Electroencephalography : basic principles, clinical applications, and related fields

1332 Pages·2005·18.125 MB·English

by  Ernst Niedermeyer, Fernando Lopes da Silva MD PhD

8 Electroencephalography: Basic Principles, Clinical Applications, and Related Fields
Neighboring Belgium was the home of a giant in electro- Alexander Forbes. When McPherson placed two electrodes
physiological neurophysiology: Frederic Bremer (1892–1982) on the exposed brain of a cat and ran the output into a string
from the Université Libre of Brussels. Bremer quickly recog- galvanometer, he saw rhythmical 10/sec EEG activity. This
nized the usefulness of EEG methods in the experimental finding was rejected as an artifact by Forbes. Was Forbes
investigation of the brain. He recognized the influence of af- completely unaware of the work from Caton to Pravdich-
ferent signals on the state of vigilance and compared his feline Neminsky?
preparation called “cerveau isolØ ” (with midbrain transection) The rise of American EEG work to international fame is
with the “encpØhale isolØ ” resulting from transection at the customarily associated with the work of Hallowell Davis,
boundary between the medulla oblongata and cervical cord. Frederic A. Gibbs, and Erna Gibbs at Harvard and also with
The former preparation would produce permanent coma; the Herbert Jasper’s work at Brown University in Providence,
latter would cause a variable state of vigilance, with waking Rhode Island. According to O’Leary and Goldring (1976),
and sleeping demonstrated on the EEG recording. In other A. J. Derbyshire, a graduate student of Hallowell Davis,
words, trigeminal-sensory, auditory, visual, and probably also brought Berger’s paper of 1929 to Davis’s attention. Der-
olfactory influences would help to keep the (artificially venti- byshire, Pauline Davis, and H. N. Simpson then tried in vain
lated) encpØhale isolØ preparation in a waking-sleeping to demonstrate their own alpha rhythms. There were finally
rhythm (Bremer, 1935). shouts of joy when Hallowell Davis himself was found to
The greatness of this investigator must be reemphasized, have a good alpha rhythm. Otherwise, the first human EEG
especially in today’s era of short memory. Whoever reads study in America would have been a negative one. This
his study entitled “Cerebral and Cerebellar Potentials” (Bre- work was done in 1934, just before human EEG studies
mer, 1958) will roughly understand the dimensions of this started to mushroom in the United States.
neurophysiologist. The EEG, however, had been used for animal experi-
ments for some years in the United States, starting with
DevelopmenOittnsh eroEpuerCaonu ntries
Bartley and Newman (1930, 1931) and Bartley (1932), who
Italy was one of the first countries where the EEG found produced EEG tracings in the dog. Howard Bartley did his
fertile soil. Mario Gozzano, for many years professor of work at Washington University in St. Louis, a place that had
clinical neurology in Bologna (later in Rome), published his already developed into a hotbed of neurophysiology due to
experiences with the new method as early as 1935. Gozzano the magnificent work of Herbert S. Gasser, Joseph Erlanger,
personifies the (not too common) example of a leading neu- and George Bishop—a group that made excellent use of
rologist assuming leadership in clinical electroencephalog- Braun’s cathode ray oscilloscope (oscillograph) in the study
raphy (Mazza et al., 2002). All too often, eminent clinical of peripheral nerve potentials. This outstanding group was
neurologists spurned the new method. joined later by James L. O’Leary, a prominent neurophysiol-
A. Gemelli came from the diametrically opposite area of ogist, electroencephalographer, and neurological clinician.
neurosciences. This great scholar was a monk, psychologist, Early experimental EEG work was done by Davis and Saul
philosopher, polyhistor, and president of the Catholic Uni- (1931), Travis and Dorsey (1931), Travis and Herren (1931),
versity in Milan. In 1937, he reported his first studies of Bishop and Bartley (1932), Bartley (1932), and Gerard et al.
thehuman EEG. Gemelli hence represents the psychological (1933) (after Grass, 1984). The work of Ralph W. Gerard
wing of EEG research, which subsequently spawned a num- (1900–1974) is linked with the introduction of a concentric
ber of outstanding Ph.D. electroencephalographers. (Others needle electrode for the stereotaxic exploration of the brain
would come from the ranks of experimental neurophys- in experimental animals. Gerard joined forces (in 1934) with
iologists.) Franklin Offner, one of the leading electronic engineers in
The Austrian psychologist Hubert Rohracher falls into the development of EEG and related equipment.
the Gemelli category. He held the chair of psychology for American EEG work in the human started, as it was
many years at the University of Vienna, but, in his early aca- pointed out before, at Harvard in Boston (Hallowell and
demic work, he fell under the spell of the alpha rhythm and Pauline Davis, Frederic and Erna Gibbs, William G. Len-
even made a “pilgrimage” to Hans Berger in Jena (in the nox), at Brown in Providence (Herbert H. Jasper), but also at
1930s). His early EEG studies can be dated back to 1938. the University of Iowa in Iowa City where Lee Travis
worked, an experimental psychologist who became the
founder of a powerful school (Herbert Jasper, Donald Linds-
AmeriEcnat etrShsce e ne
ley, John R. Knott, and Charles Henry).
Around 1935, the center of gravity in the still modest The great international breakthrough in clinical electro-
bulk of EEG work started to shift from Europe to North encephalography came in 1934 with studies of epileptic
America. Fascinating new reports came from the United patients. Frederic Gibbs had come from Johns Hopkins Uni-
States. European investigators started to travel across the At- versity in Baltimore to join the Harvard group. He sought out
lantic, and even Hans Berger was about to accept an invita- William G. Lennox, who had already become a widely
tion to the United States in 1939, when the beginning of known epileptologist. It might be interesting to point out that
World War II thwarted his plans. Lennox had started studies of the cerebral circulation by
In the pre-Berger development of experimental EEG stud- measuring the O and CO content of the jugular veins
2 2
ies, America had not played any role. Schwab (1951) reports (Lennox, 1930, 1931; Lennox and E. L. Gibbs, 1932). E. L.
that, in 1918, a medical student of Harvard Medical School, Gibbs was Erna L. Gibbs, originally the technical co-worker
Donald McPherson, worked under the eminent physiologist of Lennox but who became the wife of Frederic Gibbs and
Chapter 1 / Historical Aspects 9
one of the world’s first EEG technicians and the co-author of stages of sleep. This research was done off the academic
numerous papers. She had come to Boston as an immigrant track in Tuxedo Park, New Jersey (Loomis et al., 1935, their
from Germany. The pre-EEG work of Lennox and Gibbs on first study). The Davises eventually turned to audiology and
the cerebral blood flow was a milestone in this field. (One of moved to St. Louis. At Brown University in Providence,
the great present-day masters of cerebral blood flow, Louis Rhode Island, Jasper studied the EEG of behavior disorders
Sokoloff from the National Institutes of Health, expressed to in children before he found his niche in basic and clinical
me in a personal communication his profound admiration for epileptology at McGill University in Montreal in his epochal
this pioneering work.) EEG simply exerted a greater degree collaboration with Wilder Penfield (discussed later). Lee
of fascination to W. G. Lennox than did cerebral blood flow. Travis gradually disappeared from the scene but his foremost
Twelve children with petit mal epilepsy were the clinical disciples, John R. Knott and Charles E. Henry (Ph.D. elec-
subjects for the petit mal epilepsy study of Gibbs and Davis troencephalographers with strong clinical inclinations) were
(1935) and Gibbs et al. (1935, 1937). This work remains bound to assume a very important role in America’s EEG
an evergreen in the entire EEG literature; hardly any EEG work. Their ultimate skill and supreme dedication turned
finding has left such an indelible impression as the associa- them into the “conscience of EEG,” steering developments
tion of petit mal absences and 3/sec spike-wave complexes. into the right direction and correcting the course when there
(Of course, it was found out later that spike waves could was danger of going astray. D. Lindsley became one of the
occur without petit mal.) While Berger was gripped by the pioneers in the investigation of maturational EEG aspects; at
rhythms, Frederic Gibbs came under the fascination of the University of California at Los Angeles, he directed ex-
paroxysmal patterns such as spike waves. Shortly afterward, cellent neurophysiological EEG research.
the EEG patterns of grand mal and psychomotor seizures This was the first wave of American EEG pioneers and
were reported by the same team (Gibbs, Lennox, and Gibbs), their immediate disciples and followers. It is impossible
but the stretches of fast spikes (in grand mal) and the rhyth- for the historian to do justice to the second wave, which
mical activity in 4/sec or 6/sec frequency (in psychomotor started before the great 1930s were over. There was Robert
seizures) were no match in popularity for the 3/sec spike Schwab at Harvard and at the Massachusetts General Hos-
waves of petit mal. pital in Boston, in whom the mastery of EEG was com-
The technical quality of the EEG tracings shown in these bined with great clinical neurological talents (especially in
studies left much to be desired. Dr. and Mrs. Gibbs traveled the field of myasthenia gravis, parkinsonism, and epilepsy).
to Germany in the summer of 1935, paid a visit to Hans Across the Charles River, at the Massachusetts Institute of
Berger, spent some time at the Berlin-Buch Institute, and Technology, there was Warren McCulloch, a fiery genius
studied the “polyneurograph” instrument of Jan F. Toennies; like Grey Walter in Bristol and a profound thinker. His
they also saw the instrumentation of Matthews in England. scope would range light years beyond the limits of EEG
Frederic Gibbs then contracted Albert Grass (then at the and neurophysiology. (One must read his Embodiments of
Massachusetts Institute of Technology) to build a three- Mind to fathom his greatness, even though one may be in-
channel preamplifier. In 1935, the Grass Model I went into clined to disagree in many points.) He and Grey Walter
use; it had three channels and an ink writer that recorded on lived in the world of brain machines, but there was still a
rolls of paper (the folded paper not yet being in use). niche for a psyche (when one tries to read between the
The Gibbs-Gibbs-Lennox era of the 1930s proved to be lines). Earlier at Northwestern University in Evanston, Illi-
perhaps the most exciting period in the history of EEG. In nois, outside Chicago, McCulloch had been involved with
those years, EEG found the domain of greatest effectiveness: Dusser de Barenne in “neuronographic” work, an import
the realm of the epileptic seizure disorders. Epileptology can from Utrecht, Netherlands; this work was based on topical
be divided historically into two periods: before and after the strychnine poisoning of the cortex and exploration of
advent of EEG. Insights into the nature of the epileptic mech- transmitted spiking to other regions.
anisms deepened, not in a subtle manner but with a huge Clinical EEG research already started to conquer certain
leap. What Fischer had started in 1931 with his experimental fields outside epileptology. Grey Walter’s discovery of the
studies on picrotoxin and its effect on the cortical EEG in an- delta focus (Walter, 1936) located over hemispheric brain
imals, the Gibbses and Lennox applied to human epileptol- tumors had opened the search for further relationships be-
ogy, and a wide door was flung open for the work of future tween brain lesions and focal EEG correlates; metabolic dis-
decades. It is true that Berger in his seventh report (Berger, turbances and especially hypoglycemia were explored with
1933) had shown a few examples of paroxysmal EEG dis- EEG. (The work of H. Hoagland and his co-workers dates
charges in a case of presumed petit mal attacks and also dur- back to 1937.)
ing a focal motor seizure in a patient with general paresis. When the 1930s ended, North America found itself in a
These observations were just mentioned in passing and the leading position in the domain of EEG. By contrast, prog-
opportunity of a major breakthrough was missed. ress made in Europe was quite limited.
As to the other great pioneers of electroencephalography
in North America, Hallowell and Pauline Davis produced
aIatnI1rhd 9 e 4 0osrWlWd
fine work on the normal EEG and its variants. They were
also among the earliest investigators of the human sleep During World War II, from 1939 to 1945, research and
EEG. In the domain of sleep, A. L. Loomis and his co- clinical EEG activities were not flourishing, particularly not
workers E. N. Harvey and G. A. Hobart were the first who in Europe. There were some neurological units where the
methodically studied the human sleep EEG patterns and the EEG was used in the localization of traumatic brain lesions
10 Electroencephalography: Basic Principles, Clinical Applications, and Related Fields
and epileptogenic foci. After World War II, the gap between not fare much better at Harvard in spite of his fine clinical-
North America and Europe was bigger than ever before, and neurological talents.
European EEG research found itself at a low point. Toward the end of the 1940s, Herbert H. Jasper turned
After the war, new activities started in England and into a strong competitor of Frederic Gibbs. Jasper had
France, while the situation in Germany looked desperate. moved to the Neurological Institute of McGill University
W.Grey Walter with his associates V. J. Dovey and H. Ship- in Montreal, joining forces with Wilder Penfield, a neuro-
ton (a brilliant electronic engineer who later moved to Iowa surgeon with a profound neuroscientific background. We
City and then St. Louis) at the Burden Institute in Bristol discuss the rise of the Montreal group below (see Develop-
discovered the paroxysmal response to flickering light at ments in the 1950s).
critical frequencies between 10 and 20/sec. Further work on Two new developments started in the late 1940s. The
epileptic photosensitivity immediately shifted from Bristol EEG technique started to become invasive and, with the use
to Marseille, France, where a young and incredibly talented of special depth electrodes, the exploration of deep intra-
Henri Gastaut used this method, in combination with intra- cerebral regions began. This is discussed below (see Devel-
venous dosages of pentylenetetrazol, to determine the “seuil opments in the 1950s). Automatic frequency analysis also
Øpileptique,” i.e., the individual threshold for paroxysmal started in the 1940s, but this development reached loftier
responses (Gastaut, 1949; Gastaut et al., 1948). heights in the 1960s.
In 1947, the American EEG Society was founded and the Adiscussion of the 1940s would be incomplete without a
First International EEG Congress was held in London; a sec- brief glance at the work of the neurophysiologists. Alarge
ond one followed in 1949 in Paris (in association with clini- segment of neurophysiological work was dominated by the
cal neurology and other neurological disciplines). EEG use of EEG. One of the most fascinating results of these re-
activities in Germany were still minimal; Japan, however, searchers was the demonstration of thalamocortical relation-
gained attention by the work of K. Motokawa, a researcher ships, thus far explored solely with anatomical methods
of EEG rhythms. Switzerland started to develop its own pro- (e.g., the study of the thalamus by A. Earl Walker in 1938,
file; the neurophysiologist Marcel Monnier was instrumen- which propelled this young neuroscientist to great fame for
tal in this regard. W. R. Hess, however, a Nobelist, had decades to come). The work of Morison and Dempsey
gained great prestige by the functional mapping of thalamus (1942) on the recruiting response had great impact on the
and hypothalamus with regard to autonomic responses to neuroscientific world with the demonstration of cortical re-
electrical stimulation. sponses to relatively slow stimulation of the intralaminar
The American scene was bustling with activities. Fred- structures of the thalamus in the cat. This work emphasized
eric A. Gibbs with his co-workers Erna Gibbs and B. Fuster the role of the thalamus in the cortical electrogenesis and
from Uruguay produced another epochal study on the inter- broke the ground for the concept of a “centrencephalic
ictal anterior temporal spike or sharp wave discharge in the epilepsy,” a concept promoted by Penfield and Jasper in
interseizure interval in patients with psychomotor seizures. Montreal (somewhat naively understood as a concept of the
This was an important step in the elucidation of temporal thalamic origin of primary generalized epilepsy).
lobe epilepsy, a work with far-reaching consequences for the Even greater was the impact of the work of Horace W.
entire development of EEG laboratories and their routine Magoun, who had studied the effects of descending and
work. It was found (Gibbs et al., 1948) that the anterior mostly inhibitory influences of the brainstem reticular for-
temporal discharges were often limited to the state of sleep. mation during his work at Northwestern University. To-
This observation meant that a tracing without a sleep portion gether with G. Moruzzi (a fine neurophysiologist from Pisa,
could be insufficient, uninformative, and even misleading. Italy, and investigator of basic epileptic mechanisms), Ma-
Thus, EEG laboratories would include sleep in most (if not goun subsequently studied the ascending system of the
all) of their EEG evaluations. This required pasted elec- brainstem reticular formation (chiefly in the midbrain level)
trodes (rather than rubber bands or caps), a much longer re- and the effect of high-frequency electrical stimulation, con-
cording time, and a much smaller numerical output of sisting of EEG desynchronization and behavioral arousal, on
recordings per technician (incidentally, an evolving profes- cortical function. Magoun, who had moved to the University
sion, which is discussed later). of California at Los Angeles, subsequently investigated the
Transatlantic communication was poor at that time, and it effects of acute lesions made in the midbrain level reticular
was at this point when the routine work in American (or formation in cats. These cats remained in a comatose state
Canadian) EEG laboratories started to become more sophis- with EEG slowing in spite of electrical brainstem stimula-
ticated than that of their European counterparts because of tion because of the destruction of the all-important ascend-
the inclusion of sleep. ing portion of the brainstem reticular formation (Lindsley et
Frederic Gibbs enjoyed enormous international prestige al., 1949). It is no exaggeration when one describes the ef-
at that time as the world’s leader in clinical electroen- fect of these studies on the world of neuroscience as a
cephalography. Nevertheless, his position at Harvard was “bombshell.” For the ensuing 10 to 15 years, the association
much less prestigious; he held the academic rank of an in- of consciousness with reticular formation and Magoun’s
structor (below the professorial ranks), even though a visit name was so strong that it even had considerable influence
to his laboratory was the goal of European colleagues on the Pavlovian dogmatism of the Eastern Bloc countries.
(who could afford the trip). This disproportion drastically Nowadays, however, even talented young neuroscientists
shows the negative attitude toward EEG in neurological de- react to Magoun’s name with a blank expression—sic transit
partments (not universally, of course). Robert Schwab did gloria mundi!
Chapter 1 / Historical Aspects 11
The reason for discussing this experimental work in a exemplified by the 3/sec spike waves of petit-mal absences.
historical overview is to demonstrate the incredibly power- Penfield and Jasper listed these epilepsies as “centren-
ful role of EEG in the neurophysiology of the 1940s. This cephalic” with the concept of “center of the encephalon”
was a high water mark. Subsequently, experimental EEG (i.e., “thalamic midline structures”) serving as the starting
work started to concentrate on single neurons while the point of the bilateral discharges. Henri Gastaut from Mar-
“macro-EEG” gradually declined. seille would follow the lead and so did many others, but
Frederic Gibbs and a host of other electroencephalographers
Developmentit1hns9e 5 0s and neuroscientists became detractors of the centrencephalic
concept. It wasn’t until the late 1960s that it became clear
This is the last decade presented for historical analysis. that the centrencephalic concept stood on very shaky ground
Our story is gradually approaching the present, and a histor- and was ripe for being dismantled. Montreal’s own Pierre
ical outline must shy away from events that comprise the Gloor helped to do this in a cautious and diplomatic manner;
last 30 years. It does not behoove the historian to place liv- others buried the centrencephalic concept more bluntly.
ing and active colleagues into the focus of discussion (with Frederic Gibbs had moved to the University of Illinois
few exceptions). School of Medicine in Chicago (where full professorship was
The 1950s was the decade when EEG became a house- given to him instantly after Harvard had denied him any pro-
hold word. During the early stretch of the decade, almost motion for more than a decade). Chicago—especially the
every university (teaching) hospital had at least one EEG University of Chicago but also Northwestern University and
machine. At the end of the decade, EEG apparatuses had the University of Illinois—had become a world leader inneu-
found their way into a large number of other hospitals and rological sciences over the past 20 years. Percival Bailey, Paul
even into private practice. At university hospitals, central Bucy, Roy Grinker, A. Earl Walker, Gerhardt Von Bonin, C. J.
as well as departmental EEG laboratories emerged. The Herrick, Frederic Gibbs, and many others give testimony to
latter were usually limited to children or adults, and pedi- the glory of neurological science in Chicago at the middle of
atric EEG units evolved (while specialized neonatological that century. In the field of EEG, the Chicago group under the
EEG units followed suit about 10 years later). Some psy- Gibbses and the Montreal group under Jasper and Gloor were
chiatric departments took particular pride in their clinical strong rivals throughout the 1950s, especially with respect to
and research-oriented EEG work. It is absolutely true that leadership in epileptological electroencephalography. One of
psychiatry was always “nice” to the electroencephalogra- the greatest masters from the Chicago school, A. Earl Walker,
pher. Psychiatry’s domain was in need of organic or neuro- came to Johns Hopkins in Baltimore in 1947, introducing
physiological substrata of disorders and dysfunctions of depth EEG, electrocorticography, epilepsy surgery, and a sci-
psychiatric-psychological nature. What could the elec- entifically oriented epileptology to his new place. Walker,
troencephalographer give in return? It was very little, but who in 1972 had moved to the University of New Mexico and
the psychiatrists did not seem to mind. On the other hand, died in 1995, will always be remembered as one of the great
there was so much to give to neurology. At that time, it had scholars of neurosurgery and epileptology.
become clear that the majority of diseases affecting the The 1950s saw a strong comeback of the Europeans.
central nervous system (CNS) had more or less impressive Henri Gastaut’s intellectual brilliancy was hard to match. In
EEG correlates, but the majority of neurologists remained Marseille, disciples of great stature flocked around him, es-
either reserved or hostile to EEG. Neurosurgeons were in- pecially Robert Naquet, Joseph Roger, and Annette Beau-
terested as long as EEG could contribute to the determina- manoir, to mention only the earliest nucleus of this group. At
tion of focal cerebral lesions (and before EEG became the great world centers of neurology, Salpêtrière Hospital in
overpowered by noninvasive neuroimaging techniques). Paris and National Hospital, Queen Square, London, An-
Some epilepsy-oriented neurosurgeons like W. Penfield or toine Remond and William Cobb, respectively, represented
A. Earl Walker remained interested in EEG and its use in the EEG, but unfortunately too much in the shadow of the
the depth of the cerebrum or on the cortex. leading neurologists. Remond later turned into a protagonist
The epileptological EEG work of Herbert Jasper in col- of computerization of EEG data.
laboration with Wilder Penfield reached new heights, and The star neurologists of both Queen Square and Sal-
Montreal reigned supreme as the place for neurosurgical pêtrière lived in the world of classical neurology, which
treatment of focal epilepsies. Penfield was far more than a gave them so much satisfaction and happiness that one could
neurosurgeon. His operations for the removal of epilepto- hardly expect their openness for the world of brain poten-
genic foci and, in a later phase, large portions of affected tials. The Queen Square guard appeared to be more detached
lobes were associated with electrical stimulation and a sys- from EEG than their Parisian confrères, perhaps due to the
tematic study of the behavioral effects. At that time, local fact that Gastaut, the man from Marseille, came from the
anesthesia was still widely used in neurosurgery. Jasper was neurological ranks to achieve instant stardom with his EEG
chiefly a neuroscientist and not merely an electroencepha- achievements. Probably no other famous neurologist has ex-
lographer. The book entitled Epilepsy and the Functional pressed his opinion about EEG more scathingly than Francis
Anatomy of the Human Brain (Penfield and Jasper, 1954) M. R. Walshe has done. He is the brilliant Queen Square star
was a result of this fruitful collaboration. who apparently knew everything about neurology except
Very controversial, however, was a concept of the pri- EEG. To Sir Francis, the electrical activity of the brain was,
mary generalized form of epilepsy characterized by gen- “a bloodless dance of action potentials ... hurrying to and
eralized synchronous paroxysmal EEG discharges and fro of its molecules” (after Critchley, 1990). Let us assume,
12 Electroencephalography: Basic Principles, Clinical Applications, and Related Fields
for everyone’s benefit, that Sir Francis had meant it to be Berger (1932); he was assisted by the physicist Dietsch
ajoke. (1932), who applied Fourier analysis to short EEG sections.
Fine schools of EEG developed in the Netherlands with Further work in this field was produced by Grass and Gibbs
O. Magnus (son of a Nobel Prize winning physiologist) in (1938) and Knott and Gibbs (1939). At the Massachusetts
Wassenaar and Storm van Leeuwen in Utrecht. In Switzer- Institute of Technology near Boston, Guillemin applied
land, Rudolf Hess (also son of a Nobelist physiologist) cre- Fourier analysis to communication theory, and one of his
ated an important school of electroencephalographers at the students was Albert Grass who “could not wait to get the
Zurich University Hospital. Giuseppe Pampiglione, from Italy, Gibbs interested” (Grass, 1984). The l950s saw the early
initiated pediatric electroencephalography at the Hospital generation of automatic frequency analyzers approaching
for Sick Children in London, concurrently with William and eventually saw the end of these magnificent but mostly
Lennox’s work at the Boston Children’s Hospital. unused machines.
These European centers of EEG activities had rather an Eventually, the EEG branched out into the world of single
international flavor with strong North American influence. neurons, and the microelectrode technique was introduced in
This cannot be said about the evolving field of clinical EEG the early 1950s. Microelectrodes can be made of metal such
in West Germany, which was dominated by its prestigious as tungsten with tips of 1 to 3 μm diameter; glass electrodes
leader Richard Jung in Freiburg. Jung’s greatness pertained filled with electrolytes such as KCI have tips of 0.5 μm or
to experimental neurophysiology; he also had great interest even smaller. Because of their characteristics, microelec-
in the clinical fields and even in philosophy. This renais- trodes reach very high impedance values (1–60 megohm),
sance man designed the outline for EEG training and the which render conventional EEG recording techniques unsuit-
routine of the EEG laboratory—unfortunately not without able. The introduction of the cathode follower by Toennies
shortcomings, which hamstrung the further development of created the technical prerequisite for single-cell recordings.
clinical EEG in West Germany. Extracellular microelectrode recording was used on a
The 1950s also saw EEG sprouting into related fields. larger scale in the early 1950s (Jung et al., 1952; Li et al.,
Depth electroencephalography with implanted intracerebral 1952; Moruzzi, 1952). About 10 years later, extracellular
electrodes was used in the human for the first time by Mey- microelectrode studies were even done intraoperatively in
ers and Hayne (1948) and Knott et al. (1950) at the Univer- humans. Far more revolutionary was the introduction of the
sity of Iowa, Iowa City, and also by Hayne et al. (1949a) in extremely laborious intracellular microelectrode technology
Chicago. These short recordings served the study of EEG (Brock et al., 1952, in the spinal cord; Phillips, 1961, in the
activity in the human basal ganglia and thalamus with regard cortex). This technique opened the gates to a new world of
to basal ganglia dyskinesias and epilepsy. In the following biochemical processes. These insights taught lessons in hu-
years, deep structures were also explored in patients with mility to the electrophysiological neurophysiologist. There
psychiatric disorders until doubt was cast upon the ethical was no doubt that the chemical changes were of primary sig-
basis of this invasive approach (see Chapter 36, “Depth nificance, while the electrical phenomena were more or less
Electroencephalography”). In the 1960s, depth EEG would by-products.
find its true field in epileptic patients considered candidates We cannot leave the 1950s without mentioning epochal
for epilepsy surgery. developments in the field of sleep research. At the Univer-
The origin of intraoperative electrocorticography dates sity of Chicago, N. Kleitman stood out as one of the world’s
back to Foerster and Altenburger (1935). How was it pos- leading investigators of the organization of sleep. This insti-
sible that Otfried Foerster, perhaps the greatest clinical tution produced the first study of rapid eye movement
neurologist ever and an amazing self-taught master of neu- (REM) sleep (Aserinsky and Kleitman, 1953), but it must be
rosurgery, failed to recognize the future potential of EEG? pointed out that Blake and Gerard (1937) described a “null
Did his mind work mainly in the world of Sherringtonian stage” in the EEG of nocturnal sleep, thus indicating the
concepts? Most of the work in electrocorticography remains desynchronization of EEG in REM sleep but without obser-
associated with the Montreal Neurological Institute and the vation of the accompanying ocular, muscular, and other au-
names of Penfield and Jasper (also see Chapter 38, “Electro- tonomic changes. William C. Dement continued the work of
corticography”). Kleitman and, following his move from Chicago to Stan-
The related fields of EEG started to bloom in the 1950s. ford, became a world leader in the study of nocturnal sleep.
In a study entitled “ASummation Technique for Detecting Sleep research gradually became based on polygraphic
Small Signals in a Large Irregular Background,” George D. recording, and its share in the overall EEG research de-
Dawson from the National Hospital, Queen Square, in Lon- clined. This development led to a constantly widening gap
don demonstrated evoked potentials to electrical stimulation between EEG and nocturnal sleep research (in the 1960s and
of the ulnar nerve (Dawson, 1951). This required advanced the following decades).
analog technology. Thus, Dawson became the father of
evoked potential studies, which developed into a major out-
TRheetosS hftte o ry
cropping of electroencephalography, eventually constituting
a field of its own. The ingenious superimposition method of The last 30 years of the history of EEG and related fields
Dawson was eventually superseded by the advent of com- can be gleaned directly from this book. The events of the
puterized averaging methods in the 1960s. 1960s, 1970s, and 1980s are just too close for us to see with
Computational techniques of wave analysis started early the eyes of the historian. Nevertheless, modern trends are
in the history of EEG. First attempts were made by Hans briefly discussed in this final section.