Table Of ContentRudolf Nieuwenhuys · Luis Puelles
Towards a New
Neuromorphology
Towards a New Neuromorphology
Rudolf Nieuwenhuys Luis Puelles
(cid:129)
Towards a New
Neuromorphology
123
RudolfNieuwenhuys LuisPuelles
Netherlands Institute for Neuroscience Department ofHuman Anatomy
RoyalNL Academy of Arts andSciences andPsychobiology
Amsterdam University of Murcia
TheNetherlands Murcia
[email protected] Spain
[email protected]
ISBN978-3-319-25692-4 ISBN978-3-319-25693-1 (eBook)
DOI 10.1007/978-3-319-25693-1
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Preface
Thisbookowesitsorigintoaremarkablecoincidence.InOctober2012LuisPuelles(LP)and
I(RN)decidedtoorganizeandrealizeahighlyselectivetwo-personconference.Itsaimswere
twofold: (1) to discuss the ‘state of the art’ in developmental and comparative neuromor-
phology, our fields of interest, and (2) to look into the possibility of preparing an elementary
overviewofrecentdevelopmentsinthesefields.Atthesametime,oneofus(RN)wasinvited
to participate in a neuroscience course for a group of talented students in the Max Planck
Institute for Human Cognitive and Brain Sciences in Leipzig, involving a series of intro-
ductory lectures as well as dissections of human brains. We (LP and RN) immediately
interpretedthisinvitationasauniqueopportunitytorealizeouraims.Anoutlineofthelectures
tobedelivered wasforwarded toLeipzigandfound approvalbyProf. Dr.RobertTurner and
Dr. Stephan Geyer, the organizers of the course.
The lectures, illustrated with Powerpoint slides and delivered during March 19–21, 2013,
werewellreceived,andProf.TurnerspontaneouslyproposedthathisInstitutewouldtakethe
initiative to publish them in their entirety. This offer, which perfectly matched our original
intentions(seeabove),wasgratefullyaccepted,butthetransformationofthelecturenotesand
transcripts (see below) into the final text (the present course) turned out to be much more
complex and laborious than anticipated, hence the relatively long time interval between the
presentation of these lectures and their appearance in print. Afterwards, the mediation of
Professor Turner and his Institute in the publication of the book appeared to be unnecessary,
because Springer-Verlag was found willing to publish the work.
The authors wish to thank Professor Turner and Dr. Geyer for their generous support,
Professor L. H. Bannister for critically reading the entire text, and for making many sug-
gestions for improvements with respect to content as well as language, Professors L. Medina
andJ.L.Ferranforreadingandofferingvaluableadviceforchangesinthepartsofsection10
dealing with the concept of homology, Mrs. Sonja Schall, Juliane Dinse, Nancy Muschall,
Aline Peter and Christina Schröder for preparing a complete transcript of the videorecorded
lectures,Dr.JennekeKruisbrinkforhelpwiththecollectionofliteratureandMr.TonPutfor
help with the illustrations.
In concluding this preamble, the invaluable moral and practical support of Mrs. Suzanne
Bakker M Sc. in all phases of this project is gratefully acknowledged and finally, we extend
our most sincere thanks to our publisher, Springer-Verlag, and their staff—especially
Dr. Andrea Pillmann, Dr. Jutta Lindenborn and Mr. Alexander Subbareddy—for their kind
help during the production of this book.
Rudolf Nieuwenhuys
Luis Puelles
v
Contents
Prologue. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . x
Plan of the Course. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . xiv
1 From the Classic to Modern Neuromorphology,
an Introductory Overview. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
1.1 Neural Plate—Neural Groove—Neural Tube . . . . . . . . . . . . . . . . . . . . 1
1.2 Neural Segments or Neuromeres. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
1.3 The So-Called Brain Vesicles. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
Excursion 1: Homage to Karl Ernst von Baer (1792–1876) . . . . . . . . . . . . . . . 11
1.4 The Fundamental Morphological Units of the CNS. . . . . . . . . . . . . . . . 13
1.5 Topology Versus Topography in (Neuro) Morphology. . . . . . . . . . . . . . 15
1.6 Summary of the Introductory Overview. . . . . . . . . . . . . . . . . . . . . . . . 26
2 The Neural Plate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29
2.1 Structure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29
Insertion: Principles of molecular developmental (neuro)biology) . . . . . . . . . . . 31
2.2 From Ectoderm to Neurectoderm . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37
2.3 Regionalization and Fate Mapping . . . . . . . . . . . . . . . . . . . . . . . . . . . 39
3 From Neural Plate to Neural Tube . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 45
3.1 Neurulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 45
3.2 Differentiation and Gene Expressions . . . . . . . . . . . . . . . . . . . . . . . . . 47
3.3 Summary of Neural Plate and Neurulation. . . . . . . . . . . . . . . . . . . . . . 48
4 The Neural Tube . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 51
4.1 Historical Introduction-1 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 51
Excursion 2: The CNS of amphioxus (Branchiostoma lanceolatum. . . . . . . . . . 53
Excursion 3: Neurons as modified gland cells . . . . . . . . . . . . . . . . . . . . . . . . 59
4.2 Structure of the Neural Tube . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61
4.3 Ventrodorsal Regionalization: Longitudinal Zones. . . . . . . . . . . . . . . . . 63
4.4 Anteroposterior Regionalization: Neuromeres. . . . . . . . . . . . . . . . . . . . 67
4.5 Summary of the Neural Tube. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75
Excursion 4: Biodiversity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 77
Excursion 5: Helgoland: Evertebrates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83
5 The Axis of the Brain, Its Flexures and Correlates. . . . . . . . . . . . . . . . . . . 95
5.1 Flexures of the Axis: Changes During Development . . . . . . . . . . . . . . . 95
5.2 Flexures of the Axis: Differences Among Species. . . . . . . . . . . . . . . . . 99
5.3 Flexures of the Axis: A Historical Error and Its Correction . . . . . . . . . . 101
5.4 Correlates of the Axis: Sulcus Limitans and Alar/Basal Boundary. . . . . . 107
5.5 Summary of the Brain Axis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123
vii
viii Contents
6 The (Complex) Rostral Part of the Brain. . . . . . . . . . . . . . . . . . . . . . . . . . 125
Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 130
7 The Natural Coordinate System of the CNS. . . . . . . . . . . . . . . . . . . . . . . . 133
Excursion 6: A beautiful brain atlas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 137
Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 140
8 The Fundamental Morphological Units (FMUs) of the CNS . . . . . . . . . . . . 143
8.1 Orientation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 143
8.2 The Third Dimension . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 149
8.3 The FMUs Are Radial Entities and Developmental Modules . . . . . . . . . 151
8.4 Developmental Processes Within the FMUs. . . . . . . . . . . . . . . . . . . . . 157
8.4.1 Proliferation of Matrix Cells. . . . . . . . . . . . . . . . . . . . . . . . . . 157
8.4.2 Formation of Embryonic Layers . . . . . . . . . . . . . . . . . . . . . . . 163
8.4.3 Radial Migration of Neuroblasts . . . . . . . . . . . . . . . . . . . . . . . 173
8.4.4 Differentation of Cell Masses and Cortices. . . . . . . . . . . . . . . . 177
8.5 Summary of FMUs. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 198
9 The Structural Pattern, ‘Bauplan’ or ‘Blueprint’ of the CNS . . . . . . . . . . . 201
9.1 The Overall Structural Pattern . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 201
9.2 ‘Orthogonalized’ Maps . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 203
9.3 A More Detailed Structural Pattern: Progenitor Domains
in the Embryonic Mammalian CNS. . . . . . . . . . . . . . . . . . . . . . . . . . . 205
9.4 Summary of the CNS Structural Pattern. . . . . . . . . . . . . . . . . . . . . . . . 208
10 The Development of Grisea. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 211
10.1 Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 211
10.2 Progressive Differentition Within the FMUs. . . . . . . . . . . . . . . . . . . . . 213
10.3 The Formation of Plurisegmental Complexes . . . . . . . . . . . . . . . . . . . . 217
10.4 Tangential Migrations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 221
10.4.1 Spinal Cord . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 221
10.4.2 Branchiomotor and Visceromotor Nuclei
in the Rhombencephalon . . . . . . . . . . . . . . . . . . . . . . . . . . . . 227
10.4.3 Rhombic Lip . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 229
10.4.4 Cerebellum. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 235
10.4.5 Locus Coeruleus, Interpeduncular Nucleus
and Substantia Nigra . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 239
10.4.6 Pretectal Region and Hypothalamus. . . . . . . . . . . . . . . . . . . . . 241
10.4.7 Neocortex . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 243
10.4.8 Subpallium. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 249
10.4.9 Tangential Migrations; Summary and Concluding Remarks . . . . 251
10.5 Overview of the Development of Grisea . . . . . . . . . . . . . . . . . . . . . . . 253
10.6 The Homologization of Grisea . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 261
10.6.1 Introductory Note . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 261
10.6.2 The Swedish School . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 261
10.6.3 The Principal Homology Criterion. . . . . . . . . . . . . . . . . . . . . . 263
10.6.4 The First Auxiliary Homology Criterion. . . . . . . . . . . . . . . . . . 267
10.6.5 The Second and Third Auxiliary Homology Criteria . . . . . . . . . 269
10.6.6 The Problem of Tangential Migration of Grisea . . . . . . . . . . . . 271
10.6.7 The Problem of Multiple Origins of Grisea. . . . . . . . . . . . . . . . 271
Contents ix
11 The ‘Wiring’ of the Brain. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 273
11.1 Fibre Systems. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 273
Excursion 7: Neurotransmission. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 285
11.2 Development of Fibre Systems. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 293
11.3 Molecular Studies on the Development of Fibre Systems. . . . . . . . . . . . 299
11.4 The Basic Organization Plan of the Human Brain. . . . . . . . . . . . . . . . . 301
12 General Summary, Conclusions and Perspective. . . . . . . . . . . . . . . . . . . . . 305
12.1 Antecedents of the New Neuromorphology . . . . . . . . . . . . . . . . . . . . . 305
12.2 The Genoarchitectonic Basis of the New Neuromorphology. . . . . . . . . . 306
12.3 Significance of a Common Bauplan . . . . . . . . . . . . . . . . . . . . . . . . . . 312
12.4 Necessity of a Rigorous Topologic Approach. . . . . . . . . . . . . . . . . . . . 315
12.5 Molecular Causal Underpinning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 316
12.6 New Neuromorphology and Fibre Systems. . . . . . . . . . . . . . . . . . . . . . 320
12.7 Structure and Function . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 321
12.8 Final Conclusion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 323
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 325
Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 335
x Prologue
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