The Anatomy of the Human Embryo A Scanning Electron-Microscopic Atlas Dedicated to the memory of the great anatomists and embryologists Wilhelm His (1831–1904) and Erich Blechschmidt (1904–1992) Gerd Steding The Anatomy of the Human Embryo A Scanning Electron-Microscopic Atlas 818 fi gures, 2008 Basel • Freiburg • Paris • London • New York • Bangalore • Bangkok • Shanghai • Singapore• Tokyo • Sydney Dr. med. Gerd Steding Former Professor of Anatomy and Head of the Department of Embryology Centre of Anatomy University of Göttingen Germany Library of Congress Cataloging-in-Publication Data Steding, Gerd. The anatomy of the human embryo : a scanning electron-microscopic atlas / Gerd Steding. p. ; cm. Includes bibliographical references. ISBN 978-3-8055-8361-9 (hard cover : alk. paper) 1. Embryology, Human--Atlases. 2. Scanning electron microscopy--Atlases. I. Title. [DNLM: 1. Embryo, Mammalian--anatomy & histology--Atlases. 2. Microscopy, Electron, Scanning--Atlases. QS 617 S812t 2008] QM602.S738 2008 612.6‘40222--dc22 2008026596 All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means electronic or mechanical, including photocopying, recording, microcopying, or by any infor- mation storage and retrieval system, without permission in writing from the publisher. © Copyright 2008 by S. Karger AG, P.O. Box, CH–4009 Basel (Switzerland) www.karger.com Printed in Switzerland on acid-free and non-aging paper (ISO 9706) by Reinhardt Druck, Basel ISBN 978–3–8055–8361–9 Contents Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . VII Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . XIII 1. External Aspects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 1.1 The External Form of the Embryo . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 1.2 The Development of the Face . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14 1.3 The Development of the Pharyngeal Arches . . . . . . . . . . . . . . . . . . . 38 1.4 The Development of the Upper Limb . . . . . . . . . . . . . . . . . . . . . . . . . 66 1.5 The Development of the Lower Limb . . . . . . . . . . . . . . . . . . . . . . . . . 88 1.6 The Development of the External Genitalia . . . . . . . . . . . . . . . . . . . . 108 2. Endodermal Organs in the Head and Neck . . . . . . . . . . . . . . . . . 123 2.1 The Development of the Walls of the Oral Cavity . . . . . . . . . . . . . . 124 2.2 The Development of the Nose . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 146 2.3 The Development of the Palate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 166 2.4 The Development of the Pharynx . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 178 2.5 The Development of the Larynx . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 188 2.6 The Position of the Thymus and the Parathyroid Gland . . . . . . . . 196 3. Organs in the Thorax . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 203 3.1 The Development of the Heart . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 204 3.2 The Development of the Lungs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 254 4. Organs in the Abdomen . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 285 4.1 The Development of the Small Intestine . . . . . . . . . . . . . . . . . . . . . . . 286 4.2 The Development of the Liver . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 298 4.3 The Great Vessels of the Trunk . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 318 4.4 The Development of the Stomach . . . . . . . . . . . . . . . . . . . . . . . . . . . . 332 4.5 The Origin of the Spleen . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 348 4.6 The Development of the Pancreas . . . . . . . . . . . . . . . . . . . . . . . . . . . . 356 5. Urogenital Organs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 369 5.1–5.4 The Development of the Urinary Organs . . . . . . . . . . . . . . . . . . . . . . 370 5.5 The Development of the Gonads . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 406 5.6 The Reproductive Pathways . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 412 6. Brain and Sensory Organs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 421 6.1 The Development of the Brain . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 422 6.2 The Development of the Eye . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 468 6.3 The Middle and the Internal Ear . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 486 6.4 The Spinal Cord . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 500 VI Introduction In this atlas, the forms of the major human organs during the early weeks of prenatal development are depicted. Illustrations of the external form of human embryos have been published in great numbers and are to be found in numerous textbooks deal- ing with human embryology. However, we predominantly fi nd a description of organ development with pictures of two-dimen- sional histological sections or with more or less schematic draw- ings often made according to historical originals. It is not rare to fi nd in textbooks, even today, pictures of animal embryos as material for human development. Since it has been shown that results for animal embryos cannot always be simply and uncriti- cally applied to human development, in this atlas of human embryology, only original images of the major organs of human embryos during the fi rst few weeks of prenatal development are shown. For technical reasons, modern developmental biology is al- most exclusively concerned with animal embryos. However, it would be somewhat irresponsible to expect that the use of these new procedures could replace the investigation of human embry- os with the traditional tools for the description of form. Sometimes, however, it seems that nowadays only molecular biological tech- niques and methods of developmental biology are considered to be a suitable approach to understanding developmental process- es, whereas the classical morphological methods and procedures are increasingly seen as historical and, thereby, as hardly capable of producing good results. Regrettably, with this approach, it is often ignored that reports on the biochemical processes taking place during development can hardly provide a hint as to the ways and means in which they infl uence form. The fact that the steps taking place at the molecular level during the development of a leg of a mouse or chicken are to a large extent similar, however, off ers no explanation as to how the fi nal results of these processes are so diff erent in form. To establish under what circumstances and con- ditions the arm, for example, of a human being is given its charac- teristic form, fi rst precise knowledge of the course of development VII is necessary. We need to know which steps are involved, from the development of the anlage to the formation of the ‘fi nished’ hu- man form. Only when the course of each individual step in these external changes in form has been understood, can there be a chance of also estimating the molecular incidents in the stages of the devel- opment of form. Therefore, even nowadays, the classical observation, descrip- tion and analysis of form, its development and change cannot be ignored altogether, neither within the framework of developmen- tal biological nor embryological medical investigations. In this at- las, all that is depicted are those changes in position and form of the organs, which are visible during embryonic development. It is obvious that, together with these visible changes, a succession of processes in submicroscopic molecular dimensions, which are not directly visible, take place. There has been much conjecture as to the relationship, so to speak, between macroscopic and submicroscopic processes and much has been alleged or even postulated without there having been any success in disproving any one of the hypotheses. There- fore, I restrict myself solely to illustrating phenomena of human organ development which are directly visible and I will keep my views on theories and hypotheses to myself. The reader’s concept of human organ development will, on the basis of our specimens, hopefully become more vivid and plastic. Just as in the anatomical dissection course the organs con- cealed under the skin are exposed and become visible by dissec- tion, layer for layer, the organs of an embryo can also be exposed and, thereby, made visible in their position and spatial form. As in an anatomical atlas the position and form of human organs are shown, in this atlas the changes in position and form of some of the human organs during prenatal development are seen in pho- tographs of the specimens. For the selection of the photographs, I made sure that the developmental stages were as close together as possible to make the changes in shapes of the organs clear and comprehensible. To demonstrate the relationships in form and position more reli- ably than the standard aspects are able to do, images of the same organs photographed from diff erent directions are shown. This cannot, of course, be equally successful for every organ, sim- VIII ply because the small size of some objects sometimes makes un- expectedly high demands on the patience and dexterity of the author. It would hardly be surprising if some of the photographs shown here might appear peculiar and strange to the experienced ob- server of histological and schematic illustrations in textbooks. This could be due to the fact that these specimens also do not appear to be as simple and familiar as the two-dimensional sections and repeatedly drawn schemata so often seen. As in everyday life, also in prenatal development, it is often the inconspicuous events which are most important. Temporally close stages may some- times appear hardly distinguishable from each other and only upon more exact inspection can a characteristic developmental step be recognized. Even if it is customary to speak of ‘the’ human embryo, it must be remembered that, already in his prenatal life, the human being is a unique and unmistakable individual. As far as possible, I have also tried to keep this aspect of the individual development of form in mind. Since the growth of the embryo is precisely in the early weeks a fundamental factor in the development of form, the pictures of all stages of an organ are, in general, shown at the same magnifi cation. The introductory text to each chapter hardly off ers experts anything new. It cannot and should not replace a textbook, but rather explains, only briefl y, some of the most signifi cant develop- mental steps documented in the illustrations. To instruct or teach the readers is not the aim of this atlas, rather it simply off ers them an opportunity to develop a more precise conception of the anat- omy of the human embryo through the power of their own obser- vations. In this context, I must accept the fact that the choice of photo- graphs and their number cannot satisfy every reader in equal mea- sure and that unnecessary or even absent aspects may be criti- cized. However, I have endeavoured to give not only human embryologists but also readers on the periphery of human embry- ology and interested physicians and also laymen an opportunity to make their own observations. As expected from an atlas, the pictures of the specimens are what is most important. Some of these pictures off er an unusual aspect and often also only one small detail from a region. In order IX