A review of the theories of vertebrate neurulation and their relationship to the mechanics of neural tube birth defects.

All of the published theories of neurulation, (some of them forgotten but never disproved), are reviewed for the purpose of assessing just where we are in coming to a satisfactory explanation of this critical step in the formation of the brain and spinal cord, whose occasional failure leads to neural tube birth defects. A new approach to evaluating these theories is introduced, namely finite element analysis, along with a discussion of its promise and present limitations.

[1]  M. Adinolfi,et al.  Neural tube defects in curly-tail mice. II. Effect of maternal administration of vitamin A , 1979, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[2]  A. Burt NEURULATION IN MECHANICALLY AND CHEMICALLY INHIBITED AMBLYSTOMA , 1943 .

[3]  W. Silk DESCRIPTIONS OF DEVELOPMENT , 1984 .

[4]  F. O. Schmitt,et al.  Density studies on amphibian embryos with special reference to the mechanism of organizer action , 1941 .

[5]  I. C. Kitchin The effects of notochordectomy in Amblystoma mexicanum. , 1949, The Journal of experimental zoology.

[6]  R. G. Harrison Relations of Symmetry in the Developing Ear of Amblystoma Punctatum. , 1936, Proceedings of the National Academy of Sciences of the United States of America.

[7]  R. Jelínek,et al.  Influence of Mitotic Activity on Neurulation Movements , 1966, Nature.

[8]  M. Marín‐padilla Mesodermal alterations induced by hypervitaminosis A. , 1966, Journal of embryology and experimental morphology.

[9]  P. Tam,et al.  Cephalic neurulation in the mouse embryo analyzed by SEM and morphometry , 1982, The Anatomical record.

[10]  R. Gordon Chapter 5 – Monte Carlo Methods for Cooperative ISING Models* , 1980 .

[11]  J. Holtfreter A study of the mechanics of gastrulation , 1944 .

[12]  Joseph Needham,et al.  Order and life , 1936 .

[13]  G. Malacinski,et al.  An atlas of notochord and somite morphogenesis in several anuran and urodelean amphibians. , 1980, Journal of embryology and experimental morphology.

[14]  Hsin-yi Lee,et al.  Studies on the mechanism of neurulation in the chick: Microfilament‐mediated changes in cell shape during uplifting of neural folds , 1980 .

[15]  M. Seller The cause of neural tube defects: some experiments and a hypothesis. , 1983, Journal of medical genetics.

[16]  B. Burnside,et al.  Microtubules and microfilaments in newt neuralation. , 1971, Developmental biology.

[17]  D. Trasler,et al.  Gene-teratogen interaction in insulin-induced mouse exencephaly. , 1980, Teratology.

[18]  P. Karfunkel,et al.  The role of microtubules and microfilaments in neurulation in Xenopus. , 1971, Developmental biology.

[19]  G. Morriss-Kay,et al.  The kinetic behaviour of the cranial neural epithelium during neurulation in the rat. , 1985, Journal of embryology and experimental morphology.

[20]  J. Piatt FORM AND CAUSALITY IN NEUROGENESIS , 1948, Biological reviews of the Cambridge Philosophical Society.

[21]  M. Snow,et al.  Is compensatory growth a complicating factor in mouse teratology? , 1979, Nature.

[22]  M B Burnside,et al.  Analysis of morphogenetic movements in the neural plate of the newt Taricha torosa. , 1968, Developmental biology.

[23]  D. Kochhar Studies of vitamin A-induced teratogenesis: effects on embryonic mesenchyme and epithelium, and on incorporation of H3-thymidine. , 1968, Teratology.

[24]  H. M. Phillips Liquid-Tissue Mechanics in Amphibian Gastrulation: Germ-Layer Assembly in Rana Pipiens , 1978 .

[25]  P. Messier Effects of (β-mercaptoethanol on the fine structure of the neural plate cells of the chick embryo , 1969 .

[26]  A. Moore The individual in simpler forms , 1945 .

[27]  David R. Owen,et al.  A simple guide to finite elements , 1980 .

[28]  L. G. Tilney,et al.  The Assembly of Microtubules and Their Role in the Development of Cell Form , 1968 .

[29]  F. W. Cummings,et al.  A model of pattern and form in development , 1985 .

[30]  Richard Gordon,et al.  Questions of uniqueness and resolution in reconstruction from projection , 1978 .

[31]  C. Schorah,et al.  The effect of periconceptional supplementation on blood vitamin concentrations in women at recurrence risk for neural tube defect , 1983, British Journal of Nutrition.

[32]  C. Waddington,et al.  The ultrastructure of the developing urodele notochord , 1962, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[33]  T. E. Schroeder,et al.  Cytoplasmic filaments and morphogenetic movement in the amphibian neural tube. , 1967, Developmental biology.

[34]  R. A. Cloney Cytoplasmic filaments and cell movements: epidermal cells during ascidian metamorphosis. , 1966, Journal of ultrastructure research.

[35]  J. Holtfreter Structure, motility and locomotion in isolated embryonic amphibian cells , 1946, Journal of morphology.

[36]  M. Adinolfi,et al.  Neural tube defects in curly-tail mice. I. Incidence, expression and similarity to the human condition , 1979, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[37]  Richard Gordon Rotating Microscope For LANDSAT Photography Of Vertebrate Embryos , 1983, Optics & Photonics.

[38]  J. Cooke,et al.  Scale of body pattern adjusts to available cell number in amphibian embryos , 1981, Nature.

[39]  J. Holtfreter A study of the mechanics of gastrulation. Part I , 1943 .

[40]  A G Jacobson,et al.  Changes in the shape of the developing vertebrate nervous system analyzed experimentally, mathematically and by computer simulation. , 1976, The Journal of experimental zoology.

[41]  J. Mittenthal The rule of normal neighbors: a hypothesis for morphogenetic pattern regulation. , 1981, Developmental biology.

[42]  J. Nardi Epithelial Invagination: Adhesive Properties of Cells Can Govern Position and Directionality of Epithelial Folding , 1981 .

[43]  L. Saxén,et al.  Cells into Organs , 1986 .

[44]  H. Ghiradella,et al.  Development of ultraviolet‐reflecting butterfly scales: How to make an interference filter , 1974, Journal of morphology.

[45]  B Burnside,et al.  A mechanical model for epithelial morphogenesis , 1980, Journal of mathematical biology.

[46]  H. Hertel,et al.  Structure-form-movement , 1966 .

[47]  W. His Unsere Körperform und das physiologische Problem ihrer Entstehung Briefe an einen befreundeten Naturforscher / von Wilhelm His. , 1874 .

[48]  M. Wiley The effects of cytochalasins on the ultrastructure of neurulating hamster embryos in vivo. , 1980, Teratology.

[49]  H. Gross Congenital defects. , 1966, South Dakota journal of medicine.

[50]  J. Langman,et al.  Excess vitamin A and development of the cerebral cortex , 1967, The Journal of comparative neurology.

[51]  J. Zwaan,et al.  Cell Shape Regulation and Cell Cycle in Embryonic Lens Cells , 1974, Nature.

[52]  Stephen A. Wainwright,et al.  Mechanical Design in Organisms , 2020 .

[53]  A. Moore,et al.  On the mechanics of gastrulation in Dendraster excentricus , 1941 .

[54]  Antone G. Jacobson Computer Modeling of Morphogenesis , 1980 .

[55]  Persaud Tv,et al.  Histogenesis of experimental open neural defects in the early chick embryo. , 1979 .

[56]  Agnes S. Burt,et al.  On the locus and nature of the forces causing gastrulation in the embryos of Dendraster excentricus , 1939 .

[57]  M. Seller,et al.  Effect of hydroxyurea on neural tube defects in the curly-tail mouse. , 1983, Journal of craniofacial genetics and developmental biology.

[58]  PHOTOCHEMICAL SPECTRAL ANALYSIS OF NEURAL TUBE FORMATION , 1944 .

[59]  S Inoué,et al.  Video image processing greatly enhances contrast, quality, and speed in polarization-based microscopy , 1981, The Journal of cell biology.

[60]  P Karfunkel,et al.  The mechanisms of neural tube formation. , 1974, International review of cytology.

[61]  A G Jacobson,et al.  The shaping of tissues in embryos. , 1978, Scientific American.

[62]  K. Nakano Anencephaly: a review. , 1972, Arkhiv anatomii, gistologii i embriologii.

[63]  M. Stanisstreet,et al.  Scanning electron microscopy of wound healing in rat embryos. , 1984, Journal of embryology and experimental morphology.

[64]  C. Wardlaw Plant Morphogenesis , 1961, Nature.

[65]  C. Waddington Organisers and genes. , 1943 .

[66]  B. Källén Early Embryogenesis of the Central Nervous System with Special Reference to Closure Defects: CASEY HOLTER MEMORIAL LECTURE , 1968, Developmental medicine and child neurology.

[67]  G. Schoenwolf,et al.  Ultrastructure of secondary neurulation in the chick embryo. , 1980, The American journal of anatomy.

[68]  E. Salmon,et al.  SPINDLE MICROTUBULES: THERMODYNAMICS OF IN VIVO ASSEMBLY AND ROLE IN CHROMOSOME MOVEMENT * , 1975, Annals of the New York Academy of Sciences.

[69]  M. Furuya Cell Division Patterns in Multicellular Plants , 1984 .

[70]  P. Alberch,et al.  The mechanical basis of morphogenesis. I. Epithelial folding and invagination. , 1981, Developmental biology.

[71]  Geelen Ja Vitamin A-induced anomalies in young rat embryos. , 1973 .

[72]  K. Porter,et al.  ORIENTED MICROTUBULES IN ELONGATING CELLS OF THE DEVELOPING LENS RUDIMENT AFTER INDUCTION. , 1964, Proceedings of the National Academy of Sciences of the United States of America.

[73]  T. Gustafson,et al.  CELLULAR MOVEMENT AND CONTACT IN SEA URCHIN MORPHOGENESIS , 1967, Biological reviews of the Cambridge Philosophical Society.

[74]  W. H. Lewis,et al.  Mechanics of invagination , 1947, The Anatomical record.

[75]  C. Waddington Observations on the Forces of Morphogenesis in the Amphibian Embryo , 1942 .

[76]  N. K. Wessells,et al.  Microfilaments in Cellular and Developmental Processes , 1971, Science.

[77]  M. Bernfield,et al.  Glycosaminoglycans and Epithelial Organ Formation , 1973 .

[78]  CELL POLARITY AND THE DEVELOPMENT OF FORM IN CUCURBIT FRUITS , 1944 .

[79]  J. Hanaway,et al.  Anencephaly: a review and interpretation in terms of modern experimental embryology. , 1970, Diseases of the nervous system.

[80]  J. Löfberg Apical surface topography of invaginating and noninvaginating cells. A scanning-transmission study of amphibian neurulae. , 1974, Developmental biology.

[81]  J. Haldane Organisers and Genes , 1940, Nature.

[82]  Edward L. Wilson,et al.  Numerical methods in finite element analysis , 1976 .

[83]  J. Holtfreter Observations on the migration, aggregation and phagocytosis of embryonic cells , 1947, Journal of morphology.

[84]  A. Barson,et al.  Scanning electron microscopy of neurulation in the chick. , 1974, Journal of anatomy.

[85]  A. Gierer Physical aspects of tissue evagination and biological form , 1977, Quarterly Reviews of Biophysics.

[86]  M. A. Hinrichs MODIFICATION OF DEVELOPMENT ON THE BASIS OF DIFFERENTIAL SUSCEPTIBILITY TO RADIATION: II. ARBACIA AND VISIBLE LIGHT FOLLOWING SENSITIZATION , 1926 .

[87]  Order of Magnitude of Morphogenetic Forces , 1939, Nature.

[88]  G. Selman,et al.  The forces producing neural closure in amphibia. , 1958, Journal of embryology and experimental morphology.

[89]  S. Timoshenko Theory of Elastic Stability , 1936 .

[90]  R. Bellairs,et al.  Midbodies and beaded threads. , 1975, The American journal of anatomy.

[91]  R. Cook,et al.  Concepts and Applications of Finite Element Analysis , 1974 .

[92]  B. Crawford Development of the junctional complex during differentiation of chick pigmented epithelial cells in clonal culture. , 1980, Investigative ophthalmology & visual science.

[93]  Raymond A. Sjodin The behavior of brain and retinal tissue in mortality of the early chick embryo , 1957, The Anatomical record.

[94]  W. His Ueber mechanische Grundvorgänge thierischer Formenbildung , 1894 .

[95]  R. Keller,et al.  Vital dye mapping of the gastrula and neurula of Xenopus laevis: I. Prospective areas and morphogenetic movements of the superficial layer , 1976 .

[96]  L V Beloussov,et al.  Mechanical stresses and morphological patterns in amphibian embryos. , 1975, Journal of embryology and experimental morphology.

[97]  P Karfunkel,et al.  The activity of microtubules and microfilaments in neurulation in the chick. , 1972, The Journal of experimental zoology.

[98]  N. Berrill,et al.  Growth, development, and pattern , 1961 .

[99]  A. Read,et al.  FURTHER EXPERIENCE OF VITAMIN SUPPLEMENTATION FOR PREVENTION OF NEURAL TUBE DEFECT RECURRENCES , 1983, The Lancet.

[100]  M. Stein,et al.  Epithelia as bubble rafts: a new method for analysis of cell shape and intercellular adhesion in embryonic and other epithelia. , 1982, Journal of theoretical biology.

[101]  S. R. Hilfer,et al.  Computer simulation of organogenesis: an approach to the analysis of shape changes in epithelial organs. , 1983, Developmental biology.

[102]  W. Gardner Rupture of the Neural Tube: The Cause of Myelomeningocele , 1961 .

[103]  Keith Miller,et al.  The moving finite element method: Applications to general partial differential equations with multiple large gradients☆ , 1981 .

[104]  B. Burnside Microtubules and Microfilaments in Amphibian Neurulation , 1973 .

[105]  R. V. b. Southwell,et al.  An introduction to the theory of elasticity for engineers and physicists , 1936 .

[106]  R. Gillette Cell number and cell size in the ectoderm during neurulation (Amblystoma maculatum) , 1944 .

[107]  C. H. Waddington,et al.  Principles of Embryology , 2016 .

[108]  A. Copp,et al.  Neural tube development in mutant (curly tail) and normal mouse embryos: the timing of posterior neuropore closure in vivo and in vitro. , 1982, Journal of embryology and experimental morphology.

[109]  G. Morriss,et al.  Effect of oxygen concentration on morphogenesis of cranial neural folds and neural crest in cultured rat embryos. , 1979, Journal of embryology and experimental morphology.

[110]  M Ycas,et al.  Self-sorting of isotropic cells. , 1970, Journal of theoretical biology.

[111]  J. Bard,et al.  CELLULAR INTERACTIONS IN MORPHOGENESIS OF EPITHELIAL MESENCHYMAL SYSTEMS , 1974, The Journal of cell biology.

[112]  F. Stillinger,et al.  Packing Structures and Transitions in Liquids and Solids , 1984, Science.

[113]  N. Wald,et al.  VITAMIN SUPPLEMENTATION FOR PREVENTION OF NEURAL TUBE DEFECT RECURRENCES , 1983, The Lancet.

[114]  G. Morriss,et al.  Regional differences in mesenchymal cell morphology and glycosaminoglycans in early neural-fold stage rat embryos. , 1978, Journal of embryology and experimental morphology.

[115]  T. Shepard,et al.  Neural Tube Closure Defects caused by Cytochalasin , 1972 .

[116]  B. Gunning,et al.  Intercellular Communication in Plants: Studies on Plasmodesmata , 1976, Springer Berlin Heidelberg.

[117]  A. Jacobson Further evidence that formation of the neural tube requires elongation of the nervous system. , 1984, The Journal of experimental zoology.

[118]  N S Goel,et al.  A rheological mechanism sufficient to explain the kinetics of cell sorting. , 1972, Journal of theoretical biology.

[119]  George D. Mostow,et al.  Mathematical models for cell rearrangement , 1975 .

[120]  J. Trinkaus Cells into organs , 1969 .

[121]  W. R. Dean On the Theory of Elastic Stability , 1925 .

[122]  John Philip Trinkaus,et al.  Cells into Organs: The Forces That Shape the Embryo , 1984 .

[123]  R. Assheton The geometrical relation of the nuclei in an invaginating gastrula (e. g. Amphioxus) considered in connection with cell rhythm, and Driesch's conception of Entelechy , 1910 .

[124]  H. Jehle Bilateral symmetry in morphogenesis of embryos. , 1970, Proceedings of the National Academy of Sciences of the United States of America.

[125]  O. Glaser THE THEORY OF AUTONOMOUS FOLDING IN EMBRYOGENESIS. , 1916, Science.

[126]  J. Langman,et al.  The effect of cytochalasin B on the neuroepithelial cells of the mouse embryo. , 1978, The American journal of anatomy.

[127]  T. E. Schroeder,et al.  Neurulation in Xenopus laevis. An analysis and model based upon light and electron microscopy. , 1970, Journal of embryology and experimental morphology.

[128]  Kennan T. Smith,et al.  Practical and mathematical aspects of the problem of reconstructing objects from radiographs , 1977 .

[129]  O. Glaser On the mechanism of morphological differentiation in the nervous system. I. The transformation of a neural plate into a neural tube , 1914 .

[130]  R. Althouse,et al.  Survival and handicap of infants with spina bifida. , 1980, Archives of disease in childhood.

[131]  R. Jelínek,et al.  Mechanism of morphogenesis of caudal neural tube in the chick embryo. , 1969, Folia morphologica.

[132]  R. Bellairs,et al.  The development of the notochord in the chick embryo, studied by scanning and transmission electron microscopy. , 1976, Journal of embryology and experimental morphology.

[133]  G. Malacinski,et al.  Neural Tube (Canal) Morphogenesis in Notochordless Amphibian (Xenopus Laevis) Embryos , 1983, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[134]  W. J. Hamilton,et al.  PRINCIPLES OF EMBRYOLOGY , 1956 .

[135]  M. A. Hinrichs Modification of development on the basis of differential susceptibility to radiation. IV. Chick embryos and ultraviolet radiation , 1927 .

[136]  K. Turksen,et al.  Adhesiveness and distribution of vinculin and spectrin in retinal pigmented epithelial cells during growth and differentiation in vitro. , 1985, Developmental biology.

[137]  F. Fraser,et al.  Early changes in the mouse neuroepithelium preceding exencephaly induced by hypervitaminosis A. , 1978, Teratology.

[138]  M. Handel,et al.  Cell shape and morphology of the neural tube: implications for microtubule function. , 1971, Developmental biology.

[139]  D. Brock Early diagnosis of fetal defects , 1983 .

[140]  B. Criley,et al.  Analysis of the embryonic sources and mechanisms of development of posterior levels of chick neural tubes , 1969 .