly by ‘consciousness’—so that a conceptual entanglement remains. This is illustrated by the
it is unambiguous what we are discussing the correlates of. This is schematic in Fig. 1. Say, a human subject is tested in an fMRI exper-
the ‘consciousness’ in neural correlates of consciousness. Then, we iment. A stimulus near perception-threshold is presented several
will outline the various types of brain processes that will correlate times, sometimes perceived (conscious), sometimes not perceived
to consciousness. These are the ‘correlates’ in neural correlates of (non-conscious). The activations in the brain are compared for
consciousness. It may come as a surprise that there is not one brain the conscious versus the non-conscious trials. The differences in
‘correlate’ of a conscious experience, but we suggest there are actu- activation correlate to the differences in consciousness: we have
 T.A. de Graaf et al. / Neuroscience and Biobehavioral Reviews 36 (2012) 191–197 193

Fig. 1. The proposed current and future states of NCC research. (A) Different methods can be used to study the activity and processes in (human) brains, with the goal of
understanding how conscious vision is established. Shown here as an example are images of functional magnetic resonance imaging (fMRI) and electroencephalography
(EEG) devices; two prominent neuroimaging techniques. (B) With such techniques it is possible to correlate brain activity or processes to the perception of a conscious
image (or other kind of experience). (C) The resulting brain activity is, by definition, an NCC: a neural correlate of consciousness. As outlined in the main text, any correlate
of consciousness could actually have different functions/roles to play. Any brain activity or process that correlates to a conscious experience can be a neural prerequisite, a
neural consequence, or (part of) the neural substrate of the conscious experience. Future research may be able to empirically dissociate these options, for a given identified
NCC. The main text outlines several proposals for research programs to this end.

found an NCC! (Note that while we provide the example of an
fMRI experiment with a resulting BOLD activation that is an NCC,
nearly everything we say below applies also to NCCs of other kinds:
fMRI BOLD activations, EEG frequency-band modulations or grand
averages, single-cell spiking rates, and so on.)
We suggest that the NCC thus identified can reflect not one, but
three things. The activation differences may be (part of) the neu-
ral prerequisites for the conscious experience, may be (part of) the
neural consequences of the conscious experience, or may indeed be
(part of) the neural substrate of the conscious experience itself.
3.1. Neural prerequisites
By neural prerequisites we mean that this activation (this neu-
ral event, or process) was necessary for the conscious experience to
arise. If this activation or process had not occurred, we would not
have been conscious of the stimulus. But, and this is our point, such
activation or process is not itself the neural ‘instantiation’ of the con-
scious experience. Being an NCC does not automatically mean that
the brain process identified ‘codes for’ the conscious experience. It
merely correlates with it by being a necessary accompaniment.
In this context, one particularly difficult confounder in many
consciousness experiments is attention. Attention plays a cru-
cial role in the establishment of consciousness as indicated by
classic psychological phenomena, such as the attentional blink
(Luck et al., 1996) and inattentional blindness (Mack and Rock,
1998), both examples where a lapse or (mis)allocation of atten-
tion prevents a particular stimulus from reaching consciousness.
The relation between attention and consciousness is so strong, that
a rather severe debate rages on whether consciousness is really
nothing more than attention, or stimuli reaching attention (Beck
and Eccles, 1992; Koch and Tsuchiya, 2007; Mack and Rock, 1998;
Merikle and Joordens, 1997; O’Regan and Noe, 2001; Posner, 1994;
Velmans, 1996). Coming back to multistable perception, frontopari-
etal regions have been associated with perceptual switches and
thus consciousness (Inui et al., 2000; Kleinschmidt et al., 1998;
Lumer et al., 1998; Schoth et al., 2007; Sterzer et al., 2002). But
frontoparietal regions have also been associated with attention (e.g.
Corbetta, 1998; Coull et al., 1996; Naghavi and Nyberg, 2005; Nobre
et al., 1999; Pessoa et al., 2003). Perhaps appropriate activity in
frontoparietal regions is a prerequisite for conscious experience,
because attention may be a prerequisite of conscious experience.
We are not suggesting it here, but would attention and conscious-
ness always go together (for example because nothing can reach
consciousness without first being attended to, in a fashion), then
any brain process responsible for conscious experience would
always co-appear with the brain processes responsible for atten-
tion(al selection).
This scenario exemplifies the fundamental entanglement of
neural prerequisites and substrates of conscious experience: they
always co-occur. However, based on our view of prerequisites and
substrates of conscious experience, this would not mean that atten-
tion and consciousness are the same, but rather the opposite!
Some of the brain processes correlating to a particular conscious
experience would be the actual substrates of that experience (of
its phenomenal constituents, or qualia), while the ‘attentional
brain processes’ would merely be prerequisites. This eternal co-
appearance may seem impossible to tackle empirically, and thus
prompt one to simply treat attentional and consciousness processes
as one and the same. We suggest that this step would constitute a
premature forfeit. Neural substrates and prerequisites can still be
disentangled, not only conceptually but also experimentally (see
below). From each other, and from a third co-existing neural cor-
relate of consciousness: neural consequences of consciousness.
3.2. Neural consequences
By neural consequences, we mean that an activation (neural
event, process) was a result of the conscious experience. In other
words, because the conscious experience was there, this activation
arose. There can be two forms of this. To exemplify the first, a mul-
tistable paradigm might employ two images, namely a rose and a
house. Every time we consciously experience an image of a rose, it
reminds us strongly of the kind of roses our grandmother, recently
passed away, grew in her garden. Thus, this image gives rise to
a plethora of emotional and associative responses, all co-varying
with the conscious rose-experience. But these resulting activations
or processes are in themselves, again, not the neural instantiation
of the experience.
However, this is a content-specific (or stimulus-specific), and
probably subject-specific form of neural consequences, and it might
be countered by using different kinds of stimuli, for example. There
is a more general form of neural consequences of consciousness,
which is potentially more problematic. The conscious experience
itself may, as a consequence, trigger specific neural events: neural
events that are always triggered. Thus, there is one real NCC that
gives rise to the experience, but having an experience (i.e. any con-
scious experience) then triggers or alerts other areas, for instance
to prepare responses, change alertness level, or just to say “oh wow,
I just had an experience”. These content-invariant neural conse-
quences may not be vital at all to the experience itself, but always
follow any kind of conscious experience. In these cases, it would be
194 T.A. de Graaf et al. / Neuroscience and Biobehavioral Reviews 36 (2012) 191–197
much harder to disentangle them than in the content-specific rose
example, but we suggest possible courses of action below.
3.3. Neural substrates
The third option for the brain activation or process identified is
that it is actually the neural instantiation, or substrate, of the con-
scious experience. In other words, this brain activation is directly
underlying the experience, not a result and not a precondition and
is the minimal neural activity that is sufficient for a specific con-
scious percept (Chalmers, 2000; Koch, 2004). In identity theory
terms: this brain activation IS the conscious experience, or at least
part of the brain activation that IS the conscious experience (note
that the conceptual distinctions made apply in varying degrees
whether identity theory, epiphenomenalism, or even dualism is
adopted as the metaphysical starting point). Many studies of the
NCC find brain activation differences as described in our exam-
ples and make (implicit or explicit) claims that the activation is
the substrate, without considering the other two possibilities of
prerequisite or consequence.
Hohwy (2009) recently argued that content- (experience-) NCC
research, contrasting conscious versus non-conscious percepts,
or one conscious percept versus another conscious percept, is
methodologically problematic: the resulting brain activations or
processes would not necessarily reflect the phenomenality of our
conscious experience, but rather the selection of one conscious
experience over another. Sympathetic to his distinction, which
seems to touch on ours, we think both the phenomenality (corre-
sponding to our ‘substrate’) and the selection (corresponding to our
‘prerequisites’) must occur in the brain and can (and do) appear in
the brain activations (events, processes) identified in NCC studies.
In fact, it is inherent to our schema that whenever a conscious expe-
rience X occurs, the preconditions P and consequences Q, always
co-occur.
Indeed, that is the root of the problem: X, P, and Q are all neu-
ral correlates of consciousness. But really, would not we like to
know which brain processes, of all the NCCs that we are seeing in
a particular experiment, are X, which are P and which are Q? To
provide a concrete example, recent fMRI evidence has shown that
activity in early retinotopic cortex follows consciously experienced
size (Murray et al., 2006), color (Hsieh and Tse, 2010), and object
identity (Hsieh et al., 2010), but not the physical stimulus itself.
These neural ‘correlates’ of consciousness may reflect neural con-
sequences of consciousness, neural substrates of consciousness, or
even neural prerequisites of consciousness. How could we go about
disentangling these options?
4. How to untangle the entanglement: empirically
distinguishing the correlates
The question is: if neural prerequisites (preconditions) and con-
sequences always co-occur with the neural substrate of a ‘quale’
(experience, content of consciousness), how can we ever sepa-
rate the substrates from the non-substrates? We here propose five
general approaches for a near-future cognitive neuroscience of con-
sciousness, which we will apply to the frontoparietal cortex as a
candidate for NCC.
4.1. Cross-literature integration
First, one could examine in the literature which brain activa-
tions or processes (almost) always correlate to awareness. In other
words, which NCCs are invariant to the stimulation paradigm?
We and others before us (e.g. Dehaene and Naccache, 2001; Rees,
2007) have noted that frontoparietal cortex activations seem corre-
lated to conscious awareness in very different research paradigms
using very different stimuli, for instance, in multistable paradigms
(Lumer et al., 1998; Lumer and Rees, 1999; Schoth et al., 2007;
Sterzer et al., 2002) and masking paradigms (Dehaene et al., 1998,
2001). We would argue that, if frontoparietal cortex is active in
conscious trials (or perceptual switches), no matter what the expe-
rience is like (be it a visual rose, a blaring trumpet, a soft touch
on the cheek), these frontoparietal areas are unlikely to be the
substrate of neural experience. Rather they would likely be neu-
ral prerequisites or (content-invariant) consequences. Substrates
of conscious experience are likely to be content-specific (but see
below). After all, the visual experience of a rose is different from the
visual experience of a grandmother’s face. Therefore, the brain pro-
cesses underlying these two experiences must be different (one and
the exact same brain process cannot randomly yield one experience
sometimes and the second experience at other times). Thus, a good
starting point for separating neural substrates from neural prereq-
uisites/consequences would seem to look for neural correlates of
consciousness that are content-specific versus content-invariant.
A practical recommendation for resolving this issue might be to
use newly emerging brain activation databases. For instance, Brain-
Map holds a large number of published PET and fMRI studies and
makes meta-analyses and cross-study overviews possible (Fox and
Lancaster, 2002).
4.2. Brain interference methods
If the option of neural substrate is thus rendered less plausi-
ble for a given NCC, because it is content-invariant, the question is
how to distinguish between neural prerequisites and neural con-
sequences of consciousness. In the case of frontoparietal cortex,
either or both of frontal and parietal cortices could be prereq-
uisite: for example causing the perceptual switches directly in a
multistable situation (e.g. by starting a re-evaluation of the input;
Sterzer et al., 2009; see also Carmel et al., 2010; Kanai et al., 2010;
Zaretskaya et al., 2010). Similarly, either or both frontal and pari-
etal cortices could be activated by consequence: for example if the
breaking through to awareness of the current stimulus causes an
automatic, salient, attention-grabbing response in frontoparietal
cortex (e.g. de Graaf et al., 2011a). The second general approach
that we advocate therefore is the use of brain interference methods
to distinguish between these options.
Transcranial magnetic stimulation (TMS) is one method that
allows us to change brain activity in relatively restricted brain
regions non-invasively in conscious human volunteers. If a region
is causally relevant for a particular task, TMS disruption of that
region should result in changes on that task. Applied to conscious-
ness in one example: if frontal cortex is a neural prerequisite
for consciousness, TMS over frontal regions should be able to
interfere with conscious perception. If frontal cortex activations
frequently found in consciousness studies are ‘only’ neural conse-
quences of conscious experience, then TMS should have no effects.
Thus, TMS might be fruitfully applied to consciousness studies
in regions beyond early visual cortex, where it already has doc-
umented effects on conscious and unconscious vision (Amassian
et al., 1989; de Graaf et al., 2011b; Ro et al., 2004; Silvanto, 2008;
Silvanto et al., 2005; Thielscher et al., 2010). The usefulness of TMS
has been extended beyond merely introducing ‘noise’ to a particular
region, since TMS can induce ‘virtual lesions’ (Pascual-Leone et al.,
2000), raise excitability of a region (Hallett, 2007), and now has
been shown able to induce frequency-specific oscillations in brain
regions (e.g. Romei et al., 2010). This latter method we find particu-
larly exciting, because we might thus use TMS to test whether NCCs
found in EEG/MEG research are functionally relevant for conscious
perception. Of course, the same logic applies also to other brain
interference methods (such as tDCS, e.g. Rosenkranz et al., 2000),
which may have varying advantages and applications.
 T.A. de Graaf et al. / Neuroscience and Biobehavioral Reviews 36 (2012) 191–197
4.3. Temporal information, effective connectivity, and
pre-stimulus brain states
Third, timing information might be used. EEG is well-known for
its high temporal resolution, and we would by default classify all the
pre-stimulus “NCCs” that have recently been found as part of the
neural prerequisites of consciousness. For instance, pre-stimulus
alpha power determines whether a liminal stimulus will be per-
ceived (van Dijk et al., 2008), and even the phase of alpha-waves
has a strong influence (Busch et al., 2009; Mathewson et al., 2009).
Whether brain processes occurring after stimulus presentation (e.g.
the 200 ms ERP negativity increase; Koivisto et al., 2008; Koivisto
and Revonsuo, 2009) could automatically be defined as neural con-
sequences of consciousness is a more difficult question. We do not
believe they could, since it is not straightforward at which point in
time our phenomenal awareness of a stimulus is ‘built’ (Breitmeyer
and Ogmen, 2006; Koch, 2004; Wilenius and Revonsuo, 2007). But
other methods are increasingly applied that operate in the temporal
domain even if temporal resolution is notoriously low.
For fMRI, some form of temporal order can be inferred, either
directly using BOLD chronometry (Formisano and Goebel, 2003)
or with newer analysis tools including connectivity methods
(dynamic causal modelling: Friston et al., 2003; Granger causality
mapping: Goebel et al., 2003; Roebroeck et al., 2005; see de Graaf
et al., 2010; for an fMRI application and de Graaf et al., 2009; for
a comparison with TMS chronometry). If a regional activation is a
neural consequence of awareness, this region should receive infor-
mation, and arguably be active later, than modular regions that are
hypothesized to be part of the NCC. Another temporal approach is
to examine whether and how neural activity occurring before stim-
ulus onset can predict the initial percept in multistable paradigms,
thereby inferring the causal role of neural activity in determining
conscious perception. It has previously been shown that pre-trial
activity in higher cortical areas can be analyzed as a neural predic-
tor of subsequent memory (Turk-Browne et al., 2006), perceptual
decisions (Andrews et al., 2002; Hesselmann et al., 2008), motor
decisions (Soon et al., 2008), and moment-to-moment fluctua-
tions in cognitive flexibility (Leber et al., 2008). One can adopt this
temporal approach and ask whether the initial dominant percept
during an episode of perceptual rivalry (in multistable paradigms)
can be determined or biased by pre-trial neural activity. In gen-
eral, the interplay between pre-stimulus brain states and incoming
stimulus inputs is likely to be a relevant part of neural prerequisites
of consciousness.
4.4. Unconscious perception paradigms
However, although we have now detailed several approaches
to separate neural prerequisites from neural consequences (using
brain interference or temporal inference procedures), we have not
yet delineated a true approach to separate neural substrates from
the two non-substrates. This seems to us indeed the most severe
challenge, but several advances could be made. First, by a process
of elimination, brain processes that turn out to be consequences
or prerequisites are not substrates. Second, neural substrates are
likely to be content-specific, as mentioned above. However, even
if a brain process is found to be content-specific, does this mean
the identified brain process/activation is a substrate? One possible
approach to specifically distinguish neural prerequisites and neural
substrates of consciousness, in this regard, is to look for special
cases in which the neural prerequisites of consciousness might be
present without consciousness.
For example, with unconscious perception paradigms, one can
present subliminal stimuli and ask what neural processes can still
occur even without conscious perceptions. There are many recent
studies showing that several brain regions can be activated even
195
when stimuli are not consciously perceived (Dehaene et al., 2001;
Fang and He, 2005; Haynes et al., 2005; Luck et al., 1996; Marois
et al., 2004; Morris et al., 1999; Moutoussis and Zeki, 2002, 2006;
Naccache et al., 2005; Pasley et al., 2004; Rees et al., 2000, 2002;
Vuilleumier and Driver, 2007). These regions might contain neural
processes that are not necessary for, but still always co-occur with,
conscious perceptions in normal situations. Studies that thus show
that FFA still shows face-specific activity in the absence of con-
scious face-percepts (e.g. Moutoussis and Zeki, 2002) demonstrate
that activity in FFA alone is not sufficient for ‘face-qualia’, or the
conscious experience of a face. Other studies show that even with
‘normal’ levels of activity in modular regions, such as motion area
V5/hMT, conscious perception of motion need not occur (Goebel
et al., 2001).
Applying this strategy the other way around; drawing con-
clusions based on a lack of activity in a region with or without
conscious perception, is more difficult (de Graaf and Sack, 2011).
But the strategy of finding regions that do activate during ‘uncon-
scious perception’ should eliminate content-specific candidates
(such as a certain level of BOLD activity in V5/hMT) as substrates of
conscious experience. Subsequent studies should thus investigate,
for example, whether various combinations of content-specific and
content-invariant activations/processes are required for conscious
experience.
4.5. Orthogonal attention, performance, and consciousness
modulations
A special mention here for the problem of confounders. Among
others, Koch and Tsuchiya (2007) are proponents of a conceptual
separation of attention and consciousness, citing empirical sup-
port. However, even if attention and consciousness are not one, in
most consciousness studies, attention seems to confound the NCC
results. For instance, in multistable paradigms, a change in con-
scious experience surely affects the neural substrates in the NCCs.
But it seems logical that a change in conscious experience also grabs
attention, and it seems plausible that changes in attention might
cause a change in conscious percept. So, whether these options are
veridical or imaginary, they genuinely do confound NCCs in mul-
tistable paradigms. One way to investigate this issue is to start
including (as much as possible) orthogonal attention manipula-
tions in consciousness experiments. This can be done in multistable
paradigms (for instance by allocation of attention to the perceived
visual stimulus or to a different kind of stimulus or to a concurrent
effortful task), but might also be done in other types of studies such
as masking paradigms. We refer to a recent review for further con-
siderations on separating attention and consciousness (van Boxtel
et al., 2010).
A second confounder in many consciousness studies, particu-
larly in masking paradigms, is task performance. Hakwan Lau points
out that when consciousness differs, behavioural task performance
often differs as well (Lau, 2008). Therefore, a purer look at correlates
of conscious experience would require the delineation of condi-
tions in which behavioural (visual) task performance is equal, while
conscious experience differs. This can lead to new and interesting
results (Lau and Passingham, 2006).
These two paradigmatic advances can certainly help future con-
sciousness research to isolate the relevant neural processes behind
conscious perception, even if they may not completely disentangle
neural substrates, prerequisites, and consequences.
5. Conclusion
New methods and analysis tools, and a comprehensive search
of the literature combined, should make it possible for future cog-
196 T.A. de Graaf et al. / Neuroscience and Biobehavioral Reviews 36 (2012) 191–197
nitive neuroscience to begin a separation of neural prerequisites,
neural consequences, and neural substrates of conscious experi-
ence. At the very least an awareness of these conceptual distinctions
would be valuable for both fledgling and established consciousness
researchers. At any rate, we suggest that it will not suffice to sim-
ply identify neural correlates of consciousness without any further
consideration, if we truly want to understand what happens in the
brain to establish conscious vision.
But we will end with an assumption and a warning. The assump-
tion we should make explicit is that all three brain processes
correlated to conscious experience: neural prerequisites, neural
consequences, and neural substrates can, in principle, be observed
with brain imaging methods. Theoretically, the correlates of con-
sciousness we see in the brain in many consciousness experiments
performed to date, could reflect only neural prerequisites and con-
sequences (for example). The substrates themselves might be on a
level (of organization, or of detail) that is beyond our current, and
possibly future, imaging tools. This is a very pessimistic viewpoint,
and there is no need to entertain it further, but the caveat should
be kept in mind since this writing (along with most consciousness
scientists) does assume that substrates of conscious experience are
both in the brain and measurable.
The warning is the following: it may be tempting to conclude
that any NCCs that are not content-invariant (thus content-specific)
are by default neural substrates of experience, and that NCCs that
are content-invariant are not substrates of experience. We would
not go that far. For instance, there could be content-specific neu-
ral consequences, as in the grandmother’s roses-example, or even
content-specific neural prerequisites. It could also be, and this
would not be a good thing for consciousness purists, that content-
specific brain processes interact with content-invariant processes
and that this interaction itself is the neural substrate of conscious
experiences. If that is the case, things may become a lot more dif-
ficult to disentangle empirically. But it is too early to tell, and we
should at this juncture not be dissuaded by such prospects. Also, it
could still be that in such a situation we could disentangle neural
prerequisites, consequences, and substrates, with advanced meth-
ods and design.
For now, the distinction between the three aspects of NCCs
should find its way into the consciousness community, particularly
the empirical members, and we do believe that a lot can still be
gained by starting on the practical research proposals we have here
introduced.
Acknowledgements
T.A.G. and A.T.S. are supported by NWO, Dutch Organization for
Scientific Research, grant numbers 021-002-087 and 452-06-003,
respectively.
Funding: The research leading to these results has also received
funding from the European Research Council under the European
Union’s Seventh Framework Programme (FP7/2007-2013) /ERC
Grant agreement n◦ [263472]).
References
Amassian, V.E., Cracco, R.Q., Maccabee, P.J., Cracco, J.B., Rudell, A., Eberle, L., 1989.
Suppression of visual perception by magnetic coil stimulation of human occipital
cortex. Electroencephalogr. Clin. Neurophysiol. 74, 458–462.
Andrews, T.J., Schluppeck, D., Homfray, D., Matthews, P., Blakemore, C., 2002. Activity
in the fusiform gyrus predicts conscious perception of Rubin’s vase-face illusion.
Neuroimage 17, 890–901.
Beck, F., Eccles, J.C., 1992. Quantum aspects of brain activity and the role of con-
sciousness. Proc. Natl. Acad. Sci. USA 89, 11357–11361.
Blake, R., 2001. A Primer on Binocular Rivalry, Including Current Controversies. Brain
and Mind 2, 5–38.
Block, N., 2005. Two neural correlates of consciousness. Trendi Cogn. Sci. 9, 46–52.
Breitmeyer, B., Ogmen, H., 2006. Visual Masking: time slices through conscious and
unconscious vision. Oxford University Press, New York.
Busch, N.A., Dubois, J., VanRullen, R., 2009. The phase of ongoing EEG oscillations
predicts visual perception. J. Neurosci. 29, 7869–7876.
Carmel, D., Walsh, V., Lavie, N., Rees, G., 2010. Right parietal TMS shortens dominance
durations in binocular rivalry. Curr. Biol. 20, R799–800.
Chalmers, D., 2000. In: Metzinger, T. (Ed.), Neural correlates of consciousness: empir-
ical and conceptual questions. MIT Press.
Chalmers, D.J., 1996. The conscious mind: in search of a fundamental theory. Oxford
University Press, Oxford.
Cleeremans, A., 2006. Computational correlates of consciousness. In: Laureys, S.
(Ed.), The boundaries of consciousness: neurobiology and neuropathology:
progress in brain research. Elsevier.
Corbetta, M., 1998. Frontoparietal cortical networks for directing attention and the
eye to visual locations: identical, independent, or overlapping neural systems?
Proc. Natl. Acad. Sci. USA 95, 831–838.
Coull, J.T., Frith, C.D., Frackowiak, R.S., Grasby, P.M., 1996. A fronto-parietal network
for rapid visual information processing: a PET study of sustained attention and
working memory. Neuropsychologia 34, 1085–1095.
de Graaf, T.A., Jacobs, C., Roebroeck, A., Sack, A.T., 2009. FMRI effective connectivity
and TMS chronometry: complementary accounts of causality in the visuospatial
judgment network. PLoS One 4 (12), e8307.
de Graaf, T.A., Roebroeck, A., Goebel, R., Sack, A.T., 2010. Brain Network Dynamics
Underlying Visuospatial Judgment: An fMRI Connectivity Study. J. Cogn. Neu-
rosci. 22 (9).
de Graaf, T.A., de Jong, M.C., Goebel, R., van Ee, R., Sack, A.T., 2011a. On the functional
relevance of frontal cortex for passive and voluntarily controlled bistable vision.
Cereb. Cortex.
de Graaf, T.A., Cornelsen, S., Jacobs, C., Sack, A.T., 2011b. TMS effects on subjective
and objective measures of vision: Stimulation intensity and pre- versus post-
stimulus masking. Conscious Cogn..
de Graaf, T.A., Sack, A.T., 2011. Null results in TMS: from absence of evidence to
evidence of absence. Neurosci. Biobehav. Rev. 35, 871–877.
Dehaene, S., Naccache, L., 2001. Towards a cognitive neuroscience of consciousness:
basic evidence and a workspace framework. Cognition 79, 1–37.
Dehaene, S., Naccache, L., Cohen, L., Bihan, D.L., Mangin, J.F., Poline, J.B., Riviere,
D., 2001. Cerebral mechanisms of word masking and unconscious repetition
priming. Nat. Neurosci. 4, 752–758.
Dehaene, S., Naccache, L., Le Clec, H.G., Koechlin, E., Mueller, M., Dehaene-Lambertz,
G., van de Moortele, P.F., Le Bihan, D., 1998. Imaging unconscious semantic
priming. Nature 395, 597–600.
Fang, F., He, S., 2005. Cortical responses to invisible objects in the human dorsal and
ventral pathways. Nat. Neurosci. 8, 1380–1385.
Ferrarelli, F., Massimini, M., Sarasso, S., Casali, A., Riedner, B.A., Angelini, G., Tononi,
G., Pearce, R.A., 2010. Breakdown in cortical effective connectivity during
midazolam-induced loss of consciousness. Proc. Natl. Acad. Sci. U. S. A. 107,
2681–2686.
Formisano, E., Goebel, R., 2003. Tracking cognitive processes with functional MRI
mental chronometry. Curr. Opin. Neurobiol. 13, 174–181.
Fox, R., 1991. Binocular Rivalry. In: Regan, D.M. (Ed.), Binocular Vision and Psy-
chophysics. MacMillan Press, London, pp. 93–110.
Friston, K.J., Harrison, L., Penny, W., 2003. Dynamic causal modelling. Neuroimage
19, 1273–1302.
Fox, P.T., Lancaster, J.L., 2002. Opinion: Mapping context and content: the BrainMap
model. Nat. Rev. Neurosci. 3, 319–321.
Goebel, R., Muckli, L., Zanella, F.E., Singer, W., Stoerig, P., 2001. Sustained extras-
triate cortical activation without visual awareness revealed by fMRI studies of
hemianopic patients. Vision Res. 41, 1459–1474.
Goebel, R., Roebroeck, A., Kim, D.S., Formisano, E., 2003. Investigating directed
cortical interactions in time-resolved fMRI data using vector autoregressive
modeling and Granger causality mapping. Magn Reson Imaging 21, 1251–1261.
Hallett, M., 2007. Transcranial magnetic stimulation: a primer. Neuron 55, 187–199.
Haynes, J.D., Driver, J., Rees, G., 2005. Visibility reflects dynamic changes of effective
connectivity between V1 and fusiform cortex. Neuron 46, 811–821.
Hesselmann, G., Kell, C.A., Eger, E., Kleinschmidt, A., 2008. Spontaneous local varia-
tions in ongoing neural activity bias perceptual decisions. Proc. Natl. Acad. Sci.
U. S. A. 105, 10984–10989.
Hohwy, J., 2009. The neural correlates of consciousness: new experimental
approaches needed? Conscious Cogn. 18, 428–438.
Howard, L.P., Rogers, B.J., 1995. Binocular Vision and Stereopsis. Oxford University
Press, New York.
Hsieh, P.J., Tse, P.U., 2010. “Brain-reading” of perceived colors reveals a feature mix-
ing mechanism underlying perceptual filling-in in cortical area V1. Hum. Brain
Mapp. 31, 1395–1407.
Hsieh, P.J., Vul, E., Kanwisher, N., 2010. Recognition alters the spatial pattern of FMRI
activation in early retinotopic cortex. J. Neurophysiol. 103, 1501–1507.
Inui, T., Tanaka, S., Okada, T., Nishizawa, S., Katayama, M., Konishi, J., 2000. Neu-
ral substrates for depth perception of the Necker cube; a functional magnetic
resonance imaging study in human subjects. Neurosci. Lett. 282, 145–148.
Kanai, R., Bahrami, B., Rees, G., 2010. Human Parietal Cortex Structure Predicts Indi-
vidual Differences in Perceptual Rivalry. Curr. Biol..
Kim, C.Y., Blake, R., 2005. Psychophysical magic: rendering the visible ‘invisible’.
Trends Cogn Sci 9, 381–388.
Koch, C., Tsuchiya, N., 2007. Attention and consciousness: two distinct brain pro-
cesses. Trends Cogn. Sci. 11, 16–22.
Kleinschmidt, A., Buchel, C., Zeki, S., Frackowiak, R.S., 1998. Human brain activity
during spontaneously reversing perception of ambiguous figures. Proc. Biol. Sci.
265, 2427–2433.
 T.A. de Graaf et al. / Neuroscience and Biobehavioral Reviews 36 (2012) 191–197
Koch, C., 2004. The quest for consciousness: a neurobiological approach. Roberts &
Company Publishers, Englewood, US-CO.
Koivisto, M., Lahteenmaki, M., Sorensen, T.A., Vangkilde, S., Overgaard, M., Revonsuo,
A., 2008. The earliest electrophysiological correlate of visual awareness? Brain
Cogn. 66, 91–103.
Koivisto, M., Revonsuo, A., 2009. Event-related brain potential correlates of visual
awareness. Neurosci. Biobehav. Rev..
Lau, H.C., 2008. A higher order Bayesian decision theory of consciousness. Prog. Brain
Res. 168, 35–48.
Lau, H.C., Passingham, R.E., 2006. Relative blindsight in normal observers and the
neural correlate of visual consciousness. Proc. Natl. Acad. Sci. U. S. A. 103,
18763–18768.
Leber, A.B., Turk-Browne, N.B., Chun, M.M., 2008. Neural predictors of moment-to-
moment fluctuations in cognitive flexibility. Proc. Natl. Acad. Sci. U. S. A. 105,
13592–13597.
Levelt, W., 1965. On Binocular Rivalry. Institute for Perception RVOTNO, Soesterberg,
Netherlands.
Luck, S.J., Vogel, E.K., Shapiro, K.L., 1996. Word meanings can be accessed but not
reported during the attentional blink. Nature 383, 616–618.
Lumer, E.D., Friston, K.J., Rees, G., 1998. Neural correlates of perceptual rivalry in the
human brain. Science 280, 1930–1934.
Lumer, E.D., Rees, G., 1999. Covariation of activity in visual and prefrontal cortex
associated with subjective visual perception. Proc. Natl. Acad. Sci. U. S. A. 96,
1669–1673.
Mack, A., Rock, I., 1998. Inattentional Blindness. MIT Press, Cambridge, MA.
Marois, R., Yi, D.J., Chun, M.M., 2004. The neural fate of consciously perceived and
missed events in the attentional blink. Neuron 41, 465–472.
Massimini, M., Ferrarelli, F., Huber, R., Esser, S.K., Singh, H., Tononi, G., 2005. Break-
down of cortical effective connectivity during sleep. Science 309, 2228–2232.
Mathewson, K.E., Gratton, G., Fabiani, M., Beck, D.M., Ro, T., 2009. To see or not to
see: prestimulus alpha phase predicts visual awareness. J. Neurosci. 29, 2725–
2732.
Merikle, P.M., Joordens, S., 1997. Parallels between perception without attention and
perception without awareness. Conscious Cogn. 6, 219–236.
Morris, J.S., Ohman, A., Dolan, R.J., 1999. A subcortical pathway to the right amygdala
mediating “unseen” fear. Proc. Natl. Acad. Sci. U. S. A. 96, 1680–1685.
Moutoussis, K., Zeki, S., 2002. The relationship between cortical activation and per-
ception investigated with invisible stimuli. Proc. Natl. Acad. Sci. U. S. A. 99,
9527–9532.
Moutoussis, K., Zeki, S., 2006. Seeing invisible motion: a human FMRI study. Curr.
Biol. 16, 574–579.
Murray, S.O., Boyaci, H., Kersten, D., 2006. The representation of perceived angular
size in human primary visual cortex. Nat. Neurosci. 9, 429–434.
Naccache, L., Gaillard, R., Adam, C., Hasboun, D., Clemenceau, S., Baulac, M., Dehaene,
S., Cohen, L., 2005. A direct intracranial record of emotions evoked by subliminal
words. Proc. Natl. Acad. Sci. U. S. A. 102, 7713–7717.
Naghavi, H.R., Nyberg, L., 2005. Common fronto-parietal activity in attention, mem-
ory, and consciousness: shared demands on integration? Conscious Cogn. 14,
390–425.
Nobre, A.C., Coull, J.T., Frith, C.D., Mesulam, M.M., 1999. Orbitofrontal cortex is acti-
vated during breaches of expectation in tasks of visual attention. Nat Neurosci
2, 11–12.
Noë, A., Thompson, E., 2004. Are there neural correlates of consciousness? J. Con-
scious. Stud. 11, 3–28.
O’Regan, J.K., Noe, A., 2001. A sensorimotor account of vision and visual conscious-
ness. Behav. Brain Sci. 24, 939–973, discussion 973-1031.
Owen, A.M., Coleman, M.R., Boly, M., Davis, M.H., Laureys, S., Pickard, J.D., 2006.
Detecting awareness in the vegetative state. Science 313, 1402.
Pascual-Leone, A., Walsh, V., Rothwell, J., 2000. Transcranial magnetic stimulation
in cognitive neuroscience–virtual lesion, chronometry, and functional connec-
tivity. Curr. Opin. Neurobiol. 10, 232–237.
Pasley, B.N., Mayes, L.C., Schultz, R.T., 2004. Subcortical discrimination of unper-
ceived objects during binocular rivalry. Neuron 42, 163–172.
197
Pessoa, L., Kastner, S., Ungerleider, L.G., 2003. Neuroimaging studies of attention:
from modulation of sensory processing to top-down control. J. Neurosci. 23,
3990–3998.
Posner, M.I., 1994. Attention: the mechanisms of consciousness. Proc. Natl. Acad.
Sci. USA 91, 7398–7403.
Rees, G., Wojciulik, E., Clarke, K., Husain, M., Frith, C., Driver, J., 2000. Unconscious
activation of visual cortex in the damaged right hemisphere of a parietal patient
with extinction. Brain 123 (Pt 8), 1624–1633.
Rees, G., Wojciulik, E., Clarke, K., Husain, M., Frith, C., Driver, J., 2002. Neural cor-
relates of conscious and unconscious vision in parietal extinction. Neurocase 8,
387–393.
Rees, G., 2007. Neural correlates of the contents of visual awareness in humans.
Philos. Trans. R Soc Lond. B Biol. Sci. 362, 877–886.
Ro, T., Shelton, D., Lee, O.L., Chang, E., 2004. Extrageniculate mediation of uncon-
scious vision in transcranial magnetic stimulation-induced blindsight. Proc.
Natl. Acad. Sci. U. S. A. 101, 9933–9935.
Roebroeck, A., Formisano, E., Goebel, R., 2005. Mapping directed influence over the
brain using Granger causality and fMRI. Neuroimage 25, 230–242.
Romei, V., Gross, J., Thut, G., 2010. On the role of prestimulus alpha rhythms over
occipito-parietal areas in visual input regulation: correlation or causation? J.
Neurosci. 30, 8692–8697.
Rosenkranz, K., Nitsche, M.A., Tergau, F., Paulus, W., 2000. Diminution of training-
induced transient motor cortex plasticity by weak transcranial direct current
stimulation in the human. Neurosci. Lett 296, 61–63.
Schoth, F., Waberski, T.D., Krings, T., Gobbele, R., Buchner, H., 2007. Cerebral pro-
cessing of spontaneous reversals of the rotating Necker cube. Neuroreport 18,
1335–1338.
Silvanto, J., 2008. A re-evaluation of blindsight and the role of striate cortex (V1) in
visual awareness. Neuropsychologia 46, 2869–2871.
Silvanto, J., Lavie, N., Walsh, V., 2005. Double dissociation of V1 and V5/MT activity
in visual awareness. Cereb. Cortex 15, 1736–1741.
Soon, C.S., Brass, M., Heinze, H.J., Haynes, J.D., 2008. Unconscious determinants of
free decisions in the human brain. Nat. Neurosci. 11, 543–545.
Sterzer, P., Russ, M.O., Preibisch, C., Kleinschmidt, A., 2002. Neural correlates of spon-
taneous direction reversals in ambiguous apparent visual motion. Neuroimage
15, 908–916.
Sterzer, P., Kleinschmidt, A., Rees, G., 2009. The neural bases of multistable percep-
tion. Trends Cogn. Sci. 13, 310–318.
Thielscher, A., Reichenbach, A., Ugurbil, K., Uludag, K., 2010. The cortical site of
visual suppression by transcranial magnetic stimulation. Cereb. Cortex 20, 328–
338.
Tong, F., Nakayama, K., Vaughan, J.T., Kanwisher, N., 1998. Binocular rivalry and
visual awareness in human extrastriate cortex. Neuron 21, 753–759.
Tononi, G., 2004. An information integration theory of consciousness. BMC Neurosci.
5, 42.
Turk-Browne, N.B., Yi, D.J., Chun, M.M., 2006. Linking implicit and explicit memory:
common encoding factors and shared representations. Neuron 49, 917–927.
van Boxtel, J.A., Tsuchiya, N., Koch, C., 2010. Consciousness and attention: on suffi-
ciency and necessity. Front. Psychol. 1, 1–13.
van Dijk, H., Schoffelen, J.M., Oostenveld, R., Jensen, O., 2008. Prestimulus oscillatory
activity in the alpha band predicts visual discrimination ability. J. Neurosci. 28,
1816–1823.
Velmans, M., 1996. The Science of Consciousness. Routledge, London.
Vuilleumier, P., Driver, J., 2007. Modulation of visual processing by attention and
emotion: windows on causal interactions between human brain regions. Philos.
Trans. R. Soc. Lond. B: Biol. Sci. 362, 837–855.
Wheatstone, C., 1838. On some remarkable, and hitherto unobserved, phenomena
of binocular vision. Phil. Trans. R. Soc. Lond. 128, 371–394.
Wilenius, M.E., Revonsuo, A.T., 2007. Timing of the earliest ERP correlate of visual
awareness. Psychophysiology 44, 703–710.
Zaretskaya, N., Thielscher, A., Logothetis, N.K., Bartels, A., 2010. Disrupting pari-
etal function prolongs dominance durations in binocular rivalry. Curr. Biol. 20,
2106–2111.