seminars in Iw NE~ci~, V012, 1990 : pp 263-275

Francis Crick and Chri.dof Koch

Visual awareness ;ir a favorabk fmm of consciousness to stdy
neurobiologically. We propose that it takes two forms: a very
fat form, &z&i to iconic naemoryr, that may be dl~cu~t to
study; and a somewhat slower one involv&g visual attention
and short-term memory. In the slower form an at~tiona~
mechanism tra~~t~ binds together all those neurons whose
activily relates to the relevantfeatures of a sing& visual o&ect.
We suggest this is done by generating coherent semi-
spchronow oscillations, probabb in the 40- 70 Hz range.
These oscillations then activate a transient short-term
~workin~ ~~~. We outfit several lines ofexp~`~~~
work that might advance the understanding of the neural
mechanisms involved. The neural basis of very short-term
memory especia& needs more exjw%nental study.

Key words:  consciousness / attention I binding f 40 Hz
oscillations I short-term memory

IT IS REMARKABLE that most of the work in both
cognitive science and the neurosciences makes no
reference to porousness (or `awareness'), especially
as many would regard consciousness as the major
puzzle confronting the neural view of the mind and
indeed at the present time it appears deeply
mysterious to many people. This attitude is partly
a legacy of behaviorism and partly because most
workers in these areas cannot see any useful way of
approaching the problem. In the last few years
several books have appeared'-* that address the
question directly but most of theseI-3 have been
written largely from a functional standpoint and SO
have said rather little about neurons and other
machinery of the brain.

We suggest that the time is now ripe for an attack
on the neural basis of consciousness, Moreover,
we believe that the problem of consciousness
can, in the long run, be solved only by expl~ations
at the neural level. Arguments at the cognitive level

From the Salk Inrtitutc, 10010 N Torrey P&s Road,
La Jo&, CA 92037, USA, and Comfiutation and NeuralSyskms
216-76, Cat$omza retitle of TechnoZo~, Pasta, CA
9.2125, USA

01990 by W. B Saunders Company
10#4-5765/90/02~-0003~5.OO/U

Towards a neurobiological theory of consciousness

are undoubtedly important but we doubt whether
they will, by themselves, ever be sufficiently
compelling to explain consciousness in a convincing
manner. Attempting to infer the internal structure
of a very complex system using a `black-box'
approach (i.e. manipulating the input variables while
observing the output of the system) will never lead
to unique answers. In short, such methods are not
by themselves powerful enough ever to solve a
problem, though they are good enough to suggest
tentative solutions.

Our basic idea is that consciousness depends
crucially on some form of rather short-term memory
and also on some form of serial attentional
mechanism. This attentional mechanism helps sets
of the relevant neurons to fire in a coherent semi-
oscillatory way, probably at a frequency in the 40-70
Hz range, so that a temporary global unity is
imposed on neurons in many different parts of the
brain. These oscillations then activate short-term
(working) memory. In the later parts of the paper
we shall be mainly concerned with visual awareness.

Before approaching the problem in detail, it seems
sensible to describe our general approach to conseious-
ness and to decide what aspects of it are best left on
one side.

Prolegomenon to the study of consciousness

We make two basic assumptions, The fast is that there
is something that requires a scientific explanation.
There is general agreement that we are not conscious
of all the processes going on in our heads, though
exactly which might be a matter of dispute. While
we are aware of many of the results of perceptual
and memory processes, we have only limited access
to the processes that produce this awareness (e.g.
"How did I come up with the first name of my
grandfather?"). In fact, some psychologists5 have
argued that we have only very limited introspective
access to the origins of even higher order cognitive
processes. It seems probable, however, that at ~JV
one moment some active neuronal processes correlate
with consciousness, `while others do not. What are
the differences between them?

263


264                                                F. Crick and C. Koch

The second assumption is tentative: that all the
different aspects of consciousness, for example pain
and visual awareness, employ a basic common
mechanism or perhaps a few such mechanisms. If
we understand the mechanisms for one aspect, we
will have gone most of the way to understanding
them all. Paradoxically, consciousness appears to be
so odd and, at first sight, so difficult to understand
that only a rather special explanation is likely to
work. The general nature of consciousness may be
easier to discover than more mundane operations,
such as shape-from-shading, that could, in principle,
be explained in many different ways. Whether this
is really true remains to be seen.
The following topics will be left on one side or our
attitude to them stated without further discussion,
for experience has shown that otherwise much time
can be frittered away in fruitless argument about
them.

  1. Everyone has a rough idea of what is meant
by consciousness. We feel that it is better to avoid
a precise definition of consciousness because of the
dangers of premature definition. Until we understand
the problem much better, any attempt at a formal
definition is likely to be either misleading or overly
restrictive, or both.

  2. Arguments about what consciousness is for
are probably premature, although such an approach
may give a few hints about its nature. It is, after all,
a bit surprising that one should worry too much
about the function of something when we are rather
vague about what it is.

  3. We shall assume that some species of
animals, and in particular the higher mammals,
possess some of the essential features of consciousness,
but not necessarily all. For this reason, appropriate
experiments on such animals may be relevant to
finding the mechanisms underlying consciousness.

3.1. From this it follows that a language system
(of the type found in humans) is not essential
for consciousness. That is, one can have the key
features of consciousness without language. This is
not to say that language may not enrich conscious-
ness considerably.

3.2. We consider that it is not profitable at this
stage to argue about whether `lower' animals, such
as octopus, Drosophila or nematodes, are conscious.
It is probable, though, that consciousness correlates
to some extent with the degree of complexity of any
nervous system.

  4. There are many forms of consciousness, such
as those associated with seeing, thinking, emotion,

pain and so on. We shall assume that self-conscious-
ness, that is the self-referential aspect of consciousness,
is merely a special case of consciousness and is better
left on one side for the moment. Volition and
intentionality will also be disregarded and also
various rather unusual states, such as the hypnotic
state, lucid dreaming and sleep walking, unless they
turn out to have special features that make them
experimentally advantageous.
5, No neural theory of consciousness will explain
everything about consciousness, at least not initially.
We will first attempt to construct a rough scaffold,
explaining some of the dominant features and hope
that such an attempt will lead to more inclusive and
refined models.

6. There is also the problem of qualiae6 Some
argue that certain aspects of consciousness (such as
whether the red I see is the same as the red you see),
being essentially private, cannot in principle be
addressed by any objective, scientific study. We feel
that this difficult issue is, for the moment, best left
on one side. Our present belief is that it may prove
possible, in the fullness of time, to make it plausible
that you see red as I do (assuming that psychophysical
tests suggest you do). To decide whether one can
make a plausible case or not we shall need to know
the exact neural correlate in a human brain of seeing
red. Whatever the outcome, we believe that any
adequate theory of consciousness should explain how
we see color at all.

This outlines the framework within which we will
address the problem of consciousness. We next ask
what psychology can tell us about the phenomenon.

The: cognitive approach

The most effective way to approach the problem of
consciousness would be to use the descriptions of
psychologists and cognitive scientists and attempt to
map different aspects of their models onto what is
known about the neuroanatomy and neurophysiology
of the brain. Naturally we have attempted to do this
but have not found it as useful as one might hope,
although such models do point to the importance of
attention and short-term memory and suggest that
consciousness should have easy access to the higher,
planning levels of the motor system.

A major handicap is the pernicious influence of
the paradigm of the von Neumann digital computer.
It is a painful business to try to translate the various
boxes labeled ` fdes' , `CPU', `character buffer', and


A theory of con.wiou.mess

265

So on OCCUrring in psychological models, each with
its special methods of processing, into he language
of neuronal activity and interaction. This is mainly
because present-day computers make extensive use
of precisely-detailed pulse-coded messages. There is
no convincing evidence that the brain uses such a
system and much to suggest that it does not. For
these reasons we will not attempt to comment in
detail on these psychological models but only make
rather general remarks.

automated procedures, such as typing or swimming,
is probably largely unconscious.

Chmbmess appears to be a process that is fairly
immediate. In other words, it does not take too long
to become conscious of, at least, straightforward
things. Exactly how long is not clear, but Qures
somewhere in the 50-250ms time range might be
reasonable, rather than a few seconds.

Johnson-L~rdl proposes that the brain is a
complex hierarchy of largely parallel processors-
an idea that is almost certainly along the right
lines-and that there is an operating system at the
top of the hierarchy. He considers the conscious mind
to correspond to this operating system. Thus the
mechanism of consciousness expresses the results of
some of the computations the brain makes but not
the details of how they were done. If there is an
operating system of this type it is not easy at the
moment to see any particular brain area in which
it is located.`Johnson-Laird also lays emphasis on
self-reflection and self-awareness, topics that we have
decided to leave on one side.

General neurobiological aspects

When

An dtternative view, due to Jackendoffz is that
consciousness is not associated with tbe highest levels
in the hierarchy but with the intermediate levels. He
arrives at this point of view by considering in detail
the language system, the visual system and the music
system. His arguments are certainly suggestive,
though not completely compelling.

When is an animal conscious? This turns out not
to be a straightforward problem. It seems likely that
the essential features of consciousness are probably
not usudy present in slow-wave sleep, nor under
a deep anaesthetic. Rapid Eye Movement (REM)
or dreaming sleep is another matter, It seems to us
that a limited form of consciousness often occurs in
REM sleep. Although cognition is not completely
normal and memories cannot be put into the long-
term store, nevertheless dreams seem to have some
of the attributes of consciousness. Whether there are
any experimental advantages in studying REM sleep
to help us understand consciousness remains to be
seen. At the moment we do not see any.

Both authors emphasize the intimate relationship
between consciousness and working memory.
They also both envisage a serial process (that
we may loosely identify as attention) on top of
the parallel processes. Thus clearly we shall have
to consider the mechanisms of attention and of
working memory.

The really difficult case is that of rather light
anaesthesia or states induced by modern receptor-
specific anaesthetic agents. l2 It seems likely that in
some such states the brain is at least partly conscious.
This would not matter were it not for the large
amount of experimentation on mammals in these
states, We return to this problem later.

W7wre

The type of aemory that will be af most interest  Where in the brain are the neural correlates of
to us is short-term memory, whether it be very short  consciousness? One of the traditional answers-that
(a fraction of a second; sometimes called `iconic'  consciousness depends on the reticular activating
memory8 if it is visual) or short-term memory  system in the midbrain-is misleading. Certainly the
proper (meaning a few seconds) sometimes called  relevant parts of the brain need to be activated in
working memory. Q,lO These are so important that  various ways, but this is a little like believing that
we shall take up each of these subjects later. It does  the characte&ic part of a television set is its electrical
not seem essential for consciousness that the brain  supply. It is more likely that the operations correspond-
should be able to put anything into the long-term  ing to consciousness occur mainly (though not
episodic memory system," since people with certain  exclusively) in the neocortex and probably also in
brain damage (to be discussed below) cannot lay  the pdeocortex, associated with the olfactory system,
down new episodic memories but appear in all other  since local damage to the cerebral cortex often
respects to be fully conscious. Procedural memory,l'  removes particular aspects of consciousness (as, for
i.e. that part of memory responsible for highly  example, in face agnosia).


The hippoc~p~ system (the allacortex) is a little
more complicated. A person with complete bilateral
damage to the hip~~c~pal system and to all the
higher order association cortices that are connected
with it, appears to have most aspects of conscious-
nessr3 (including short-term conjunctions over at
least'three modalities) so the hippocampal system is
unlikely to be essential. But it could be argued that
what goes on in the normal hippocampus does indeed
reach consciousness, so it may be important to
consider in detail the inputs and outputs of the
hippocampal system.

Structures in the midbrain or hindbrain, such as
the cerebellum, are probably not essential for
consciousness. It remains to be seen whether certain
other structures, such as the thalamus, the basal
ganglia and the claustrum, all intimately associated
with the neocortex, are closely involved in conscious-
ness. We shall include these structures together with
the cerebral cortex as `the cortical system'.

The study of persons with `split brains' gives us
information about some of the pathways that are (or
are not) involved in consciousness. It is a weil-
established fact'4 that for persons whose corpus
callosum-the massive fiber bundle connecting the
two cortical hemispheres- has been cut, the left-hand
side of the brain (for right-handed people) is not
aware of the activity in the visual system taking place
on the right side, whereas in a normal person it is.
(We leave on one side the somewhat controversial
matter as to whether the right side, on its own,
is as conscious as the left side.) This wrongly
suggests that some of the information associated with
consciousness can traverse the normal corpus
edlosum. It also suggests that such information, with
the exception of some emotional states, cannot be
transmitted from one side of the cortex to the other
by the subcortical pathways that remain intact in this
operation.

It now seems generally agreed that blindsight is a
genuine phenomenon. l5 Certain people with cortical
blindness can point fairly accurately to the position
of objects in their blind visual field, while denying
that they see anything. It was previously suspected

that the neural pathway was subcortical, through the
superior co&ct.&s, but this has recently been brought
into question. Ifi The motor output appears to be
voluntary and the subject is certainly aware what
movements he is making. It is now an urgent matter
to decide experimentally, by comparative work on
humans and monkeys, exactly which neural pathways
are used in blindsight, since this information may
suggest which neural pathways are used for conscious
ness and which not.

We shall not discuss here other cases in which
peopfe respond to a stimulus such as an auditory or
visual cue, but claim to be unaware of the stimulus
(for example, subliminal perception and priming,~7Js
and also galvanic skin responsesig). Such stimuli
may affect ongoing mental processea, including
higher order processes, without being registered in
working or long-term memory.

What is the general character of neural behaviors
associated, or not, with consciousness? We think it
plausible that consciousness in some sense requires
neuronal activity, in which we include not only
neurons that fire action potentials but also non-
spiking neurons such as amacrine cells,
Our basic hypothesis at the neural level is that it
is useful to thii of consciousness as being correlated
with a special type of activity of perhaps a subset of
neurons in the cortical system, Consciousness can
undoubtedly take different forms, depending on
which parts of the cortex are involved, but we
hypothesize that there is one basic mechanism (or
a few such) underly~g them all. At any moment
~onsciou~ess corresponds to a particular type of
activity in a transient set of neurons that are a subset:
of a much larger set of potential candidates. The
problem at the neural level then becomes:

1. Where are these neurons in the brain?
2. Are they of any particular neuronal type?
3. What is special (if anything) about their
connections?
4. What is special (if anything) about the way they
are firing?

Visual awareness

At this point we propose to make a somewhat arbitrary
personal choice. Since we hypothesize that there is
a basic mechanism for consciousness that is rather


similar in different parts of the brain (and, in
particular, in different parts of the neocortex), we
propose that the visual system is the most favorable
for an initial experimental approach. The visual
system has several well-known advantages as an
experimental system for investigating the neuronal
basis of consciousness. Unlike language, it is fairly
similar in man and the higher primates. There is
already much experimental work on it, both by
psychophysicists and by neuroscientists. Moreover
we believe that it will be easier to study than the more
complex aspects of consciousness associated with self-
awareness. From now on, then, we shall discuss not
consciousness in all its aspects but visual awareness
and only the awareness that does not involve the
laying down of long-term episodic memory. Johnson-
Lairdl has called this `bare awareness', which does
indeed convey the idea that it is simpler than self-
awareness. Although here we mainly consider visual
perception, many of the processes we discuss are also
likely to be used in visual inagery.

The mammalian visual system

The visual system of mammals is complex and we only
give an outline description. In the macaque monkey
there are many distinct visual areas in the neocortex,
perhaps as many as two dozen.20 One reason for
these multiple areas is that to handle all activity in one
single very large neural net, with everything connected
to everything else, would make the brain both
cumbersome and prohibitively large. Loosely speaking
these areas are connected in several hierarchies, with
the processing within any one area being largely
parallel (see Figure 1). There are also many back
projections (and some cross connections) between
cortical areas, and also from the cortex back to the
thalamus, the functions of all of which are unknown.

The dominant output of the retina projects-
through the lateral geniculate nucleus of the
thalamus-to the primary visual cortex at the back
of the brain. This area has neurons responding to
fairly simple features (such as an oriented edge)
occupying a tiny part of the visual field.

The neurons in the higher cortical areas respond
to more complex features, e.g. aspects of faces, and
their receptive fields cover much larger areas. The
different cortical areas respond, in general, to
different features. For example, the neurons in area
MT are mostly interested in motion and depth, those
in area ~4 in color and shape, and those in 7a in

A theory of ~on.wiousne.ss

267

position in space relative to the head or the body.
sofa? no single mea ha been found whose neurons COVG~~~~
to everything we see. HOW is it, then, that we seem to
have a single coherent visual picture of the scene
before us?

The obvious suggestion is that at any one time the
relevant neurons in many cortical areas cooperate
together to form some sort of global activity md that
this global activity corresponds to visual awareness.
This is the hypothesis that we shall try to fdl out with
psychological and neurobiological details.

Convergence zones

Which particular cortical areas contribute directly
to visual awareness? For example, is the first visual
area, Vl, closely involved? Damasio7 has also
suggested that many cortical areas take part at any
moment at several different levels. It is probably
significant that Damasio arrived at this idea largely
from considering the detailed effects of various types
of brain damage, evidence rarely used by other
theorists. He suggests that the synchronous activity
in the various cortical areas is coordinated by
feedback projections from `convergence zones'.

What exactly convergence zones means in neural
terms is somewhat obscure. We suggest that
convergence zones may mainly refer to the neurons
(or a subset of them) that project `backwards' (see
Figure l), such as those that project from the second
visual area back to the first one. Thus the term zones
may turn out to convey a somewhat misleading
impression, since such neurons may be sprinkled
fairly uniformly through certain layers of the
neocortex. Nevertheless the basic idea is a valuable
one. It points to the possibility that, in addition,
convergence zones may also exist in other places,
such as the thalamus or the claustrum. (The
&ustrum*i is a thin sheet of cells located just below
the neocortex of the insula. It receives axons from
almost all cortical areas and, in return, projects back
to them. Its caudal region is largely visual.)

One would certainly expect areas near to the hippo-
campus, such as the inferotemporal region, as well as
those near to the higher levels of the motor system
to be closely involved in visual awareness. How far
awareness is directly correlated with every neocor&l
level of the visual system remains uncertain, as is
the involvement of the thalarnus, although certain
parts of it, such as its reticular nucleus** and the
pulvina+ may be involved with attention.


268

F. Crick and C. Koch

(FORM)    (ATTENTION)   (MOTION)    (EYE
                          MOVEMENT)

Figure 1. Some of the major cortical and sub-cortical visual areas in the macaque monkey.
Major pathways are indicated by bold lines, minor pathways by thin lines; dashed lines weak
or uncertain. The shaded ellipsoids correspond to higher-level visual-motor areas. Most cortical
areas project back to the superior colliculus as well as to the different maps in the pulvinar, which
is part ofthe thalamus. Furthermore, every forward projection has usually an equally strong,
if not stronger, back-projection associated with it (not shown). These feedback pathways usually
terminate outside cortical layer IV, while the forward projection terminates most densely in
this layer. Areas related to the control and expression of visual attention include the superior
colliculus and the pulvinar, as well as areas POa and 7a, part of the posterior parietal cortex.
Abbreviations: FEF-frontal eye fields; IT-inferior temporal lobe; LGN-lateral geniculate
nucleus; MT, MST-motion-processing areas; Vl-primary visual area; V2-4-higher-order
visual processing areas; VIP-ventral interparietal area; VP-ventral posterior. The figure is
from D. Van Essen and J. Maunsell, personal communication. For more information, see ref 20.

Binding and selective visual attention

The binding problem

specialized neurons responding to very specific and
ecological highly significant objects, such as the
neurons responding to aspects of faces in infero-
temporal cortex of primates. 24

There are an almost infinite number of possible,   It seems likely that at any moment any individual
different objects that we are capable of seeing. There  object in the visual field is represented by the firing
cannot be a single neuron, often referred to as a  of a set of neurons. This would not cause any special
grandmother cell, for each one. The combinatorial  problem if the members of the set were in close
possibilities for representing so many objects at all  proximity (implying that they probably interact
different values of depth, motion, color, orientation  somewhat), received somewhat similar inputs and
and spatial location are simply too staggering. This  projected to somewhat similar places. But because
does not preclude the existence of sets of somewhat  any object will have different characteristics (form,


A theory of consciousness                                                 269

color, motion, orientation) that are processed in
several different visual areas, it is highly reasonable
to assume that seeing any one object often involves
neurons in many different visual areas. The problem
of how these neurons temporarily become active as
a unit is often described as `the binding problem',
As an object seen is often also heard, smelt or felt,
this binding must also occur across different sensory
modalities.

Our experience of perceptual unity thus suggests
that the brain in some way binds together, in a
mutually coherent way, all those neurons actively
responding to different aspects of a perceived object.
In other words, if you are currently paying attention
to a friend discussing some point with you, neurons
in area MT that respond to the motion of his face,
neurons in area V4 that respond to its hue, neurons
in auditory cortex that respond to the words coming
from his face and possibly the memory traces
associated with recognition of the face all have to be
`bound' together, to carry a common label identifying
them as neurons that jointly generate the perception
of that specific face.

Types of binding

Binding can be of several types. In a sense a neuron
responding to an oriented line can be considered to
be binding a set of points. The inputs to such a neuron
are probably determined by genes and by develop-
mental processes that have evolved due to the
experience of our distant ancestors. Other forms of
binding, such as that required for the recognition
of familiar objects such as the letters of a well-known
alphabet, may be acquired by frequently repeated
experience; that is, by being overlearnt. This probably
implies that many of the neurons involved have as a
result become strongly connected together. (Recall
that most cortical neurons have many thousands of
connections and that initially many of these may be
weak.) Both these types of binding are likely to have
a large but limited capacity. These are the types of
binding with which Damasio7 is mainly concerned.

The binding we are especially concerned with is
a third type, being neither epigenetically determined
nor overlearnt. It applies particularly to objects
whose exact combination of features may be quite
novel to us. The neurons actively involved are
unlikely all to be strongly connected together, at least
in most cases. This binding must arise rapidly. By
its very nature it is largely transitory and must have

an almost unlimited potential capacity, although its
capacity at any one time may be limited. If a
particular stimulus is repeated frequently, this third
type of transient binding may eventually build up
the second, overlearned type of binding.

The role of attentionz5-z8

This form of transient binding probably depends on
a serial attentional mechanism, sometimes called the
spotlight of attention. 25~2* It is thought by some to
concentrate on one place in the visual field after
another, possibly moving every 60 ms or so. It is
faster than eye-movements (another, slower, form of
attention), and can work across different spatial scales.
We suggest (the idea goes back to the last century2g)
that what reaches visual awareness is usually the
result of this attentional step. In other words, l/rat
awareness and attention are intimately bound together. Note
that although the results of attention are postulated
to reach consciousness, the attentional mechanisms
themselves are probably largely unconscious.

Short-term memory

It has long been argued that awareness is not only
associated with attention but also with some form of
short-term memory. We have to distinguish two
forms, iconic and working memory. Iconic memory
is similar to a sensory input buffer, storing information
mainly at a pre-categorical level, i.e. in terms of
simple visual primitives such as orientation or
movement, although it may also involve more
complex features, such as familiar words. It has a
very large capacity but decays very quickly, perhaps
in half a second or less.8 Working memory, in
contrast, may last for seconds;g,`O it seems to have
a rather limited capacity (a figure often quoted is
seven item$`J), is different for different modalities
and seems to use a much more abstract
representation (post-categorical memory). It can be
prolonged by rehearsal, as when one rehearses a
telephone number, We suspect that it is this form
of memory that is strongly activated in the binding
process.

Neural basis of short-term memory

The neural basis of these two forms of memory is
much understudied. Three broad types of mechanisms


270

F. Crick and C. Koch

might underlie either iconic or working memory,
either singly or in combination:

(i)  the strength of certain synapses is temporarily
  increased or decreased;
(ii) a neuron keeps on firing for some time due
mainly to its intrinsic biophysical properties;
(iii) a neuron keeps on firing mainly due to
  extrinsic circuit properties (`reverberatory
  circuits').
Intracellular recordings show that the cell bodies

of retinal ganglion cells remain depolarized for
200 ms or longer following a very brief flash of light
within their receptive field. 31 How neurons further
in the system express a transient memory remains
to be seen. In a memory task in which a trained
monkey had to discriminate and retain individual
features of compound stimuli, about 15% of the
neurons in inferotemporal cortex continued to fire
for 10-20s after the stimulus.32 The mechanism
producing (and terminating) this sustained firing is
unknown. It is not yet known whether this firing is
oscillatory or not. It may not have to be oscillatory,
since a task can be remembered well enough without
one being vividly conscious of it all the time.

A phenomenon that may correspond to the first
mechanism was discovered many years ago at the
neuromuscular junction and called post-tetanic
potentiation. This is not to be confused with the
much studied long-term potentiation (LTPJs3 that
has a longer time course. The terminology for these
short-lasting changes has now become more compli-
cated,34l35 with effects variously labelled facilitation
(with two time constants of decay, of 50ms and
300 ms), augmentation (7 s) and potentiation (30 s
to minutes). There is also depression (5 s). We shall
refer to all these collectively as `short-term synaptic
modification'. Note that the decay times are in
general in the same range as the times required for
the decay of working memory. Short-term modification
has also been observed in the hippocampus and, in
one case, in the neocortex. These temporary changes
in synaptic strength can be surprisingly large (see
figures 11 and 13 in ref 33).

Hebbiun or non-lTebb&mt?

The causes of the various aspects of short-term
modification are not fully understood but many of
them seem to result from calcium accumulation in
the presynaptic termina13*z35 and are not influenced

by activity in the postsynaptic cell. For this reason
they are probably all non-Hebbian36 in character.
(`Hebbian' means that the alteration in synaptic
strength depends on activity, at about the same time,
in both the presynaptic and the postsynaptic cell.)
Non-Hebbian implies that the change is not (to a
first approximation) just at an individual synapse but
at all the synapses associated with that particular
presynaptic cell, so that the `unit of change' is the
presynaptic cell, not a single synapse. Such changes
may form part of the neuronal basis of (short-term)
priming."

Von der Malsbur?' in 1981 postulated on
theoretical grounds a- fast (fraction- of a second)
mechanism for increased synaptic efficiency, having
a broadly Hebbian36 character. So far this transient
Hebbian alteration to synaptic strength has not been
observed, although if it existed it would provide very
considerable theoretical advantages.

We know almost nothing concerning the anatomical
localization of iconic and working memory, except
that (as discussed above's) the hippocampal system
need not be present in order to remember for short
times. Both iconic and working memory are likely
to be distributed throughout the appropriate cortical
areas, with auditory events transiently stored in
auditory cortices, visual events in the visual cortices,
and so on. No case of a person who is conscious but
has lost all forms of short-term memory has been
reported.

Neuronal oscillations

It has often been hypothesized, in particular by von
der Malsburg,s7 that in neural terms binding means
the temporarily correlated firing of the neurons
involved, In other words, neurons in different parts
of cortex responding to the currently perceived object
fire action potentials at about the same time. The
main theoretical requirement is for correlated firing.
It now seems theoretically plausible that this is most
easily implemented using oscillations. There are
many oscillations known in the cortex, among them
the a-rhythm and the &rhythm of the hippocampus.
Experimental work on `y-oscillations' in mammalian
olfactory cortex38g3g and in the visual cortex@-46
indicates that an important mechanism may involve
neurons firing in semisynchrony at a frequency in
the 40-70 Hz range (at least in the cat) (see Figure 2).
In the visual cortex, only a proportion of the active
neurons ,fire in this way. Most of the neurons that


A theory of consciousness

271

Figure 2. The local field potential (upper trace) and
multiunit activity (second trace) recorded from an electrode
in the first visual area of an adult cat in response to an
optimally oriented light bar moving across the receptive
field. The third and fourth traces show a corresponding
part of the first and second ones (respectively) on an
expanded time scale. Note the presence of rhythmic
oscillations (35-45 Hz). The multiunit activity occurs near
the peak negativity of the local field potential.
Reproduced, by permission, from ref 42.

do oscillate appear to be complex cells rather than
simple cells, so that very few are found in cortical
layer IV.45

It has been shown*' in cat primary visual cortex
that in many cases two neurons some distance apart,
but both responding to a particular moving bar, can
-show frequency-locked oscillations with no measurable
phase shift in their cross-correlations. More tellingly,
the activity of two relevant neurons, some 7 mm
apart, showed4' more highly correlated oscillations
(at about 50 Hz) to a single moving bar than did the
same two neurons stimulated by two shorter,
separate, moving bars. That is, the correlation was
much greater in response to an obviously single
object than to a pair of somewhat distinct objects.

The activity of the relevant neurons in both the first
and second visual areas has also been shown to
be correlated.@ We shall refer to these neuronal
oscillations as the 40 Hz oscillations, though the
frequency on any one occasion is not very precise
and can vary between 35 and 75 Hz.

Most of these experiments have been done on
lightly-anaesthetized cats whose exact state of
awareness is unknown but as similar oscillations have
also been seen in neurons in alert cats,6 they are
unlikely to be merely an artifact of the anaesthetic.

A sketch of a theory

The role of the oscillations in binding may be as
follows. Objects in the visual field give rise to
appropriate responses in the appropriate cortical
areas. Visual attention now has to select one of these
objects at a particular location. Exactly how this
works is not yet known. One possible solution*5J**47
is that the brain has some sort of topographic saliency
map that codes for the conspicuousness of locations
in the visual field in terms of generalized center-
surround operations. This map would derive its
input from the individual feature maps and give a
very `biased' view of the visual environment,
emphasizing locations where objects differed in some
perceptual dimension, i.e. color, motion, depth, from
objects at neighboring locations. Where this map
might be located is unclear but parts `of the
thalamus,22>23 such as the pulvinar, might be in-
volved. (Note that the pulvinar receives a projection
from the superior colliculus, an area that could
be thought of as having a saliency map for eye
movements .)

Once a particular salient location has been selected,
probably by a winner-take-all mechanism, the
information associated with it must be activated by
referring back to the individual feature maps. The
various parts of the visual thalamus axe well suited
to influence the behavior of neurons in those parts
of the neocortex from which they receive-information
and to which they project back. Some such feedback
pathways then activate or synchronize the oscillations
at the corresponding locations in areas such as Vl ,
V4 and MT, so that a coherent set of features is
bound. Of course, the system had to decide, using
the categorical knowledge stored in the connections,
exactly which neurons must oscillate together to
produce a veridical representation of the object being
attended to. This is probably not an easy task. These


272                                                    F. criclk and c. Kuch

are the problems that concern much theoretical
work in cognitive science and computational neuro-
science, It is well known that making sense of our
perceptual inputs is an `ill-posed' problem and much
`computation' must be done to produce veridical
solutions.

It seems likely that, for one reason or another,
certain neurons in the cortical areas involved tend
to oscillate at around 40 Hz. This could make it
easier to activate such oscillations quickly. The effects
of the 40 Hz oscillations is probably greater than the
same amount of random firing for two reasons: first,
because spikes arriving at a neuron simultaneously
will produce a larger effect at the soma; and second,
because the 40 Hz oscillations may promote 40 Hz
`resonances' elsewhere.

To be effective the phases of the relevant neurons
must be synchronized.  A recent mathematical
analysis 48 shows that a set of oscillating neurons can
very quickly be frequency- as well as phase-locked
if there is a centralized feedback unit. On the other
hand phase-locking is much slower and more difficult
to achieve if the interactions have to pass over long
chains of interneuronal connections.
As there has probably been strong evolutionary
pressure to produce appropriate phase-locking as
quickly as possible, it may be a general principle that
all phase-locking interactions use only pathways with
as few links as possible; these may be within a cortical
area, between cortical areas (in adjacent levels in the
hierarchy), or to and from one or more global
coordinating regions, such as the thalamus or the
claustrum.

We suge;est that one of the funaions of consciousness
is to present the result of various underlying
computations and that this involves an attentional
mechanism that temporarily binds the relevant
neurons together by synchronizing their spikes in
40 Hz oscillations. These oscillations do not
themselves encode additional information, except in
so far as they join together some of the existing
information into a coherent percept. We shall call
this form of awareness `working awareness'. We
further postulate that ob$crS for wht.2h the b~n~~~~ab~
has been salved areplaced into working memory. In other
words, some or all of the properties associated with
the attended location would automatically be
remembered for a short time. One very attractive
possibility, with no experimental support, is that the
40 Hz oscillations themselves preferentially activate
the mechanisms underlying working memory and
possibly other longer-term forms of memory as well,

The liielihood that only a .few simultaneous,
distinct oscillations can exist happily together might
explain,4g in a very natural way, the well-known
limited capacity of the attentional system. The 40 Hz
oscillations may also be an important element in
laying down and improving stored, categorical
information, because at any moment they represent
the brain's consensus as to what it is seeing.

Fleeting awareness

Can a spotlight of attention, moving over the visual
field from one `salient' location to the next, explain
the perceptual richness of our environment? Would
such a mechanism not lead to a sort of `tunnel
vision', in which the currently attended location
appears in vivid detail with its associated perceptual
attributes while everything else is invisible? We
suggest, very tentatively, that this richness may be
mediated by another form of awareness that is very
transient, being associated with iconic memory and
having a very large capacity at any one time. This
form, that we propose to call `fleeting awareness',
we expect not to solve the ad &crc binding problem
(as working awareness does) but to embody `features'
that are bound only epigenetically or by overlearning.
Attention can then focus on a subset of relevant items
within iconic memory for further processing. Because
fleeting awareness is very transient it may be
especially difficult to study. Whether it really exists
remains to be seen.

Experimental problems

To understand working awareness it seems clear that
experimental studies of three somewhat different
phenomena are needed. The first is the 40 Hz
oscillations, and indeed all other oscillations and any
other kinds of coherent firing. In what cortical areas
are oscillations found, especially in alert animals?
What is their natural history: when do they occur?
How long do they take to set up? How long does
any one of them last? Are there, simultaneously,
several different frequencies and/or phases? Are they
indeed mainly correlated with objects? Do they solve
the well-known figure-ground problem? Do they ever
occur in the thalamus or the basal ganglia? Is the
claustrum21 involved-it is ideally placed to help
synchronize neurons in different places?

The second is attention. Are any of the dsciliations
associated with it? How does the mechanism work


A theory of constiotmess                                             273

in neural terms? It is already known that neurons in
area VP and in the parietal region5' in the macaque
monkey are influenced by attention. Evidence on
humans with brain damage implicate parts of the
thalamus in certain aspects of attention,** as do
certain experiments on monkeys,23 but we need to
know much more about how attention works
neurobiologically.

The third is the neural basis of both iconic and
working memory. These are neglected subjects that
urgently demand an experimental attack. If there
are reverberating circuits, where are they? Under
what circumstances do they oscillate? Are there
special mechanisms within certain neurons that make
it easy for them to continue firing? How widely is
the short-term synaptic modification mechanism
dis~ibuted? What are its characteristics in different
places? Is there any sign of a Hebbian form of
modification? What exactly are the biochemical and
biophysical mechanisms34*35 underlying it? In
addition we need to relate the neural activity to
psychological observations.

We plan to discuss these experimental questions
more fully in a later paper and to offer some tentative
answers based on mom detailed theoretical arguments.

Some experimental approaches

There are at least three possible methods of directly
approaching working awareness. One is to exploit
the process known as rivalry, an example of which
is the two alternative ways of viewing the well-known
Necker cube drawing. Here the visual input is
constant but the percept varies from one ~t~~tation
to the other. A form of rivalry that is easier to study
neurophysiologically is binocular rivalry, where one
eye is given one constant visual input and the other
a constant but rivalrous one. An example studied by
John Allman and his colleagues (personal communi-
cation) involved projecting a small horizontal grating
into one eye of a macaque monkey and a small
vertical one into the other eye so that their visual
fields overlap. In the same circumstances people see
first one grating and then the other, the two percepts
alternating every second or so. Detailed psychophysical
studies on both monkeys and humans, where the
monkeys signalled the change by pressing one of two
keys, give fairly similar results, so it is reasonable
to assume that the monkey has an awareness of the
changing percepts. Most neurons in the first visual
area fire in response to the constant visual input and
do not change but the firing of others tends to change

with the monkey's apparent percept. A similar
experiment involving horizontal gratings moving
either upwards (in one eye) or downwards (in the
other) produces a similar variety of responses in area
MT of the monkey.52*53

The second approach,5* using cats, is to let the
animal view the same set of visual signals first while
it is awake and then again when it is in slow-wave
sleep. The neurons studied were mainly in the first
visual area. The general result is that the response
of any given neuron is broadly the same in the two
conditions but neurons in the lower layers are often
markedly less active in slow-wave sleep. This was
confirmed by experiments in which activity was
monitored ~st~h~i~y using deoxyglucose. (Note
that all this was done before the 40 Hz oscillations
were discovered.) Both these types of experiments
are obviously in their infancy but they certainly
suggest that visual awareness can be directly
approached by suitably designed experiments.

A third approach to working awareness would be
to study the effect of anaesthetics on awareness and
recall in humans and on neuronal responses in monkey
under similar conditions. Surprisingly, no reliable
means exists today to test whether a patient is uncon-
scious during modern anaesthetic procedures, l2
which usually includes muscle relaxants to block
voluntary and involuntary movements. Even the
EEG is no reliable indicator of depth of anaesthesia,
as it is often not distinguishable from that of a sleeping
person. It has been claimed, however, that the
disappearance of a 40 $3~ wave in the auditory evoked
potential correlates with loss of consciousness under
anesthesia,55 Four to six cycles of such an oscillation,
with a period of about 25 ms, can he seen following
stimulation by a single or a series of sharp clicks.s6
More work on this is obviously very desirable.

Much useful information can also be obtained by '
careful studies on humans with brain damage who
have selective impairment of different aspects of visual
perception7~57 and especially of attention and binding.

Conclusion

Our tentative theory, most of the elements of which
have already been proposed by others, is a program
for research rather than a detailed modeI.

What are the essential features of visual
awareness? The first requirement is for a form of
running short-term memory, an idea that is certainly
more than 100 years old (see ref 29).. We postulate
two distinct forms of this running memory, a very


274                                                 F. Crick and C. Koch

transient iconic one that records built-in visual
features and a working memory that lasts for a
somewhat longer time and can also store com-
binations of features. We presume that parts
of iconic memory form the basis of working
memory.

The information about a single object is distributed
about the brain, There has, therefore, to be a way
of imposing a temporary unity on the activities of
all the neurons that are relevant at that moment.
(Incidentally we see no reason at all why this global
unity should require fancy quantum effects.) The
achievement of this unity may be assisted by a fast
attentional mechanism, the exact nature of which is
not yet understood. This mechanism is postulated
to concentate on one object at a time, choosing by
a winner-take-all process the next object that appears
to it to be the most salient. The required unity takes
the form of the relevant neurons firing together in
semi-synchrony, probably at a frequency in the
40-70 Hz range. We tentatively suggest that this
activates the appropriate parts of the working-
memory system. The neural basis of this memory
system is at the moment obscure, although the
transient alteration of synaptic strengths is one likely
mechanism.

There is also much neural activity in the visual
system that does not reach full awareness. Much of
this corresponds to the computations needed to arrive
at the best interpretation of all the incoming
information that is compatible with the stored,
categorical information acquired in the past. It
is this `best interpretation' of which we become
aware.

Why, then, is consciousness so mysterious? A
striking feature of our visual awareness (and of
consciousness in general) is that it is very rich in
information, even if much of it is retained for only
a rather brief time. Not only can the system switch
rapidly from one object to another, but in addition
it can handle a very large amount of information in
a coherent way at a single moment. We believe
it is mainly these two abilities, combined with
the very transient memory systems involved,
that has made it appear so strange. We have no
experience (apart from the very limited view
provided by our own introspection) of machines
having complex, rapidly changing and highly
parallel activity of this type. When we can both
construct such machines and understand their detailed
behavior, much of the mystery of consciousness may
disappear.

Acknowledgements

We thank John Allman, Bernard Baars, Patricia
Churchland, Paul Churchland, Antonio Damasio,
Charles Gray, Bela Julesz, Dan Kammen, Georg Kreisel,
and Leslie Ox-gel for helpful comments on earlier versions
of the manuscript and thank Jennifer Altman especially
for extensive improvements to the sumitted manuscript.
F.C. is supported by the J. W. Kieckhefer Foundation.
C.K. is supported by the Air Force Office of Scientific
Research, a Presidential Young Investigator Award from
NSF and by the James S. McDonnell Foundation.

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