THE EMBRYONIC HUMAN BRAIN An Atlas of Developmental Stages SECOND EDITION RONAN O'RAHILLY, M.D., D.Sc., Dr.h.c. FABIOLA MULLER, Dr.habil.rer.nat. School of Medicine University of California at Davis Davis, California and Institut d'Embryologie Speciale Universite de Fribourg, Fribourg, Switzerland WILEY-LISS A JOHN WILEY & SONS, INC., PUBLICATION 1999 CONTENTS Preface 1 Historical Aspects 1 2 Techniques 5 3 Prenatal Measurements 7 4 Embryonic Staging 9 5 Prenatal Age 13 6 Terminology and Definitions 15 7 Early Stages 35 8 Stage 8: The First Appearance of the Nervous System 39 9 Stage 9: The Major Divisions of the Brain 47 10 Stage 10: The Neural Tube and the Optic Primordium 59 11 Stage 11: Closure of the Rostral Neuropore 73 12 Stage 12: Closure of the Caudal Neuropore and the Beginning of Secondary Neurulation 87 13 Stage 13: The Closed Neural Tube and the First Appearance of the Cerebellum 105 14 Stage 14: The Future Cerebral Hemispheres 115 15 Stage 15: Longitudinal Zoning in the Diencephalon 129 16 Stage 16: Evagination of the Neurohypophysis 139 17 Stage 17: The Future Olfactory Bulb and the First Amygdaloid Nuclei 155 18 Stage 18: The Future Corpus Striatum, the Inferior Cerebellar Peduncle, and the Dentate Nucleus 173 19 Stage 19: The Choroid Plexus of the Fourth Ventricle and the Medial Accessory Olivary Nucleus 195 20 Stage 20: The Choroid Plexus of the Lateral Ventricles, the Optic and Habenular Commissures, and the Interpeduncular and Septal Nuclei 217 21 Stage 21: The First Appearance of the Cortical Plate in the Cerebral Hemispheres 239 22 Stage 22: The Internal Capsule and the Olfactory Tract 265 23 Stage 23: The Brain at the End of the Embryonic Period 287 24 Trimester 1, Postembryonic Phase 339 25 Trimester 2 387 26 Trimester 3 and the Newborn 405 27 Early Postnatal Life 421 Bibliography427 Appendix 1. Computer Ranking of the Sequence of Appearance of Features of the Brain 441 Appendix 2. Sequence and Stage of Appearance of Median Features of the Brain 447 Appendix 3. Sequence and Stage of Appearance of Tracts of the Brain 448 Appendix 4. Sequence and Stage of Appearance of Features Associated with the Rhombencephalon 449 Index 451 FROM THE BACK COVER: As a wholly unique atlas and the only book specializing on the prenatal human brain during both the embryonic and fetal periods, this updated version of The Embryonic Human Brain: An Atlas of Developmental Stages provides the latest information on human development with more than one hundred new pages and sixty additional illustrations. Written by one of the world's foremost authorities in the field of human embryology, this monograph gives professionals up-to-date, detailed drawings and texts based on three-dimensional reconstructions of varied morphological processes of the brain. Clearly written and detailed, this Second Edition presents the most accurate photographs, drawings, and photomicrographs of the human brain, including lateral views and median reconstructions of the brain at each stage, with revised tables and ages conforming with the most current ultrasonic findings in the field. The Embryonic Human Brain: An Atlas of Developmental Stages, Second Edition contains essential information on the embryonic period proper (the first eight postovulatory weeks) by providing: -New figures on arteries, based on the well-known studies of Padget -Over 300 figures of the embryonic and fetal human brain -The latest information concerning the cerebellum in both the embryonic and fetal periods, with special attention paid to hippocampal formation -An expanded account of the fetal period, emphasizing continuity of development, with supplemental postnatal images -A timely, expanded bibliography, and new appendices relating to median features, tracts, and the rhombencephalon The Embryonic Human Brain: An Atlas of Developmental Stages, Second Edition is an authoritative and indispensable resource for neuroscientists, developmental biologists, neurologists, and neurosurgeons, and is an essential handbook on current knowledge of human development for psychiatric and psychological professionals worldwide. PREFACE The main objective of this monograph is to provide drawings, photographs, and photomicrographs of the human embryonic brain, and to include summarizing statements of the morphological status of the brain at each stage. The staging used is the internationally accepted Carnegie system. The drawings include at least a lateral view and a median reconstruction of the brain at each stage, as well as a clear indication of the plane of section of further illustrations, either drawings or photomicrographs. The vast majority of the drawings are based on extremely precise graphic reconstructions. At the end of the description of the normal at most stages, a brief statement concerning relevant anomalous conditions is added. The reasons for concentrating on the embryonic period proper (the first eight postfertilizational weeks) are: 1. The embryonic brain is extremely difficult to comprehendand to visualize; 2. Serial sections of first-class quality that show the human embryonic brain are rarely accessible; 3. The correct interpretation of the appropriate serial sections requires years of specialized work; 4. The time-consuming preparation of accurate three-dimensional reconstructions is essential for correct interpretation; 5. The embryonic period is of particular importance because most major congenital anomalies appear during that time; 6. Until the publication of the first edition of this book, in 1994, no accurate, detailed, well-illustrated account of the human embryonic brain was available in book form, or even in a chapter of a book. A set of standardized abbreviations, mostly self-evident, is used throughout for the illustrations, and a list of them is placed immediately inside the front cover. A selection of references to the chief studies of the prenatal human brain is included, but is not intended to be complete. In the interest of brevity, as well as of immediate relevance, items from the profuse literature relating to other species have not been included. This edition has been enlarged by the addition of 100 pages and the inclusion of more than 60 new illustrations, as well as a number of new tables. The ages assigned to the stages have been revised to conform to the latest ultrasonic findings. The definitions given in Chapter 6 have been expanded considerably and are an important prelude to the later chapters. Further details of neurulation and the neuropores are given. Neuromeres, which currently are of particular interest in relation to gene expression, are clarified for the first time in the human embryo, in line with recent investigations by the present authors. Several new figures showing the arteries, based on the well-known studies of Padget, are presented. More information concerning the cerebellum in both the embryonic and the fetal period is supplied, and the hippocampal formation is given special attention. The account of the fetal period has been expanded, thereby emphasizing the continuity of development, and a few postnatal images have been included. The Bibliography has been enlarged and brought up to date. A computer ranking of the sequence of appearance of features of the brain is provided in Appendix 1, and newly added appendices are concerned with median features, tracts, and the rhombencephalon. Morphology has acquired ever increasing importance since the advent of imaging in vivo, and the emphasis in this book remains primarily morphological. By the same token, an atlas of the embryonic human heart along lines similar to those of the present work would be a very valuable contribution. As stated in the first edition, the authors wish to acknowledge the great help given by the U.S. National Institutes of Health, which have supported their research; (chiefly through Grant HD16702, Institute of Child Health and Human Development). Except where otherwise indicated, the photomicrographs and photographs are reproduced by courtesy of the Carnegie Institution of Washington. It is a pleasure to thank all at Wiley-Liss for their cheerful assistance. RONAN O'RAHILLY FABIOLA MULLER Rue du Coteau 57 CH-1752 Villars-sur-Glane Switzerland WHERE TO ORDER: John Wiley & Sons, Inc. 1 Wiley Dr. Somerset, NJ, 08875-1272 U.S.A. Phone: 800-225-5945 Fax: 732-302-2300 Price: Cloth $199.95 (ISBN: 0-471-25450-9)
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