The Embryonic Human Brain: An Atlas of Developmental Stages, Third Edition

361 Pages·2006·16.286 MB·English

by  Dr.h.c. Ronan O'Rahilly, Dr.habil.rer.nat. Fabiola Muller(auth.)

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THE
EMBRYONIC
HUMAN BRAIN
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The brain at the end of the embryonic period (stage 23, 8
postfertilizational weeks). The color scheme used here
(telencephalon in yellow, diencephalon in blue,
mesencephalon in brown) will be repeated in a number of
illustrations throughout the book.
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THE
EMBRYONIC
HUMAN BRAIN
AN ATLAS OF
DEVELOPMENTAL STAGES
THIRD 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 Spe´ciale
Universite´ de Fribourg, Fribourg, Switzerland
A JOHN WILEY & SONS, INC., PUBLICATION
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Illustrationsonthecover:
Ultrasonicinvivoimageat6weeksshowingthefourthventricle.
cf.Fig.23-35.CourtesyofDr.Harm-GerdBlaas.
Perspektomatreconstructionat8weeks,stage23.
SeeFig.2-1.
Obliquesectionat7weeks,stage20.
SeeFig.20-4.
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LibraryofCongressCataloging-in-PublicationData:
ISBN-13:978-0-471-69462-5
ISBN-10:0-471-69462-2
PrintedintheUnitedStatesofAmerica
10 9 8 7 6 5 4 3 2 1
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In memory of
Ernest Gardner, M.D.,
neuroscientist, colleague, and friend
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...ce feroit vn grand bon-heur pour le genre humain, fi cette
partie, qui eft la plus delicate de toutes, & qui eft fujette ´a
des maladies tres-frequentes, & tres-dangereufes, eftoit auffi
bien connue¨, que beaucoup de Philofophes & d’Anatomiftes
fe l’imaginent.
Niels Stensen, Discovrs svr 1’Anatomie du cerveau, 1669.
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CONTENTS
Preface to the Third Edition ix
1. Historical Aspects 1
2. Techniques 5
3. Prenatal Measurements 9
4. Embryonic Staging 11
5. Prenatal Age 15
6. Terminology 17
7. Early Stages 21
8. Stage 8: The First Appearance of the Nervous System 25
9. Stage 9: The Major Divisions of the Brain 31
10. Stage 10: The Neural Tube and the Optic Primordium 39
11. Stage 11: Closure of the Rostral Neuropore 51
12. Stage 12: Closure of the Caudal Neuropore and the Beginning of
Secondary Neurulation 61
13. Stage 13: The Closed Neural Tube and the First Appearance of
the Cerebellum 75
14. Stage 14: The Future Cerebral Hemispheres 84
15. Stage 15: Longitudinal Zoning in the Diencephalon 93
16. Stage 16: Evagination of the Neurohypophysis 103
17. Stage 17: The Future Olfactory Bulbs and the First Amygdaloid Nuclei 115
18. Stage 18: The Future Corpus Striatum, the Inferior Cerebellar Peduncles,
and the Dentate Nucleus 133
19. Stage 19: The Choroid Plexus of the Fourth Ventricle and the Medial
Accessory Olivary Nucleus 149
20. Stage 20: The Choroid Plexus of the Lateral Ventricles, the Optic and
Habenular Commissures, and the Interpeduncular and Septal Nuclei 169
21. Stage 21: The First Appearance of the Cortical Plate in the Cerebral
Hemispheres 187
22. Stage 22: The Internal Capsule and the Olfactory Bulbs 205
23. Stage 23: The Brain at the End of the Embryonic Period 219
24. Trimester 1, Postembryonic Phase 263
Early Postembryonic Phase 265
Later Postembryonic Phase 285
25. Trimester 2 297
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viii
CONTENTS
26. Trimester 3 and the Newborn 305
Supplement: Early Postnatal Life 319
Bibliography 323
Glossary 331
Appendix 1: Changing Lengths of the Brain and its Subdivisions from 31/ to 51/
2 2
Weeks (Stages 9–16) 341
Appendix 2: Computer Ranking of the Sequence of Appearance of Features
of the Brain 343
Appendix 3: Sequence and Stage of Appearance of Median Features of the Brain 349
Appendix 4: Sequence and Stage of Appearance of Tracts of the Brain 351
Appendix 5: Sequence and Stage of Appearance of Features Associated
with the Rhombencephalon 353
Index 354
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PREFACE TO THE
THIRD EDITION
T hemainobjectivesofthismonographaretoprovide Theauthors’schemeoftheneuromeres,whichdiffers
andtointerpretdrawings,photographs,andphotomi- fromothersinbeingbasedonthehuman,isdetailedhere.
crographs of the human embryonic brain. The drawings Other topics emphasized include segmentation, not only
includeatleastalateralviewandamedianreconstruction oftheneuralaxisbothrostrallyandcaudally,butalsothat
ofthebrainateachstage,aswellasaclearindicationofthe ofoccipitocervicaldifferentiation.Stemandcrestcellsin
planeofsectionoffurtherillustrations,eitherdrawingsor the olfactory region are elaborated, and the cerebellum,
photomicrographs. Summarizing statements of the mor- theamygdaloidcomplex,thehippocampalregion,andthe
phological status of the brain at each stage are supplied, corpusstriatumaregivenspecialattention.
andbriefstatementsconcerningrelevantanomalouscon- This edition has been enhanced by the use of color,
ditionsareincluded. as well as by the inclusion of more that 100 new illus-
Theembryonicperiodproper(thefirsteightpostfer- trationsand26newtables.Moreover,somerepresentative
tilizationalweeks)isparticularlyimportantbecause(1)the examplesofultrasonicimageshavebeeninterspersed.The
embryonicbrainisextremelydifficulttocomprehendand definitionsformerlygiveninChapter6havebeenexpanded
to visualize, (2) serial sections of first-class quality that considerablyandcollectedasanimportantGlossarynear
show the human embryonic brain are rarely accessible, theendofthebook.
and (3) most major congenital anomalies appear during The Bibliography has been enlarged and brought up
that time. A briefer account of the fetal period has been todate.Itcomprisesmorethan350referencestothechief
includedandemphasizesthecontinuityofdevelopment. studiesoftheprenatalhumanbrain.Theprofuseliterature
Despite a general, superficial similarity in the devel- relatingtootherspecies,however,isbeyondthescopeof
opment of the brains of various vertebrates, significant, thisbook.
subtledifferencesexistsothat,undoubtedlyimportantas A set of standardized abbreviations, mostly self-
arethefindingsinotherspecies,contributionsspecifically evident,isusedthroughoutfortheillustrations,andalist
to the prenatal human brain are as essential as they are ofthemisplacedimmediatelyinsidethefrontcover.
fascinating. The number assigned to chapters 8–23 and the first
The external and internal structure of the develop- number given to each illustration indicate the develop-
ingbrain,theprimaryconcernofthisbook,isanessential mentalstage.
prolegomenonforsubsequentinvestigationsrangingfrom The authors wish to acknowledge the valuable sup-
immunocytochemistrytoimaginginvivo.Structuralrep- portfortheirresearchprovidedbytheU.S. NationalInsti-
resentation, however, needs to be completed by interpre- tutesofHealthovermanyyears.Exceptwhereotherwise
tation. In the present context two necessary components indicated, the photomicrographs as well as many of the
ofpreciseinterpretationare(1)morphologicalstaging(as photographsarefromtheCarnegieCollection.Thescan-
distinct from mere seriation, such as length or supposed ningimagesareincludedthroughthekindnessofDr.med.
age),withoutwhichindividualeventscannotbearranged Harm-GerdBlaasandothercolleagueswhoarecreditedin
in correct sequence, and (2) accurate three-dimensional theappropriateplaces.ItisapleasuretothankallatWiley-
reconstructions,withoutwhicherroneousassumptionsof Lissfortheirencouragementandassistance.
interpretation can be (and frequently are) made. These
desiderata, which have been used by the authors in their RONANO’RAHILLY
research over many years, are a unifying feature of this FABIOLAMU¨LLER
treatise: (1) the Carnegie system of staging originated by Villars-surGlaˆne,Switzerland
Streeterandnamedanddevelopedbytheauthorsisfunda- July2006
mentaltothepresentation,and(2)mostofthedrawings
here are based on extremely precise graphic reconstruc-
tionspreparedbytheauthors.Nosimilarworkisavailable.
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ABBREVIATIONS
a. Artery I.-v.f. Interventricularforamen
Aff. Afferent Lat.f. Laterallongitudinalfasciculus
A.-H. Adenohypophysis Lat.em. Lateralventriculareminence
Amyg. Amygdaloidregion,nuclei,complex L.l.f. Laterallongitudinalfasciculus
Bas.a. Basilarartery LMP Lastmenstrualperiod
BM Basementmembrane Long.fiss. Longitudinalfissure
BV Bloodvessel L.t. Laminaterminalis
C Cervical MorMes. Mesencephalon
Cbl Cerebellarplate,cerebellum M1,M2 Mesencephalicneuromeres
Ch. Chiasmaticplate M.l.f. Mediallongitudinalfasciculus
Ch.tymp. Chordatympani Mam. Mamillaryregion,nuclei,body
CN Cranialnerve Mam.teg.tr. Mamillotegmentaltract
CNS Centralnervoussystem Med.fore.b Medialforebrain(orprosencephalic)
Comm. Commissuralplate bundle
C-R Crown-rumplength Med.tectobulb.tr. Medialtectobulbartract
D1,D2 Diencephalicneuromeres Med.em. Medialventriculareminence
Di Diencephalon Mes.tr.5 Mesencephalictractoftrigeminal
nerve
Dors.f. Dorsallongitudinalfasciculus
n. Nerve
Eff. Efferent
Nas. Nasalplate,pit,sac,septum
End.div. Endolymphaticdiverticulum
N.-H. Neurohypophysis
Ep. Epiphysis
Not. Notochord
Ext.cbl Externalcerebellarswelling
NTD Neuraltubedefect
Ggl Ganglion
Nu.mes.5 Mesencephalictrigeminalnucleus
GL Greatestlength
Nu.post.X Nucleusofposteriorcommissure
Hab.-interp.tr. Habenulo-interpedunculartract
Olf.bulb Olfactorybulb
Hem. Cerebralhemisphere
Olf.n. Olfactorynerve
Hipp. Hippocampus
Olf.tub. Olfactorytubercle
Hyp.-th.sulc. Hypothalamicsulcus
Opt. Opticsulcus,vesicle,cup
Hyp.-th.-teg.-tr. Hypothalamotegmentaltract
Opt.stalk Opticstalk
Infund. Infundibulum
Ot. Oticplate,pit,vesicle
Int.cbl Internalcerebellarswelling
Par. Parencephalon
Interest.nu. Interstitialnucleus
Post.-lat.fiss. Posterolateralfissure
Isth. Isthmusrhombencephali
Post.X Posteriorcommissure
Isth.rec. Isthmicrecess
1