Awareness and Consciousness
Awareness and Consciousness
Neuropsychological
Rehabilitation: An International
Journal
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What do we mean by
“conscious” and “aware”?
a
Adam Zeman
a
Peninsula Medical School, Exeter, UK
Published online: 24 Feb 2007.
To cite this article: Adam Zeman (2006) What do we mean by “conscious” and
“aware”?, Neuropsychological Rehabilitation: An International Journal, 16:4, 356-376,
DOI: 10.1080/09602010500484581
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NEUROPSYCHOLOGICAL REHABILITATION
2006, 16 (4), 356– 376
Adam Zeman
Peninsula Medical School, Exeter, UK
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Correspondence should be addressed to: Adam Zeman, Professor of Cognitive and Beha-
vioural Neurology, Peninsula Medical School, Mardon Neurorehabilitation Unit, Wonford
Road, Exeter EX2 4UD, UK. E-mail: [email protected]
This paper has been adapted, in part, from “What in the world is consciousness?”, in press in
Altered States of Consciousness (Progress in Brain Research), edited by Steven Laureys
(Elsevier), 2005; “Consciousness”, in Psychogenic Movement Disorders, edited by Mark
Hallett (Lipincott, Williams and Wilkins), 2006, and “Theories of Visual Awareness”, in The
Roots of Visual Awareness, edited by C. A. Heywood, A. D. Milner, and C. Blakemore,
Progress in Brain Research, Vol. 144 (Elsevier), 2004.
INTRODUCTION
Impairment of consciousness is a ubiquitous problem in medicine generally,
and especially so in neurology and neurosurgery which focus on the function-
ing of the chief organ of awareness, the brain. In our everyday practice we
routinely categorise states of consciousness, like sleep and coma, and we
readily quantify its levels, with tools like the Glasgow Coma Scale (Teasdale
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& Jennett, 1974) and the Wessex Head Injury Matrix (WHIM) (Shiel et al.,
2000); our clinical efforts are often directed toward restoring it, where it
has been abolished by injury or disease, and to removing it, for example in
anaesthesia and the treatment of insomnia, where it is an impediment to treat-
ment or an unwanted gift. We are, in other words, experts in the assessment
and manipulation of consciousness: but what, precisely, is the function we are
observing and treating? Is it a straightforward physiological process like
digestion, a behavioural output, like dancing a waltz, or an essentially
private, scientifically inaccessible, subjective event?
Consciousness is not alone, among psychological concepts, in calling
simultaneously for biological, behavioural and first-person styles of explora-
tion. But this requirement seems to be particularly acute in the case of
consciousness: this concept, above all others, focuses our attention on the
divide between body and mind, the tension between the objective and the sub-
jective realms, analysis by science and synthesis through experience. This is
what makes the study of consciousness both so attractive and so difficult.
Janus-faced, it looks out on one side towards the sciences of the human
body and human behaviour, on the other towards our subjectivity and an
ancient set of beliefs about what constitutes personhood. In understanding
consciousness we may hope to make sense of a web of interconnected
ideas, like the self, the soul and the will. Naturally, many of us have strong
background assumptions about the nature of these, which science may be
hard-pressed to accommodate fully.
We recently probed these assumptions in a survey of 250 undergraduates at
the University of Edinburgh, sampling their views on the relationship of mind
to brain (see Figure 1; Liew, Sharpe, Zeman: data submitted for publication).
The results are a reminder that consciousness and its associated terms are by
no means straightforward terms of science: both consciousness researchers
and the wider educated public inherit a vocabulary of terms which are
steeped in religious, philosophical and cultural history. This makes it worth-
while to spend a little time at the outset reminding ourselves of the complex-
ities of the concepts of consciousness and awareness. I shall approach these
358 ZEMAN
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Figure 1. The results of a survey of 250 students from several disciplines at the University of
Edinburgh on attitudes to mind and brain (Liew, Zeman et al., data submitted for publication).
sense—anyone who can obey your instructions and tell you the date is pre-
sumably aware—but it has a much stronger connotation of subjectivity
than the first sense: As we all know, it is often hard to be sure about what
is passing through another’s mind on the basis of their behaviour.
The general properties of awareness—the contents of consciousness—have
been much discussed. There is a consensus about the following properties: The
contents of consciousness are relatively stable for short periods of a few
hundred milliseconds, but characteristically changeful over longer ones; they
have a narrow focus at a given moment, but over time our awareness can
range across the spectrum of our psychological capacities, allowing us to be
aware of sensations, percepts, thoughts, memories, emotions, desires and inten-
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tions (our current awareness often combines elements from several of these
psychological domains); our awareness is personal, allowing us a distinctive,
limited perspective on the world; it is fundamental to the value we place on
our lives—keeping people alive once their capacity for awareness has been
permanently extinguished is widely regarded as a wasted effort (Jennett, 2005).
The relationships between wakefulness, awareness and their behavioural
indices are more involved than they appear at first sight (see Figure 2). As a
rule, while we are awake we are aware. But the phenomena of wakefulness
and awareness do not always run in parallel. The vegetative state, which
results from profound damage to the cerebral hemispheres and thalami, with
relative preservation of the brainstem, is a state of “wakefulness without aware-
ness”. Conversely, when we dream, we are asleep yet aware. Nor can we always
rely on behavioural criteria to diagnose consciousness: Patients paralysed for
surgery may be fully aware—if the anaesthetic drug has failed to reach
them—but completely unable to manifest their awareness; patients “locked
in” by a brainstem stroke may appear unconscious until someone recognises
their ability to communicate by movements of their eyes or eyelids.
Figure 2. Inter-relationships between arousal and awareness. See text for explanation. “Zombies”
are theoretical beings discussed by philosophers who display the signs of consciousness, yet lack
experience. The plausibility of such beings is controversial.
soon described the fundamental rhythms of the EEG (see Figure 3): beta,
at .13 Hz, which accompanies mental effort; alpha, at 8 –13 Hz, the signa-
ture of relaxed wakefulness; theta (4–7 Hz) and delta (,4 Hz) which predo-
minate in deep sleep.
In the 1950s Kleitman and his co-workers in Chicago discovered that sleep
itself has an internal architecture (Aserinsky & Kleitman, 1955; Dement &
Kleitman, 1957). Over the first hour of sleep, the sleeper descends through
a series of deepening stages into stage III and IV sleep in which slow
waves predominate (slow wave sleep, SWS, known as non-REM, NREM,
sleep), only to ascend back through these stages into a state resembling wake-
fulness in its EEG appearance, accompanied by rapid eye movements, pro-
found muscular atonia, autonomic arousal and vivid mentation—
dreaming, paradoxical or rapid eye movement sleep (REM) (see Figure 4).
This cycle repeats itself four or five times in the course of the night, with
decreasing amounts of SWS and increasing amounts of REM as the night pro-
ceeds. Recent work on the brain’s electrical rhythms has highlighted the
potential importance of rapid, widely synchronised, high frequency gamma
oscillations (25–100 Hz) in wakefulness and REM (Llinas & Ribary,
1993), although their true significance is not yet clear.
WHAT DO WE MEAN BY “CONSCIOUS” AND “AWARE”? 361
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Figure 3. The rhythms of the EEG: Records from diagnostic encephalograms performed in four
different patients, exemplifying beta rhythm (.14 Hz); alpha rhythm (8–13 Hz); theta rhythm
(4–7 Hz); delta rhythm (4 Hz). In each case the dotted line bisects a 2-second sample.
Figure 4. The architecture of sleep: An example of sleep staging over the course of a single night.
The sleeper passes from wakefulness to deep sleep and then ascends to REM sleep (dark bars).
Five similar cycles occur in the course of the night. The EEG tracings to the left show the EEG
appearances associated with the stages of sleep; the EEG in REM resembles the “awake” trace.
362
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Figure 5. The pharmacology of the brainstem activating systems. A: the origin and distribution of the central noradrenergic pathways in the rat brain;
B: dopaminergic pathways; C: the cholinergic pathways; D: the serotonergic pathways. CTT ¼ central tegmental tract; dltn ¼ dorsolateral tegmental
nucleus; DNAB ¼ dorsal noradrenergic ascending bundle; DR ¼ dorsal raphe; DS ¼ dorsal striatum; HDBB ¼ horizontal limb nucleus of the diagonal band
of Broca; Icj ¼ islands of Calleja; IP ¼ interpeduncular nucleus; LC ¼ locus ceruleus; MFB ¼ medial forebrain bundle; MS ¼ medial septum;
NBM ¼ nucleus basalis magnocellularis (Meynert in primates); OT ¼ olfactory tubercle; PFC ¼ prefrontal cortex; SN ¼ substantia nigra; tpp ¼ tegmental
pedunculopontine nucleus; VDBB ¼ vertical limb nucleus of the diagonal band of Broca; VNAB ¼ ventral noradrenergic ascending bundle; VS ¼ ventral
striatum (Robbins & Everitt, 1995).
WHAT DO WE MEAN BY “CONSCIOUS” AND “AWARE”? 363
ness, SWS, and REM. Pathological states include coma (Glasgow Coma
Score ,7, eyes closed), the vegetative state mentioned above, brain death
and the locked in syndrome (Working party of the Royal College of
Physicians, 2003) (Table 1). While wakefulness, SWS and REM are as a
rule mutually exclusive, overlaps between these states occasionally occur
(Mahowald & Schenck, 1992) (see Figure 7). For example, sleepwalking
reflects motor activation of the kind seen during wakefulness occurring at a
time when much of the brain is deactivated as during SWS (Bassetti et al.,
2000); REM sleep behaviour disorder, in which sufferers enact their
Figure 6. The AIM model: Hobson’s AIM model locates the three principle states of health
consciousness in a “state space” defined by input (I: external in wakefulness, internal during
REM), activation (A: high in REM and wakefulness, low in NREM sleep) and mode (M: during
REM, prefrontal regions involved in regulation of waking behaviour and encoding of memories are
deactivated) (Hobson & Pace-Schott, 2002).
364
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TABLE 1
The differential diagnosis of impaired awareness (Adapted from Working party of the Royal College of Physicians, 2003)
Figure 7. State boundary dissociation. The states of wakefulness, REM and NREM sleep are
normally distinct. Many parasomnias can be understood as the result of a fusion of two or more
states. For example, overlap between the phenomena of REM sleep and wakefulness (shaded)
gives rise to REM sleep behaviour disorder; overlap between NREM sleep and wakefulness occurs
during sleepwalking and night terrors (Mahowald & Schenck, 1992).
dreams, results from a failure of the normal atonia of REM sleep, allowing
dream mentation to give rise to behaviour, like self-defence, of a kind
which would normally be confined to wakefulness (Schenck, Bundlie,
Ettinger, & Mahowald, 1986).
Knowledge of the neural basis of awareness, of our experience, has also
been transformed by the path-breaking work of the past century on the
biology of cognition, exploring the neurology of perception, language,
memory, emotion, and action. Work on these psychological processes, and
their disruption by disease, is demonstrating increasingly fine-grained corre-
lations between features of our experience and details of neural processes.
The key role of visual area V4 in the conscious perception of colour, and
in its loss in central achromatopsia (Zeki, 1990) (loss of colour vision), and
the key role of area V5 in the perception of visual motion, and in its loss in
central akinetopsia (Zeki, 1991) are much cited examples. Correlation, of
course, does not imply cause. Recent work in this area has tried to tighten
the link between brain activity and conscious experience by investigating
how cerebral activity changes when our experience changes without any cor-
responding change in the world: examples include studies of imagery (Ishai,
Ungerleider, & Haxby, 2000), hallucinations (Ffytche et al., 1998) and the
modulation of awareness by attention or during binocular rivalry (Kanwisher,
2001). A second strategy for defining the neurology of consciousness is to
approach awareness by stealth, so to speak, by exploring the neurology of
unconscious processing. I shall discuss this line of work and fill out our
366 ZEMAN
Markova, 2003). I shall try to tease apart the principle strands of self-con-
sciousness/self-awareness.
The distinction between “self” and “other” is biologically crucial. There
are many activities which we need to direct towards other objects in the
world—like eating them—which it would be disastrous if we directed
towards ourselves. We should expect to find strategies for drawing this
distinction in the simplest organisms. But “self-consciousness” implies
more than an ability to behave differently towards self and other: It requires
a representation of self and other. A variety of different kinds of
representation fall out of the senses I shall discuss (and number for ease of
reference).
The colloquial sense of self-consciousness (1)—a proneness to embarrass-
ment in the presence of others—is rather sophisticated, as it implies the
person’s awareness that the awareness of others is directed on him or her.
A second sense (2), self-consciousness as self-detection, refers to a family
of forms of self-consciousness which are probably present in many
animals. This family includes awareness of stimuli which directly impinge
on the body (the ant walking up your arm); of proprioceptive information
about bodily position which contributes substantially to our body image; of
information about actions which we are about to perform or are performing,
giving rise to a sense of agency; of information about bodily state (hunger,
thirst, etc); and of emotions, like fear or affection, which signal the state of
our relationship to objects and to people around us, and without which we
are liable to lose the sense of our own reality or that of the world, as in “deper-
sonalisation” and “derealisation”.
A third sense, (3)—self-consciousness as self-monitoring—extends self-
detection in time into past and future, and in range, to encompass more
plainly cognitive abilities. It refers to the ability to recall the actions we
have recently performed (Beninger, Kendall, & Vanderwolf, 1974), and to
our ability to predict our chances of success in tasks which challenge
memory (Hampton, 2001) or perception (Smith, Shields, & Washburn,
2003): we undoubtedly possess these abilities, and ingenious experiments
WHAT DO WE MEAN BY “CONSCIOUS” AND “AWARE”? 367
TABLE 2
“Contrastive analysis”: Studies comparing conscious and unconscious brain activity
Laureys et al., 2000 Vegetative state vs recovery Increase in cortical metabolic rate
(Vegetative state) and restoration of connectivity
with recovery
John et al., 2001 Anaesthesia vs awareness Loss of gamma band activity and
(Anaesthesia) cross-cortical coherence under
anaesthesia
Sahraie et al., 1997 Aware vs unaware mode of Aware mode associated with
(Blindsight) perception in blindsight DLPF and PS activation,
patient GY unaware with medial F and
subcortical
Dehaene, 1998 Perceived numbers vs backward Unreported numbers underwent
(Backward masked but processed perceptual, semantic and motor
masking) numbers processing similar but less
intense to reported numbers
Kanwisher, 2000 Attention to “face” or “place” Activity in FFA and PPA locked to
(Binocular rivalry) when stimuli of both kinds presence or absence of
are simultaneously in view, awareness of face and place
or perception of face or place
during binocular rivalry
Moutoussis & Zeki, 2002 Perceived vs “invisible” but Similar but less intense activation
(Invisible stimuli) processed faces/houses of FFA and PPA by Invisible
stimuli
Engel et al., 2000 Perception of one or other of Firing of cells processing currently
(Binocular rivalry) a pair of rivalrous stimuli perceived stimulus better
synchronised than firing of cells
processing suppressed stimulus
Tononi & Edelman, 1998 Perception of high vs low More widespread and intense
(Binocular rivalry) frequency flicker during activation by
binocular rivalry perceived stimulus
Petersen et al., 1998 Effortful verb generation LPF, ant cing and cerebellar
(Task automatisation) task vs performance after activitation shifts to left
training perisylvian activation
with training
Key: ant cing ¼ anterior cingulate; DLPF ¼ dorsolateral prefrontal cortex; FFA ¼ fusiform face
area: LPF ¼ lateral prefrontal cortex; medial F ¼ medial frontal cortex; PPA ¼ parahippocampal
place area; PS ¼ prestriate.
370 ZEMAN
in their early days but so far indicate that several plausible candidates can
influence the chances that a given stream of neural processing will give
rise to awareness: The amplitude and duration of the associated activity, its
degree of synchronisation, its site (for example, cortical or subcortical) and
its neural “reach” or connectivity.
The most popular current model of conscious processing proposes that it
occurs when individually unconscious modules of cognitive function—con-
ceived of in either psychological or anatomical terms—join forces and com-
municate. In Baars’ Global Workspace Theory (Baars, 2002) and Dehaene’s
Neuronal Workspace Model (Dehaene & Naccache, 2003), information
becomes conscious when it is broadcast widely through the brain, allowing
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by a range of basic facts about experience and the brain. For example, dreams,
hallucinations, mental imagery and brain stimulation experiments teach us
that certain kinds of brain activity are all that is needed to produce experience.
The resulting experience looks nothing like the brain activity which causes it
and must therefore be different in kind from it, a stream of autonomous
mental events which arises from the physical ones in the brain.
This widespread conception of consciousness implies that awareness is a
deeply private matter, inaccessible to observation by third parties (Zeman,
2004). On this view, awareness casts an “inner light” on a private perform-
ance. In a patient just regaining awareness we imagine the light casting a fal-
tering glimmer, which grows steadier and stronger as a richer awareness
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turned into the wine of experience” in the words of another philosopher, Colin
McGinn (1991). Given the inner notion of consciousness this distinction
becomes an important one: Science promises to solve the hard but not the
easy question. Given the outer view, the distinction collapses: Explain how
the brain facilitates conscious behaviour, and consciousness is explained.
CONCLUSION
I have tried to give a guide, in this chapter, to the ambiguous concepts of con-
sciousness and awareness. I began with the uncontroversial distinction
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between the two key colloquial senses of consciousness, the relatively objec-
tive notion of wakefulness and the more subjective concept of awareness. I
outlined some key findings in neuroscience which have illuminated con-
sciousness in these two senses: They include the discoveries that conscious
states have electrical correlates which can be recorded from the surface of
the scalp; that these are regulated by pharmacologically specific structures
in the brainstem, thalamus and basal forebrain; and a multitude of findings
which support the general principle that the features of experience will corre-
spond to features of neural processing. We made a detour via self-conscious-
ness, teasing apart six related but separable senses of the term. Returning to
the main topic of consciousness, we identified a spectrum of senses that
extends between consciousness “narrow” and consciousness “broad”—con-
sciousness in its strong sense of knowledge shared with oneself, available
for report and the control of voluntary action, and consciousness in its
broad sense of “knowledge” pure and simple. I reviewed the evidence that
underpins global workspace theory, from contrasts between neural processes
that do and do not give rise to consciousness. We then examined the intuition
that what really matters to us when we are deciding whether a person or a state
is conscious is simply the occurrence of “experience”, not the possibility of
report or deliberate action: On this “inner” conception of consciousness,
experience is conceived as an immaterial, invisible and private process. I con-
trasted this to an “outer” conception which regards “consciousness” as short-
hand for intelligent behaviour. Finally we saw that those who are wedded to
the inner conception are likely to see the science of consciousness as con-
fronted by an insurmountable challenge—to solve the “hard” problem of con-
sciousness, bridging the explanatory gap between the physical and the
mental—while for those who accept the outer conception there is no worrying
gap between the two.
The complexities of the concepts of consciousness and awareness have
practical import: In scientific work we need to be clear which concept of con-
sciousness we hope to understand; in clinical work we need to be clear about
what kind of awareness we are hoping to restore; in communicating with
374 ZEMAN
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