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52 SCIENTIFIC AMERICAN MIND N O V E M B E R /D EC E M B E R 2 0 16

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The Footprints of
Consciousness
The bits and pieces of the brain that render us
conscious reside in places few suspected

By Christof Koch
ILLUSTRATION BY ARMANDO VEVE

“It is in the brain that the poppy is red, that the apple is odorous, that the skylark sings.”
— Oscar Wilde (1854–1900)

e moderns take it for granted that consciousness is intimately tied up with the
brain. But this assumption did not always hold. For much of recorded history,
the heart was considered the seat of reason, emotion, valor and mind. Indeed,
the fi rst step in mummification in ancient Egypt was to scoop out the brain
through the nostrils and discard it, whereas the heart, the liver and other internal
organs were carefully extracted and preserved. The pharaoh would then have ac-
cess to everything he needed in his afterlife. Everything except for his brain!
Several millennia later Aristotle, one of the greatest of all biologists, taxonomists,
embryologists and the fi rst evolutionist, had this to say: “And of course, the brain is
not responsible for any of the sensations at all. The correct view [is] that the seat and
source of sensation is the region of the heart.” He argued consistently that the primary
function of the wet and cold brain is to cool the warm blood coming from the heart.
Another set of historical texts is no more insightful on this question. The Old and the
New Testaments are filled with references to the heart but entirely devoid of any men-
tions of the brain.
Debate about what the brain does grew ever more intense over ensuing millen-
nia. The modern embodiment of these arguments seeks to identify the precise areas
within the three-pound cranial mass where consciousness arises. What follows is an
attempt to size up the past and present of this transmillennial journey.
The field has scored successes in delineating a brain region that keeps the neural
engine humming. Switched on, you are awake and conscious. In another setting, your

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1 2 3

body is asleep, yet you still have experi- scientist by testing the hypothesis that ble for carrying out specific functions.
ences — you dream. In a third position, the brain controls all muscles by means Locationism rose to dominance after
you are deeply asleep, effectively off- of the nerves. Famously, Galen argued 1861, when French neurologist Paul
line. What is more, I and others have la- that the vital spirit that animates hu- Broca presented the landmark case of a
bored on discovering critical brain re- mans flows up from the liver to the heart patient unable to speak except for a sin-
gions that imbue us with specific forms and into the head. There, inside the ven- gle word. The patient’s brain exhibited
of conscious experience: perceptions of tricles— the brain’s interconnected fluid- widespread damage to the left inferior
the orange hues of a sunset, pangs of fi lled cavities — the vital spirit becomes frontal gyrus, part of the neocortex that
hunger or the stabbing pain of a tooth- purified and gives rise to thought, sensa- crowns the top part of the brain. An
ache. Those are in the neocortex, the tion and movement. analysis of a second patient reinforced

D E A /C. S A P PA G e t t y I m a g e s (1); D E A /A . D A G L I O R T I G e t t y I m a g e s (2); W O R L D H I S T O R Y A R C H I V E A l a m y (3); I N T E R F O T O A l a my (4 )


brain’s outer surface, which generates For more than 12 centuries after- Broca’s conclusion that this small region
the particular content of experience as it ward, the world plunged back into dog- was responsible for productive speech
plays out from one moment to the next. ma, mumbo jumbo, exorcism and mys- (touch the bottom of your left temple to
ticism until the beginning of the Europe- get an idea of where it is). The identifica-
From Heart to Head an Enlightenment. The publication of tion of this region, which has been
By and large, classical Greece and Cerebri anatome in 1664 by English named Broca’s area, also fortified the
Rome were in thrall to cardio-centric doctor Thomas Willis heralded the be- view of the neocortex as the jewel in the
thinking. The brain proper looked too ginning of today’s neuro-centric age. It crown of the central nervous system, the
mushy, coarse and cold to host the sub- featured meticulous drawings (by the region most closely associated with
lime soul. Yet some clinicians and anat- young Christopher Wren, England’s higher-order cognitive functions, in-
omists had already deduced that the most acclaimed architect) of the brain’s cluding consciousness.
brain was intimately tied to sensation convolutions that transcended previous In those early days during the Sec-
and movement. Two remarkable exam- renditions, which greatly resembled a ond Empire in France, doctors depend-
ples are the fourth-century b.c. work by tangle of intestines. ed on keen observations of symptoms
Hippocrates — On the Sacred Disease — Neuroscience has always retained a and on dissection of the brains of pa-
that combines a rejection of superstition creative tension between holists, who ar- tients who had died to reliably infer the
in treating brain disorders with an accu- gue that mental activity and other brain site of a lesion and connect it to its like-
rate clinical description of epilepsy. Lat- functions cannot be tied to a specific re- ly function. Today neurologists can
er, in second-century a.d. Rome, the re- gion in the brain, and locationists, who make these connections by directly peer-
nowned Greek physician Galen became, claim that specific loci, hot spots in the ing inside the heads of their living pa-
in essence, the fi rst experimental neuro- language of brain imagers, are responsi- tients using x-ray computed tomogra-
phy, magnetic resonance imaging and
other powerful imaging techniques.
FAST FACTS
Damage to the brain comes in many
WHERE CONSCIOUSNESS LIVES
forms: strokes, hemorrhages, tumors,
ΠUntil the 17th century, widespread beliefs held that the heart was the seat of sensation, viruses, bullets and blows. Examining
volition and the soul.
such destruction, when limited in size,
 It took until the 1980s for studies on the nature and physiology of consciousness to become
more than a theoretical exercise. can illuminate the link between the
Ž Research has demonstrated that a region in the lower brain—the brain stem—is necessary brain’s complex structure and what hap-
for switching on activity in areas devoted to higher cognitive functions. pens when a particular region shuts
 A posterior area of the brain appears to be key for conscious seeing, hearing and feeling. down. Interpreted carefully, such clini-

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The quest for the seat of consciousness began
in all the wrong places. Embalming procedures
in ancient Egypt (1) discarded the brain because
it was thought that the heart, liver and other
organs hosted the soul. Hippocrates and Galen,
physicians from antiquity depicted in a 13th-cen-
tury fresco (2), realized that the brain controlled
our thoughts and actions. During the Renais-
sance, Andreas Vesalius, credited as the father of
modern anatomy, captured details of the brain’s
surface (3), a prelude to René Descartes’s specu-
lation that the pineal gland (onion-shaped struc-
ture, 4) is where consciousness resides.

cal studies have by far been the most fe- pressed, consciousness will flee the vic- During and after World War I, a re-
cund source of knowledge concerning tim. Indeed, even a small injury to parts markable wave of “sleepy sickness,” or
the relation between the physical brain of it can lead to a profound and sus- encephalitis lethargica, swept the world.
and the conscious mind. tained loss of consciousness. The patient The condition helped to point to the
can go into stupor and can only be par- brain stem as a mediator of sleep and
The Brain’s Light Switch tially aroused after vigorous and pro- wakefulness. This form of encephalitis
Some areas of the brain are more in- longed stimulation. Worse, the patient induced in many of its victims a state of
strumental than others in generating a can lapse into a coma, an enduring, almost permanent and statuelike sleep,
conscious state. The brain stem at the sleeplike state of immobility with closed from which they would awaken only for
top of the spinal cord is one of them. If eyes, from which arousal may prove to a few hours at a time. It was the astute
the brain stem is damaged or com- be difficult. observation by Austrian neurologist

Occipital Cortex
A Guided Tour Broca’s Area
Visual information about form and
Scientists fall into two In 1861 Paul Broca discovered a small region
motion gets processed in this area
camps when discussing at the brain’s surface that is responsible for
at the back of the brain.
the brain. Holists argue producing speech.
that consciousness is gen-
erated by the entire three-
pound mass made up of
170 billion cells, of which
half are nerve cells. Loca-
tionists support the idea
that specific neural circuits Fusiform Gyrus
are responsible for specific Parts of this structure
functions, including con- play a critical role in
sciousness. On closer recognizing faces,
inspection, neuroanato- among other visual
mists have realized that tasks. Damage to it
one confined area, the causes face blindness.
brain stem, ensures that
we do not lapse into a coma
or suffer from a sleeping
sickness. Meanwhile rear
areas on the surface of the
brain are needed to gener-
ate mental imagery and oth-
er specific conscious expe- Cerebellum
riences, such as recognizing Brain Stem This mini brainlike structure
your grandmother. enables precise motor
Neurons in the brain stem con-
control. Lesions in part
trol the level of arousal or wake-
of the cerebellum do not
© I S T O C K .C O M

fulness. If these do not properly


appear to lead to a loss of
function, the patient lapses into
conscious experiences.
stupor or a coma or may die.

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Baron Constantin von Economo of vic- control internal bodily processes, such as and its connection to consciousness.
tims of this epidemic that led to the hy- breathing, thermal regulation, muscle When we began this labor of love in
pothesis that a brain center in the hypo- tone, heart rate, and so on and process the late 1980s, writing about conscious-
thalamus actively promotes sleep, signals relating to the working condition ness was viewed as a fringy subject, a
whereas another in the upper brain stem of the body’s organs. sign of a scientist’s cognitive decline. Re-
produces wakefulness. Brain stem neurons promote con- tired Nobel laureates did it, as did phi-
A more precise localization came sciousness by suffusing the cortex with losophers and mystics, but not hard-core
from classical experiments by Italian Giu- a cocktail of these neurochemicals to scientists. When the topic arose, gradu-
seppe Moruzzi and American Horace keep cortical neurons in an aroused ate students, always finely attuned to the
Magoun in the late 1940s, demonstrating state. These substances alone are inca- mores and attitudes of their elders,
that a brain stem region known as the pable of producing an experience. Rath- rolled their eyes and smiled indulgently.
er they form the background — a Betraying an interest in consciousness
neural palette — on which any con- was ill advised for a young professor,
scious experience occurs, and this particularly one who had not yet at-
chemical mix acts as a “switch.” tained the holy state of tenure.
When we began But if the cortex is severely dam- Those attitudes have since changed.
this labor of love in the aged, it cannot receive the signals Together with a handful of colleagues,
late 1980s, conscious- that maintain the light of conscious
experience . Patients who have
Crick and I gave birth to a science of con-
sciousness. Its physical basis in the brain
ness was viewed as brain stem function that has been is now investigated worldwide, and ques-
a fringy subject, a sign relatively spared but who have tions concerning what makes any system,
widespread cortical destruction biological or man-made, exhibit a con-
of a scientist’s typically remain in a vegetative scious state are hotly debated. Conscious-
cognitive decline. state, permanently unresponsive ness is no longer the unspoken taboo.
but with eyes open, experiencing or Our goal from the outset was to iden-
feeling nothing. tify the mechanisms in the brain that, at
a minimum, are needed to create a spe-
midbrain reticular formation modulates Where Consciousness Resides cific conscious experience: seeing the set-
the level of wakefulness (“reticular” here At this point, the story gets personal. ting sun, recognizing your grandmother
refers to the mesh or netlike appearance In the late 1980s, as a freshly baked as- or feeling that god-awful toothache. We
of this part of the brain). sistant professor at the California Insti- called these the “neuronal correlates of
In more recent years this notion of a tute of Technology, I started having reg- consciousness,” or NCC. The definition
monolithic system that activates con- ular conversations with Francis Crick of an NCC was by no means clear. Must,
sciousness has given way to a recognition about the mind-body problem. Crick for instance, some nerve cells vibrate at
that 40 or more nuclei are housed with- was the physical chemist who, together a particular magical frequency? And if
in the brain stem, all of which exhibit a with James Watson, discovered in 1953 that is true, what is it about the biophys-
specific neurochemical identity. These the double-helical structure of DNA, the ics of particular bits and pieces of high-
conglomerations of neurons are pro- molecule of heredity. In 1976, at age 60, ly excitable brain matter vibrating at a
foundly different in structure from the when Crick’s interests shifted from mo- specific frequency that is able to produce
layered organization of the cortex. Cells lecular biology to neuroscience, he left the glorious surround sound and Tech-
in different nuclei manufacture, store Cambridge, England, in the Old World nicolor that constitute the sounds and
and release different neurotransmitters to establish his new home in La Jolla, Ca- sights of life? Are these special con-
or neuromodulators at their synaptic ter- lif. Despite an age difference of 40 years, sciousness neurons all located in a par-
minals — acetylcholine, serotonin, nor- Crick and I struck up an easy friendship ticular part of the brain, as René Des-
adrenaline, GABA, histamine and orex- and a collaboration that would last for cartes famously postulated back in the
in. Many of these brain stem nuclei mon- 16 years and result in two dozen scien- middle of the 17th century for the pine-
itor and modulate our conscious state, tific papers, essays and two books. al gland, probably the first hypothesized
including wake-to-sleep transitions. All of them focused on the anatomy neuronal correlate of consciousness?
Collectively they transmit signals that and physiology of the mammalian brain It is important to stress the “mini-
mal” in defining the NCC. Without that
qualifier, all of the brain could be consid-
THE AUTHOR
ered a correlate: after all, the brain does
CHRISTOF KOCH is president and chief scientific officer at the Allen Institute for Brain generate consciousness, day in and day
Science in Seattle. He serves on Scientific American Mind’s board of advisers. out. But Crick and I wanted to fi nd the

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specific synapses, neurons and circuits and colors but not keys. Yet if she grasps ognition in volunteers within regions of
that generate — that, in fact, cause — an them or if they are jingled, she immedi- the ventral temporal cortex, called the fu-
equally specific conscious experience. Be- ately knows what they are. Poetically siform gyri (bottom area toward the back
ing careful scientists, we used the more termed Seelenblindheit in German (lit- of the head). Found bilaterally, the re-
cautious “correlates” in place of the more erally, “blindness of the soul”), this con- gions are referred to as the fusiform face
definitive “causes” of consciousness. dition was rechristened agnosia by Sig- area and respond more strongly to pic-
Based on our knowledge of the high- mund Freud, a term that persists. The tures of faces, compared with scrambled
ly sophisticated nature of cortical nerve late neurologist Oliver Sacks brilliantly faces or other objects and scenes.
cells and their response to stimuli in the wrote about patients with agnosia and Epileptic patients have played an out-
external world, we set our sights on the how their loss shaped the way they expe- sized role in consciousness research. This
cortex, the gray matter on the brain’s rienced the world. is especially true of those who had elec-
outer surface. The cortex is a laminated Consider A.R., who suffered a block- trodes implanted to control their sei-
sheet of nervous tissue about the size of age to the cerebral artery that damaged zures. A study of 10 such patients con-
a large pizza. Two of these sheets are a small region on one side of his occipi- ducted in 2014 at Stanford University
crammed into the skull, side by side, tal cortex. The stroke briefly blinded used the electrical signals recorded by
making up the left and right cortical him. He eventually recovered sight but implanted electrodes to confirm that
hemispheres. The cortex is subdivided permanently lost color vision in the up- both the left and the right fusiform gyri
into the neocortex— a defining hallmark per left quadrant of his field of view, cor- responded selectively to faces, compared

The brain stem (left, highlighted in yellow) serves as an engine of consciousness. When injured, it may extinguish all conscious activity.
The modern search for key brain loci that imbue us with consciousness began with Francis Crick, the author’s mentor (above), decades
after he had co-discovered the structure of DNA.
G E T T Y I M A G E S (l e f t ); D A N I E L M O R DZ I N S K I G e t t y I m a g e s (r i g h t )

of mammals — and the evolutionarily responding to the site of a pea-sized le- with pictures of body parts, cars or hous-
older archicortex. All available evidence sion in his right occipital visual cortex. es. These electrodes could also directly
points toward certain key regions with- A.R.’s low-level vision — detection of excite the underlying cortical tissue us-
in the 11 ounces of highly structured brightness, lines, and so on— and his mo- ing electrical pulses. Stimulating the
neocortical tissue as the location of con- tion and depth perception were normal. right fusiform gyrus led to reports of per-
tent-specific NCCs. The only other deficit was a difficulty ceiving faces. In one study, a patient who
Lesions to the rear section of the distinguishing — he could not read text— looked at his neurologist remarked:
neocortex— for instance, from a stroke but this problem was confined again, to “You just turned into someone else. Your
or some other damage — demonstrate the upper left quadrant. face metamorphosed. Your nose got sag-
what happens when activity in the back Functional MRI and EEG are some of gy and went to the left. You almost
of the brain shuts down. A patient so af- the most common ways to look for neu- looked like somebody I’d seen before but
flicted cannot recognize a set of keys on ral correlates of consciousness in healthy somebody different. That was a trip”
a chain dangling in front of her. She volunteers. These techniques can identify [see box on page 59].
looks at them and sees texture and lines a bevy of brain areas related to face rec- When the left fusiform gyrus was

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stimulated, patients either did not make of the world appears intact and nor-
such reports, or they were restricted to mal. Consider the rare, and ex- Large portions of
simple, nonface imagery, such as twin- treme, case of a 24-year-old wom-
kling and flashing lights or traveling an born without a cerebellum. the front of the brain
blue and white balls. Although she has mild mental can be excised without
This study underscores the truth be- impairment and moderate motor
hind the oft-repeated mantra that corre- deficits and talks with a slight trem-
having a major impact
lation is not causation. Just because the or, she can speak clearly about her on conscious
left fusiform gyrus is selectively activat- daily experiences, her likes and dis- experience.
ed by a sight, sound or action does not likes, and her life with a young
imply that the area is essential for vision, daughter. This is surprising given
hearing or movement. These patients that her brain scans [see 2 below]
also teach us that electrically stimulat- show she has only a fluid-filled cav-
ing the right ventral temporal cortex can ern where her cerebellum should be. Indeed, it is common surgical
give rise to imagined faces. Indeed, this This absence is remarkable because knowledge that removing much of the
region is the best candidate we have for the cerebellum contains Purkinje cells, front of the cortex causes no apparent
a content-specific NCC like “seeing” a whose fan-shaped structures are among major defi cit! This surprising realiza-
face. Its activity correlates closely and the most beautiful and complex of all tion stems from insight gained from
systematically with facial perception. neurons. And astonishingly another cell hundreds of neurosurgeries for tumors,
Stimulation of it induces or alters the type in the cerebellum— the granule neu- epileptic seizures and other neurologi-
perception of faces, and, crucially, peo- ron— outnumbers cortical ones by a fac- cal conditions during the fi rst half of

I M A G I N G F I N D I N G S I N A L I V I N G PAT I E N T,” B Y F E N G Y U E T A L ., I N B R A I N. P U B L I S H E D O N L I N E A U G U S T 2 2, 2 0 14 (2)


A J P H O T O G e t t y I m a g e s (1); F R O M “A N E W C A S E O F C O M P L E T E P R I M A R Y C E R E B E L L A R A G E N E S I S: C L I N I C A L A N D
1 2

ple become face-blind when this region tor of four. Despite this intricate physi- Tools in the hunt for consciousness include
is destroyed. ology, neural activity in the cerebellum EEG (1) and MRI brain scans (2). These
Sometimes not finding something does not give rise to consciousness. scans show a woman with an empty space
where her cerebellum should be.
where you expected it can be as impor- Even more intriguing than the cere-
tant and revealing as fi nding it. This ob- bellum are the frontal lobes of the neo-
servation applies to the cerebellum, cortex. Traditionally they are thought to the 20th century, when neurosurgeons
tucked below the cortex at the back of be the key hallmark of our species, hav- routinely excised large swathes of fron-
the brain, and even pertains to parts of ing expanded more in Homo sapiens tal or prefrontal cortex on both sides.
the cortex. than in all other higher primates. Func- What is remarkable is how unremark-
If the cerebellum is damaged, both tional MRI has also shown them to be able these patients appear from their
animals and people have difficulty mak- involved in tasks that involve planning, clinical description.
ing precise movements, and the move- short-term memory, language, reason- The most dramatic example is Mr. A,
ments they do make lose precision and ing and self-monitoring. Yet more than a patient of neurosurgeon Walter Dandy
become erratic, jerky and uncoordinat- a century of reports describing electrical in 1930. Because of Mr. A.’s massive tu-
ed. Yet patients with cerebellar lesions brain stimulation carried out during mor, the surgeon had to amputate the pa-
do not complain of being unable to see, neurosurgery while the patient is awake tient’s frontal poles, the protruding sec-
hear or feel. Nor do they experience suggest that it is difficult to directly elic- tions at the front of the brain. The patient
transient or permanent loss of con- it sensory experiences from stimulation survived this bilateral frontal lobectomy
sciousness. Their subjective experience of frontal sites. for 19 years and continued to speak. A

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Now You See Me, Now You Don’t
Electrical stimulation of the right fusiform gyrus, seen from below, in four epileptic patients undergoing surgery caused distorted perception
of faces. The red dots represent electrodes that produced distorted views, whereas the blue ones did not do so in one patient.

Front of brain

1 2 3 4

“Like you weren’t you. “You turned into some- “That orange part “[The eye] looked
You were a different one else. Your face looked like a person ... like a circle and
person. I noticed the metamorphosed.... like a face and a body.... then changed to
eyes. I was able to see Your nose got saggy Like a hallucination a rectangle shape.”
almost your whole body and went to the left.” of the curtains.”
on your right side.”
E F F EC T S I N C O N S C I O U S FA C E P E R C E P T I O N ,” B Y V I N I T H A R A N G A R A J A N E T A L ., I N J O U R N A L O F N EU R O S C I E N C E ,

note in his file observed that “one of the might then be involved in unconscious brain that make us conscious appear to be
S O U R C E : “ E L EC T R I C A L S T I M U L AT I O N O F T H E L E F T A N D R I G H T H U M A N F U S I F O R M GY R U S C A U S E S D I F F E R E N T

salient traits of Mr. A’s case was his abil- planning, strategizing, forming memo- centered on a more restricted hot zone in
ity to pass as an ordinary person under ries and focusing attention. the posterior part of the neocortex, with
casual circumstance.” When he toured some possible additional contributions
the Neurological Institute in the compa- The Hot Zone from some anterior regions.
V O L . 3 4, N O. 3 8; S E P T E M B E R 17, 2 0 14; D E A G O S T I N I P I C T U R E L I B R A R Y G e t t y I m a g e s (b r a i n)

ny of distinguished neurologists, “no one Since the modern quest for the NCCs These fi ndings raise the question of
noticed anything unusual.” Mr. A. did at the end of the 20th century, progress why the seats of consciousness are so cir-
exhibit some of the behaviors associated has been rapid compared with previous cumscribed. Is there something so differ-
with frontal lobe removal, such as child- millennia. First, conceptual work has ent in the wiring or behavior of neurons
like behavior, lack of inhibition and a clarified the importance of investigating in the back of the cortex from those in the
need to tell jokes. Neither he nor other pa- the neural correlates of both specific con- front? Future investigations will be need-
tients who submitted to similar surgeries scious contents and consciousness as a ed in the decades — maybe centuries —
were robbed of conscious behaviors. whole. Second, some parts of the brain ahead to further illuminate the types of
Their capacity to see, hear or experience have been identified as contributing little neural activity that underlie the infinite
the world remained intact, despite the to conscious experience. The areas of the varieties of human experience. M
drastic surgical intervention.
That the anterior cortex may not be
necessary for sensory consciousness does MORE TO EXPLORE
not imply that it does not contribute di- ■ Brain of Patient A. after Bilateral Frontal Lobectomy; Status of Frontal-Lobe Problem.
rectly to any given aspect of conscious- R. M. Brickner in AMA Archives of Neurology and Psychiatry, Vol. 68, No. 3, pages 293–313; 1952.
ness. After all, being self-conscious (re- ■ Electrical Stimulation of the Human Brain: Perceptual and Behavioral Phenomena
Reported in the Old and New Literature. A. Selimbeyoglu and J. Parvizi in Frontiers in Human
flecting on what one perceives) is differ-
Neuroscience, Vol. 4, Article 46, pages 1–11; May 2010.
ent from perceiving something, yet both ■ The Neural Correlates of Consciousness: Progress and Problems. C. Koch, M. Massimini,
are subjective experiences. Perhaps re- M. Boly and G. Tononi in Nature Reviews Neuroscience, Vol. 17, pages 307–321; May 2016.
flection, effort, and so on are generated From Our Archives
by the anterior cortex, although no firm ■ The Face as Entryway to the Self. Christof Koch; Consciousness Redux, January/February 2015.
evidence exists yet. The prefrontal cortex ■ Sleeping While Awake. Christof Koch; Consciousness Redux, November/December 2016.

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