How Does Consciousness Happen? - Christof Koch and Susan Greenfield
Contents
1. HIS THEORY: For each conscious
experience, a unique set of neurons in particular brain regions fires in a
specific manner.
2. HER THEORY: For each conscious
experience, neurons across the brain synchronize into coordinated assemblies,
then disband.
3. KOCH SPEAKS
4. "Specific groups of
neurons mediate distinct conscious experiences."
5. Greenfield Speaks
6. "Consciousness is
generated by a quantitative increase in the holistic functioning of the
brain."
7. CONSCIOUSNESS EXPLAINED
8. BASIC ARGUMENTS
9. KOCH'S MODEL
10. GREENFIELD'S MODEL
Section:
DEBATE
Two
leading neuroscientists, Christof Koch and Susan Greenfield, disagree about the
activity that takes place in the brain during subjective experience
HIS
THEORY: For each conscious experience, a unique set of neurons in particular
brain regions fires in a specific manner.
HER
THEORY: For each conscious experience, neurons across the brain synchronize
into coordinated assemblies, then disband.
How
brain processes translate to consciousness is one of the greatest unsolved
questions in science. Although the scientific method can delineate events
immediately after the big bang and uncover the biochemical nuts and bolts of
the brain, it has utterly failed to satisfactorily explain how subjective
experience is created.
As
neuroscientists, both of us have made it our life's goal to try to solve this
puzzle. We share many common views, including the important acknowledgment that
there is not a single problem of consciousness. Rather, numerous phenomena must
be explained--in particular, self-consciousness (the ability to examine one's
own desires and thoughts), the content of consciousness (what you are actually
conscious of at any moment), and how brain processes relate to consciousness
and to nonconsciousness.
So
where does the solution begin? Neuroscientists do not yet understand enough
about the brain's inner workings to spell out exactly how consciousness arises
from the electrical and chemical activity of neurons. Thus, the big first step
is to determine the best neuronal correlates of consciousness (NCC)--the brain
activity that matches up with specific conscious experiences. When you realize
you are seeing a dog, what has happened among which neurons in your brain? When
a feeling of sadness suddenly comes over you, what has happened in your brain?
We are both trying to find the neuronal counterpart of each subjective
experience that an individual may have. And this is where we differ.
Our
disagreement over the best NCC emerged during a lively debate between us at the
University of Oxford in the summer of 2006, sponsored by the Mind Science
Foundation in San Antonio. Since then, we have continued to explore and
challenge each other's views, a dialogue that has resulted in the article here.
We are bound, nonetheless, by one fundamental commonality: our views stem
primarily from neuroscience, not just philosophy. We both have considered a
tremendous amount of neuroscientific, clinical and psychological data, and it
is from these observations that our arguments arise.
KOCH
SPEAKS
"Specific
groups of neurons mediate distinct conscious experiences."
Both
Susan Greenfield and I are searching for the most appropriate neuronal
correlates of consciousness. If we can find the right NCC, the direct
cause-and-effect mechanisms that create consciousness may follow.
In
my view, which has evolved since Francis Crick and I began investigating
consciousness in 1988, every conscious percept (how the brain represents
stimuli from the senses) is associated with a specific coalition of neurons
acting in a specific way. There is a unique neuronal correlate of consciousness
for seeing a red patch, another for seeing one's grandmother, a third for
feeling angry. Perturbing or halting any neuronal correlate of consciousness
will alter its associated percept or cause that percept to disappear.
Physiologically,
the likely substrate for NCC is a coalition of pyramidal neurons--a type of
neuron that communicates over long ranges--within the cerebral cortex. Perhaps
only a million such neurons--out of the 50 billion to 100 billion in our
heads--are needed to form one of these coalitions. When, say, Susan enters a
crowded room and I see her face, a coalition of neurons suddenly chatters in
concert for a fraction of a second or longer. The coalition reaches from the
back of the cortex, where representations of visual stimuli are first
processed, into the front of the cortex, which carries out executive functions
such as providing perspective and enabling planning. Such a coalition would be reinforced
if I paid attention to the stimulus of her image on my retina, which would
strengthen the amplitude or the synchrony of the activity among the select
neurons. The coalition sustains itself and suppresses competing coalitions by
feeding excitatory signals back and forth among the neurons in the back and
front of the cortex. If, suddenly, someone calls my name, a different coalition
of neurons in the auditory cortex arises. This coalition establishes two-way
communication with the front of the brain and focuses my consciousness on the
voice, suppressing the earlier coalition representing Susan's face, which fades
from my awareness.
One
universal lesson from biology is that organisms evolve specific gadgets, and
this is true for the brain. Nerve cells have developed myriad shapes and
functions, along with specific wiring patterns among them. This heterogeneity
is refleeted in the neurons that constitute-NCC. It is here that I differ most
from Susan. In my view, consciousness is not some holistic property of a large
collection of firing neurons that are bathed in a solution of
neurotransmitters, as she argues. Instead I maintain that specific groups of
neurons mediate, or even generate, distinct conscious experiences.
And
soon enough, the growing ability of neuroscientists to delicately manipulate
populations of neurons will move us from observing that a particular conscious
state is associated with some neuronal activity to pinpointing
causation--observing that a given population is partially or wholly responsible
for a conscious state.
But
how do we determine which set of neurons, and what activity among them,
constitutes a conscious percept? Do NCC involve all the pyramidal neurons
present in the cerebral cortex at any given time? Or do they just involve a
subset of long-range projection cells communicating between the frontal lobes
and the sensory cortices in the back of the brain? Or do they involve neurons
anywhere that are firing in synchrony?
Much
of the contemporary work on NCC has concentrated on vision. Visual
psychologists have perfected techniques to hide things from our conscious
perception, like a magician who misdirects us so that we do not see what is
happening in front of our eyes. One example is flash suppression, a phenomenon
discovered by then graduate student Naotsugu Tsuchiya and myself in 2005.
Perception of a small, stationary image shown to one eye--say, a faint, gray,
angry face projected into the right eye--is completely suppressed by a stream
of constantly changing color patches flashed into the other eye. This
suppression can last for minutes, even though the scary face is perfectly
visible if the viewer blinks his or her left eye; although legions of neurons
in the primary visual cortex are firing vigorously in response to the
stimulation from the left eye, they do not contribute to consciousness. This
result is hard to explain in Susan's view that any coherent firing by a large
collection of neurons is a correlate of consciousness. Researchers are using
such illusions to find NCC in the brains of trained monkeys and humans.
Before
Francis passed away, he and I offered several proposals about how consciousness
works, based on experimental results. One is that NCC include pyramidal neurons
that are strategically located in an output zone of the cerebral cortex known
as layer 5. These cells send out signals to, and directly receive strong
excitatory inputs from, another set of pyramidal neurons in a different region.
Such an arrangement could implement a positive feedback loop, a coalition of
neurons that, once triggered, would keep on firing until shut off by another
coalition of neurons. These groups also fire over fractions of a second, much
closer to the timescale of conscious awareness than single-neuron firings
This
notion about networks of neurons has received a boost from recent results by
researchers at the Mount Sinai School of Medicine, Columbia University and the
New York State Psychiatric Institute, working under Stuart C. Sealfon of Mount
Sinai and Jay A. Gingrich of Columbia. Sealfon's and Gingrich's teams have
demonstrated in genetically modified mice that hallucinogens--such as LSD,
psilocybin (an ingredient of mushrooms) and mescaline--act on a type of
molecule, called a serotonin receptor, found on the pyramidal cells that
cluster in layer 5. The hypothesis that the mind-bending effects of
hallucinogenic compounds come from activation of one receptor type on a
specific set of neurons--rather than from "messing up" the brain's
circuits in some holistic manner--can be further tested with molecular tools
that can toggle layer 5 pyramidal cells on and off until the exact set of
neurons being affected is identified.
A
second proposal for how NCC underlie consciousness involves the claustrum, a
sheetlike structure within the cortex. Remarkably the neurons composing this
structure receive input from almost all regions of the cortex and project back
to almost all as well. This structure may be perfectly situated to bind the
activity of the sensory cortices into a single, coherent percept.
To
advance these ideas, neuroscientists must sample the chattering electrical
activity of a very large number of neurons at many locations. This work is
delicate and difficult, but the miniaturization of electrodes is making it
possible. Preliminary efforts confirm that specific groups of neurons express
the types of perceptions that form our daily experiences.
None
of these insights imply that one, 100 or even one million neurons living in a
lab dish could be conscious. Neurons are part of vast networks and can generate
consciousness only in that context. An analogy is helpful: although DNA
molecules in a cell spell out the composition of the proteins in our bodies,
many other molecules must also be present in the cell to construct and maintain
those proteins.
The
varying extent and provenance, or origin, of coalitions of neurons can also
account for the different content of consciousness in infants, adults and
animals. That any coalition can exist at all depends on the existence of
arousal circuits in the brain stem and thalamus (which relays sensory inputs to
the cortex) that are continuously active and that perfuse the cortex and its
satellite structures with neurotransmitters and other substances. If a person's
arousal circuits are silent--as they are when one is in deep sleep or under
anesthesia or when one has suffered trauma akin to that of Terri Schiavo, the
woman who fell into a persistent vegetative state that captivated the media--no
stable coalition of cortical neurons can arise and the person is not conscious.
Although
this model can be tested by physiological experiments, a valid criticism is
that it is not a theory built from a set of principles--that is, it cannot
predict what type of system has conscious experiences. Neuroscience needs a
theory that predicts, based on physical measurements, which of the following
organisms is conscious: a fruit fly, a dog, a human fetus five months after
conception, an unresponsive Alzheimer's patient, the World Wide Web, and so on.
Some
experts, including Giulio Tononi of the University of Wisconsin-Madison, are
working on such theories. But we are still so ignorant about the brain that we
can only speculate. Specific hypotheses that can be tested with today's technology
will help. As Francis was fond of saying, what drove his and James Watson's
1953 discovery of the double-helical structure of DNA were experiments, not a
theory of how genetic information might be encoded in molecules.
Fundamentally,
my explanation is that qualitative, not quantitative, differences in neuronal
activity give rise to consciousness. What matters is not the sheer number of
neurons involved, as Susan stresses, but the informational complexity that they
represent. A specific network of neurons is needed for a specific percept, not
any random collection of neurons that become highly active. Furthermore, for
full consciousness, a coalition of neurons must encompass both sensory
representation at the back of the cortex as well as frontal structures involved
in memory, planning and language. The brain works not by dint of its bulk
properties but because neurons are wired up in amazingly specific and
idiosyncratic patterns. These patterns reflect the accumulated information an
organism has learned over its lifetime, as well as that of its ancestors, whose
information is represented in genes. It is not crucial that a sufficient number
of neurons are active together but that the right ones are active.
GREENFIELD
SPEAKS
"Consciousness
is generated by a quantitative increase in the holistic functioning of the
brain."
If
neuronal correlates of consciousness are nothing more than the discharges of
certain neurons and not others, as Christof Koch suggests, then consciousness
resides in the neurons themselves. Yet Christof offers no explanation as to
what qualitative property such neurons or regions have, compared with others.
Moreover, if not even a million neurons can generate consciousness without
being part of "vast networks," then the burden of identifying NCC
shifts to describing what these networks are. By looking at specific brain
connections for different forms of consciousness, Christof is guilty of a
21st-century form of phrenology, in which different functions are related
directly to different brain regions, especially the cortex. His enthusiasm for
the cortex should be tempered by the fact that many species, such as birds,
have no cerebral cortex yet are considered conscious. Even if such
compartmentalization were possible, it would not explain how consciousness is
generated.
In
my view, consciousness cannot be divvied up into different, parallel
experiences. Indeed, we know that visual stimulation can change how we hear,
and vice versa. This merging of the sensorium's components argues against
concepts such as an isolated visual consciousness. Most important, either you
are conscious or you are not. In Christof's lab, subjects are conscious
throughout experiments performed on their neurons; therefore, it is not
consciousness that the experiments manipulate but the content of that
consciousness. Any consequent explanation is really a foray into answering
"What is attention?" That question is certainly valid, but it is a
different one from "What is consciousness?" I contend that to define
the best NCC we must elucidate the difference between consciousness and
unconsciousness.
My
own starting assumption is that there is no intrinsic, magical quality in any
particular brain region or set of neurons that accounts for consciousness. We
need to identify a special process within the brain. And to be a truly robust
correlate of consciousness, this neuronal process must account for a variety of
everyday phenomena, including the efficacy of an alarm clock, the action of
anesthetics, the distinction of dreams from wakefulness, the existence of
self-consciousness, the possible difference between human and animal
consciousness, and the possible existence of fetal consciousness. A more
plausible view of consciousness is that it is not generated by a qualitatively
distinct property of the brain but by a quantitative increase in the holistic
functioning of the brain. Consciousness grows as brains grow.
But
what is the key neuronal mechanism in this process? The attempt to show a process-related
correlate of consciousness has been inspired by various findings, including
those of German neurophysiologist Wolf Singer. Singer demonstrated that a huge
population of neurons between the thalamus and the cerebral cortex transiently
fire together at a frequency of 40 times a second. But because the same
activity can arise in this tissue kept alive in a lab dish, an additional
condition must be a prerequisite for consciousness.
Neuroscientist
Rodolfo Llinas of New York University Medical Center more recently suggested
that this coordinated, transient firing sets up two complementary loops between
the thalamus and the cerebral cortex that work in conjunction to maintain
consciousness: a "specific" system relating to the content of consciousness
and a "nonspecific" system relating to the arousal and alertness of
consciousness. This account does indeed provide an explanation for why the
strong sensory input of an alarm clock triggers full consciousness. Moreover,
Llinas's model distinguishes between the consciousness of dreams and that of
wakefulness; in dreams, there is no sensory input to feed the arousal loop, so
only the content loop functions.
The
central problem is that models developed by Llinas and others conceive of
consciousness as an all-or-nothing condition. They fail to describe how the
physical brain can accommodate the ebb and flow of a continuously variable
conscious state. I favor an alternative. For more than a decade, scientists
have known that the activity of tens of millions of neurons can synchronize for
a few hundred milliseconds, then disband in less than a second. These
"assemblies" of coordinating cells can vary continuously in just the
right space and timescales for the here-and-now experience of consciousness. Wide-ranging
networks of neurons assemble, disassemble and reassemble in coalitions that are
unique to each moment. My model is that consciousness varies in degree from one
moment to the next and that the number of neurons active within an assembly
correlates with the degree of consciousness present at any given time.
This
neuronal correlate of consciousness--the transient assembly--satisfies all the
items on the shopping list of phenomena above. The efficacy of an alarm clock
is explained as a very vigorous sensory input that triggers a large,
synchronous assembly. Dreams and wakefulness differ because dreams result from
a small assembly driven by weak internal stimuli, whereas wakefulness results
from a larger assembly driven by stronger external stimuli. Anesthetics restrict
the size of assemblies, thus inducing unconsciousness. Self-consciousness can
arise only in a brain large and interconnected enough to devise extensive
neuronal networks. The degree of consciousness in an animal or a human fetus
depends on the sizes of their assemblies, too.
Recall
that neither Christof nor I is attempting to explain how consciousness arises.
We are not attempting to answer what Australian philosopher David Chalmers has
dubbed the "hard problem": determining how physiological events in
the brain translate into what you experience as consciousness. We are seeking a
correlation--a way to show how brain phenomena and subjective experiences match
up, without identifying the all-important middle step of how a phenomenon
causes an experience. Neuronal assemblies do not "create"
consciousness but rather are indices of degrees of consciousness. Because an
assembly's size and the corresponding degree of consciousness result from a
variety of physiological factors--such as degree of connectivity, strength of
stimuli and competition from other assemblies--each factor could eventually be
manipulated experimentally. The assembly model's ability to generate
falsifiable hypotheses and account for the diverse range of phenomena related
to consciousness surely makes it particularly powerful.
An
obvious criticism of the assembly model, which Christof articulated during our
Oxford debate, is that it merely posits that "size is everything."
But most of science is indeed "all about measurement"--the objective
quantification of observations. Size is everything in science. Other skeptics
say that assemblies are too vague a notion, but several researchers have
revealed detailed characterizations of neuronal mechanisms that underlie the
generation of assemblies lasting less than a second, such as Amiram Grinvald of
the Weizmann Institute of Science in Rehovot, Israel, Ole Paulsen of Oxford and
John G. Jefferys of the University of Birmingham in England.
Decisive
tests in humans must await better noninvasive imaging techniques that have a
time resolution commensurate with the milliseconds-long timescale of the
formation and disbanding of neuronal assemblies. Once these techniques are
available, we should be able to observe assemblies that correlate with the subjective
experiences of, for example, neuropathic pain, depression and schizophrenia.
Nevertheless, researchers have already observed the assembly model in action.
In 2006 Toby Collins and others in my group at Oxford showed that in rats, the
formation, activity and duration of assemblies correlate selectively with the
action of anesthetics. Pilot observations in our laboratory, yet unpublished,
also show that the number of neurons active in assemblies in the sensory cortex
of an anesthetized rat reflects degrees of anesthesia. Earlier this year
another member of my team, Subhojit Chakraborty, demonstrated that in rats,
assemblies in the visual and auditory systems might serve as a good basis for
distinguishing the subjectivity of seeing versus hearing.
Other
criticisms relate to time and space. In epilepsy, for example, a prolonged
neuronal assembly sustains a seizure, which equates with a loss of
consciousness. But the whole point of assemblies as the appropriate NCC is that
they are highly transient; a seizure acts as a jamming mechanism that prevents
that transience, thus allowing a single assembly to last orders of magnitude
longer than normal. Collins, Michael Hill, Eleanor Dommett and I have similarly
suggested in a recent paper that anesthetics also may act as a jamming
mechanism.
Another
area of objection is that the assembly model does not have any spatial
properties; there is no identified anatomical locus. But all too often we place
far too much significance on localization as an end in itself. There is no need
for a "center" for any given brain function, much less for
consciousness.
A
more plausible scenario would be that many different brain regions, in
generating highly transient assemblies, converge as inputs to a space-time
manifold. The present difficulty is that we cannot describe such a manifold
using current experimental techniques. Perhaps the manifold could eventually be
modeled mathematically. Such models and their interactions may be the way
forward.
A
final problem, and one that applies to NCC at the basic level, is how they
might be harnessed to tackle the hard problem: determining how physiological
events in the brain translate into what you experience as consciousness. We
will not be in a position to find a solution until we know what kind of
evidence would satisfy us: A brain scan, a performing rat, a robot, a formula?
Or perhaps an induced change in one's subjective state, such as if Christof's
brain could be manipulated so that he would experience the world as I do--and
even agree with me.
***************
Why
does an alarm clock induce consciousness in a sleeping (unconscious) person?
POINT/COUNTERPOINT
Koch's
view: Neurons in a region of the brain stem called the locus coeruleus respond
to a sudden, large input from the auditory nerve. They spring into action,
widely broadcasting a chemical signal to the thalamus and the cerebral cortex.
Other neurons release the neurotransmitter acetylcholine throughout the brain.
The net effect is that the cerebral cortex and its satellite structures become
aroused. Once that occurs, a widespread but tightly interconnected grouping of
neurons in the auditory cortex, and its counterparts in the front of the brain
and in the medial temporal lobes that support planning and memory, establishes
a stable coalition using recurrent feedback. This activity takes only a
fraction of a second and causes you to become conscious of the alarm.
Greenfield's
view: Any strong sensory stimulus, such as a bright light, will induce consciousness,
so no one particular area of the brain can be responsible for waking you up.
The alarm clock prompts consciousness not because of the quality of the
stimulus (in this case, auditory) but because of its quantity (loudness).
Transient neuronal assemblies--many neurons acting in concert---correlate with
varying degrees of consciousness: the size of an assembly from one moment to
the next is determined by how readily neurons can be corralled into transient
synchrony. One key factor is the strength of sensory stimulation, the effects
of which are akin to a stone thrown in a pond. The larger the stone, the more
extensive the ripples on the water. The louder the alarm (or brighter the
light), the more likely it will be to recruit an extensive assembly of neurons,
and the more extensive the assembly, the more likely that you will be awakened.
How
do anesthetics work?
POINT/COUNTERPOINT
Koch:
Today's anesthesiologists administer a diverse collection of chemicals. Yet all
abolish consciousness. Scientists used to believe that anesthetics interfered
systemically with lipids in the cellular membranes of neurons. But we now know
that the compounds interfere with various neuronal processes by binding to
certain membrane proteins. There is no single unique mechanism that causes
consciousness to stop functioning. Among the most important causes, however, is
that anesthesia strengthens synaptic inhibition, or reduces synaptic
excitation, in large regions of the brain. Activity is not fully shut down, but
the ability of groups of neurons to form stable coalitions is severely
compromised. When neurons that encompass the back and the front of the cerebral
cortex cannot set up synchronized communication, consciousness becomes
impossible.
Greenfield:
Anesthetics do not switch off any single brain area; they depress neuronal
activity in different regions across the whole brain. Anesthetics therefore
achieve their effect by altering an emergent property of the holistic brain:
neuronal assemblies. As anesthetics reduce the size of neuronal assemblies,
they reduce the degree of consciousness until it is nonexistent. This scenario
also explains the different stages of consciousness that can occur as
anesthesia takes effect, such as hyperexcitability and delirium. I have suggested
elsewhere that people who have brains with underfunctioning neuronal
connections, and who hence have small assemblies, often exhibit strong emotions
and lack of reason--just the types of states many patients exhibit while
anesthesia is taking effect and their assemblies are shrinking.
Why
is there a subjective difference between dreaming and wakefulness?
POINT/COUNTERPOINT
Koch:
Although the brain is highly active during the rapid eye movement phase of
sleep that is most associated with vivid dreams, the regional pattern of brain
activity is quite distinct from that of wakefulness. In particular, the limbic
system (loosely, the system of emotions and memory) is very active, but the
parts of the frontal lobes that are involved in rational thought are subdued.
In both dreaming and wakefulness, coalitions of neurons form, but they include
neurons in different parts of the brain. During wakefulness, the coalitions
include many more neurons in the prefrontal cortex, where reason and sensible
narratives are imposed to order perceptions, but that activity is notably
lacking during dreams. These features reflect the often bizarre and strong
emotional content of dreaming.
Greenfield:
Dreams most likely correlate with assemblies of neurons that are much smaller
than those occurring when we are awake. The assemblies would be limited because
no strong external stimuli are engaging large numbers of neurons. The transient
recruitment of neurons during dreams is thus driven purely by response to
spontaneous, intrinsic brain activity. And because the assemblies are not
triggered by a sequential narrative of events in the outside world, the
linkages among assemblies are haphazard, idiosyncratic or nonexistent, leaving
dreams as random images or events. The lack of extensive, operational neuronal
connections would also account for the notable absence of the checks and
balances that normally characterize adult cognition when awake.
*******
Christof
Koch is professor of cognitive and behavioral biology at the California
Institute of Technology, where he teaches and has conducted research on the
neuronal basis of visual attention and consciousness for more than two decades.
He is an avid hiker and rock climber who has scaled several noted peaks.
Susan
Greenfield is professor of pharmacology at the University of Oxford, director
of the Royal Institution of Great Britain and member of the British
Parliament's House of Lords. Her research focuses on novel brain mechanisms,
including those underlying neurodegenerative diseases. Her favorite pastimes
are squash and dancing.