1600 John F. Kennedy Blvd. Ste 1800 Philadelphia, PA 19103-2899 CLINICAL NEUROPHYSIOLOGY OF INFANCY, CHILDHOOD, AND ADOLESCENCE Copyright © 2006, Elsevier Inc. ISBN 0-7506-7251-X All rights reserved.No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Permissions may be sought directly from Elsevier’s Health Sciences Rights Department in Philadelphia, PA, USA: phone (+1) 215 239 3804, fax: (+1) 215 239 3805, e-mail: [email protected]. You may also complete your request on-line via the Elsevier homepage (http://www.elsevier.com), by selecting ‘Customer Support’ and then ‘Obtaining Permissions.’ Notice Knowledge and best practice in this field are constantly changing. 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The Publisher Library of Congress Cataloging-in-Publication Data Clinical neurophysiology of infancy, childhood, and adolescence/Gregory L. Holmes, Solomon L. Moshé, H. Royden Jones, Jr.—1st ed. p. cm. ISBN 0-7506-7251-X 1. Pediatric neurology. 2. Neurophysiology. 3. Electroencephalography. 4. Evoked potentials (Electrophysiology) I. Holmes, Gregory L. II. Moshé, Solomon L. III. Jones, Jr., H. Royden RJ488.C56 2006 618.92′8—dc22 2005042084 Acquisitions Editor:Susan Pioli Developmental Editor:Kim J. Davis Publishing Services Manager:Frank Polizzano Senior Project Manager:Peter Faber Design Direction:Steven Stave Printed in the United States of America Last digit is the print number: 9 8 7 6 5 4 3 2 1 Dedicated to the many children who have passed through our neurophysiology labs. To my wife Colleen, for her enthusiasm and perseverance. GLH To my mentor and father-in-law Dr. Marvin Cornblath (1925–2005), my wife Nancy, my son Jared, and all the children. SLM To my mom, a wonderful and vigorous, now 99-year-old, retired school teacher who loves children dearly, our own kids Roy, Kate, Fred and David, and to my wife Mary who is a terrific grandmother for Erik, Kristin, Kendall, Sam, and Natalie. HRJ Contributors P. IAN ANDREWS, MBBS, FRACP SAMUEL L. BRIDGERS, MD Senior Lecturer, School of Women’s and Children’s Assistant Clinical Professor, Department of Neurology, Health, University of New South Wales; Paediatric Yale University School of Medicine; Director, EEG Neurologist, Division of Neurology, Sydney Children’s Laboratory, Hospital of St. Raphael, New Haven, Hospital, Sydney, Australia Connecticut Neuromuscular Transmission Defects Ambulatory Electroencephalography WARREN T. BLUME, MD, FRCPC PHILIP J. BRUNQUELL, MD Professor of Neurology and Paediatrics, Department of Associate Professor of Pediatrics and Neurology, Clinical Neurosciences, University of Western Ontario; University of Connecticut School of Medicine, Neurologist, Department of Clinical Neurosciences, Farmington, Connecticut; Medical Director, Clinical University Hospital, London, Ontario, Canada Neurophysiology Laboratories, Connecticut Children’s Normal Development of the Electroencephalogram: Infancy Medical Center, Hartford, Connecticut Through Adolescence Head Trauma CHARLES F. BOLTON, MD TED M. BURNS, MD Adjunct Professor, Department of Medicine, Division of Assistant Professor, Department of Neurology, University Neurology, Queen’s University, Kingston, Ontario, of Virginia, Charlottesville, Virginia Canada Clinical Neurophysiology of Pediatric Polyneuropathies Neuromuscular Problems of the Critically Ill Neonate, Child, Autonomic Testing in Childhood and Adolescent Clinical Neurophysiology of Pediatric Polyneuropathies ALEXIS D. BORO, MD EDUARDO M. CASTILLO, PHD Assistant Professor, Department of Neurology, Albert Assistant Professor, Department of Neurosurgery, Einstein College of Medicine; Attending Physician, University of Texas at Houston Medical School; Department of Neurology, Montefiore Medical Center, Faculty, MEG Laboratory, Hermann Hospital, Bronx, New York Houston, Texas Basic Principles of Electroencephalography Magnetoencephalography The Diagnosis of Brain Death THOMAS O. CRAWFORD, MD DEBORAH Y. BRADSHAW, MD Associate Professor of Neurology and Pediatrics, Clinical Associate Professor, Department of Neurology, Departments of Neurology and Pediatrics, Johns Upstate Medical University, Syracuse, New York Hopkins University; Associate Professor of Neurology Clinical Neurophysiology of Pediatric Polyneuropathies and Pediatrics, Department of Neurology, Johns Hopkins Hospital, Baltimore, Maryland Spinal Muscular Atrophies and Other Disorders of the Anterior Horn Cell vii viii Contributors BASIL T. DARRAS, MD WILLIAM D. GOLDIE, MD Professor of Neurology, Department of Neurology, Associate Clinical Professor, Departments of Pediatrics Harvard Medical School; Director, Neuromuscular and Neurology, University of California—Los Angeles; Program, Department of Neurology, Children’s Associate Clinical Professor, Division of Child Hospital Boston, Boston, Massachusetts Neurology, Children’s Hospital—Los Angeles, Los Neuromuscular Problems of the Critically Ill Neonate, Child, Angeles, California; Director, Child Neurology, and and Adolescent Director, Clinical Neurophysiology, Ventura County The Interrelation of DNA Analysis with Clinical Medical Center, Ventura, California Neurophysiology in the Diagnosis of Chronic Neuromuscular Visual Evoked Potentials in Pediatrics—Normal Disorder of Childhood Visual Evoked Potentials in Pediatrics—Abnormal MICHAEL DUCHOWNY, MD SANDRA L. HELMERS, MD Professor of Clinical Neurology, University of Miami Associate Professor, Department of Neurology, Emory School of Medicine; Director, Comprehensive Epilepsy University School of Medicine; Associate Professor, Program, Miami Children’s Hospital, Miami, Florida Department of Neurology, Grady Health System, Long-Term Electroencephalogram and Video Monitoring Atlanta; Associate Professor, Department of Neurology, Children’s Healthcare of Atlanta, Atlanta, Georgia KARIN EDEBOL EEG-OLOFSSON, MD Brainstem Auditory Evoked Potentials in Pediatrics—Normal Associate Professor, University of Uppsala, Institute of Intraoperative Neurophysiologic Monitoring Using Evoked Neuroscience; Assistant Professor, Department of Potentials Clinical Neurophysiology, Neurocentre, University Brainstem Auditory Evoked Potentials in Pediatrics— Hospital, Uppsala, Sweden Abnormal Transcranial Magnetic Stimulation: An Overview Sphincter Dysfunction GREGORY L. HOLMES, MD Professor of Medicine (Neurology) and Pediatrics, ALAN B. ETTINGER, MD Dartmouth Medical School; Chief, Section of Director, Comprehensive Epilepsy Center and Chief of Neurology, Dartmouth-Hitchcock Medical Center, EEG, Department of Neurology, Long Island Jewish Lebanon, New Hampshire Medical Center, New Hyde Park, New York; Chief of Basic Principles of Electroencephalography EEG, Department of Neurology, North Shore Visual Analysis of the Neonatal Electroencephalogram University Hospital, Manhasset, New York; Chief of Age-Specific Seizure Disorders EEG and Epilepsy, Department of Neurology, Drug Effects on the Human Electroencephalogram Huntington Hospital, Huntington, New York Basic Principles of Electroencephalography PAUL A. L. S. HWANG, MDCM, MSC, FRCPC Associate Professor of Neurology, University of Toronto KEVIN J. FELICE, DO Epilepsy Program; Head of Paediatric Neurology, Professor of Neurology and Director, Neuromuscular North York General Hospital, Toronto, Ontario, Canada Program and EMG Laboratory, Department of Age-Specific Seizure Disorders Neurology, University of Connecticut School of Medicine, Farmington, Connecticut PRASANNA JAYAKAR, MD, PHD Focal Neuropathies in Children Director, Neuroscience Center, Children’s Brain Institute, Miami Children’s Hospital, Miami, Florida ROBIN L. GILMORE, MD Long-Term Electroencephalogram and Video Monitoring Staff Neurologist, Department of Neurology, Neurology Center of Middle Tennessee; Staff Neurologist, H. ROYDEN JONES, JR., MD Department of Medicine, Maury Regional Hospital, Jaime Ortiz-Patiño Chair in Neurology, Lahey Clinic, Columbia, Tennessee Burlington, Massachusetts; Clinical Professor of Somatosensory Evoked Potentials in Pediatrics—Normal Neurology, Harvard Medical School; Director, Somatosensory Evoked Potentials in Pediatrics—Abnormal Electromyography Laboratory, Children’s Hospital Boston, Boston, Massachusetts The Floppy Infant Plexopathies and Nerve Root Lesions Focal Neuropathies in Children Contributors ix Clinical Neurophysiology of Pediatric Polyneuropathies WILLIAM N. MAY, MD, MBA Neuromuscular Problems of the Critically Ill Neonate, Child, Associate Professor, Department of Pediatrics and and Adolescent Neurology, University of Tennessee; Chief Medical The Interrelation of DNA Analysis with Clinical Officer, Administration Department, Le Bonheur Neurophysiology in the Diagnosis of Chronic Neuromuscular Children’s Medical Center, Methodist Healthcare— Disorder of Childhood Memphis Hospitals, Memphis, Tennessee Electroencephalography and Structural Disease of the Brain SUSAN K. KLEIN, MD, PHD Assistant Professor, Department of Pediatrics, Case FAYE MCNALL, MED, REEG T Western Reserve University; Child Neurologist, Director of Education, American Society of Department of Pediatrics, University Hospitals of Electroneurodiagnostic Technologists, Kansas City, Cleveland—Rainbow Babies and Children’s Hospital, Missouri Cleveland, Ohio Drug Effects on the Human Electroencephalogram Neurophysiology of Language and Behavioral Disorders in Children THOMAS A. MILLER, MD, FRCPC Associate Professor, Department of Physical Medicine SAMUEL E. KOSZER, MD and Rehabilitation, Schulich School of Medicine; Associate Professor of Neurology, Section Head, Epilepsy Faculty of Medicine and Dentistry, University of and Neurophysiology, Department of Neurology, Western Ontario; Director, Electrodiagnostic Albany Medical College Hospital, Albany, New York Laboratory, Co-Director, Peripheral Nerve Clinic, Visual Analysis of the Neonatal Electroencephalogram Consultant Physiatrist, Hand and Upper Limb Centre, Visual Analysis of the Pediatric Electroencephalogram St. Josephs Health Care, London, Ontario, Canada Plexopathies and Nerve Root Lesions SURESH KOTAGAL, MD Professor, Departments of Neurology and Pediatrics, SOLOMON L. MOSHÉ, MD Mayo Clinic, Rochester, Minnesota Professor of Neurology, Neuroscience and Pediatrics, Childhood Sleep-Wake Disorders Vice Chair, Department of Neurology, Albert Einstein College of Medicine of Yeshiva University; Director, EDWARD H. KOVNAR, MD Child Neurology and Clinical Neurophysiology at Attending Physician, Department of Pediatric Neurology, Montefiore, The University Hospital of Albert Einstein Children’s Hospital of Wisconsin, Milwaukee, College of Medicine and Jacobi Medical Center, Wisconsin Bronx, New York Drug Effects on the Human Electroencephalogram Basic Principles of Electroencephalography Manifestations of Metabolic, Toxic, and Degenerative Visual Analysis of the Neonatal Electroencephalogram Diseases Visual Analysis of the Pediatric Electroencephalogram Infectious Diseases The Diagnosis of Brain Death NANCY L. KUNTZ, MD HIROSHI OTSUBO, MD Assistant Professor of Neurology and Pediatrics, Assistant Professor, Department of Paediatrics, University Department of Neurology, Mayo College of Medicine; of Toronto; Director of Operations, Department of Consultant in Child and Adolescent Neurology, Clinical Neurophysiology and Epilepsy Monitoring, Department of Neurology, Mayo Clinic, Rochester, Division of Neurology, Hospital for Sick Children, Minnesota Toronto, Ontario, Canada Clinical Neurophysiology of the Motor Unit in Infants and Age-Specific Seizure Disorders Children Clinical Neurophysiology of Pediatric Polyneuropathies ANDREW C. PAPANICOLAOU, PHD Autonomic Testing in Childhood Professor and Director, Division of Clinical Muscle Disorders in Children: Neurophysiologic Neurosciences, Department of Neurosurgery, Contributions to Diagnosis and Management University of Texas—Houston Medical School; Director, MEG Center, Memorial-Hermann Hospital; Director, Institute of Rehabilitation and Research; Adjunct Professor, Department of Psychology, University of Houston; Adjunct Professor, Department of Linguistics, Rice University, Houston, Texas Magnetoencephalography x Contributors MATTHEW PITT, MD, FRCP MARK S. SCHER, MD Attending Physician, Clinical Neurophysiology, Great Professor of Pediatrics and Neurology, Department of Ormond Street Hospital for Children NHS Trust, Pediatrics, Case School of Medicine; Division Chief, London, United Kingdom Pediatric Neurology, Director, Pediatric/Epilepsy and Maturational Changes vis-à-vis Neurophysiology Markers Fetal/Neonatal Neurology and Programs, Rainbow and the Development of Peripheral Nerves Babies and Children’s Hospital, University Hospitals of Cleveland, Cleveland, Ohio SUSANA QUIJANO-ROY, MD, PhD Electroencephalography of the Newborn: Normal Features Assistant, Faculty of Medicine, Université de Versailles Neonatal Electroencephalography: Abnormal Features Saint-Quentin-en-Yvelines; Pediatric Neurologist, Department of Pediatrics, Intensive Care and Neuro- KATHRYN J. SWOBODA, MD respiratory Rehabilitation Department, Hôpital Associate Professor, Department of Neurology, University Universitaire Raymond Poncaré, Garches, France; of Utah School of Medicine; Adjunct Associate Assistant, Pediatric Neurophysiology Unit, Hôpital Professor, Department of Pediatrics, Primary d’Enfants Armand-Trousseau, Paris, France Children’s Medical Center, Salt Lake City, Utah Facial and Bulbar Weakness The Floppy Infant FRANCIS RENAULT, MD ROBERTO TUCHMAN, MD Associate Professor, Université Pierre et Marie Curie; Associate Professor, Department of Neurology, University Head, Pediatric Neurophysiology Unit, Hôpital of Miami, Florida; Director, Autism Program, d’Enfants Armand-Trousseau, Paris, France Department of Neurology, Miami Children’s Hospital Facial and Bulbar Weakness Dan Marino Center, Weston, Florida Neurophysiology of Language and Behavioral Disorders in TREVOR J. RESNICK, MD Children Associate Professor and Director, Division of Pediatric Neurology, University of Miami School of Medicine; JAMES W. WHELESS, MD Chief, Department of Neurology, Miami Children’s Professor and Chief of Pediatric Neurology, Le Bonheur Hospital, Miami, Florida Chair in Pediatric Neurology, University of Tennessee Long-Term Electroencephalogram and Video Monitoring Health Science Center; Director, Pediatric Neuroscience Center; Director, Le Bonheur JAMES J. RIVIELLO, JR., MD Comprehensive Epilepsy Center, Le Bonheur Professor of Neurology, Department of Neurology, Children’s Medical Center; Clinical Director and Chief Harvard Medical School; Director, Epilepsy Program, of Pediatric Neurology, St. Jude Children’s Research Division of Epilepsy and Clinical Neurophysiology, Hospital, Memphis, Tennessee Department of Neurology, Children’s Hospital Boston, Magnetoencephalography (MEG) Boston, Massachusetts Age-Specific Seizure Disorders ELAINE WYLLIE, MD Drug Effects on the Human Electroencephalogram Head, Section of Pediatric Neurology and Pediatric Infectious Diseases Epilepsy, Department of Neurology, Cleveland Clinic Foundation, Cleveland, Ohio MONIQUE M. RYAN, MBBS, M MED, FRACP Electroencephalography in the Evaluation for Epilepsy Senior Lecturer, Discipline of Paediatrics and Child Surgery in Children Health, University of Sydney; Paediatric Neurologist, T. Y. Nelson Department of Neurology and LEON ZACHAROWICZ, MD, MA Neurosurgery, Children’s Hospital at Westmead, Neurologist, Department of Psychiatry, North Shore Sydney, Australia Child and Family Guidance Center, Roslyn Heights, Autonomic Testing in Childhood New York Visual Analysis of the Pediatric Electroencephalogram DONALD B. SANDERS, MD Professor, Division of Neurology, Duke University Medical Center, Durham, North Carolina Neuromuscular Transmission Defects Preface Neurophysiologic testing is an important component Rather one should strive to make a “clinical correlation” of the clinical assessment of children with neurologic of the neurophysiologic data vis-à-vis the history and disorders. Early in the history of clinical neurophysiology, examination findings. To this end, we have asked our testing primarily involved electroencephalography (EEG), contributors to provide succinct descriptions of clinical and later on measuring the speed of conduction along disorders where neurophysiologic testing is a valuable peripheral nerves became available. This field has adjunct. Our authors have accepted this challenge and dramatically expanded during the past decades and now have provided beautiful summaries of clinical features additionally includes evoked potentials, electromyography and neurophysiologic findings for both common and (EMG), magnetoencephalography, and magnetic stimulation. rare neurologic disorders. We made every effort to blend The physiologic parameters measured in the child’s the details important to classic electrophysiologic nervous system change rapidly from birth to the teenage techniques of EEG and EMG studies with the newest years, with age-specific patterns expressed during discrete techniques such as magnetic stimulation and developmental periods. Clinical neurophysiologists must magnetoencephalography. be aware of the challenges in testing and interpreting Since the era of Hans Berger, who made the first EEG neurophysiologic studies in a continuously evolving sys- recording at Jena, Germany, in 1924, and Edward tem. Although many of the clinical neurophysiology tech- Lambert, in Rochester, Minnesota, who brought clinical niques in adults can be extrapolated to children, there is a EMG to the fore in the early 1950s and later became the need to have a textbook dedicated solely to the perfor- teacher of more than 50% of North American electro- mance and interpretation of these various neuro- myographers, clinical neurophysiology has attracted physiologic testing modalities in infancy and childhood. talented and prolific investigators. The early contributions The wide diversity of clinical neurophysiologic studies in the field remain important and are frequently cited in has made it impossible for a single physician to review this these chapters. We asked our contributing authors to entire field in detail. We have been successful in obtaining balance the “classic, old,” but pertinent literature with contributions from a wonderful group of authors with more recent studies. Although it is not possible to cite expertise in all aspects of pediatric neurophysiology. All of every paper dealing with childhood clinical neuro- our contributors have graciously accepted the difficult task physiology, our authors have succeeded in accurately and of providing a state-of-the-art perspective of the key concisely surveying the neurophysiology literature. elements appropriate to the performance and inter- This textbook was designed to be of value to both pretation of clinical neurophysiologic studies in children of trainees and established clinicians. While we hope some all ages. readers, particularly those in fellowships, will read the Neurophysiologic studies provide an important exten- book cover to cover, it is likely that other colleagues will sion to the clinical evaluation and are predicated on a find specific chapters of primary interest. By providing a careful neurologic history and examination. These various systematic and critical approach to childhood clinical parameters should never be interpreted in isolation from neurophysiologic studies, this volume should serve as a the neurologic condition for which testing was obtained. stand-alone reference source of clinical neurophysiology xi xii Preface information for professionals working with children who We greatly appreciated the efforts of Mr. Dennis Druin have one of the many neurologic disorders that can be for his expertise in producing many of the illustrations in better defined with neurophysiologic testing. this volume and the wonderful assistance provided by our We extend our heartfelt thanks to all of the authors who support staff: Emily R. Clough at Dartmouth Medical contributed to this volume. Because of each person’s well- School; Ms. Pat Clements, the supervisor of the EEG deserved reputation in his or her respective fields of laboratory at Montefiore Medical Center; and Mrs. Mary expertise, their contributions provide a special strength to Kreconus of the Lahey Clinic. this first monograph dedicated to the principles of No project of this sort can come to fruition without the pediatric clinical neurophysiology. Each clinical neuro- dedication of a top-notch executive publisher. Each of the physiologist has provided a special dedication to this editors is particularly indebted to Susan Pioli for her faith project, and for this the editors are most grateful. We know in this project and her unceasing urging, cajoling, and good that no first effort is perfect, and we hope our readers will humor while asking us to bring this project to conclusion. feel free to advise us of any areas of confusion or mistakes We also thank her colleague at Elsevier, Kim Davis, a that we have inadvertently overlooked. We very much developmental editor who was most helpful as we entered appreciate the alacrity that our authors applied to our the gun lap for this project. ministrations as well as their good humor when we Lastly, we thank our many neurologic colleagues in our occasionally applied pressure to come to closure. At times respective institutions who have provided us support and one has to state there is enough paint on the canvas and constructive critique over the years. We are proud to have move forward in hopes the next round will provide oppor- worked with each and every one of you! tunity to enhance the color. That is often difficult to achieve with such dedicated and conscientious colleagues, Gregory L. Holmes who seek perfection in their given fields as they have with H. Royden Jones, Jr. their participation in this venture. Solomon L. Moshé 1 Basic Principles of Electroencephalography ALAN B. ETTINGER, ALEXIS D. BORO, GREGORY L. HOLMES AND SOLOMON L. MOSHÉ Successful electroencephalograph (EEG) interpretation maintain the correct metabolic milieu for neuronal and analysis are predicated on a thorough understanding signaling); (2) the oligodendrocytes (which myelinate of the basic concepts of electrical neurophysiology. This neurons); and (3) the microglia (which serve as the brain’s chapter discusses the physiologic basis of the EEG, the macrophages and assist in brain recovery from injury). fundamental principles of the electrical circuit, filters, Neurons are classified into three broad types on the the EEG apparatus, electrodes and their application to the basis of the shape of the cell body and the patterns of the scalp, special electrodes, digital technology, the EEG pen- dendrites and axons. These types are the multipolar, writing apparatus, frequency and voltage considerations, pseudounipolar, and bipolar cells. Multipolar neurons are testing the recording system, sources of the EEG, localiza- characterized by multiple dendrites that emerge from the tion of activity, artifacts, electrical safety, and special consid- cell body, resulting in a polygonal shape. The cell body of erations in performing the EEG in children. Definitions of a pseudounipolar neuron is round and gives rise to a single terms used in the chapter are presented in Appendix I. dendritic process that divides close to the cell body into a peripheral and central branch. The peripheral branch transmits incoming sensory information while the central PHYSIOLOGIC BASIS OF THE EEG branch relays information onward to its target in the central nervous system. The two processes therefore act The human brain contains more than 1012 neurons as a combined axon and dendrite. An example of a interconnected and communicating with each other via pseudounipolar neuron is the cell that relays information 1015 synaptic connections. It is through this communi- from the periphery into the central nervous system in the cation process, termed signaling, that electrical activity is dorsal root ganglion. Bipolar neurons have a round or oval- generated, resulting in the human EEG. shaped cell body with a large process emanating from The cells of the nervous system can be divided into two each end of the cell body. Bipolar cells occur in the reti- major categories: neurons and neuroglial cells. Although nal and olfactory epithelium, vestibular ganglion, and neurons come in many shapes and sizes, the major compo- auditory ganglion. nents of most neurons consist of the dendrites (which Neurons are organized into neuronal ensembles of receive information), the cell body (which processes and circuits that process specific kinds of information. Neurons integrates the information), and the axon (which conducts that carry information into the circuit are termed afferent signals to other brain regions). Neuroglial cells, often neurons, whereas neurons signaling information away referred to as glia, may also be involved. The three major from the circuit are referred to as efferent neurons. Nerve categories of glial cells are (1) the astrocytes (which cells that participate only in the local aspects of a circuit 3