Niedermeyer’s

Electroencephalography
Basic Principles, Clinical Applications, and Related Fields

SIXTH EDITION
Niedermeyer’s
Electroencephalography
Basic Principles, Clinical Applications, and Related Fields

SIXTH EDITION

Donald L. Schomer, MA, MD

Professor of Neurology
Harvard Medical School
Director, Laboratory for Clinical Neurophysiology
Chief, Comprehensive Epilepsy Program
Beth Israel Deaconess Medical Center
Boston, Massachusetts

Fernando H. Lopes da Silva, MD, PhD

Emeritus Professor
Swammerdam Institute for Life Sciences
Center of Neurosciences
Faculty of Science
University of Amsterdam
Amsterdam, The Netherlands
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Library of Congress Cataloging-in-Publication Data

Niedermeyer’s electroencephalography: basic principles, clinical applications, and related fields/

[edited by] Donald L. Schomer, Fernando H. Lopes da Silva.—6th ed.
p. ; cm.
Electroencephalography
Rev. ed. of: Electroencephalography/[edited by] Ernst Niedermeyer, Fernando H. Lopes da Silva.
5th ed. c2005.
Includes bibliographical references and index.
ISBN-13: 978-0-7817-8942-4 (hardback: alk. paper)
ISBN-10: 0-7817-8942-7 (hardback: alk. paper) 1.
Electroencephalography. I. Niedermeyer, Ernst, 1920– II. Schomer, Donald L. III. Lopes da Silva,
F. H., 1935– IV. Title: Electroencephalography.
[DNLM: 1. Electroencephalography. 2. Central Nervous System Diseases—diagnosis. WL 150]
RC386.6.E43N54 2011
616.8’047547—dc22
2010037480

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10 9 8 7 6 5 4 3 2 1
 Dedicated to Ernst Niedermeyer, M.D.
for all of the help and inspiration offered to us and
to countless clinical neurophysiologists worldwide
over his truly remarkable career.
Preface to the First Edition
The history of clinical electroencephalography (EEG) has just
passed the 50-year mark. The age of the pioneers was followed
by the stage of expansion. What began in a few prestigious cen-
ters gradually became a tool of all academic medical institu-
tions, and eventually of all major hospitals. In more recent
years, EEG even invaded the private offices of practicing neurol-
ogists and other specialists interested in central nervous system
(CNS) disease.
From this perspective, the history of clinical EEG looks like
the “via triumphalis” of a buoyantly dynamic new subspecialty.
The elucidation of the electrophysiologic process underlying
epileptic seizure disorders and a variety of other CNS dysfunc-
tions was indeed a unique achievement made possible by the
new method. The original intention of the founder of clinical
EEG, Hans Berger, had been the exploration of mental and psy-
chological processes, and even in this domain the yield has been
substantial. Moreover, electroencephalographers have not con-
fined themselves to the spontaneous wave patterns of the brain;
forms of EEG data analysis with the aid of computers were
introduced in order to demonstrate evoked and event-related
potentials and to investigate the wealth of frequencies that con-
stitute the EEG. In the search for the sources of EEG generation,
the brain tissue became the target of exploration.
Depth electrodes became one of the most important tools of
experimental neurophysiologists, who also investigated the sin-
gle neuron using microelectrodes. The implantation of depth
electrodes in the human brain has aided in the evaluation of
chronic epileptics considered candidates for seizure surgery.
This impressive progress, however, has been counterbal-
anced by signs of pessimism, fatigue, and resignation. A certain
malaise has inched its way into the hearts of thousands of elec-
troencephalographers who have started to feel the grip of stag-
nation. Generation of EEG potentials has proved to be
extremely complex and difficult to understand; the feeling of
doing pragmatically useful work with an ill-understood
method has been depressing to many workers in the field. The
pragmatists have further suffered from the limitations of EEG
as a method of localization of cerebral lesions. These feelings
have been nourished by the phenomenal achievements of non-
invasive radionuclear and radiologic scanning methods; this
progress of new methods in the field of structural diagnosis has
been a matter of concern for many electroencephalographers.
A more real danger, perhaps, is presented by the poorly trained
colleagues who are tarnishing the image of EEG.
In reality, however, these challenges present a stimulus for
the electrophysiologic field. The function-oriented aspects of
neurologic sciences will always be of paramount significance.
The loss of function-oriented neurology would foreshadow the
death of neurology. With all due respect for the structural
vi
aspects of lesions and tissue changes, neurology would be
shallow and barren without awareness of the constant fluctua-
tion of functional states in the CNS. Another important sti-
mulus has been the establishment of standards of quality for
electroencephalographers and EEG laboratories.
In these times of challenge, a review of the state of affairs in
EEG seems to be appropriate. Such thoughts have prompted the
genesis of this large one-volume textbook, which, by its mere
size, sets itself apart from the group of smaller introductory
textbooks and from the huge multivolume handbook. The one-
volume character of the book symbolizes the spirit of unity that
should reign among clinical electroencephalographers, basic
science researchers, and the workers in the field of compu -
terized data analysis.
One author can hardly undertake such a task alone. For this
reason, we have reached out across the ocean for collaboration.
It became clear, however, that a two-man effort would not
suffice to cover the entire field in the relatively short working
period of 2 years. We solicited for assistance and found a
wonderful group of contributors in various special areas. Above
all, coverage of the fields of neurophysiology and neurophar-
macology has depended most heavily on the assistance of
prestigious specialists.
Attempts at synthesis have not been the goal of this book.
Instead the reader will find a more individualistic approach
from which the personal basic philosophy of each author can be
derived. No effort has been made to achieve strict standardiza-
tion of symbols and terminology; as an example, frequencies
are described in various terms (10 cps, 10/sec, 10 Hz, etc.).
There is also some overlap between certain chapters; we feel
that the reader will benefit from the presentation of a given
topic as seen from two somewhat different viewpoints.
A piece of technical information might be worthwhile.
Unless the filter setting is specifically indicated in the illus-
trations of EEG tracings, a time constant between 0.15 and
0.5 seconds was used (above 0.4 seconds when slow frequencies
played a major role). The use of “muscle filters” was avoided.
We have tried to combine didactic and academic elements in
this book. Hence, trainees as well as seasoned professionals in
the field will, we hope, find what they are searching for. This
dual approach does mean that some parts of the book require
greater sophistication of the reader than do others.
Acknowledgments for invaluable help in this undertaking
come from the depth of our hearts. Mr. Braxton Dallam
Mitchell, President of Urban & Schwarzenberg in Baltimore,
Maryland, deserves the honor of having been the initiator of
this book. His encouragement has been very much appreciated.
Detlev Moos has coordinated the production of this book with
care and efficiency; Suzanne Lohmeyer has copyedited and

indexed it well; and Nan Tyler, Carola Sautter, and Victoria
Doherty at the publisher’s Baltimore office assisted with their
experience. In the Johns Hopkins Hospital in Baltimore,
Maryland, the technical staff of the laboratory deserves great
praise: Mrs. Judy Nastalski, R. EEG T. and chief technologist,
Mr. Eric DeShields, Mrs. Debbie Reichenbach, R. EEG T.,
Miss Sharon Vaughan, Mrs. Kathleen Daniecki, R. EEG T.,
Mrs. Cindy Haywood, and Miss Kim Rimel. How deeply the
electroencephalographer depends on the quality of the record-
ings and the dedication of the technologists! Truly invaluable
was the secretarial assistance of Mrs. Catherine Bonolis. The
operation of the laboratory was further aided by the experience
of Mrs. Marie Simpson. Important contributions came from
Mr. Joe Dieter, who is responsible for the pictorial artwork,
Mr. Ron Garret (lettering of tracings), and Mr. Zuhair Kareem
and Mrs. Lillian Reich, the staff of Medical Photography.
Assistance and advice in the clinical EEG field was given
most freely by Dr. Gisela Freund, visiting assistant professor at
the John Hopkins Hospital EEG Laboratory (1980/81), of the
Department of Clinical Neurophysiology, Free University
Berlin (Klinikum Westend). E.N.’s principal teacher in the field
of EEG, Dr. John R. Knott (presently of Boston, Massachusetts),
and the great master of neurosurgery, epileptology, and neuro-
Preface vii
physiology, Dr. A Earl Walker (presently of Albuquerque, New
Mexico), deserve special gratitude.
Gratitude is expressed (by F.L.S.) to professor Dr. W. Storm
von Leeuwen, Dr. G. Wieneke, and Dr. K. Van Hulten (Utrecht
University Hospital), Mr. N.J.I. Mars (Twente University of
Technology), and Mr. A. Van Rotterdam (Institute of Medical
Physics, Utrecht) for their advice and encouragement. The high
professional competence of Mrs. Ada Van Schaik and Mr. Nico
Haagen (Institute of Medical Physics, Utrecht) in their fields of
secretarial work and artwork was of invaluable help.
Heartfelt thanks are also expressed to the contributing authors
of the book; they have naturally become a part of this undertak-
ing. The response of these splendid coworkers was exemplary.
Joseph J. Tecce and Lynn Cattanach, the authors of the article on
contingent negative variation, substituted for a colleague who
had to step down from his obligations at the last minute. They
made possible the almost impossible when they declared their
willingness to join the team of coworkers. To them, and to all the
contributing authors of this volume, our deepest thanks.
Ernst Niedermeyer
Fernando H. Lopes da Silva
Spring 1981
Preface to the Sixth Edition
We would like to express our most sincere thanks to Dr. Ernst
Niedermeyer for his leadership and direction over the past several
years as we have moved forth to produce this sixth edition of the
textbook that he had first introduced back in 1982. Additionally,
we would like to honor him as he is so richly deserving by renam-
ing this book Niedermeyer’s Electroencephalography: Basic
Principles, Clinical Applications, and Related Fields.
Dr. Niedermeyer was born in Vienna, Austria, in 1920. He
attended medical school in Austria but, during his third year in
medical school, he was witness to the rise of Nazism in
Germany and Austria and was inducted into the German army
just prior to the onset of World War II. He was stationed in
Berlin and was then literally drafted into the medical service
even though he had not yet graduated from medical school. He
said that he was basically treating wounded soldiers coming
back from the eastern front during the first several years of the
German invasion of the Soviet Union. He remained there until
Nazi officials learned that his maternal grandmother was Jewish
which, according to German law, made him an “undesirable.”
However, because of his medical background, he was not
interned but rather was sent to Normandy. He mentioned that
he was, as were many of the soldiers in Normandy, well aware of
the coming invasion by the Allied forces and he looked upon
the day of the invasion as one of his “happiest.” He said he was
wounded during the invasion and was taken as a POW by the
American forces taking part in the invasion. He was sent back as
a POW to Kansas where he remained and served out the rest of
the war as the prison camp doctor. He returned to Austria fol-
lowing cessation of fighting and finished his medical school and
stayed on in Austria, interested in and learning neurology/psy-
chiatry. He was introduced into clinical neurophysiology
through some of the historical works in neurophysiology that
had been conducted in Europe prior to World War II, including
the work of Hans Berger. He became a clinical neurophysiology
addict and was offered a training position at the University of
Iowa with Dr. John Knott. He took that position and stayed
with Dr. Knott for a number of years but was then offered a
position to work with Dr. A. Earl Walker at the Johns Hopkins
Hospital, Baltimore. He continued to do his clinical and basic
science research at Hopkins, where his career blossomed and he
became well known in the field. He has been an inspiration to
many trainees and colleagues, both at Johns Hopkins and
worldwide. Many of our colleagues have come to know him
through his kindness and his willingness to personally take an
interest in their research and to make recommendations and
suggestions about directions for further study. His knowledge
of the field is legendary and his personality is truly “old world”
in the best sense of the term. It is our most sincere desire that
viii
this classic volume continue for the years to come and evolve
with the field as we have seen Dr. Niedermeyer do so success-
fully over the last 25 years as its senior editor.
This edition has several new features, reflective of the changes
that have occurred in our field over the past 5 years since the fifth
edition. More and more, the field of digital recording has
expanded; however, in order to understand some of the short-
comings and pitfalls of digital EEG, people need to still address
the issues of basic analog recording principles. With an increased
use of digital recording, laboratories have collected new and dif-
ferent “technical artifacts.” We present here an attempt to start a
database for such artifacts in a hope that future editions will
continue to expand upon this and offer a fairly complete library
for beginners interested in our field. As noted in the fifth edition,
epilepsy monitoring units (EMUs) have continued to mush-
room. Similar growth has occurred in the use of EEG monitor-
ing in newborn, cardiac, trauma, and postoperative intensive
care units. With the significant advances in wireless communica-
tion and easy access to the Internet, such recordings can also be
viewed and transmitted locally virtually instantaneously and can
allow well-trained clinical neurophysiologists to see and opine
about patients’ conditions on a very time-relevant basis.
Hopefully, as future generations may show, this ability will sig-
nificantly influence our patients’ outcomes. Similarly, the field of
intraoperative clinical neurophysiology for spinal cord function,
cranial nerve function, and cranial vascular therapies has con-
tinued to evolve along with the wireless and Internet communi-
cations. This has allowed for close monitoring of neurologic
function during critical periods of operations, again with a time
course that allows for corrective actions to be taken on a mean-
ingful time frame.
We have reorganized the text regarding normal EEG and
epilepsy to more closely follow the normal aging patterns. We
have continued to present some of the more classical chapters
that have evolved over years on evoked potentials and routine
electroencephalography, including EEG in common neuro-
logic, metabolic, and heredito-degenerative diseases. We have
added and updated chapters and text regarding automated and
specialized mathematics-based analysis techniques to try to
keep up with this rapidly expanding field. We will continue to
update these techniques in future editions. We have included a
chapter on linking clinical neurophysiology to other investiga-
tive techniques such as functional MRI. We have updated the
chapter on magnetoencephalography to, again, reflect the sig-
nificant changes that have taken place, both from a technical
and a clinical perspective, in this field. The last several chapters
of this textbook attempt to present an overview of clinical neu-
rophysiology research that intersects with many other aspects of

the realm of brain sciences such as consciousness and cognitive
processing.
We would like to encourage the readers of these words and
this text to please let us know if they are aware of other areas of
interest that could or should be involved in future editions of
this textbook that reflect either oversights on our part or are
harbingers of future development. Finally, we thank all of the
authors and coauthors of the chapters of this book for their
tremendous effort in keeping this textbook relevant to our field.
Special thanks go to Fran Destefano and Franny Murphy who
Preface ix
have offered tremendous help and support in the technical
aspects of getting the chapters organized and together and for
Tom Gibbons from Lippincott and all those who have helped
again in getting the textbook prepared for publication. Again, in
the words of Dr. Niedermeyer, “many, many thanks.”
Donald L. Schomer
Fernando H. Lopes da Silva
ix
Contributors

Florin Amzica, Ph.D. Sudhansu Chokroverty, M.D., F.R.C.P.

Associate Professor of Stomatology Professor of Neuroscience
Montreal University Seton Hall University
Montreal, Canada South Orange, NJ
Clinical Professor of Neurology
Mary Repole Andriola, M.D.
Robert Wood Johnson Medical School
Professor of Neurology and Pediatrics
New Brunswick, NJ
Director, Divisions of Child Neurology, Clinical Neurophysiology
Professor and Co-chair of Neurology
and Pediatric Epilepsy
Program Director, Sleep Medicine and Clinical Neurophysiology
SUNY at Stony Brook
New Jersey Neuroscience Institute at JFK Medical Center
Stony Brook, NY
Edison, NJ
Helen Barkan, M.D., Ph.D.
Nathan E. Crone, M.D.
Assistant Professor of Neurology
Associate Professor of Neurology
Upstate Medical University Hospital
Johns Hopkins University
SUNY Upstate Medical University
Attending
Syracuse, NY
Johns Hopkins Hospital
Gerhard Bauer, M.D. Baltimore, MD
Professor of Neurology
Edgar dePeralta, M.D.
Medical University Innsbruck
Fellow in Neurology and Clinical Neurophysiology
Innsbruck, Austria
State University of New York Upstate
Richard Bauer, M.D., M.Sc. Syracuse, NY
Oberarzt, Department of Neurosurgery
Frank W. Drislane, M.D.
Medical University Innsbruck
Professor of Neurology
Innsbruck, Austria
Harvard Medical School
Robert L. Beach, M.D., Ph.D. Neurologist
Professor of Neurology Comprehensive Epilepsy Center
Upstate Medical University Beth Israel Deaconess Medical Center
Director, Epilepsy Program and EEG Laboratories Boston, MA
Upstate Medical University Hospital
Barbara Ann Dworetzky, M.D.
Syracuse, NY
Assistant Professor of Neurology
Steve Bild, R. EEG/ EP T., C.N.I.M. Harvard Medical School
Manager of Clinical Services, EEG/Evoked Potentials Lab Chief, Division of Epilepsy, EEG, and Sleep Neurology
Rush University Medical Center Brigham and Women’s Hospital
Chicago, IL Boston, MA
Gastone G. Celesia, M.D. Günter Edlinger, M.Sc., Ph.D.
Professor of Neurology (Retired) CEO
Loyola University of Chicago g.tec Medical Engineering GmbH
Chicago, IL Schiedlberg, Austria
Bernard S. Chang, M.D., M.M.Sc. Jonathan Charles Edwards, M.D.
Assistant Professor of Neurology Associate Professor of Neurosciences
Harvard Medical School Director, Comprehensive Epilepsy Center and Clinical
Comprehensive Epilepsy Center Neurophysiology Laboratories
Beth Israel Deaconess Medical Center Medical University of South Carolina
Boston, MA Charleston, SC
Keith H. Chiappa, M.D. Christian E. Elger, M.D., F.R.C.P.
Associate Professor of Neurology Professor of Epileptology
Harvard Medical School University of Bonn
Director, Electroencephalography Laboratory Head, Department of Epileptology
Massachusetts General Hospital University of Bonn Medical Centre
Boston, MA Bonn, Germany

x
 Contributors xi

Ronald G. Emerson, M.D. Richard A. Hrachovy, M.D.

Professor of Clinical Neurology Professor of Neurology
Columbia University College of Physicians and Surgeons Baylor College of Medicine
Attending Neurologist Medical Director of Neurophysiology
New York Presbyterian Hospital St. Luke’s Episcopal Hospital
Columbia University Medical Center Houston, TX
New York, NY
Aatif M. Husain, M.D.
Charles M. Epstein, M.D. Department of Neurology
Professor of Neurology Duke University Medical Center and Neurodiagnostic Center
Emory University School of Medicine Veterans Affairs Medical Center
Emory Healthcare Durham, NC
Atlanta, GA
Kai Kaila, Ph.D.
Bruce J. Fisch, M.D. Professor of Biological and Environmental Sciences
Professor of Neurology Neuroscience Center
University of New Mexico University of Helsinki
Director, Neurodiagnostic Laboratories and MEG Center Helsinki, Finland
University of New Mexico Hospital
Stiliyan Kalitzin, M.D.
Albuquerque, NM
Image Sciences Institute
John N. Gaitanis, M.D. University Medical Center Utrecht
Assistant Professor of Neurology and Pediatrics, Clinical Utrecht, The Netherlands
Warren Alpert School of Medicine at Brown University
Anton Kamp
Director of Pediatric Epilepsy
Biological Centre
Rhode Island Hospital/Hasbro Children’s Hospital
University of Amsterdam
Providence, RI
Amsterdam, The Netherlands
Ali Gorji, M.D.
Andres M. Kanner, M.D.
Institute for Physiology
Professor of Neurological Sciences and Psychiatry
Münster University
Rush Medical College at Rush University
Münster, Germany
Director, Laboratories of EEG and Video-EEG-Telemetry
Jean Gotman, Ph.D. Associate Director, Epilepsy Section
Professor Rush University Medical Center
Montreal Neurological Institute Chicago, IL
McGill University
Peter W. Kaplan, M.B., F.R.C.P.
Montreal, Québec, Canada
Department of Neurology
Riitta Hari, M.D., Ph.D. Johns Hopkins Bayview Medical Center
Academy Professor Baltimore, MD
Brain Research Unit, Low Temperature Laboratory
Andrew D. Krystal, M.D., M.S.
Aalto School of Science and Technology
Professor of Psychiatry and Behavioral Sciences
Espoo, Finland
Director, Quantitative EEG Laboratory
Consultant
Director, Insomnia and Sleep Research Laboratory
Department of Clinical Neurophysiology
Duke University School of Medicine
HUSLAB, Helsinki University Central Hospital
Durham, NC
Helsinki, Finland
Ekrem Kutluay, M.D.
Adam L. Hartman, M.D.
Associate Professor of Neurology
Assistant Professor of Neurology and Pediatrics
Medical College of Wisconsin
Johns Hopkins University School of Medicine
Milwaukee, WI
Attending Physician
Johns Hopkins Hospital Emma Laureta, M.D.
Baltimore, MD Assistant Professor of Neurology
Albert Einstein College of Medicine
Bin He
Attending
Department of Biomedical Engineering and Center for
Montefiore Medical Center
Neuroengineering
New York, NY
University of Minnesota
Minneapolis, MN Alan D. Legatt, M.D., Ph.D.
Professor of Neurology
Susan T. Herman, M.D.
Albert Einstein College of Medicine
Assistant Professor of Neurology
Director of Intraoperative Neurophysiology
Harvard Medical School
Montefiore Medical Center
Beth Israel Deaconess Medical Center
New York, NY
Boston, MA
xii Contributors

Ronald P. Lesser, M.D. Ernst Niedermeyer, M.D.

Professor of Neurology and Neurosurgery Professor Emeritus of Neurology and Neurological Surgery
Johns Hopkins University Johns Hopkins University School of Medicine
Johns Hopkins Medical Institutions Baltimore, MD
Baltimore, MD
Douglas R. Nordli, Jr., M.D.
Fernando H. Lopes da Silva, M.D., Ph.D. Professor of Pediatrics
Emeritus Professor Northwestern University Feinberg School of Medicine
Swammerdam Institute for Life Sciences, Center of Neurosciences Lorna S. and James P. Langdon Chair of Pediatric Epilepsy
Faculty of Science Children’s Memorial Hospital
University of Amsterdam Chicago, IL
Amsterdam, The Netherlands
Marc R. Nuwer, M.D., Ph.D.
François Mauguière, M.D. Professor of Neurology
Head, Department of Functional Neurology and Epileptology UCLA School of Medicine
Lyon University and Lyon Federative Institute of Neuroscience Department Head
Neurological Hospital Clinical Neurophysiology
Lyon, France Ronald Reagan UCLA Medical Center
Los Angeles, CA
Douglas Maus, M.D., Ph.D.
Assistant Professor of Neurology Trudy D. Pang, M.D., M.M.Sc.
SUNY Downstate Medical Center Instructor in Neurology
State University of New York at Brooklyn Harvard University
New York, NY Staff Neurologist
Beth Israel Deaconess Medical Center
Christoph M. Michel, M.D.
Boston, MA
Functional Brain Mapping Laboratory
Neurology Clinic and Department of Basic Neuroscience Alvaro Pascual-Leone, M.D., Ph.D.
University Hospital Professor of Neurology
University of Geneva Harvard Medical School
Geneva, Switzerland Director, Department of Neurology
Berenson-Allen Center for Noninvasive Brain Stimulation
Eli M. Mizrahi, M.D.
Beth Israel Deaconess Medical Center
Chair, Department of Neurology
Boston, MA
Professor of Neurology and Pediatrics
Peter Kellaway Section of Neurophysiology, Department of Neal S. Peachey, M.D., Ph.D.
Neurology Professor of Ophthalmology
Section of Pediatric Neurology, Department of Pediatrics Cleveland Clinic Lerner College of Medicine
Baylor College of Medicine Associate Chief of Staff for Research
Houston, TX Cleveland VA Medical Center
Cleveland, OH
Solomon L. Moshé, M.D.
Professor of Neurology Pediatrics, and Neuroscience Gert Pfurtscheller, Ph.D.
Albert Einstein College of Medicine Emeritus Professor
Director, Pediatric Neurology and Clinical Neurophysiology Laboratory of Brain–Computer Interfaces (BCI-Lab)
Montefiore Medical Center Institute for Knowledge Discovery
New York, NY Graz University of Technology
Graz, Austria
Janet M. Mullington, Ph.D.
Associate Professor of Neurology Rodney A. Radtke, M.D.
Harvard University Professor of Neurology
Beth Israel Deaconess Medical Center Duke University
Boston, MA Medical Director
Duke Hospital Sleep Disorder Center
Christa Neuper, Ph.D.
Duke University Hospital
Professor
Durham, NC
Institute of Psychology
University of Graz James J. Riviello, Jr., M.D.
Head of Institute George Peterkin Endowed Chair in Pediatrics
Laboratory of Brain–Computer Interfaces (BCI-Lab) Professor of Pediatrics and Neurology
Institute for Knowledge Discovery Baylor College of Medicine
Graz University of Technology Director, Epilepsy and Neurophysiology Program
Graz, Austria Director, Neurocritical Service, Section of Neurology
Chief of Neurophysiology
Texas Children’s Hospital
Houston, TX
 Contributors xiii

Alexander Rotenberg, M.D., Ph.D. William O. Tatum IV, D.O.

Assistant Professor of Neurology Professor of Neurology
Harvard Medical School Mayo School of Medicine
Attending Staff Physician, Neurology Director, Epilepsy Monitoring Unit
Children’s Hospital Mayo Clinic and Hospital
Boston, MA Jacksonville, FL
Erik Rumpl, M.D. Barbara Tettenborn, M.D., Ph.D.
Professor of Neurology Chair, Department of Neurology
Landeskrankenhaus Kantonsspital St. Gallen
Klagenfurt, Austria St. Gallen, Switzerland
Johannes Gutenberg University
Donald L. Schomer, M.A., M.D.
Mainz, Germany
Professor of Neurology
Harvard Medical School Ab van Rotterdam, Ph.D.
Director, Laboratory for Clinical Neurophysiology Senior Researcher (Retired)
Chief, Comprehensive Epilepsy Program Radiobiological Laboratory
Beth Israel Deaconess Medical Center Radiobiological Institute TNO
Boston, MA Rijswijk, The Netherlands
Margitta Seeck, M.D. Sampsa Vanhatalo, M.D., Ph.D.
Professor Department of Clinical Neurophysiology
Director of the EEG and Epilepsy Unit Children’s Castle
University Hospital of Geneva Helsinki University Central Hospital
Geneva, Switzerland Helsinki, Finland
Megan Selvitelli, M.D. Juha Voipio, Ph.D.
Maine Medical Partners Neurology Professor of Biological and Environmental Sciences
Scarborough, Maine University of Helsinki
Helsinki, Finland
Erw in-Josef Speckmann, M.D.
Professor Emeritus Thoru Yamada, M.D.
Institute of Physiology (Neurophysiology) Professor of Neurology
University of Münster Roy J. and Lucille A. Carver College of Medicine
Münster, Germany University of Iowa
Director, Division of Clinical Electrophysiology
Cornelis Jan Stam, M.D.
University of Iowa Hospitals and Clinics
Department of Clinical Neurophysiology
Iowa City, IA
VU University Medical Center
Amsterdam, The Netherlands Malcolm Yeh, M.D.
Associate Clinical Professor of Neurology
Travis R. Stoub, Ph.D.
Division of Clinical Electrophysiology
Assistant Professor of Neurological Sciences
Roy J. and Lucille A. Carver College of Medicine
Affiliated Scientist
University of Iowa
Rush University Medical Center
Staff Neurologist
Chicago, IL
University of Iowa Hospitals and Clinics
Takeo Takahashi, M.D. Iowa City, IA
Yaotome Clinic
Sendai, Japan
Contents
Preface to the First Edition vi
Preface to the Sixth Edition viii
Contributors x
Part I Basic Principles
1 Historical Aspects of EEG . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
Ernst Niedermeyer and Donald L. Schomer
2 Neurophysiologic Basis of EEG and DC Potentials . . . . . . . . . . 17
Erwin-Josef Speckmann, Christian E. Elger, and Ali Gorji
3 Cellular Substrates of Brain Rhythms . . . . . . . . . . . . . . . . . . . . . 33
Florin Amzica and Fernando H. Lopes da Silva
4 Dynamics of EEGs as Signals of Neuronal Populations:
Models and Theoretical Considerations . . . . . . . . . . . . . . . . . . . 65
Fernando H. Lopes da Silva
5 Biophysical Aspects of EEG and Magnetoencephalogram
Generation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 91
Fernando H. Lopes da Silva With an Appendix by Ab Van Rotterdam
6 Analog Signal Recording Principles . . . . . . . . . . . . . . . . . . . . . . 111
Charles M. Epstein
7 Digital EEG . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 119
Douglas Maus, Charles M. Epstein, and Susan T. Herman
8 Polarity and Field Determinations . . . . . . . . . . . . . . . . . . . . . . . 143
Bruce J. Fisch
Part II Normal EEG
9 Normal EEG and Sleep: Preterm and Term Neonates . . . . . . . 153
Eli M. Mizrahi, Solomon L. Moshé, and Richard A. Hrachovy
10 Normal EEG and Sleep: Infants to Adolescents . . . . . . . . . . . . 163
James J. Riviello, Jr., Douglas R. Nordli, Jr., and Ernst Niedermeyer
11 Normal EEG and Sleep: Adults and Elderly . . . . . . . . . . . . . . . 183
Bernard S. Chang, Donald L. Schomer, and Ernst Niedermeyer
12 Activation Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 215
Takeo Takahashi and Keith H. Chiappa
13 Artifacts of Recording . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 239
Barbara Dworetzky, Susan Herman, and William O. Tatum IV
Part III Clinical EEG: General
14 Patterns of Unclear Significance . . . . . . . . . . . . . . . . . . . . . . . . . 267
Jonathan Charles Edwards and Ekrem Kutluay
15 EEG of Degenerative Disorders of the Central
Nervous System . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 281
John Gaitanis
16 The EEG in Congenital Malformations of Cortical
Development, Neurocutaneous Disorders, Cerebral Palsy,
Autism/Mental Retardation, and ADHD/Learning
Disabilities of Childhood . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 299
Mary Repole Andriola
17 Brain Tumors and Other Space-Occupying Lesions . . . . . . . . 321
Adam L. Hartman and Ronald P. Lesser
18 The EEG in Inflammatory CNS Conditions . . . . . . . . . . . . . . . 331
Robert L. Beach, Helen Barkan, and Edgar DePeralta
xiv
19 Cerebrovascular Diseases and EEG . . . . . . . . . . . . . . . . . . . . . . 351
Barbara Tettenborn, Ernst Niedermeyer, and Donald L. Schomer
20 Dementia and EEG . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 375
Cornelis Jan Stam
21 Metabolic Disorders and EEG . . . . . . . . . . . . . . . . . . . . . . . . . . 395
Trudy Pang, Megan Selvitelli, Donald L. Schomer, and Ernst Niedermeyer
22 EEG and Craniocerebral Trauma . . . . . . . . . . . . . . . . . . . . . . . . 411
Erik Rumpl
23 Anoxia, Coma, and Brain Death . . . . . . . . . . . . . . . . . . . . . . . . 435
Peter W. Kaplan and Gerhard Bauer
24 The EEG in Patients with Migraine and Other
Forms of Headache . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 457
Ernst Niedermeyer and Donald L. Schomer
Part IV Clinical EEG in Epilepsy
and Related Disorders
25 Seizures and Epilepsies in the Preterm and Term Neonate ... 465
Emma Laureta, Eli M. Mizrahi, and Solomon L. Moshé
26 Seizures and Epilepsy in Infants to Adolescents . . . . . . . . . . . . 479
Douglas R. Nordli, Jr., James J. Riviello, Jr., and Ernst Niedermeyer
27 Epilepsy in Adults and the Elderly . . . . . . . . . . . . . . . . . . . . . . . 541
Bernard S. Chang, Donald L. Schomer, and Ernst Niedermeyer
28 Convulsive Status Epilepticus . . . . . . . . . . . . . . . . . . . . . . . . . . . 563
Frank W. Drislane, Susan T. Herman, and Peter W. Kaplan
29 Nonconvulsive Status Epilepticus . . . . . . . . . . . . . . . . . . . . . . . 595
Frank W. Drislane, Peter W. Kaplan, and Susan T. Herman
30 Anticipating Seizures Based on EEG . . . . . . . . . . . . . . . . . . . . . 645
Fernando H. Lopes da Silva and Stiliyan Kalitzin
31 Nonepileptic Attacks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 659
Megan Selvitelli, Trudy Pang, Donald L. Schomer, and Ernst Niedermeyer
Part V Complementary and Special Techniques
32 Nasopharyngeal, Anterotemporal,
and Sphenoidal Electrodes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 669
Andres M. Kanner, Travis Stoub, and Steve Bild
33 Intracranial Monitoring: Depth, Subdural,
and Foramen Ovale Electrodes . . . . . . . . . . . . . . . . . . . . . . . . . . 677
Margitta Seeck, Donald L. Schomer, and Ernst Niedermeyer
34 Electrocorticography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 715
Marc R. Nuwer
35 Principles and Techniques for Long-Term EEG Recording
(EMU, ICU, Ambulatory) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 725
Jean Gotman, Marc Nuwer, and Ronald G. Emerson
36 Infraslow EEG Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 741
Sampsa Vanhatalo, Juha Voipio, and Kai Kaila
37 High-Frequency EEG Activity . . . . . . . . . . . . . . . . . . . . . . . . . . 749
Jean Gotman and Nathan E. Crone
38 Intraoperative Evoked Potential Monitoring . . . . . . . . . . . . . . 767
Alan D. Legatt
39 Monitoring EEG during Carotid Surgery . . . . . . . . . . . . . . . . . 787
Thoru Yamada and Malcolm Yeh
 Contents xv

40 Polygraphy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 809 50 Neurocognitive Processes and the EEG/MEG . . . . . . . . . . . . . 1083

Anton Kamp, Gert Pfurtscheller, Günter Edlinger, Fernando H. Lopes da Silva
and Fernando H. Lopes da Silva

41 Polysomnography: Technical and Clinical Aspects . . . . . . . . . 817 Part VIII EEG and Neurocognitive Functions
Sudhansu Chokroverty, Rodney Radtke, and Janet Mullington
51 Psychiatric Disorders and EEG . . . . . . . . . . . . . . . . . . . . . . . . . 1113
42 Magnetoencephalography: Methods and Applications . . . . . . 865 Andrew D. Krystal
Riitta Hari
52 Technical Aspects of Transcranial Magnetic
Part VI EEG: Neuropharmacology and Anesthesia and Electrical Stimulation of the Brain . . . . . . . . . . . . . . . . . . 1129
Alan D. Legatt, Alvaro Pascual-Leone, and Alexander Rotenberg
43 EEG, Drug Effects, and Central Nervous System Poisoning . . 901 53 Transcranial Magnetic Stimulation (TMS):
Gerhard Bauer and Richard Bauer
Clinical Applications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1139
Alexander Rotenberg and Alvaro Pascual-Leone
Part VII Evoked Potentials and Event-Related EEG
Phenomena Part IX Computer-Assisted EEG Analysis
44 Event-Related Potentials: General Aspects of 54 EEG Analysis: Theory and Practice . . . . . . . . . . . . . . . . . . . . . 1147
Methodology and Quantification . . . . . . . . . . . . . . . . . . . . . . . 923 Fernando H. Lopes da Silva
Fernando H. Lopes da Silva
55 EEG Mapping and Source Imaging . . . . . . . . . . . . . . . . . . . . . 1179
45 EEG Event-Related Desynchronization (ERD) Christoph M. Michel and Bin He
and Event-Related Synchronization (ERS) . . . . . . . . . . . . . . . . 935 56 Computer-Assisted EEG Pattern Recognition
Gert Pfurtscheller and Fernando H. Lopes da Silva
and Diagnostic Systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1203
46 Visual Evoked Potentials and Electroretinograms . . . . . . . . . . 949 Fernando H. Lopes da Silva
Gastone G. Celesia and Neal S. Peachey
57 EEG-Based Brain–Computer Interfaces . . . . . . . . . . . . . . . . . 1227
47 Brainstem Auditory Evoked Potentials (BAEPs) Gert Pfurtscheller and Christa Neuper
and Other Auditory Evoked Potentials . . . . . . . . . . . . . . . . . . . 975 58 Multimodal Monitoring of EEG and Evoked Potentials . . . . 1237
Gastone G. Celesia Gert Pfurtscheller
48 Somatosensory-Evoked Potentials: Normal Responses,
Abnormal Waveforms, and Clinical Applications
in Neurologic Diseases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1003 Index 1243
François Mauguière

49 Evoked Potentials in Children and Infants . . . . . . . . . . . . . . . 1057

Aatif M. Husain

Historical Aspects of EEG
ERNST NIEDERMEYER AND DONALD L. SCHOMER
DISCOVERY OF ELECTRICAL PHENOMENA
Thales from Miletos has been credited with the discovery of
static electricity produced by friction (rubbing fur or glass with
silk). He was one of the pre-Socratic “natural philosophers” of
Greece (around 620–550 BC) and considered water the origin
of all things. Thus, friction was recognized as the generator of a
phenomenon that derived its name from the Greek work “elec-
tron,” which stands for amber. This discovery fell into a dor-
mant stage for more than two millennia.
Around 1600, William Gilbert began to study the electrical
properties of various substances, and Otto von Guericke
(1602–1686) invented the friction machine to create electrical
fields. This machine eventually found its way into doctors’
offices and even university hospitals. Its electrical field would
make a patient’s hair stand up, creating a strong impression on
a psychologically gullible patient. These friction machines now
ornament high school laboratories and technical museums. In
the 17th and 18th centuries, the friction machine taught invalu-
able lessons on attraction and repulsion of charged bodies, on
conductors and nonconductors, and on the rather questionable
dualism of positive and negative electricity.
A new and very important piece of electrical equipment
entered the scene in 1746 when the Leyden jar was introduced
by Pieter van Musschenbroek (following the earlier work of
Ewald von Kleist). This invention resulted in the storage of elec-
tricity, and its upshot, the condenser or capacitor, turned into
an indispensable part of modern electronics. Benjamin
Franklin’s bold experiment caught electrical discharges of a
thunderstorm in a Leyden jar.
What the friction machine could generate, the Leyden jar
could store. Its sudden discharge was used in many experiments
(O’Leary and Goldring, 1976).
The role of static electricity in medicine appeared to be for-
gotten for about 150 years and became resurrected with the
introduction of the defibrillating cardioversion by William B.
Kouwenhoven and his coworkers in the 1950s and 1960s; this
approach may hold promises for cerebral applications
(Niedermeyer, 2003a).
A serious scientific controversy developed in Italy between
Luigi Galvani (1737–1798), a professor at the University of
Bologna, and Alessandro Volta (1745–1832) in the wake of
Galvani’s discovery of frog leg contractions within an electrical
circuit and especially in the presence of a thunderstorm (1780).
Volta doubted the biologic nature of the contraction (animal
Part I Basic Principles
CHAPTER
1
electricity) and placed the emphasis on physics—on his “pile,”
the first battery (around 1800). This bimetallic pile was a gen-
erator capable of producing a steady flow of electricity. Volta’s
view more or less prevailed in this hotly debated argument. The
laws governing flowing electricity were soon discovered by
Georg Ohm in 1827.
Nevertheless, Galvani’s belief in “animal electricity” was not
lost with other discarded false ideas. There still remained the
nagging question of an active electrical contribution of animal
muscle tissue.
BEGINNINGS OF ELECTROPHYSIOLOGY
The introduction of the galvanometer has been associated
chiefly with the name of Nobili in Florence; this instrument was
refined in 1858 by William Thompson (Lord Kelvin) in
England (O’Leary and Goldring, 1976). These galvanometers
would faithfully demonstrate continuous electrical currents
and their variations in intensity but failed in the detection of
instantaneous electrical phenomena.
Carlo Matteucci (1811–1868) in Bologna and Emil Du Bois-
Reymond (1818–1896) in Berlin became the major proponents of
an electrophysiologically based physiology of the nervous system.
(The French name of Du Bois-Reymond indicates the Huguenot
origin of this Prussian investigator.) Du Bois-Reymond coined the
term negative variation for a phenomenon occurring during mus-
cle contraction when the galvanometer indicated an unexpected
decrease in current intensity (O’Leary and Goldring, 1976). This
term was later resurrected in earliest electroencephalogram (EEG)
research (Caton, 1875) and with the discovery of the “contingent
negative variation” (Walter, 1964).
Hermann von Helmholtz (1821–1894) accurately measured
the velocity of nerve conduction, which had been vastly overes-
timated up to that time. The electrodes used in physiologic
research were improved and made nonpolarizable (Du Bois-
Reymond). The concept of “action current” was introduced by
L. Hermann (1834–1919) and thus clarified Du Bois-Reymond’s
negative variations found during muscle contraction. Julius
Bernstein (1839–1917) proposed a membrane theory of nerve
tissue, which ultimately was elucidated as late as 1939 and the
following years by A. L. Hodgkin and A. F. Huxley in England.
Against this background of strongly evolving electrophysiology
of the nervous system, the first observation of EEG-like electri-
cal brain activity took place.
1
2 Part I ■ Basic Principles
CATON: THE FIRST ATTEMPT AT THE
ELECTRICAL ACTIVITY OF THE BRAIN
Richard Caton (1842–1926) (Fig. 1.1) was a physician practic-
ing in Liverpool who became deeply interested in electrophysi-
ologic phenomena and eventually received a grant from the
British Medical Association to explore electrical phenomena of
the exposed cerebral hemispheres of rabbits and monkeys.
According to Brazier (1961), Caton presented his findings to the
association on August 24, 1875, and a very short report of 20
lines subsequently appeared in the British Medical Journal. A
more detailed report was presented in the same journal in 1877
on experiments of more than 40 rabbits, cats, and monkeys, the
rabbit having been principally employed.
Caton used a galvanometer. A beam of light was thrown on
the mirror of the galvanometer and reflected on a large scale
placed on the wall. With this type of visualization, Caton found
that “feeble currents of varying direction pass through the mul-
tiplier when the electrodes are placed on two points of the
external surface, or one electrode on the grey matter, and one
on the surface of the skull.” This sentence is regarded as indicat-
ing the birth of the electrophysiologram because one can
assume that EEG phenomena made the needle move from one
direction to the other. (The suffix “gram” naturally is out of
place since “graphein” means “to write” and there was no writ-
ten recording.) Even though artifacts could have played a major
role, Caton deserves credit for the discovery of the fluctuating
potentials that constitute the EEG.
Figure 1.1 Richard Caton at the time of his work on the electrical
activity of the brain. (From Brazier MAB. A History of the Electrical
Activity of the Brain. The First Half-Century. London: Pitman; 1961, with
permission from Macmillan.)
Caton also described a few more interesting observations.
He noted that the external surface of the gray matter was posi-
tive in relation to deep structures of the cerebrum. He also
noted that the electric currents of the cerebrum appeared to
have a relation to underlying function: “When any part of the
grey matter is in a state of functional activity, its electric current
usually exhibits negative variation.” Thus, Caton has also been
credited with pioneer work on evoked potential. Furthermore,
the difference in polarity found between cortical surface and
deeper areas could be interpreted as the discovery of the “steady
potential” (“DC potential”), but it might be wise to refrain from
such statements that cannot be fully supported by the evidence.
With regard to the fluctuations, Geddes (1987) pointed out that
Caton’s galvanometer had a very limited frequency response
range from 0 to 6 Hz.
Caton found some measure of success and recognition with
this work and held the chair of physiology at the University
College of Liverpool from 1884 to 1891, when he resigned from
this post. Later he became dean of the medical faculty and, in
1907, mayor (Lord Mayor) of Liverpool. The electrical activity of
the brain did not occupy a predominant position in his further
endeavors. Even though Caton became an EEG research dropout,
his bold work will always remain a milestone in the history of the
electrical activity of the brain. (More information on Caton’s life
and work is found in Mary Brazier’s (1961) fine account.)
EASTERN EUROPEAN STUDIES OF
ELECTRICAL BRAIN ACTIVITY
The time was ripe for further studies of electrical phenomena of
the cerebrum. Concurrent with Caton’s epochal work of 1875,
physiologists of Eastern Europe began to demonstrate their
independent observations and discoveries concerning the brain
and its electrical activity. Another discovery of the 1870s had
an incomparably greater impact on the neuroscientific world
than Caton’s demonstration of electrical activity of the brain.
The capability of the human cerebral cortex to be electrically
stimulated was discovered by G. Fritsch (1838–1927) and Julius
Eduard Hitzig (1838–1907) in a joint study in 1870. According
to O’Leary and Goldring (1976), an unusual observation had
prompted Fritsch in his work: he had observed contralateral
muscle contractions during dressing of an open brain wound in
the Prussian–Danish War of 1864. The work of Fritsch and
Hitzig was furthered by D. Ferrier and G. F. Yeo in 1880, who
performed electrical stimulations of the cerebrum in apes and
also in a patient who was operated on for a brain tumor. The
repercussions of the stimulation studies were considerable since
many investigators of that time held the view that the entire
cerebrum is a homogeneous organ that harbors mental functions.
The response of the cortex to electrical stimulation probably
was a special incentive for the study of its spontaneous electri-
cal phenomena. This incentive was particularly strong in
Eastern Europe, that is, in laboratories of Russian and Polish
universities. (In spite of the important historical ethnic and
national differences, the fact cannot be ignored that most of
Poland was part of the Czarist Russian Empire throughout the
19th century.)