Psychological Medicine The neural basis of consciousness

cambridge.org/psm
Chris D. Frith1,2
1
Wellcome Centre for Human Neuroimaging at University College London, UK and 2Institute of Philosophy,
Institute of Advanced Study, University of London, UK

Invited Review
Abstract
Cite this article: Frith CD (2019). The neural
Consciousness has evolved and is a feature of all animals with sufficiently complex nervous
basis of consciousness. Psychological Medicine
1–13. https://doi.org/10.1017/ systems. It is, therefore, primarily a problem for biology, rather than physics. In this review,
S0033291719002204 I will consider three aspects of consciousness: level of consciousness, whether we are awake
or in a coma; the contents of consciousness, what determines how a small amount of sensory
Received: 7 July 2019 information is associated with subjective experience, while the rest is not; and meta-consciousness,
Revised: 1 August 2019
Accepted: 5 August 2019 the ability to reflect upon our subjective experiences and, importantly, to share them with
others. I will discuss and compare current theories of the neural and cognitive mechanisms
Key words: involved in producing these three aspects of consciousness and conclude that the research
Consciousness; evolution; in this area is flourishing and has already succeeded to delineate these mechanisms in
meta-consciousness; working memory
surprising detail.
Author for correspondence:
Chris D. Frith,
E-mail: c.frith@ucl.ac.uk

© Cambridge University Press 2019
Introduction
The scientific study of consciousness remains as controversial as ever. It is widely taken for
granted that this is a ‘hard’ problem (Chalmers, 1995) and some thinkers (known as myster-
ians McGinn, 2012) claim that the problem is sufficiently hard that we will not be able to solve
it. Nevertheless, accounts of the neural basis of consciousness continue to be developed and
arguments between proponents can be fierce (e.g. Odegaard et al., 2017). There is an interest-
ing distinction between the theories that get media exposure and those that are discussed at
scientific meetings such as the Association for the Scientific Study of Consciousness (see
e.g. Michel et al., 2019). The media like philosophical approaches such as panpsychism, lead-
ing to headlines such as ‘Everything from spoons to stones is conscious’ (Goldhill, 2018). In
contrast, neuroscientists and psychologists like experimental data and there is now a great deal
of such data to discuss. In these circles, the dominant approach is global workspace theory
(Baars, 1988; Dehaene et al., 2003) to which I will return later in this essay.
The standard definition of being conscious, which I will use here, is having subjective
experiences. Two aspects of this definition are particularly worth considering. The first is
sometimes known as the level of consciousness. At one extreme, when I am in a coma or
deep sleep, I am not having any subjective experiences. At the other extreme, when I am
wide awake, I am having many rich and complex experiences. In relation to this aspect of con-
sciousness, we can ask ‘what neural systems are necessary and sufficient for being conscious,
rather than being in a coma?’
The second aspect is known as the content of consciousness, that is, what it is that I am
subjectively experiencing. This is a specific conscious state (sometimes called state con-
sciousness). The key insight driving research on this topic is that much precise and well-
adapted behaviour in a fully awake person can occur without consciousness (Jacob and
Jeannerod, 2003; Goodale and Milner, 2004). Furthermore, there are cases where perform-
ance actually deteriorates when people become conscious of what they are doing (Beilock
et al., 2002). It is therefore possible to contrast brain activity associated with neural pro-
cesses that lead to consciousness and those that do not. The paradigm example of this
approach is binocular rivalry. When different stimuli are presented to the left and right
eye (e.g. a house and a face) we do not see a mixture of a house and a face. Our conscious
perception alternates every few seconds between a house and a face, even though the sen-
sory input does not change. We can use this paradigm to track the neural activity that
changes with the conscious experience (Leopold and Logothetis, 1996). This strategy is
often referred to as the search for the neural correlates of consciousness (Rees et al.,
2002a; Kim and Blake, 2005).
In this review, I shall treat consciousness as a problem for biology rather than physics.
I assume that consciousness is a feature of living things and that it has evolved
(Carruthers, 2000; Bronfman et al., 2016). There was unconsciousness before consciousness,
and humans have richer conscious experiences than many other creatures. I will also set
aside the hard problem, making no attempt to explain how physical processes in the
brain can lead to subjective experiences. Instead, I shall consider some of the easier

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 2 Chris D. Frith
problems, exploring the neural processes that seem to be neces-
sary and sufficient for different aspects of consciousness.
Markers of subjective experience
To identify a neural correlate of consciousness we have to link
neural activity with subjective experience. But how do we access
subjective experience when it is not our own? The most direct
way is via some form of a report. This approach is particularly
useful for studying the contents of consciousness. So, in the
case of binocular rivalry, we ask participants to press the left but-
ton when they see a house and the right button when they see a
face. Such reports depend upon introspection and can vary in
sophistication.†1 The participant might simply report whether
they saw a stimulus or not or they might indicate how visible
the stimulus was on, say, a four-point scale (Ramsøy and
Overgaard, 2004). Introspection used to be the mainstay of
experimental psychology but fell into disrepute with the rise of
behaviourism. Nevertheless, simple introspective reports have
been used in studies of psychophysics from the work of Fechner
(1860) until today. Such studies are among the most replicable
in psychology (Read, 2015). Used carefully, introspection is a
robust source of data about subjective experience.
One problem with the use of report as a marker of subjective
experience is that the neural activity associated with the experi-
ence may be confounded with the neural activity associated
with reporting. ‘No report’ paradigms have been developed, but
they cannot avoid the problem that they have to be validated
via introspective reports (Overgaard and Fazekas, 2016). My
own view is that reportability is not a nuisance, but an important
feature of certain kinds of subjective experience (Frith and
Metzinger, 2016).
Another problem with the use of reports is that these largely,
although not entirely, depend on language. Of course, this is not
to claim that non-human animals and preverbal infants are not
conscious. But the study of subjective experience in such groups
is far more difficult.
A non-verbal sign that someone is conscious could be that
they engage in deliberate, intentional action rather than automatic
behaviour. This sign is particularly relevant to the study of levels
of consciousness. For example, a patient is typically considered to
be conscious if they can perform an arbitrary action in response to
the command. This is the basis of the test developed by Owen
et al. (2006) to demonstrate signs of consciousness in ∼20% of
patients apparently in a persistent vegetative state. Here, one
such command is to ‘imagine that you are playing tennis’.
When such a command is obeyed, activity is seen in specific
brain regions concerned with planning for action (Jeannerod,
2001). The idea is that, while the patient is unable to produce
any overt movements, she can still deliberately imagine making
a movement and the brain activity associated with such imagining
will be generated.
As with introspection, this approach is not fool proof. There
will be cases where it is difficult to tell whether an action is auto-
matic or deliberate (see e.g. Nachev and Husain, 2007). This prob-
lem is not only of academic interest. There is a great need for a
robust marker that tells us whether or not a comatose patent
still has some subjective experiences. Also, the distinction between
automatic and deliberate actions plays a critical role in the
†
The notes appear after the main text.
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application of the automatism defence in law. This defence can
allow a person who commits a crime to go free if the act was com-
mitted while unconscious (Rolnick and Parvizi, 2011). This
defence was successfully used in the case of a man who strangled
his wife while asleep (de Bruxelles, 2009). It is widely considered
that people should not be held responsible for acts performed in
the absence of consciousness (Shepherd, 2012).
The neural control of the level of consciousness
Our understanding of the neural control of the level of conscious-
ness is largely based on studies of brain activity in patients in
coma and related states. Through such studies, different levels
of consciousness can be compared and changes in activity asso-
ciated with recovery from coma can be recorded. In coma proper,
the patient is entirely unresponsive. In the vegetative state, the
patient goes through the sleep wake cycle (shown by EEG and
other signs), but does not respond to stimuli or show any signs
of intentional behaviour. A patient in a minimally conscious
state shows some responsiveness to stimuli and will sometimes
follow simple commands.
An important characteristic of the brain activity associated
with these states of reduced consciousness is that metabolic
activity is reduced. It has been estimated that consciousness
will not be found where metabolic activity has fallen below
∼40% of normal cortical activity (Stender et al., 2016). The
reduction of metabolism in the vegetative state is most pro-
nounced in the frontal and parietal cortex (Stender et al.,
2015), two brain regions that are strongly connected anatomic-
ally. Reduction of activity is accompanied by a loss of functional
connectivity between brain regions. In other words, distant brain
regions become disconnected, leading to a disruption of
large-scale information integration. This loss of connectivity is
correlated with the degree of clinical impairment, the loss
being greatest in coma patients and vegetative state, less in the
minimally conscious, while patients with locked-in syndrome
resemble healthy controls (Soddu et al., 2009). A similar loss
of connectivity and lack of integration is seen during the unre-
sponsiveness associated with anaesthesia (see Hudetz and
Mashour, 2016 for a review).
Of particular importance is the connectivity between intrala-
minar thalamic nuclei and prefrontal and anterior cingulate cor-
tices. A lack of such connectivity is seen in the vegetative state but
returns to normal after recovery of consciousness (Laureys et al.,
2000). Furthermore, after severe traumatic brain injury, behav-
ioural improvements in patients in the minimally conscious
state can be achieved via thalamic stimulation (Schiff et al.,
2007). This stimulation has the effect of reactivating thalamo-
cortical connectivity.
Connectivity in the cortico-cortical and cortico-thalamic brain
networks runs in both directions: forwards, for example, from
early sensory processing regions to prefrontal cortex (bottom-up)
and back again (top-down). The feedback connections are more
numerous and extensive than the feedforward connections
(Salin and Bullier, 1995). Boly et al. took account of this distinc-
tion in a study of vegetative state patients. They found that the
reduced connectivity in these patients was restricted to the feed-
back (top-down) connections, while feedforward connections
were preserved (Boly et al., 2011).
My conclusion from these studies is that wakeful, contentful
consciousness is associated with long range functional connectiv-
ity between distant brain regions. Of particular importance are
 Psychological Medicine
thalamo-cortical loops and large-scale cortical networks involving
frontal and parietal cortex. In particular, it is the top-down con-
trol instantiated in these networks that is important.
Relation to the current major theories of consciousness
These results provide a useful framework for introducing four
major theories currently available for understanding the neural
bases of consciousness. All of these theories receive partial sup-
port from these studies of the neural activity associated with dif-
ferent levels of consciousness. I suspect that, ultimately, all these
approaches will be combined in any viable account of the neural
basis of consciousness.
Integrated Information Theory (Tononi, 2008) assumes that
conscious experience requires a specific kind of integration of
information from many brain regions. Long-range brain connect-
ivity seems necessary for consciousness, but is it sufficient?
Recurrent Processing Theory (Lamme and Roelfsema, 2000)
assumes that conscious perceptual experience requires recurrent
processing (i.e. top-down feedback) in sensory areas. Top-down
neural feedback seems necessary for consciousness, but is it
sufficient?
Global Neuronal Workspace (Dehaene et al., 2003) assumes
that the contents of conscious experience can be equated with
the contents of a work space, a form of working memory, contain-
ing ‘momentarily active, subjectively experienced’ events that can
be compared and manipulated (Baddeley, 1992; Baars, 2002).
While consciousness does not seem to be necessary for contents
to maintained in working memory, it does seem to be required
for manipulation of the content (Trübutschek et al., 2019).
On this account, consciousness requires the involvement of
the fronto-parietal network associated with working memory
(see, e.g. Collette and Van der Linden, 2002). The loss of activity
in the fronto-parietal network associated with the vegetative state
is consistent with the global workspace hypothesis. But can con-
sciousness occur without working memory processes and the
associated brain regions being engaged (see, e.g. Moutoussis and
Zeki, 2002)?
Higher-Order Theories (Lau and Rosenthal, 2011) assume that
consciousness involves thinking about (i.e. representing) first-order
mental states. This requires a higher-order re-representation of, for
example, seeing a face. Such higher-order representations involve
frontal cortex. This theory is also compatible with the observation
that frontal activity is reduced in vegetative state patients. But is an
intact frontal cortex necessary for consciousness?
Altered states of consciousness
The characterisation of the level of consciousness as a single
dimension varying from coma to alert wakefulness has been cri-
ticised as inadequate (Bayne et al., 2016). Consider, for example,
the conscious experiences of a patient with dense amnesia. One
such patient kept a note book in which he repeatedly wrote
‘I have just woken up’ (Wilson et al., 1995). This patient was
alert and awake, but his subjective experience was very different
from that of most people since it lacked any temporal continuity.
This is an example of an altered state of consciousness. Bayne
et al. (2016) suggest that the state of consciousness can vary
along with a number of dimensions, so that altered states of con-
sciousness should be characterised by their position in this multi-
dimensional space rather than being ordered along a single
dimension of the level of consciousness. It remains to be seen
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3
Fig. 1. The effects of high and low doses of psilocybin, redrawn from (Lewis et al.,
2017).
what these dimensions might be, but temporal continuity might
be one of them.
Altered states of consciousness have more typically been asso-
ciated with the effects of psychoactive drugs and questionnaires
have been developed for characterising these states (e.g.
Studerus et al., 2010). This questionnaire provides scores on a
number of dimensions, including experience of unity, disembodi-
ment, and complex imagery. There is evidence that different sub-
stances relocate users in different parts of a multi-dimensional
space of conscious experience. For example, experiences after tak-
ing LSD are dominated by changes in visual perception (e.g. com-
plex imagery and audio-visual synaesthesia). ‘Blissful state’ is also
elevated, while ‘anxiety’ is least elevated (Carhart-Harris et al.,
2016). In another study, psychedelics (LSD and psilocybin)
increased the phenomenological richness of experience, while
reducing the sense of bodily self (Millière et al., 2018). There is
also evidence that even micro-doses of LSD can alter the percep-
tion of time (Yanakieva et al., 2018).
It is probable that the precise location in the ‘space’ of con-
sciousness created by different substances can be related to the
mode of action of the drug, for example, whether it targets sero-
tonin receptors (e.g. mescaline, LSD, psilocybin) or opioid recep-
tors (e.g. opium, morphine) (Zamberlan et al., 2018). This role for
neurotransmitters in sculpting the space of conscious experience
confirms the importance of long-range brain connectivity.
Neurotransmitters alter the weighting of the various modes of
connectivity in the brain (e.g. Hahn et al., 2012) and the rising
monoamine pathways have distinct, modulatory effects on sen-
sory processing (Jacob and Nienborg, 2018) (Fig. 1).
The contents of consciousness
The majority of studies on the neural basis of consciousness are
concerned with the contents of consciousness. A classic paradigm,
mentioned already, is a binocular rivalry. Here we can look at the
brain activity when a face is presented to one eye and a house to
the other. During binocular rivalry, brain activity shifts to match
the current contents of consciousness (but see Giles et al., 2016).
When we perceive the face, activity is higher in the face area of the
fusiform cortex. When we perceive the house, activity is higher in
the place area of the para-hippocampal cortex (Tong et al., 1998)
(see also Moutoussis and Zeki, 2002).
 4 Chris D. Frith
Visual masking is another widely used paradigm for identify-
ing brain activity associated with the content of consciousness.
Using this paradigm, it is possible to identify brain activity asso-
ciated with stimuli that influence behaviour in the absence of any
subjective experience. This is because visual masking terminates
neural processing before the stimulus is finally represented in
consciousness. For example, if a fearful face is presented for
33 ms and immediately replaced by a neutral face, participants
report seeing only the neutral face. Nevertheless, activity is elicited
in the amygdala in response to the unseen fearful face (Whalen
et al., 1998). This technique has been used in series of studies
of word reading by Dehaene et al. who have shown that unseen
masked words alter the processing of subsequently presented
words (semantic priming) (Dehaene et al., 1998). These masked
words elicit activity in the visual word form area of fusiform cor-
tex. When the same words are perceived consciously, activity in
the visual word form area is greater and additional activity is
seen in the parietal and frontal cortex (Dehaene et al., 2001). A
similar result was obtained using the phenomenon of change
blindness, where participants often fail to notice a change in rap-
idly repeating stimuli (Jensen et al., 2011). Using this paradigm, it
is possible to compare three well matched conditions: no change
occurs, undetected change occurs, detected change occurs. Beck
et al. (2001) used this approach with faces as the changing stimuli.
In comparison to no change an undetected change in the identity
of the face elicited activity in the face area of the fusiform cortex
(FFA). When detected changes were compared with undetected
changes greater activity was seen in the FFA as well as activity
in the parietal and frontal cortex. The parallels with the results
of Dehaene et al. are striking (but see Moutoussis and Zeki, 2002).
A role for parietal cortex in specific conscious experiences was
already suspected on the basis of the spatial neglect that can occur
after damage to the right parietal cortex (Driver and Vuilleumier,
2001). In patients with such lesions, awareness of a stimulus (e.g.
a face) on the left side of space can be extinguished if a second
stimulus is presented on the right side. However, an extinguished
face stimulus on the left still robustly activates the fusiform face
area in the right cortex. When the left visual stimulus is con-
sciously perceived, greater activity is seen in the frontal and par-
ietal areas of the intact hemisphere (Rees et al., 2002b). These
results suggest that activity in the FFA is necessary for the con-
scious experience of a face, but not sufficient.
Essential nodes for specific conscious experiences
The FFA is just one of many specific brain regions that are essen-
tial for different specific conscious experiences. For example, area
V5/MT is necessary for the experience of visual motion (Zeki,
1991). But, to confirm that these nodes are indeed essential for
specific conscious experiences, we need to show that conscious
experience is affected when activity in these areas is directly
manipulated. This can be achieved by electrical stimulation or
as the result of lesions.
Electrical stimulation of discrete regions of visual cortex can
elicit a variety of visual experiences the precise nature of which
depends upon the location of the stimulation. Simple visual
forms are elicited by stimulation of the striate cortex, experiences
of colour and motion by stimulation of distinct regions of extra-
striate visual cortex, and complex forms by stimulation of the fusi-
form gyrus (Lee et al., 2000). Visual hallucinations of complex
scenes can be elicited by stimulation of the para-hippocampal
place area in the inferior temporal cortex (Mégevand et al.,
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2014). These results also demonstrate that visual input from the
retina and subcortical structures is not necessary for a conscious
visual experience.
Conversely, loss of the conscious experience of colour or visual
motion occurs after circumscribed damage to extra-striate areas
V4 (achromatopsia, Zeki, 1990) and V5/MT (akinetopsia, Zeki,
1991).
Not just visual experience
The search for the neural correlates of consciousness has been
dominated by studies of vision because the visual system in the
brain is more amenable to study than any other system. As a
result, we have much less information about the location of the
essential nodes for other aspects of conscious experience. In the
case of audition, secondary auditory cortex, in particular, the pla-
num temporale (Griffiths and Warren, 2002), is probably an
essential node for the experience of sound (Dykstra et al.,
2017). In the rare cases where auditory cortex has been damaged
bilaterally, profound deafness results. One such patient was
entirely unable to interpret sounds, but could detect onsets and
offsets of sounds when cued to attend (Engelien et al., 2000).
More or less complicated auditory hallucinations occur when
this region is activated during temporal lobe epilepsy (Florindo
et al., 2006) or by direct electrical stimulation (Penfield and
Perot, 1963).
The primary somatosensory cortex is likely to be the essential
node for the experience of touch (Schwartz et al., 2004), while the
anterior insula is likely to be an essential node for interoceptive
experience (awareness of bodily states such as ones’ own heart-
beat, thirst, &c. Craig, 2009).
The conscious experience that accompanies voluntary actions
has been repeatedly linked to the pre-SMA (Altena et al., 2013).
Neuronal activity in the pre-SMA is related to the awareness of
intentions to act (Lau et al., 2004; Fried et al., 2011), whereas dir-
ect electrical stimulation of this area can elicit the experience of an
‘urge’ to move a specific body part (Fried et al., 1991).
The nodes are necessary, but not sufficient: the role of parietal
and frontal cortex
Although these nodes are essential for various types of content of
conscious experience, they are not sufficient. Several studies sug-
gest that long range coupling of these regions with frontal and
parietal cortex are also necessary.
The parietal cortex has a role in a range of different conscious
experiences (see, e.g. Bor and Seth, 2012). After the damage to
this region, visual cortex activity alone is not sufficient to result
in awareness. For example, after parietal lesions, patients suffer
from a loss of awareness of stimuli on one side of space (unilateral
neglect). In these cases, the visual cortex is intact and processing
can still take place for neglected stimuli, without reaching the
patient’s awareness (Driver and Vuilleumier, 2001). The same
phenomenon can be observed for tactile stimuli. After parietal
damage, activity in the somatosensory cortex may not lead to tact-
ile awareness (Valenza et al., 2004). Similarly, amygdala and orbi-
tofrontal cortex can be activated by emotional stimuli without
awareness after parietal damage (Vuilleumier et al., 2002).
Patients with parietal lesions can no longer report the time at
which they had the intention to move, although they can still
report the time at which they initiated a movement (Sirigu
et al., 2004).
 Psychological Medicine
Disruption of parietal or prefrontal cortex in normal volun-
teers receiving transcranial magnetic stimulation impairs change
detection (e.g. Beck et al., 2006) and alters the dynamics of bin-
ocular rivalry (Zaretskaya et al., 2010). The prefrontal cortex
also has a role in awareness of action. Patients with prefrontal
lesions can make normal adjustments to their movements when
performing tasks in which there is sensory-motor conflict, while
at the same time being unaware of the conflict (Slachevsky
et al., 2001).
The limited capacity of conscious experience. These results sug-
gest that an interaction between frontal and parietal cortex with
stimulus-specific information in sensory cortices may be neces-
sary for specific conscious experiences. But what is the role of par-
ietal and frontal cortex in conscious experience? Prefrontal cortex
and parietal cortex are the major neural substrates for the cogni-
tive processes required for working memory, especially for the
selection of the content that enters the work space (Quentin
et al., 2019) and for the manipulation of the items held there
(Wager and Smith, 2003). So, the role of these regions in con-
sciousness is consistent with the idea that we can equate the con-
tents of consciousness with the contents of working memory.
A well-established feature of working memory is that it has a
very limited capacity (Cowan, 2001). It would follow, therefore,
that, like working memory, our conscious experience also has a
very limited capacity. At first glance, this idea seems incompatible
with the extra-ordinary richness of our conscious experience.
However, phenomena, such as change blindness (Jensen et al.,
2011), suggest that our visual experience is actually rather sparse.
It comes as a surprise to learn that very little of the information
that is currently striking our senses is included in our experience.
Rather, the richness of our visual experience is confined to the
centre of our gaze and attention (Kouider et al., 2010), and we
know that this rich experience will be carried over to wherever
we may shift our gaze (Noe et al., 2000).
There is, however, another aspect of our conscious experience
that makes it rich. If I am gazing at a strawberry, I am not simply
experiencing its colour, I am also experiencing its shape, its smell,
what it would feel like in my hand and in my mouth, and whether
I can reach for it.2 All these lower level features are bound
together to form the rich experience of the strawberry. This bind-
ing together of low-level features to form a highly compressed sin-
gle representation is a form of chunking. Chunking is a
long-established feature of working memory, often put forward
as a mechanism for overcoming its limited capacity (Miller,
1956; Gobet et al., 2001). For example, it is noted that we can
remember four letters, four words or four sentences, revealing
increasing amounts of information being stored in the same lim-
ited number of slots. Chunking takes advantage of redundancies
in the information to be stored so that it can be recoded and com-
pressed into a form that is optimal for the task in hand (Bor and
Seth, 2012).
I suggest that this process of compression is not simply a
mechanism to compensate for a limited capacity system. The
right kind of compressions can create representations that allow
better communication of information within the space of working
memory and also when reporting to others (Shea and Frith,
2019). Coarse graining, for example, provides a compressed
representation in which the effective information is greater than
would be the case if unlimited capacity allowed for representation
at a microscale level of detail (Hoel, 2017). Such simplifications
are also necessary in order to solve complex, multi-step planning
problems (Huys et al., 2015).
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5
Parietal and frontal cortex are the likely substrates in which
these compressed representations are created. For example, par-
ietal cortex has been implicated in sensory feature binding (e.g.
Friedman-Hill et al., 1995; Rohe and Noppeney, 2015), while
the requirement to chunk items has been shown to robustly acti-
vate the prefrontal-parietal network (Bor and Seth, 2012).
In summary, these studies offer a more precise definition of
the neural basis of the contents of consciousness. This aspect of
consciousness relies on an interaction between two systems, the
essential nodes (e.g. the fusiform face area), which determine
the specific content, and a frontal and parietal network, which
binds the content into the compressed and enriched form that
we experience. This formulation is compatible with Global
Workspace Theory (Dehaene et al., 2003), but also suggests that
the other theories provide additional relevant explanations.
Critical here is long-range connectivity. This is required so that
information can be integrated in a manner that optimises com-
pression. This would be consistent with a version of the
Integrated Information Theory (Tononi, 2008). Top-down feed-
back from higher-level cortical regions to sensory cortical areas
is involved, implying that recurrent processing is necessary
(Lamme and Roelfsema, 2000). There is clearly a role for frontal
cortex in the conscious experience via some sort of interaction
with lower-level sensory information, but whether this involves
the kind of re-representation proposed by Higher-Order
Theories (Lau and Rosenthal, 2011) remains unclear.
A higher level of consciousness: explicit metacognition
The contents of subjective experience discussed so far are some-
times referred to as being at the object level (or C1 Dehaene
et al., 2017), as, for example, in my experience of the strawberry:
a representation in consciousness of an object in the outside
world. But there is another level of consciousness, the meta
level (C2), which monitors the representation at the object level
(Nelson and Narens, 1990). For example, I might suddenly realise
that I have been so fixated on the strawberry, that I have stopped
listening to what my dining companion is saying. I have become
aware that my mind has wandered from my intended focus
(Schooler, 2002). This higher level of consciousness, sometimes
referred as meta-consciousness or self-monitoring, often involves
a subjective experience of error (Dehaene et al., 2017).
Another way of distinguishing C1 and C2 is that C1 involves
awareness of representations (contents), while C2 involves the
additional awareness of processes (Shea and Frith, 2016). This
distinction relates to dual process theory as applied to problem
solving (Evans and Stanovich, 2013). In intuitive problem solving
(system 1), we are typically aware of the problem and of the
answer (C1), but not of the process by which the answer is
derived. This process occurs rapidly and automatically without
consciousness. In contrast, system 2 reasoning involves deliberate
attention to the processes by which the problem is solved (C2).
This monitoring of cognitive processes, thinking about think-
ing, is often referred to as metacognition. Early studies of meta-
cognition mostly concerned memory. A striking example is the
tip-of-the-tongue phenomenon (Brown and McNeill, 1966) an
example of the feeling of knowing. This is the experience of not
being able to retrieve some item from memory, while, at the
same time, being confident that the item is available and will
soon be retrieved (Proust, 2010). Metacognitive judgement can
be made about various aspects of memory. For example, prospect-
ive and retrospective confidence in one’s learning of new material
 6 Chris D. Frith
and the ordering of one’s confidence about learning different
kinds of material (Metcalfe and Shimamura, 1994). The experi-
ence of confidence has also been extensively studied in perceptual
decision tasks. In such tasks, participants are asked not only
object level questions about the stimulus ‘Were the dots moving
left or right?’, but also meta-level questions about their percep-
tion, ‘How well could you see the stimulus?’ or ‘How confident
are you in your decision?’.
Metacognition, since it involves the monitoring and control of
lower-level cognitive processes, is a component of executive func-
tion (Shallice, 1982) and therefore prefrontal cortex is likely to
have a critical role (Shimamura, 2000). A recent meta-analysis
examined imaging studies of metacognition in perceptual decision
making and memory tasks (Vaccaro and Fleming, 2018). In these
studies, brain activity was elicited by requiring participants to
make judgements of confidence. The medial and lateral prefrontal
cortex, precuneus (medial parietal), and anterior insula were iden-
tified as important for such judgements for both decision-making
and memory.
More recently, a computational approach derived from signal
detection theory has been applied to the measurement of confi-
dence in perceptual decision tasks (Fleming and Lau, 2014).
The signal-detection approach assumes that there are two aspects
to metacognition in these tasks: bias of confidence and accuracy
of confidence. Bias measures a general level of confidence, such
that an over-confident person over-estimates the probability of
being correct on every trial of a perceptual task. The person
with accurate confidence is more confident in trials where she
is correct and less confident in trials where she is wrong. This sen-
sitivity of confidence to the correctness of trials is independent of
the overall level of confidence (bias).
At the level of signal-detection, we can measure objectively how
good people are at recognising when a signal is present or absent. At
the metacognitive level, we can measure objectively how good people
are at distinguishing between their correct and incorrect decisions
independently of any bias they may have. In other words, people
know, to some extent, when they are guessing. Accuracy at this
meta-level can be independent of accuracy at the object level. A per-
son might be good at detecting the signal, while, at the same time,
not very good at knowing when they were right or wrong.
Fleming et al. looked at individual differences in metacognitive
sensitivity that were independent of objective signal detection per-
formance (Fleming et al., 2010). They found that greater metacog-
nitive accuracy was associated with greater grey matter volume in
the anterior prefrontal cortex (Brodmann area 10). A subsequent
study (McCurdy et al., 2013) confirmed this result and indicated
that the precuneus might also have a role in metacognitive sensi-
tivity. The role of PFC in metacognitive accuracy has been con-
firmed in a lesion study and a brain stimulation study. Anterior
PFC lesions had no effect on signal detection performance at
the object level, but resulted in a ∼50% loss in metacognitive sen-
sitivity (Fleming et al., 2014). These patients’ confidence reports
no longer related to their performance. Application of TMS to
the prefrontal cortex in healthy volunteers produces very similar
results. TMS has no effect on signal detection, but it impairs
metacognitive accuracy (Rounis et al., 2010).
Monitoring our actions
We have a very little subjective experience of the precise details of
our actions (e.g. Fourneret and Jeannerod, 1998). But we are very
much aware when things go wrong. We experience a loss of
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control when the movement that we intended is not the one
that occurred. We experience a loss of agency when the effect
that we intended in the outside world does not occur.
After an error has occurred in a choice reaction time task, the
next response is typically slower (Rabbitt, 1966). This post-error
slowing indicates that the performance is being monitored. The
actor detects an error and slows down so as to avoid further
errors. Post-error slowing is therefore a consequence of metacog-
nition, although, in this case, no report of confidence is involved.
However, this post-error slowing can occur in the absence of
awareness. In a study of skilled typists, real errors of which the
typist was unaware, were followed by post error slowing, while
fake ‘errors’, inserted by the experimenters, were reported as
errors, but were not followed by post-error slowing (Logan and
Crump, 2010). A similar distinction between conscious and
unconscious monitoring of errors was found when visual masking
was used so that participants sometimes made decisions about
targets that they classified as ‘unseen’ (Charles et al., 2013).
Even on unseen trials, actors performed better than chance.
However, the error related negativity, an EEG response associated
with error detection, was only elicited by errors occurring on trials
in which the target was seen. These results suggest that there are
two forms of meta-cognition; implicit (without awareness) and
explicit (with awareness).
Source localisation based on magneto-encephalography
(MEG), suggested that the unconscious detection of errors was
associated with a short-lived response confined to anterior cingu-
late cortex. In contrast, conscious detection of errors was asso-
ciated with robust activity in anterior and posterior cingulate
cortex. Recording activity in neurons in the posterior cingulate
cortex of the monkey has also revealed a robust response to errors
during the learning of a conditional association task (Heilbronner
and Platt, 2013). These responses were especially marked when
performance was poor and the task was difficult. These are con-
ditions in which the detection of errors would be highly relevant
for learning.
An important aspect of the experience of action is the ease or
fluency with which the action can be selected. Reduced fluency is
associated with a reduced feeling of control (e.g. Chambon and
Haggard, 2012) and increased likelihood of errors. When partici-
pants are asked to monitor the fluency of action selection greater
activity is seen in anterior cingulate and anterior insula (Teuchies
et al., 2019). When actors are required to make metacognitive
judgments about the extent of their own control compared with
when they are required to make judgments that are not about con-
trol (i.e. judgments about performance), increased activity is
observed in the anterior PFC (Miele et al., 2011). This area is
located close to the region identified in studies of metacognitive
sensitivity in perceptual decisions (e.g. Fleming et al., 2010).
Imaging studies of the experience of agency have explored the
ability to distinguish between whether an outcome was caused
by the self or another. Activity in temporo-parietal junction
(TPJ), pre-SMA, precuneus and dorsomedial prefrontal cortex
(dMPFC) was higher during the experience of external-agency,
while insula activation was associated with self-agency (Sperduti
et al., 2011).
Explicit metacognition and the brain: awareness of the self
and the other
The results reviewed above identify a discrete network of brain
areas associated with explicit metacognition (C2, meta-
 Psychological Medicine
consciousness), which is largely independent of whether memory,
decision making, or action is involved. This network includes
anterior prefrontal cortex (Brodmann area 10), anterior insula,
and midline structures, including anterior cingulate, posterior cin-
gulate and precuneus.
The anterior insula and various midline cortical structures
have previously been proposed as critical for the experience of
the self. The anterior insula has been associated with interocep-
tion and the experience of the bodily self (Craig, 2009). More
abstract aspects of the self, such as autobiographical memory,
are associated with midline cortical structures; ventro-medial pre-
frontal cortex, dorso-medial prefrontal cortex, anterior cingulate,
and posterior cingulate/precuneus (Northoff et al., 2006).
There is also a striking overlap between the network of brain
regions associated with explicit metacognition and that associated
with the ability to mentalise, suggesting that these regions are
required for thinking about the thoughts of others as well as
about one’s own thoughts (Vaccaro and Fleming, 2018).
The evolution of consciousness
At the beginning of this essay, I suggested that consciousness is a
biological phenomenon found in many living creatures. In par-
ticular, I proposed that consciousness has evolved (see e.g.
Carruthers, 2000). This assumption raises two questions: When
did consciousness emerge in the history of evolution? What is
the survival value of consciousness that drove its evolution?
The question about the survival value of consciousness is
probably easier to answer, since it should be possible to identify
tasks which can be achieved without consciousness and contrast
these with tasks that require consciousness, or, at least, are per-
formed much better with consciousness. But we also need a prin-
cipled way of specifying the differences between the tasks so
identified. In the brief speculations presented here, I shall attempt
to distinguish between the classes of a task in terms of the under-
lying computations.
With regard to C1 or primary consciousness (sometimes called
sentience), it is widely held that this is a feature of many animals,
and not just humans (e.g. Low et al., 2012). This means that tasks
that depend upon a report will not be a useful basis for our con-
siderations. As I mentioned at the beginning of this essay, one
non-verbal sign that someone is conscious is that they engage
in deliberate, intentional action rather than automatic behaviour.
But what is the computational distinction between automatic
behaviour and deliberate, intentional behaviour?
Automatic, unconscious behaviour and model-free learning
Automatic behaviours can be precise and well adapted (Jacob and
Jeannerod, 2003; Goodale and Milner, 2004), but are inflexible
and can sometimes be difficult to suppress when inappropriate
(Aarts and Custers, 2010). These automatic behaviours, some-
times referred to as habits, are acquired through a form of associ-
ation learning in which direct connections are developed between
stimuli and responses so that presentation of the stimulus auto-
matically elicits a habitual response (Daw et al., 2002). They are
essentially reflexes that can be modified by experience. In more
recent computational formulations, they are considered to arise
through model-free learning. Model-free learning is a slow process
by which we evaluate how good (valuable) actions are through a
process of trial and error. This requires no knowledge of the state
of the world or of the consequences of actions. Furthermore, since
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7
the values are continually updated, no information is retained
about the past. Model-free learning does not make complex com-
putational demands, but does require extensive experience and is
therefore slow (Huys et al., 2013). Studies in humans show that
such automatic behaviours and the learning associated with
them can occur in the absence of conscious experience of the
stimuli (e.g. Eimer, 1999) or of the outcomes of actions (e.g.
Pessiglione et al., 2007).
Deliberate, intentional action and model-based learning
In contrast to model-free learning, model-based learning produces
rapid, flexible goal directed behaviour. While model-free systems
learn about rewards, model-based systems learn about states of
the world and their relationships. Model-based learning uses
models of the world to evaluate possible actions on the basis of
anticipated future outcomes (Doll et al., 2012). These internal
models release the organism from subservience to the environ-
ment and to habitual behaviour. A prototypical example of
such a world model would be the cognitive map of a maze,
which enables an animal to select a novel route through it
when established routes are blocked (Tolman et al., 1946).
Models of the immediate past enable one of the most basic func-
tions of working memory, that is, the ability to respond on the
basis of a stimulus which is no longer physically present.
Models of the more distant past, episodic memory, can be used
when a new situation is encountered and a decision must be
made concerning what action to take. A model of the current situ-
ation is compared with models of past situations. The action cho-
sen is the one associated with the highest value, based on the
outcomes of the past situations that are most similar to the pre-
sent (Botvinick et al., 2019).
A model of the task currently being performed, for example,
knowing about the set of appropriate responses, permits a simple
form of counterfactual learning. For example, in serial reversal
learning, where there are only two options, a drop in the value
of one option (go left) implies an increase in the value of the
other option (go right). A model-free system would be blind to
such a structure since it can only update the value of the action
performed. A slow process of trial and error learning would be
needed to respond to the change in the state created by the rever-
sal. In contrast, a model-based system recognises that, if the cho-
sen option has not been rewarded, then the other option would
have been rewarded and its value should be increased. This
requires counterfactual reasoning, considering what would have
happened if the other option had been chosen (Lee et al.,
2005). At the same time a model of the task, which recognises
that there are two possible states of the task, allows an immediate
switch to the alternative action when the reversal occurs. The
‘learning to learn’ (Harlow, 1949) that is possible with model-
based learning enables a much more rapid response to environ-
mental changes than is possible for model-free learning.
The studies reviewed above show that model-based learning
enables fast and flexible responses to changes in the environment
and is plausibly identified as the computational basis for the
deliberate, intentional action that is a non-verbal sign of con-
sciousness. In this framework, the contents of consciousness
would be identified as the mental models currently active for
decision-making, essentially a reformulation of the idea that con-
scious contents can be equated with the content of working
memory.
 8 Chris D. Frith
Fig. 2. A hierarchy of control.
Brain imaging studies implicate subcortical areas, in particular,
the basal ganglia, as underlying model-free learning. For example,
learning through outcomes of which the participants were
unaware (Pessiglione et al., 2007) was associated with activity in
the ventral pallidum. In another brain imaging study, a distinction
could be made between reward prediction errors, associated with
model-free learning and state prediction errors associated with
model-based learning (Gläscher et al., 2010). Activity associated
with reward prediction errors (model-free) was observed in the
ventral striatum, while activity associated with state prediction
errors (model-based) was observed in the inter-parietal sulcus
and the lateral prefrontal cortex.
These results are consistent with the claim that, in mammals,
conscious experience is associated with cortical activity, with a
special role for parietal and frontal cortex. However, this conclu-
sion cannot be applied to sentient animals such as birds or cepha-
lopods, with very different nervous systems. Rather than linking
consciousness to particular brain regions, it should be linked to
specific, cognitive mechanisms at Marr’s algorithmic level of ana-
lysis (Marr, 1982). The precise instantiation of the relevant algo-
rithms in the CNS will vary from one species to another.
It has been argued that primary consciousness (minimal con-
sciousness or sentience) emerged ∼520 million years ago during
the Cambrian explosion. For Bronfman et al. (2016) the argu-
ment was based on the emergence of a CNS that could perform
‘unlimited association learning’, a version of model-based learn-
ing. For Feinberg and Mallatt (2016) a critical event in the devel-
opment of sentience was the emergence of sensory maps (mental
images) in the CNS, such as, for example, the topographical maps
in the optic tectum of the fish. The limited consciousness experi-
enced by fish must be very different from the subjective experi-
ence of mammals. However, this difference is quantitative
rather than qualitative. All these different species are alike in hav-
ing subjective experiences. But the conscious experience of the
mammal is richer as a result of the evolution of, among other
things, more complex sense organs and a greater information
processing capacity.
Meta-consciousness: a higher level of consciousness
With the evolution of the processes underlying explicit metacog-
nition, however, there was a qualitative change in consciousness.
It is reasonable to assume that C2 has evolved much more
recently than C1 and explicit metacognition is much more devel-
oped in humans compared to other animals (Metcalfe, 2008).
While there is some evidence that non-human animals can take
account of their confidence in a decision (Smith et al., 2003), it
remains to be shown that this involves the kind of second-order
computations that I will discuss below (see Fleming and Daw,
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2017 for a discussion of how the kind of metacognition observed
in non-human animals can arise from first-order computations).
Meta-consciousness provides a number of advantages over and
above primary consciousness. For example, a well calibrated feel-
ing of confidence can act a signal for learning when no external
feedback is available (Guggenmos and Sterzer, 2017), since a con-
fident decision is likely to be correct, while a non-confident one
will often be wrong. Lack of confidence in our model of the
world will lead us to collect more information (to explore, rather
than exploit Boldt et al., 2019). Monitoring our decision processes
can also help us to identify the source of an error (Purcell and
Kiani, 2016). Is it a consequence of inadequate sensory process-
ing, indicated by low perceptual confidence, or is it the result of
poor understanding of the task, indicated by low response confi-
dence? Distinguishing between these two sorts of error enhances
the efficiency of model-based learning.
However, an even greater advantage arising from this higher
level of consciousness is the possibility for sharing our experiences
with others that it makes possible. Sharing experiences may be a
uniquely human ability which can optimise social interactions
(Shea et al., 2014). For example, discussions of confidence make
it possible for two people to make perceptual decisions that are
better than either person working on their own (Fusaroli et al.,
2012). Even more important is that the ability to share experi-
ences, such as the feeling of agency, can give rise to cultural con-
cepts such as personal responsibility and, more generally, can
enable the emergence of cumulative cultural norms (Frith, 2014).
The model-based system associated with primary conscious-
ness probably evolved on top of an earlier model-free system,
rather than separately and in parallel (Doll et al., 2012). It freed
organisms from subservience to the immediate environment
and from habit. In the same way, the system subserving meta-
consciousness evolved on top of the model-based system and
freed us from subservience to our models of the world. As a result,
we can now question the validity of our models of the world and
discuss them with others (Fig. 2).
Fleming and Daw (2017) have recently provided a Bayesian
framework for the computation of confidence which highlights
this second order aspect of meta-consciousness. They argue that
correctly judging confidence requires inferences about the causes
of one’s own behaviour. In other words, while the decision mech-
anism makes use of a model of the world, the metacognitive
mechanism that estimates confidence in the decision makes use
of a model of the decision-maker. Wokke et al. (2019) also con-
cluded, on the basis of an EEG study, that explicit metacognition
is a second-order process, integrating sensory evidence with esti-
mates of the state of the decider during decision-making.
As yet we do not know precisely how the components of these
computational models map onto underlying brain activity. Are
 Psychological Medicine
there critical nodes that are necessary but not sufficient for the
experience of confidence and other metacognitive feelings? Can
we identify the higher-order brain regions with which these
nodes must interact for the experience to emerge? Fleming and
Daw (2017) suggest that fronto-polar cortex (FPC, Brodmann
area 10) is one potential high-order convergence zone for inte-
grating state and action information to enable the second-order
computations necessary for meta-consciousness. This is consist-
ent with its anatomical positioning at the top of a cognitive hier-
archy, and the observation that it receives information from
dorsolateral prefrontal, cingulate and anterior temporal cortex
(Ramnani and Owen, 2004). It has been proposed that the contri-
bution of FPC to metacognition may be to represent internal
states in a format suitable for explicit communication (Fleming
et al., 2012).
A role for FPC in meta-consciousness is consistent with the
more recent evolution of this area. In the human brain, this region
is larger relative to the rest of the brain than it is in the other apes,
with more space available for connections with other higher-order
cortical areas (Semendeferi et al., 2001; Donahue et al., 2018).
Another brain region implicated in meta-consciousness, the pre-
cuneus, has also expanded recently during human evolution
(Bruner et al., 2017).
Conclusions and possible relevance for psychiatry
While writing this review I was struck by how many empirical
studies there are concerned with the neural basis of consciousness.
Only a small fraction of these studies is cited here and, inevitably,
the choice will reflect my biases and preferences as to the nature of
consciousness. Given the wealth of information, many alternative
stories can be told. With regard to the four accounts that I alluded
to above, I believe that, while all have something to offer, none, on
their own, provide an adequate explanation of consciousness. The
brain systems underlying consciousness require long range inte-
gration of information from many brain regions (Tononi, 2008)
with top-down, re-entrant processes having a critical role
(Lamme and Roelfsema, 2000). Global workspace theory (Baars,
2002; Dehaene et al., 2003) remains a leading contender through
its greater specificity. Brain regions associated with various
aspects of working memory (frontal and parietal cortex) are con-
sistently implicated in experimental studies of consciousness.
However, higher-order thought theory (Lau and Rosenthal,
2011) also fits very nicely with the hierarchical nature of the com-
putational approaches I have outlined above. In particular, the
second-order account of meta-consciousness with its models of
models resembles high-order thought theory and strongly impli-
cates prefrontal cortex in its instantiation.
I mentioned earlier that delineating the neural basis of con-
sciousness has already had important implications for clinical
and legal practice. I believe that the more recent concept of meta-
consciousness (C2) could have important implications for the
study of psychiatric patients. Abnormalities of conscious experi-
ence are a defining feature of many psychiatric disorders, espe-
cially schizophrenia (Frith, 1979). But it is now possible to be
much more precise about the nature of some of these abnormal-
ities. For example, lack of insight, in the form of denial of one’s
disabilities, has long been recognised as a feature of psychosis
(David, 1990; Lysaker et al., 2010). Lack of insight is a failure of
metacognition.
Experimental studies have linked specific failures of metacog-
nition with positive psychotic symptoms such as delusions of
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9
control (Farrer and Franck, 2007) and auditory hallucinations
(Brebion et al., 2012). More detailed examination, however, sug-
gests that these metacognitive failures relate only to explicit meta-
cognition and not to implicit metacognition. For example,
schizophrenia is associated with failures of explicit source mem-
ory (‘remember’ responses), in the absence of failures of implicit
source memory (‘know’ responses) (Danion et al., 1999). Patients
in the first episode of paranoid schizophrenia are not impaired on
the first-order detection of stimuli but show reduced metacogni-
tive accuracy for the most visible stimuli (Bliksted et al., 2017).
A large-scale study found that psychiatric symptoms were asso-
ciated with impairments in metacognition but not decision per-
formance, while old age was associated with changes in decision
performance but not metacognition (Rouault et al., 2018).
These results suggest schizophrenia is a disorder of meta-
consciousness, rather than of consciousness more generally.
An important feature of explicit metacognition is that it enables
us to reflect on our conscious experiences and describe them to
others. Furthermore, our experiences and beliefs are altered by dis-
cussions with others (Shea et al., 2014). Schizophrenia is associated
with great difficulty in describing even ordinary experiences to
others (e.g. Cohen, 1976) and the beliefs and experiences of
these patients are influenced very little by what other people say.
Their delusions are defined not so much by bizarreness, but by
lack of consensus with the beliefs of others. ‘A false belief [] that
is firmly sustained despite what almost everyone else believes’
‘The belief is not one ordinarily accepted by other members of
the person’s culture or subculture’ (American Psychiatric
Association, 2013, Psychosis & Explicit Metacognition p. 819).
Experiments developed for the study of meta-consciousness
and computational accounts of the underlying neural mechan-
isms have the potential to greatly enhance our understanding of
psychiatric disorders such as schizophrenia.
Acknowledgements. In writing this essay I benefited greatly from Wayne
Wu’s entry on the neuroscience of consciousness in the Stanford
Encyclopedia of Philosophy (https://plato.stanford.edu/entries/consciousness-
neuroscience/). I am grateful to Steven Fleming, Uta Frith, Hakwan Lau,
Raphael Millière, Rosalind Ridley, Nicholas Shea, and Semir Zeki for their
comments on earlier drafts of this paper. Chris Frith is not any receipt of
any funding and has no conflicts of interest to declare.
Notes
1
Not all reports reflect introspection. We might be reporting what we think is
out there in the world, rather than our subjective experience.
2
The possibility of reaching would have two components: physical – is it
within my reach?, social – is it appropriate for me to take it?
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