Clinical Neuroembryology: Development and Developmental Disorders of the Human Central Nervous System

544 Pages·2006·44.61 MB·English

by  Hans J. ten Donkelaar MD

Hans J.ten Donkelaar,Martin Lammens,Akira Hori
Clinical Neuroembryology
Development and Developmental Disorders
of the Human Central Nervous System
Hans J.ten Donkelaar
Martin Lammens
Akira Hori
Clinical
Neuroembryology
Development and Developmental Disorders
of the Human Central Nervous System
In co-operation with:
Cor W.R.J.Cremers Gerard van Noort
Johannes R.M.Cruysberg John M.G.van Vugt
Ben Hamel Berit Verbist
Reinier Mullaart Christl Vermeij-Keers
Willy O.Renier Pieter Wesseling
Kohei Shiota Michèl Willemsen
Ton van der Vliet
Illustrated by Marlu de Leeuw and Ad Gruter
With 405 Figures in 1222 parts,Mostly in Colour,
and 51 Tables
12
3
Hans J.ten Donkelaar,MD,PhD
935 Department of Neurology
Radboud University Nijmegen Medical Centre
P.O.Box 9101
6500 HB Nijmegen
The Netherlands
Martin Lammens,MD,PhD
812 Department of Pathology
Radboud University Nijmegen Medical Centre
P.O.Box 9101
6500 HB Nijmegen
The Netherlands
Akira Hori,MD,PhD
Research Institute for Longevity Medicine
Fukushimura Hospital,Noyori-Yamanaka 19–14
Toyohashi 441-8124
Japan
ISBN-10 3-540-29140-7 Springer Berlin Heidelberg New York
ISBN-13 978-3-540-29140-4 Springer Berlin Heidelberg New York
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Preface
The spectacular progress in developmental neurobi- Cor Cremers and Hans Cruysberg (Nijmegen),Mark
ology, the tremendous advances in (neuro)genetics D’hooghe (Bruges), Jennian Geddes (London), Ben
and the high resolution ofthe modern imaging tech- Hamel (Nijmegen), Frans Hoevenaars (Nijmegen),
niques applicable to developmental disorders of the Nomdo Jansonius (Groningen), Akiyoshi Kakita
human brain and spinal cord have created a growing (Niigata), Max Kros (Rotterdam), Hajime Miyata
interest in the developmental history of the central (Tottori), Masashi Mizuguchi (Tokyo), Reinier
nervous system (CNS). This new book provides a Mullaart,Willy Renier and Jan Rotteveel (Nijmegen),
comprehensive overview of the development of the Harvey B.Sarnat (Calgary),Ben Semmekrot (Nijme-
human CNS in the context of its many developmen- gen), Waney Squier (Oxford), Sachio Takashima
tal disorders due to genetic, environmental and (Fukuoka), Rudy van Coster and Caroline Van den
hypoxic/ischemic causes. The book contains three Broecke (Gent),Christl Vermeij-Keers (Rotterdam),
general,introductory chapters in which an overview Michèl Willemsen (Nijmegen),and Mieko Yoshioka
of the development of the human brain and spinal (Kobe). Imaging data were kindly provided by
cord,a summary of mechanisms of development as Drs. Harm-Gerd Blaas (Trondheim), Berit Verbist
obtained in experimental studies in various inverte- (Leiden),John van Vugt and collaborators (Amster-
brates and vertebrates,and an overview ofthe causes dam),Henk Thijssen and Ton van der Vliet (Nijme-
of congenital malformations with some notes on gen), and Guido Wilms (Leuven). Several figures
prenatal diagnosis,are presented.The developmen- were contributed by Drs. Jo Curfs (Nijmegen),
tal disorders ofthe human brain and spinal cord are Marieke de Heer and Jeannette Hoogeboom (Rotter-
presented in a regional,more or less segmental way, dam),Raoul Hennekam (Amsterdam),Jan E.Jirásek
starting with neurulation and the neural tube (Prague), Enrico Marani (Leiden), Loreta Medina
defects,and ending with developmental disorders of (Murcia),Zoltán Molnár (Oxford),Ronan O’Rahilly
the cerebral cortex. These chapters are abundantly (Villlars-sur-Glâne), Annemieke Potters (Deven-
illustrated with clinical case studies with imaging ter), Kohei Shiota (Kyoto), Henny van Straaten
data and,when available,postmortem verification of (Maastricht), Michiel Vaandrager (Rotterdam), Jan
the developmental disorders involved. The book is Voogd (Oegstgeest),and Shigehito Yamada (Kyoto).
intended for advanced medical students, and all Most of the drawings were made by Mrs.Marlu de
those clinicians working with children and adults Leeuw and Mr. Ad Gruter. Financial support was
with developmental disorders ofthe CNS. generously provided by the “Stichting Neurologie en
This book would not have been possible without Wetenschap”ofthe Department ofNeurology (Head:
the help ofmany colleagues in The Netherlands and Prof.Dr.George W.A.M.Padberg) and the Department
from abroad.Their help is gratefully acknowledged. of Pathology (Head: Prof. Dr. Han van Krieken),
Most of the neuropathological material comes from both of the Radboud University Nijmegen Medical
the extensive collections of Drs. Akira Hori and Centre, supporting the costs of the drawings. The
Martin Lammens.Many cases were kindly provided Japan Society for the Promotion of Science granted
by Drs. Pieter Wesseling (Nijmegen), Gerard van the first author a short-term fellowship in May 2004
Noort (Enschede),and Kohei Shiota (Kyoto).Photo- at the Congenital Anomaly Research Centre (Head:
graphical assistance was provided by Mrs.Roelie de Prof.Dr.Kohei Shiota) ofKyoto University.
Boer-van Huizen (Nijmegen), Mrs. Chigako Uwabe
(Kyoto) and Richard Rieksen (Enschede). Material Hans J.ten Donkelaar,Nijmegen
for the clinical case studies was provided by many
Martin Lammens,Nijmegen
clinical colleagues, including Drs. Ellsworth C.
Alvord Jr (Seattle), Harm-Gerd Blaas (Trondheim), Akira Hori,Toyohashi
Contents
Chapter 1 2.5 Neurogenesis,Gliogenesis
Overview of the Development and Migration . . . . . . . . . . . . . . . . 63
of the Human Brain and Spinal Cord 2.5.1 Neurogenesis:Primary and Secondary
Hans J.ten Donkelaar and Ton van der Vliet Proliferative Compartments . . . . . . . . 63
1.1 Introduction . . . . . . . . . . . . . . . . . 1 2.5.2 Gliogenesis. . . . . . . . . . . . . . . . . . 66
1.2 Major Stages in the Development 2.5.3 Migration. . . . . . . . . . . . . . . . . . . 68
of the Human Brain and Spinal Cord. . . . 1 2.6 Axon Outgrowth and Guidance. . . . . . 70
1.3 The First 3 Weeks of Development . . . . . 5 2.6.1 Pioneer Fibres . . . . . . . . . . . . . . . . 70
1.3.1 Implantation . . . . . . . . . . . . . . . . . 6 2.6.2 The Guidance of Axons to their Targets . . 72
1.3.2 Gastrulation . . . . . . . . . . . . . . . . . . 6 2.6.3 Axon Guidance at Choice Points . . . . . . 74
1.3.3 Folding of the Embryo . . . . . . . . . . . . 9 2.6.4 Formation of Thalamocortical
1.4 Neurulation . . . . . . . . . . . . . . . . . . 11 and Corticofugal Projections . . . . . . . . 75
1.5 Development of the Spinal Cord . . . . . . 13 2.6.5 Formation of Topographic Maps . . . . . . 77
1.6 Pattern Formation of the Brain . . . . . . . 14 2.7 Programmed Cell Death . . . . . . . . . . 80
1.7 Early Development of the Brain . . . . . . 16 References . . . . . . . . . . . . . . . . . . 82
1.7.1 Imaging of the Embryonic Brain . . . . . . . 17
1.7.2 Neuromeres . . . . . . . . . . . . . . . . . . 18 Chapter 3
1.7.3 The Ganglionic Eminences . . . . . . . . . . 20 Causes of Congenital Malformations
1.8 Fetal Development of the Brain . . . . . . 20 Martin Lammens,Hans J.ten Donkelaar,
1.8.1 The Cerebellum . . . . . . . . . . . . . . . . 20 John M.G.van Vugt,Gerard van Noort,
1.8.2 The Cerebral Cortex. . . . . . . . . . . . . . 23 Michèl Willemsen and Ben Hamel
1.8.3 Cerebral Commissures . . . . . . . . . . . . 28 3.1 Introduction . . . . . . . . . . . . . . . . . 97
1.8.4 Imaging of the Fetal Brain . . . . . . . . . . 28 3.2 Causes of Congenital Malformations. . . 97
1.9 Development of the Meninges 3.2.1 Genetic Disorders . . . . . . . . . . . . . . 97
and Choroid Plexuses . . . . . . . . . . . . 30 Clinical Case 3.1
1.10 Development of the Blood Supply Meckel–Gruber Syndrome . . . . . . . . 104
of the Brain . . . . . . . . . . . . . . . . . . 31 Akira Hori
1.11 Development of Fibre Tracts 3.2.2 Environmental Causes . . . . . . . . . . . 106
(Including Development of Myelination) 37 Clinical Case 3.2
References . . . . . . . . . . . . . . . . . . 40 Cytomegalovirus Encephalopathy . . . . 110
Gerard van Noort
Chapter 2 Clinical Case 3.3
Mechanisms of Development Amnion Rupture Sequence . . . . . . . . 112
Hans J.ten Donkelaar Martin Lammens
2.1 Introduction . . . . . . . . . . . . . . . . . 47 3.3 Prenatal Diagnosis . . . . . . . . . . . . . 109
2.2 Neural Induction . . . . . . . . . . . . . . . 47 3.3.1 Ultrasound and Magnetic Resonance
2.2.1 The Spemann–Mangold Organizer . . . . . 47 Examination . . . . . . . . . . . . . . . . . 109
2.2.2 The Molecular Basis of Neural Induction . . 49 3.3.2 Invasive Tests. . . . . . . . . . . . . . . . . 118
2.2.3 Polarity and the Establishment Clinical Case 3.4
of the Neuraxis . . . . . . . . . . . . . . . . 50 Traumatic Amniocentesis . . . . . . . . . 119
2.2.4 Neural Induction in Amniote Embryos . . . 50 Waney Squier
2.2.5 Specific Pathways for Head Induction. . . . 52 3.3.3 Genetic Diagnosis . . . . . . . . . . . . . . 120
2.3 Cell Lineage Studies and Fate Mapping . . 53 3.4 Inborn Errors of Metabolism Affecting
2.4 Pattern Formation . . . . . . . . . . . . . . 55 the CNS. . . . . . . . . . . . . . . . . . . . 121
2.4.1 Regionalization of the Forebrain . . . . . . 58 3.4.1 Inborn Errors of Metabolism
2.4.2 The Midbrain–Hindbrain Boundary that Mainly Affect the CNS . . . . . . . . . 122
Organizer . . . . . . . . . . . . . . . . . . . 59
2.4.3 Segmentation of the Hindbrain . . . . . . . 61
VIII Contents
3.4.2 Multisystem Disorders Clinical Case 4.2
with CNS Involvement . . . . . . . . . . . 122 Tectocerebellar Dysraphia . . . . . . . . . 166
Clinical Case 3.5 Akira Hori
Congenital Disorders Clinical Case 4.3
of Glycosylation . . . . . . . . . . . . . . . 124 Cranial Meningoceles . . . . . . . . . . . 167
Gerard van Noort Gerard van Noort and Akira Hori
Clinical Case 3.6 Clinical Case 4.4
Zellweger Syndrome . . . . . . . . . . . . 128 Rudimentary Occipital Meningocele . . . 169
Mark D’hooghe Pieter Wesseling
3.5 Myelination Disorders . . . . . . . . . . . 127 4.8 Spinal Neural Tube Defects . . . . . . . . 171
Clinical Case 3.7 4.8.1 Myeloceles,Myelemeningoceles
Vanishing White Matter Disease . . . . . 130 and Spinal Meningoceles . . . . . . . . . . 171
Caroline Van den Broecke Clinical Case 4.5
and Rudy Van Coster The Spectrum of Deranged Neurulation 173
3.6 Vascular Disorders . . . . . . . . . . . . . 127 Reinier Mullaart
Clinical Case 3.8 4.8.2 Spinal Lipomas. . . . . . . . . . . . . . . . 175
Porencephaly . . . . . . . . . . . . . . . . 131 Clinical Case 4.6
Pieter Wesseling Spinal Lipomas . . . . . . . . . . . . . . . 176
Clinical Case 3.9 Reinier Mullaart
Twin-to-Twin Transfusion . . . . . . . . . 133 4.8.3 Spina Bifida Occulta
Martin Lammens and Related Disorders. . . . . . . . . . . . 177
Clinical Case 3.10 4.9 The Chiari Malformations . . . . . . . . . 178
Multicystic Leukoencephalopathy . . . . 135 4.10 Caudal Dysgenesis . . . . . . . . . . . . . 180
Martin Lammens Clinical Case 4.7
Clinical Case 3.11 OEIS Complex . . . . . . . . . . . . . . . . 184
Neonatal Alloimmune Pieter Wesseling
Thrombocytopenia . . . . . . . . . . . . . 136 References . . . . . . . . . . . . . . . . . . 185
Martin Lammens
3.7 Classifications of CNS Malformations . . 136 Chapter 5
References . . . . . . . . . . . . . . . . . . 138 The Neural Crest and Craniofacial Malformations
Hans J.ten Donkelaar and Christl Vermeij-Keers
Chapter 4 5.1 Introduction . . . . . . . . . . . . . . . . . 191
Neurulation and Neural Tube Defects 5.2 Induction of the Neural Crest . . . . . . . 192
Hans J.ten Donkelaar,Reinier A.Mullaart, 5.3 Derivatives of the Neural Crest . . . . . . 193
Akira Hori and Kohei Shiota 5.3.1 The Cranial Neural Crest . . . . . . . . . . 193
4.1 Introduction . . . . . . . . . . . . . . . . . 145 5.3.2 The Trunk Neural Crest . . . . . . . . . . . 195
4.2 Primary Neurulation . . . . . . . . . . . . 145 5.4 Craniofacial Development . . . . . . . . . 196
4.2.1 Primary Neurulation in Chick 5.4.1 Early Development of the Face . . . . . . . 196
and Mammalian Embryos . . . . . . . . . . 145 5.4.2 Development of the Pharyngeal Arches . 198
4.2.2 Primary Neurulation in Human Embryos 149 5.4.3 Further Development of the Face . . . . . 199
4.3 Secondary Neurulation . . . . . . . . . . 152 5.4.4 Development of the Skull. . . . . . . . . . 202
4.4 Genetic Mouse Models 5.5 Neurocristopathies . . . . . . . . . . . . . 204
for Neural Tube Defects . . . . . . . . . . 154 5.5.1 Retinoic Acid Syndrome . . . . . . . . . . 204
4.5 Aetiology of Human Neural Tube Defects 156 5.5.2 Oculoauriculo-vertebral Spectrum. . . . . 205
4.5.1 Genetic Basis:Neural Tube Defects 5.5.3 Treacher Collins Syndrome . . . . . . . . . 206
as a Multifactorial Trait . . . . . . . . . . . 156 5.5.4 DiGeorge Sequence
4.5.2 Environmental Factors . . . . . . . . . . . 157 and Related Disorders. . . . . . . . . . . . 206
4.6 Prenatal Diagnosis . . . . . . . . . . . . . 157 5.5.5 Waardenburg Syndrome . . . . . . . . . . 209
4.7 Cranial Neural Tube Defects . . . . . . . . 158 5.6 Holoprosencephaly. . . . . . . . . . . . . 209
4.7.1 Anencephaly . . . . . . . . . . . . . . . . . 158 Clinical Case 5.1
4.7.2 Encephaloceles Alobar Holoprosencephaly . . . . . . . . 214
and Cranial Meningoceles . . . . . . . . . 161 Harm-Gerd Blaas
Clinical Case 4.1
Occipital Encephalocele . . . . . . . . . . 165
Max Kros
Contents IX
5.7 Abnormal Development of the Skull 6.8.5 Abnormal Course or Absence
with CNS Manifestations. . . . . . . . . . 213 of Fibre Tracts . . . . . . . . . . . . . . . . 256
5.7.1 The Craniosynostoses . . . . . . . . . . . . 213 Clinical Case 6.3
Clinical Case 5.2 Absence of the Pyramidal Tracts . . . . . 260
Apert Syndrome . . . . . . . . . . . . . . 218 Pieter Wesseling
Pieter Wesseling References . . . . . . . . . . . . . . . . . . 262
Clinical Case 5.3
Thanatophoric Dysplasia . . . . . . . . . 219 Chapter 7
Pieter Wesseling Development and Developmental Disorders
5.7.2 Cranial Base Abnormalities . . . . . . . . . 220 of the Brain Stem
References . . . . . . . . . . . . . . . . . . 220 Hans J.ten Donkelaar,Martin Lammens,
Johannes R.M.Cruysberg and Cor W.J.R.Cremers
Chapter 6 7.1 Introduction . . . . . . . . . . . . . . . . . 269
Development and Developmental Disorders 7.2 Pattern Formation and Segmentation
of the Spinal Cord of the Brain Stem . . . . . . . . . . . . . . 270
Hans J.ten Donkelaar and Akira Hori 7.2.1 Pattern Formation of the Brain Stem . . . . 270
6.1 Introduction . . . . . . . . . . . . . . . . . 229 Clinical Case 7.1
6.2 Gross Development of the Spinal Cord 229 Agenesis of the Mesencephalon
6.2.1 A Few Notes on the Development and Metencephalon
of the Vertebral Column . . . . . . . . . . 231 with Cerebellar Hypoplasia . . . . . . . . 272
6.2.2 Ascensus Medullae . . . . . . . . . . . . . 232 Harvey Sarnat
6.3 Developmental Events 7.2.2 Segmentation of the Brain Stem . . . . . . 271
in Spinal Neuronal Populations . . . . . . 233 7.3 Development and Developmental
6.4 The Specification of Cell Fates Disorders of the Cranial Nerves . . . . . . 274
in the Spinal Cord . . . . . . . . . . . . . . 234 7.3.1 Development of the Cranial Nerves
6.4.1 Specification of Neuronal Fates and Their Nuclei in Rodents . . . . . . . . 274
in the Ventral Spinal Cord . . . . . . . . . . 235 7.3.2 Development of Cranial Nerve Ganglia
6.4.2 Patterning Cell Types in Rodents . . . . . . . . . . . . . . . . . . 277
in the Dorsal Spinal Cord . . . . . . . . . . 237 7.3.3 Developmental and Developmental
6.5 Development of Dorsal Root Projections 237 Disorders of the Human Cranial Nerves . . 277
6.6 Development of Spinal Ascending 7.3.4 Congenital Cranial Dysinnervation
Projections. . . . . . . . . . . . . . . . . . 241 Disorders . . . . . . . . . . . . . . . . . . . 279
6.7 Development of Descending Projections Clinical Case 7.2
to the Spinal Cord. . . . . . . . . . . . . . 242 Congenital Facial Palsy . . . . . . . . . . . 283
6.7.1 Descending Projections Martin Lammens
from the Brain Stem . . . . . . . . . . . . . 243 Clinical Case 7.3
6.7.2 Development of the Pyramidal Tract Möbius Syndrome . . . . . . . . . . . . . 285
in Rodents . . . . . . . . . . . . . . . . . . 245 Pieter Wesseling and Martin Lammens
6.7.3 Development of the Pyramidal Tract 7.3.5 The Sudden Infant Death Syndrome. . . . 286
in Macaque Monkeys . . . . . . . . . . . . 248 7.4 Development of the Auditory System . . 286
6.7.4 Development of the Human 7.4.1 Development of the Ear. . . . . . . . . . . 287
Pyramidal Tract . . . . . . . . . . . . . . . 249 7.4.2 Development of the Auditory Projections 291
6.8 Developmental Anomalies 7.4.3 Developmental Disorders
of the Spinal Cord. . . . . . . . . . . . . . 250 of the Auditory System . . . . . . . . . . . 293
6.8.1 Anomalies of Histogenesis . . . . . . . . . 250 7.4.4 Genes Involved in Deafness . . . . . . . . 294
6.8.2 Duplications of the Spinal Cord . . . . . . 251 Clinical Case 7.4
Clinical Case 6.1 Branchio-oto-renal Syndrome . . . . . . . 298
Diplomyelia . . . . . . . . . . . . . . . . . 252 Cor W.J.R.Cremers
Akira Hori Clinical Case 7.5
6.8.3 Neurenteric Cysts . . . . . . . . . . . . . . 253 Usher Syndrome . . . . . . . . . . . . . . 300
Clinical Case 6.2 Cor W.J.R.Cremers
A Spinal Intradural Enterogenous Cyst . . 254 References . . . . . . . . . . . . . . . . . . 301
Pieter Wesseling
6.8.4 Syringomyelia . . . . . . . . . . . . . . . . 256
X Contents
Chapter 8 Chapter 9
Development and Developmental Disorders Development and Developmental Disorders
of the Human Cerebellum of the Forebrain
Hans J.ten Donkelaar,Martin Lammens, Hans J.ten Donkelaar,Martin Lammens,
Pieter Wesseling and Akira Hori Johannes R.M.Cruysberg,Akira Hori,Kohei Shiota
8.1 Introduction . . . . . . . . . . . . . . . . . 309 and Berit Verbist
8.2 Some Notes on the Anatomy 9.1 Introduction . . . . . . . . . . . . . . . . . 345
of the Cerebellum. . . . . . . . . . . . . . 309 9.2 Prosomeres and Pattern Formation
8.2.1 Subdivision . . . . . . . . . . . . . . . . . . 309 of the Forebrain . . . . . . . . . . . . . . . 346
8.2.2 Compartmentalization . . . . . . . . . . . 310 9.3 Development of the Diencephalon. . . . 347
8.2.3 Major Fibre Connections . . . . . . . . . . 311 9.3.1 Development of the Thalamus . . . . . . . 348
8.2.4 Precerebellar Nuclei . . . . . . . . . . . . . 312 9.3.2 Development of the Hypothalamus . . . . 354
8.3 Morphogenesis of the Cerebellum . . . . 312 9.3.3 Development of the Pituitary Gland . . . . 356
8.4 Four Basic Steps in the Histogenesis 9.3.4 Developmental Disorders
of the Cerebellum. . . . . . . . . . . . . . 314 of the Hypothalamus
8.4.1 Characterization and the Pituitary Gland . . . . . . . . . . . 358
of the Cerebellar Territory. . . . . . . . . . 314 Clinical Case 9.1
Clinical Case 8.1 Duplication of the Pituitary Gland . . . . 359
Rhombencephalosynapsis. . . . . . . . . 317 Akira Hori
Jennian Geddes Clinical Case 9.2
8.4.2 Formation of Two Proliferative Pharyngosellar Pituitary . . . . . . . . . . 360
Compartments. . . . . . . . . . . . . . . . 318 Akira Hori
8.4.3 Inward Migration of Granule cells . . . . . 319 9.4 Development of the Visual System . . . . 362
8.4.4 Differentiation of Cerebellar Neurons . . . 321 9.4.1 Development of the Eye . . . . . . . . . . 362
Clinical Case 8.2 9.4.2 Congenital Malformations of the Eye . . . 365
Cerebello-cortical Heterotopia Clinical Case 9.3
in the Dentate Nucleus . . . . . . . . . . . 324 Aniridia. . . . . . . . . . . . . . . . . . . . 365
Akira Hori Hans Cruysberg
8.5 Development of the Precerebellar Nuclei 325 Clinical Case 9.4
8.5.1 Upper Precerebellar System . . . . . . . . 326 Retinitis Pigmentosa
8.5.2 Lower Precerebellar System . . . . . . . . 326 with CNS Malformations . . . . . . . . . . 366
8.5.3 Inferior Olivary Malformations . . . . . . . 327 Hans Cruysberg
8.6 Mouse Mutants 9.4.3 Development of the Visual Projections . . 370
with Cerebellar Malformation . . . . . . . 327 Clinical Case 9.5
8.7 Developmental Disorders Isolated Absence of the Optic Chiasm . . 372
of the Cerebellum. . . . . . . . . . . . . . 329 Nomdo M.Jansonius and Ton van der Vliet
8.7.1 Midline or Vermis Malformations. . . . . . 329 9.5 Overview of the Development
Clinical Case 8.3 of the Telencephalon . . . . . . . . . . . . 371
Dandy–Walker Syndrome . . . . . . . . . 333 9.6 Development of the Rhinencephalon . . 380
Gerard van Noort 9.7 The Prosencephalies . . . . . . . . . . . . 384
Clinical Case 8.4 9.7.1 Aprosencephaly . . . . . . . . . . . . . . . 386
Joubert Syndrome . . . . . . . . . . . . . 334 Clinical Case 9.6
Pieter Wesseling Aprosencephaly . . . . . . . . . . . . . . . 385
8.7.2 Cerebellar Hypoplasia . . . . . . . . . . . . 332 Gerard van Noort
8.7.3 Pontocerebellar Hypoplasias . . . . . . . . 332 9.7.2 Holoprosencephaly . . . . . . . . . . . . . 386
Clinical Case 8.5 Clinical Case 9.7
Pontocerebellar Hypoplasia . . . . . . . . 336 Middle Interhemispheric Variant
Martin Lammens of Holoprosencephaly . . . . . . . . . . . 391
8.7.4 Cortical Dysplasias. . . . . . . . . . . . . . 337 Martin Lammens
Clinical Case 8.6 9.7.3 Septo-optic Dysplasia . . . . . . . . . . . . 394
Dysplasia of the Cerebellum Clinical Case 9.8
with Extreme Hydrocephalus . . . . . . . 338 Septo-optic Dysplasia . . . . . . . . . . . 395
Martin Lammens Akira Hori
References . . . . . . . . . . . . . . . . . . 339 9.7.4 Isolated Arhinencephaly . . . . . . . . . . 394
Contents XI
9.8 Development and Developmental Clinical Case 10.5
Disorders of the Basal Ganglia Tuberous Sclerosis Complex . . . . . . . . 470
and the Amygdala . . . . . . . . . . . . . 396 Gerard van Noort
9.8.1 Development of the Basal Ganglia . . . . . 396 Clinical Case 10.6
9.8.2 Congenital and Acquired Disorders Hemimegalencephaly . . . . . . . . . . . 472
of the Basal Ganglia . . . . . . . . . . . . . 403 Willy Renier
Clinical Case 9.9 10.7.2 Malformations due to Abnormal
Familial Striatal Degeneration Cortical Migration . . . . . . . . . . . . . . 473
(Glutaric Aciduria Type 1) . . . . . . . . . 406 Clinical Case 10.7
Martin Lammens Bilateral Periventricular
Clinical Case 9.10 Nodular Heterotopia . . . . . . . . . . . . 477
Leigh Syndrome . . . . . . . . . . . . . . . 408 Akiyoshi Kakita
Martin Lammens Clinical Case 10.8
9.8.3 Development of the Amygdala. . . . . . . 410 Miller–Dieker Syndrome . . . . . . . . . . 479
References . . . . . . . . . . . . . . . . . . 411 Martin Lammens
Clinical Case 10.9
Chapter 10 Subcortical Band Heterotopia . . . . . . . 480
Development and Developmental Disorders Masashi Mizuguchi
of the Cerebral Cortex Clinical Case 10.10
Hans J.ten Donkelaar,Martin Lammens,Willy Renier, Lissencephaly
Ben Hamel,Akira Horiand Berit Verbist with Cerebellar Hypoplasia . . . . . . . . 482
10.1 Introduction . . . . . . . . . . . . . . . . . 429 Hajime Miyata
10.2 Overview of the Cerebral Cortex . . . . . 429 Clinical Case 10.11
10.2.1 The Neocortex . . . . . . . . . . . . . . . . 429 Walker–Warburg Syndrome . . . . . . . . 484
10.2.2 The Allocortex . . . . . . . . . . . . . . . . 432 Gerard van Noort
10.3 Overview of Main Cortical Connections 435 Clinical Case 10.12
10.3.1 Thalamocortical Projections . . . . . . . . 435 Fukuyama-Type Congenital
10.3.2 The Pyramidal Tract . . . . . . . . . . . . . 436 Muscular Dystrophy . . . . . . . . . . . . 486
10.3.3 The Corpus Callosum . . . . . . . . . . . . 437 Mieko Yoshioka and Sachio Takashima
10.4 Development of the Neocortex . . . . . . 437 10.7.3 Malformations due to Abnormal
10.4.1 Development of the Neocortex in Rodents 439 Cortical Organization and Late Migration 488
10.4.2 Development of the Human Neocortex . . 446 10.7.4 Disorders of Cortical Development
Clinical Case 10.1 and Epilepsy . . . . . . . . . . . . . . . . . 489
Precocious Cerebral Development . . . . 448 Clinical Case 10.13
Akira Hori Neuronal Migration Disorders
10.5 Development of the Hippocampal and Epilepsy . . . . . . . . . . . . . . . . . 490
Formation . . . . . . . . . . . . . . . . . . 453 Willy Renier
10.6 Development of the Main Cortical Clinical Case 10.14
Connections . . . . . . . . . . . . . . . . . 457 Ammon’s Horn Sclerosis . . . . . . . . . . 493
10.6.1 Development of Thalamocortical Martin Lammens
Projections . . . . . . . . . . . . . . . . . . 457 10.7.5 Vascular Disorders . . . . . . . . . . . . . . 492
10.6.2 Development of the Pyramidal Tract. . . . 457 10.7.6 Disorders of Cortical Connectivity . . . . . 494
10.6.3 Development of the Corpus Callosum. . . 457 Clinical Case 10.15
Clinical Case 10.2 Callosal Agenesis . . . . . . . . . . . . . . 496
Temporal Lobe Dysgenesis . . . . . . . . 458 Pieter Wesseling and Gerard van Noort
Akira Hori 10.7.7 Mental Retardation . . . . . . . . . . . . . 496
10.7 Developmental Disorders Clinical Case 10.16
of the Cerebral Cortex . . . . . . . . . . . 463 Male Rett Syndrome . . . . . . . . . . . . 500
10.7.1 Malformations due to Abnormal Jan Rotteveel
Neuronal/Glial Proliferation/Apoptosis . . 464 10.7.8 Neurobehavioural Disorders . . . . . . . . 501
Clinical Case 10.3 References . . . . . . . . . . . . . . . . . . 504
Extreme Microcephaly . . . . . . . . . . . 466
Pieter Wesseling Subject Index . . . . . . . . . . . . . . . . . . . . 519
Clinical Case 10.4
Microlissencephaly . . . . . . . . . . . . . 468
Martin Lammens