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Journal of Dental Research http://jdr.sagepub.com/ The Time-Structure Relationship of Tooth Development in Human Embryogenesis C.H. Tonge J DENT RES 1969 48: 745 DOI: 10.1177/00220345690480052301 The online version of this article can be found at: http://jdr.sagepub.com/content/48/5/745 Published by: http://www.sagepublications.com On behalf of: International and American Associations for Dental Research Additional services and information for Journal of Dental Research can be found at: Email Alerts: http://jdr.sagepub.com/cgi/alerts Subscriptions: http://jdr.sagepub.com/subscriptions Reprints: http://www.sagepub.com/journalsReprints.nav Permissions: http://www.sagepub.com/journalsPermissions.nav Citations: http://jdr.sagepub.com/content/48/5/745.refs.html >> Version of Record - Sep 1, 1969 What is This? Downloaded from jdr.sagepub.com at PENNSYLVANIA STATE UNIV on March 4, 2014 For personal use only. No other uses without permission. The Time-Structure Relationship of Tooth Development in Human Embryogenesis C. H. TONGE Department of Oral Anatomy, University of Newcastle upon Tyne, Newcastle upon Tyne, England The sequence of appearance of the cytological and morphological features of oral and tooth differentiation was assessed, relative to general embryological processes, in Inhuan embryonic material. The phases considered were as follows: potentiality (022 days); interaction (23-32 days); and specificity of individual structural formation (3248 days). allocating specimens to Streeter ho- rizons.'0-'2"7'35'38'39 (3) Recording menstrual age and Streeter horizons.23 (4) Using various different technics basing the age according to crown rump measurement of embryo. 14-16,18-2 0,24-26,3 2-34,36 (5) Measurements alone with no for the the ag- ing.3,21,22,27-3' Detailed information on the timing of human odontogenesis relative to other structural differentiations is necessary to apply the results of animal in vitro studiesl-5 to man. Human embryos have been described before and during implantation, forming endoderm, the embryonic disk, the primitive streak and its head process, and showing neural grooves and neural crest migra- The purpose of the present investigation was to define, within the first 48 days after ovulation. the sequence of appearance and identification of the oral structures, indicating general embryological processes and local features, such as innervation, ossification, myogenesis, oral epithelial differentiation, and the isolation and continued differentiation within a limited local environtions.6-9 ment of the early developing tooth. Separate descriptions of different embryMaterials and Methods onic collections have been recorded for mouth development:10 early odontogeneA range of 31 human embryos (Table 1) SiS :11,12 permanent-tooth germ formation;'3 was allocated38 to Streeter horizons XIIIthe morphogenesis of the dental arches;'4"15 XXIII, 27 to 48 days ovulation age. Serial the development of taste buds;16 palatal sections at 8 micrometers (pm) of cold morphogenesis;17-19 oral mucosa;20 its kera- neutral formalin, paraffin-embedded material tinization21 and hemopoiesis;22 facial nerve23 were stained by various cellular and connecand muscle development;24 the relationship tive tissue stains. Wax-plate reconstructions of trigeminal nerve fibers to tooth germ,25 were made of selected specimens. Comparioral mucosa, and cutaneous areas.26 Other son was made with published illustrarecent human developmental studies include tions.1-38 The photographs of the normal 19 observations on the motor end plate in specimens (Streeter horizons XVI-XXIII) tongue musculature;27 a 34-mm sku1128 and in Kraus, Kitamura, and Latham39 were also mandible;29 the tubotympanic recess;30 the studied. remains of Meckel's cartilage;2' the tempoResults romandibular joint;32,33 accessory thyroid 0-27 DAYS.-The literature has retissue;34 the third bronchial duct;35 and the histogenesis of the bronchial cyst.36'37 corded6-9,38 a two-cell stage at 1½2 to 21/2 Methods employed for timing the se- days; a 12-cell morula at 3 days; and a 107cell blastocyst, of which eight are embryoquence of events include: forming at 4 to 41/2 days, endoderm at 71/2 (1) Knowledge of the ovulation age.7-9 (2) Estimation of the ovulation age by days, an ectodermal plate at 91/2 days, and 745 Downloaded from jdr.sagepub.com at PENNSYLVANIA STATE UNIV on March 4, 2014 For personal use only. No other uses without permission. 746 TONG E, 7 Dent Res Supplemnent to No. S BLE EMBRYO ALLOCATION TO STREETERt HORIZONS Streeter lorizoll XIII XIV XV XVI XVII XVIII XIX XX XXI XXiI XXIII Number of olinbrvo s C(row n -Rump Range (nr m) I 2 5.0 5.6- 7.0 11.0 11.0-12.0 12.0-15.0 15.0-21.0 18.0 19.0 3 3 5 4 3 2 2 5 20.0-20.6 22.824.0 25.0 28.0--31.4 O( vllatioln \ge (days) 27- 29 28-30 31 32 32-24 34---36 36--38 38 -40 40 42 42 44 44--46 46--48 lay in contact. The epithelium lining the roof of the pharynzgeal region was singlecell cuboidal; that lining the floor and lateral walls was proliferative with marginal epithelial outgrowths. The first aortic artery traversed the mandibular arch. It was endo- thelially lined and contained nucleated blood cells passing toward the epithelial surface (Fig 1 ). Lingual swellings, tuberculunm impar, and thyroid Outgrowth were identified. The atrial myocardium was two to three-cells thick; the ventricular myocardium showed trabeculation. and the endocardial cushions of the atrioventricular valves were outlined. The lower limb bud was smaller but similar to the arm bud. No identifiable tooth-bearing region nor salivary gland formation was present. HORIZON xiv, 28-30 DAYS.-Lens disks were invaginated and communicated by narrow pores with the surface. Arm buds projected as appendages from the body wall. but no differentiated hand plates were seen. Mandibular and hyoid arches marked surface elevations, with the third arch being much smaller. Thyroid diverticulum wasS still connected with the pharyngeal surface. Rathke's pouch and pituitary were observed. The trachea was separate from the esophagus. Primary bronchi and epithelial-lined lung buds were formed. Bowman's capsule was identified cephalically with the single vesicles of the mesonephros caudally. Mesenchyme condensing around the notochord and posterior nerve root ganglia and spinal nerves were differentiating. The tissue, in which the structures of the floor of the an embryonic disk by 12 days. The presomite phase was completed with the primitive streak at 15 days, its head (notochordal) process at 18 days, and neural groove at 1 6 days. The notochord elongated cephalically; early somites and the neural folds appeared by 21 to 23 days. At 23 to 25 days the first heart pulsations and a simple vascular plexiform arrangement of endothelium aided fluid movement. Neural ectoderm was separating from skin ectoderm, early neurl crest migrations occurred, and the anterior neuropore was closing. The mandibular and hyoid arches and 13 to 20 somites were present. The buccopharyngeal membrane had not ruptured, and pituitary formation was commencing. The brain vesicles were becoming defined, as were the fifth, seventh. and eighth cranial nerves, with the ninth and tenth less definite. Embryos between 25 to 27 days had 21 to 29 somites, arm buds, three bronchial arches, partial closure of the posterior neusropore, and epithelial differentiation for the liver, lung, stomach. and pancreas. Pharyngeal epithelial proliferations included the thyroid, parathyroid, and thymic outgrowths. An adequate blood suIpply reached the liver, yolk sac, cranial ganglia, bronchial arches, and the surface of the central nervous system. HORIZON XiiI, 27-29 DAYS. The nCuropores were closed; a retinal region bulged backward into the l]umen of the optic 4s o evagination with no lens formation. The m' t) otocyst opening on to the surface had ,'. Aw, thick epithelium, contrasted with the single FIG 1. The floor of the oral region in 5layer of flattened cells lining the skin. The mm-crown-rump embryo, horizon X1I1, 27-29 frontonasal process, mandibular, hyoid and The first aortic arch artery traverses the third arches, with the pericardium were days. tissue, and numeroLus nucleated blood cells identified together with three bronchial mem- can be seen in it and close to the epithelial branes where skin and pharyngeal epithelial surface. I'm~~~~~~~~~~~ 4 E a ' '. B it R: Downloaded from jdr.sagepub.com at PENNSYLVANIA STATE UNIV on March 4, 2014 For personal use only. No other uses without permission. ff Vol 48, 1969 HUMAN EMBRYOGENESIS RELATIVE TO ODONTOGENESIS mouth form, had become defined by the growth of the mandibular processes. The lingual swellings and midline intermandibular sulcus were seen; the mandibular arch was packed with mesenchymal cells laterally, although these were less dense centrally. An amorphous matrix packed the interstices between the irregular mesenchyma cells, which had long slender processes. A potentially odontogenic epithelium of the tall cuboidal variety was well marked in the premaxillary (primitive palate) and mandibular regions. There was an ill-defined mesenchymal condensation beneath it. No salivary gland formation was observed but there was a thickened epithelium in the maxillary-mandibular junctional area. HORIZON XV, 31-32 DAYS.-The olfactory pit was sufficiently invaginated for its edges to be defined and the lateral nasal process and primitive palate to be easily identified. Lens vesicles were closed. Cranial ganglia of trigeminal, facial, glossopharyngeal, and vagus had formed. Trachea and esophagus were contained in a common mesenchymal condensation. The posterior part of the tongue and adjacent posterior pharyngeal wall were lined by a cuboidal epithelium arranged in several layers; the anterior part by one or two cell layers. The thyroid diverticulum was losing its attachment to the lingual pit. There was evidence of migration of the occipital myotomes forming the tongue muscles. The orientation of the cells beneath the epithelium suggested the direction of the superior longitudinal muscle layer, although the presence of myoblasts was not confirmed. The epithelium of the oral cavity and the odontogenic area was similar to the last horizon. No salivary glandular epithelium was identified, but a region later forming the mesenchymal bed of the submandibular gland was located. HORIZON XVI, 3 2-34 DAYS-.Nasal placodes were directed laterally. The deepest part of the olfactory pit was visible from the side, together with separate medial and lateral nasal processes. Auricular tubercles were present. The handplate with the primary marginal vein was separate from the arm and shoulder in which precartilage condensations were observed. The surface elevations of underlying somites and spinal ganglia were restricted to the region caudal to the arm bud. The ventricles were separating and the aorta and pulmonary trunk were 747 forming from the truncus arteriosis. The trachea and primary bronchi lay in mesenchyma separate from that surrounding the esophagus. The bronchial region, without cartilage formation, was characterized by the presence of recognizable cellular condensations related to nerve trunks. The chorda tympani nerve was entering the mandibular arch; the mandibular nerve had a cellular collection around it, the whole forming a nerve-ganglion mass giving rise to the lingual nerve and submandibular ganglion. Small blood vessels accompanied the nerves. The facial nerve lay within the second arch tissue. The genioglossus and geniohyoid muscles formed a common mass toward which the hypoglossal nerve was passing. The central region between the muscles of the two sides was less cellular. A condensation beneath the surface was probably associated with the intrinsic musculature. In the most developed embryo allocated to this horizon the mylohyoid muscle condensation was identifiable. The thyroid gland freed from the surface was located within the central zone of less condensed cells. Rathke's pouch was well developed. In the posterior pharyngeal wall, lined with two to three layers of cuboidal cells, the underlying notochord was surrounded by dense mesenchyma. The scalp was covered by a single layer of cells. The underlying mesenchyma was condensed beneath the developing forebrain and in the region in which the facial muscles form. A clearly defined odontogenic epithelium, comprising two to three layers of columnar cells, could be traced over the premaxillary and mandibular regions. The underlying condensed and proliferating mesenchyma showed a definite orientation relative to the odontogenic epithelium (Fig 2). HORIZON XVII, 34-36 DAYS.-An olfactory region was recognizably different from the respiratory region, and the vomeronasal organ was differentiating. Primary palate and primitive posterior nares were observed. The maxillary processes were forming the earliest shelves for the secondary palate. Precartilage condensations for Meckel's cartilage, hyoid bar, tracheal and laryngeal cartilages were identified. Condensing perichondrium existed around the limb cartilages. Early muscle formation appeared in the walls of the alimentary canal. Aortic and pulmonary valves were present. In the floor of the Downloaded from jdr.sagepub.com at PENNSYLVANIA STATE UNIV on March 4, 2014 For personal use only. No other uses without permission. 748 F/ONGE FIG 2. The premaxilla (A) and mandibular area (B) in an 11.5-mm-crown-rump embryo, horizon XVI, 32-34 days. In both areas odontogenic epitheliUm with underlying mesenchyma becoming oriented relative to it can be observed. It is made up of coluimnar cells in contrast to the flat cuiboidal cells elsewhere. J D7eONt Res.6 Supplement In No. for the lower incisors being more pr1 onounced (Fig 3). The mylohyoid muscle formed a complete floor to the mouth between the Meckelfs cartilages to the perichondrium to which it was attached. The anterior belly of the digastric reinforced its anterior part, and behind the posterior part of the mylohyoid the submandibular gland mesenchyma, now clear rlv delineated, conilt1 be observed (Fig 4). A well-marked condensation was appearing lateral to the Meckel's cartilage and was the precursor of mandibular development. The superficial group of facial muscles was not separately identifiable, with the exception of the orbicularis-oculi groUp. The posterior belly of the digastric was visible. In the limbs, hyaline cartilage, a perichondrium, and muscle groups were observed. The development ol the femur was the most complete. HORIZON XIX, 38-40 DAYS. The vCstilbL- mouth, the lingual and inferior dental nerves together, the submandibular ganglion, and the hypoglossal nerve were identified. The epithelial bud of the submandibular gland extended toward the mesenchymal condensation, which had not yet clearly defined limitations. The geniohyoid was identified separately from the genioglossus. The nerve to the mylohyoid entered a premUscle condensation in which differentiating myoblasts formed the mylohyoil. The more superficial cells of this condensation may form the anterior belly of the digastric muscle. Tooth development is essentially similar to the previous horizon. HORIZON XVIII, 36-38 I)AYS.-The basic external features of the face had become established. The base of the skull in the sphenoidal region was a. precartilaginous mesenchymra in which the notochord had lost its separate identity, although Rathke's pouch had not disappeared. The epithelium of the oral cavity was cuboidal, with one or more layers of flattened cells upon its surface. The anterior two-thirds of the tongue was similar, the cells showing frequent evidence of mitosis; but no taste bud formation had occurred. The cells on the posterior third of the tongue were taller, with a reduction in cell layers. Within the odontogenic regions some specialized formation for individual teeth was occurring as a result of the formation of well-marked cellular clusters. Individual regions for the incisor teeth could be demonstrated, those Ar * .t,*, 'V4 v .* FIG; 3.- The Lipper (AI) and lower (B) inareas of cl '2-mm-crown rump ernbryo, horizon XV111, .36-38 days, in which individl-iY1 centers are forming for the teeth within tile odontogenic epithelium. The proliferating cells are arranged in c1 asters, concentrically aroulL the center. cisor Downloaded from jdr.sagepub.com at PENNSYLVANIA STATE UNIV on March 4, 2014 For personal use only. No other uses without permission. Vol 48, 1969 IIUANAN EMBRYOGENESIS RELATIVE TO ODONTOGENESIS The floor of the mouth in a 16-mmembryo, horizon XVIII, 36-38 days. The submandibular ganglion and lingual nerve (A); mesenchymal bed of the submandibular gland (B), in which the epithelial downgrowth is invaginating; and the mylohyoid mUscle and nerve (C) can be observed. FIG 4. crown-rump lar sulcus was forming in both jaws, the epithelial invagination into condensing mesenchyma was occurring in the identifiable odontogenic regions, which were now recognizable for the incisor, canine, and firstmolar entities of both jaws. The epithelial region for the lower second molar was identified in one specimen allocated to this horizon. There is some evidence of papillae formation on the surface of the anterior twothirds of the tongue. Meckel's cartilages were complete, and ossification in the mandibular region had commenced, the early osteoid being demonstrable. A mesenchymal condensation for the elevator muscles and associated mandibular ramus region was observed. HORIZON xx, 40-42 DAYS.-The palatal shelves of the maxillary processes lay alongside the tongue, the muscles of which had myoblasts with single nuclei, and which oc- 749 cupied a large part of the common buccobasal cavity. The parotid outgrowth was a solid mass of cells lying close to the condensation for the masseter muscle. The inferior dental nerve lay in a gutter formed by the developing mandible. There was evidence of maxillary ossification in the canine and incisor regions. The dental lamina was forming as the tooth buds, each having a different shape and size, entered the mesenchyma from the odontogenic epithelial surface. In the interdental regions there was little cell proliferation and almost no penetration into the mesenchyma. The limits of the future gingival regions, both palatally or lingually and on the vestibular aspect, could be determined. The genial tubercles could be identified with the attached geniohyoid and genioglossus muscles. HORIZON XXI, 42-44 DAYS.- The parotid and submandibular outgrowths were tubular. Bone was forming around Meckel's cartilage. The temporalis, masseter, medial, and lateral pterygoid muscles could be identified with individual muscle fiber formation for the mylohyoid and anterior belly of the digastric. HORIZON xXII1, 44-46 DAYS. Well-marked dental papilla with a dental follicle surrounding it were observed. There was increasing emphasis on the separation of the lip, the development of the vestibular sulcus, and the formation of the dental lamina. HORIZON XXIII, 46-48 DAYS. The membranous skull was forming; nasal meati and spheno-ethmoidal recess lined by olfactory epithelium was defined. Secondary palatal shelf fusion was occurring, but no nasal septal fusion was seen. Costal cartilages, ribs, intercostal muscles, laryngeal muscles, and vocal cords were identified. The muscles of facial expression were separately demonstrated. Meckel's cartilage was being replaced by bone anteriorly Mylohyoid was attached to a well-marked raphe anteriorly and the hyoid bone posteriorly with a cleft for blood vessels and lymphatics passing toward the developing submandibular lymphatic glands. The submandibular salivary gland showed a branching canalization of its duct system. Individual tooth germs with restricted interdental regions, well-formed dental laminae, and dental papillae contained within a dental follicle were observed. The superficial part of the dental lamina stained histologically and histochemically like the oral mucosa and was nonodonto- Downloaded from jdr.sagepub.com at PENNSYLVANIA STATE UNIV on March 4, 2014 For personal use only. No other uses without permission. TONGE 750 J Dent Res Supplement to No. 5 genic, the deeper part being similar to the external dental epithelium. Discussion The literature is extensive concerning the determination of embryonic age, but there is no certain method for ascertaining it with absolute accuracy. The work of Streeter,38 by establishing identifiable developmental horizons linked to ovulation age, has become the accepted basis for recording the sequence of embryonic development. In considering the significance of any particular embryonic organization relative to mouth and tooth differentiation, the classical studies of Spemann40 point the way by indicating the necessity of having ectoderm in contact with mouth endoderm before tooth formation can occur. Indeed, the endoderm seem to be the more important, since only after induction does the ectoderm become labeled as tooth forming. Further differentiation proceeds as an interdependence of ectoderm on the underlying mesenchyma. Studies in cell bi- ology41 have shown that a chemical and largely protein basis is involved in the complex mechanisms concerned with the progressive limitation of genetic potentiality associated with the progressive cytodifferentiation and tissue organization that is necessary in the formation of separate organ systems. This clearly adds to the knowledge of the mode of action of organizers and is a logical extension of the principles elaborated by Waddington.42 In applying the results of this investigation to an assessment of the sequence of events associated with the appearance and identification of oral structures, it seems reasonable to divide the first 48 days after ovulation into three phases: (1) potentiality (2) interaction, and (3) specificity (Table 2). Potentiality is essentially that period during which the initial genetic totality of cells is being limited as differentiation takes place. This is the phase during which the embryonic disk is formed, the primitive streak and notochord differentiate, while regionalization TABLE 2 EMBRYONIC FORMATIONS 0-48 DAYS Phase Potentiality 112 3 4Y2 712 912 12 15 16 18 22 Interaction 23-25 25-27 27-29 28-30 31-32 Specificity Observation Days 32-34 34-36 36-38 38-40 40-42 42-44 44-46 46-48 Two-cell stage Morula Embryo-forming cells Endoderm Ectoderm + endoderm Embryonic disk Primitive streak Neural groove Notochord Closure of neural tube with open neuropores, optic and otic vesicles, 7 somites Neural crest migration; heart pulsations; 1st, 2nd bronchial arches; pituitary; 5th, 7th, 8th nerves; 13-20 somites Arm buds, 3 bronchial arches, liver, lung, stomach, pancreas, thyroid, parathyroid and thymic growths Neuropores closed, no lens, 3 bronchial arches and membranes, lingual swellings, tuberculum impar Trachea separate from esophagus, primary bronchi, lung buds, mandibular arch packed with mesenchyma, primitive palatal process Odontogenic epithelium; occipital myotomes for tongue; 5th, 7th, 9th, 10th nerve ganglia formed; lateral nasal process Handplate, submandibular ganglion, lingual N, parotid gland, genioglossus and geniohyoid muscles, 12th nerve Secondary palatal shelves, precartilage bronchial bars, mylohyoid mass, submandibular gland Face formed, incisor tooth regions, oral floor complete Vestibular sulcus, canine and first molar areas, mandibular ossification, mandibular ramus condensation with elevator muscles Maxillary ossification, genial tubercles, dental laminas Tubular outgrowths for parotid and submandibular glands Dental papillae with dental follicle formation Secondary palatal fusion, facial muscles, individual tooth germs, salivary gland ducts branching Downloaded from jdr.sagepub.com at PENNSYLVANIA STATE UNIV on March 4, 2014 For personal use only. No other uses without permission. Vol 48, 1969 HUMAN EMBRYOGENESIS RELATIVE TO ODONTOGENESIS 751 Germs in a Chemically Defined Proteinoccurs, and the neural plates and tubes show Free Medium, Arch Oral Biol 9:27-30, morphological differences at the various 1964. axial levels. Cranially, a potential brain PouRTois, M.: Contribution a l'Ptude des forms, optic and otic outgrowths arise, and 3. Burgeons Dentaires Chez la Souris: I. early somites develop. Potentiality in man Periodes d'Induction et de Morphodiflasts for 22 to 23 days and then merges with ferenciation, Arch Biol (Paris et Lietge) interaction. Interaction, extending from 23 72:17-95, 1961. to 32 days, is essentially the phase when an 4. PouRTois, M.: Comportement en Culture inductive relationship exists between one in vitro des Abauches Dentaires de Rongeurs Prdelevees aux Stades de Predifferenciagroup of differentiated cells and other groups tion, J Embryol Exp Morph 12:391-405, in such a way that tissue organization can 1964. occur. Innumerable mechanisms belong to L.C.: The Epigenetics of Early this category and include the formation of 5. DRYBURGH, in the Mouse, J Dent Tooth Development the lens from the surface ectoderm by means Res 46:6 (suppl) 1264, 1967. of the inductive capacity of the optic cup. 6. HERTIG, A.T., and ROCK, J. Implantation Similarly, a mouth forms. The interaction of and Early Development of Human Ovum, cell layers continues until the completion of Amer J Obstet Gynec 61A (suppl); 8-14, induction results in the labeling of cells to 1951. form specific structures without the capacity 7. HERTIG, A.T., and ROCK, J. Two Human Ova of the Pre-villous Stage, Having and for dedifferentiation. Specificity, from 32 to Ovulation Age of about Seven and Nine 48 days, is the phase during which individual Days Respectively, Contr Embryol Carneg structures are formed independently of other (No. 200) 31:65-84, 1945. structures. Bone develops, teeth form, sal- 8. Inst HERTIG, A.T.; ROCK, J.; and ADAMS, E.C. ivary glands differentiate, and all have their A Description of 34 Human Ova within own precisely defined territories. The tooth the First 17 Days of Development, Amer germ has a dental follicle43 to maintain its J Anat 98:435-493, 1956. histological and histochemical independence 9. BARTELMEZ, G.W., and DEKABAN, A.S. The Early Development of the Human Brain, of other structures. Contr Embryol Carneg Inst (No. 621) 37: Summary 13-32, 1962. A study of the first 48 days after ovulation 10. TONGE, C.H. Basic Aspects of Mouth Development, Proc Roy Soc Med 50:185-190, has been made on human material, indicat1957. ing the general embryological processes and 11. TONGE, C.H. Advances in Dental Embryof diforal and tooth the regional features ology, Int Dent J 16:328-349, 1966. ferentiation. The sequence of appearance of 12. TONGE, C.H. Identification of Cell Patterns the different cytological and morphological in Human Tooth Differentiation J Dent differentiations has been arranged in phases: Res 46:5 (suppl) 876-878, 1967. of potentiality, 0 to 22 days; of interaction, 13. OOE, T. A Study of the Ontogenetic Origin of Human Permanent Tooth Germs, 22 to 32 days; and of specificity of individOkajimas Fol Anat Jap 40:429-437, 1965. ual formation, 32 to 48 days. In the case of 14. Buim, A.R., and LILLIE, J.H. A Catenary 31 human embryos allocated to Streeter Analysis of the Maxillary Dental Arch durHorizons XIII-XXIII, 27 to 48 days, deing Human Embryogenesis, Anat Rec 154: scriptions of each stage have been given 13-20, 1966. with particular emphasis on oral and tooth 15. BURDI, A.R. Morphogenesis of Mandibular Dental Arch Shape in Human Embryos, differentiation. In each horizon reference J Dent Res 47:50-58, 1968. has been made to the major general developBRADLEY, R.M., and STERN, I.B. The Demental processes taking place at the same 16. velopment of the Human Taste Bud during time. the Foetal Period, J Anat 101:4, 743-752, The author thanks D. Golding for preparing the illustrations and E. Breese for secretarial assistance. References 1. GLASSTONE, S.: Regulative Changes in Tooth Germs Grown in Tissue Culture, J Dent Res 42:1364-1368, 1963. 2. GLASSTONE, S.: Cultivation of Mouse Tooth 1967. 17. WOOD, N.K.; WRAGG, L.E.; and STUTEVILLE, O.H. The Premaxilla: Embryological Evidence that it Does Not Exist in Man, Anat Rec 158:485-490, 1967. 18. WOOD, P.J., and KRAuS, B.S. Prenatal Development of the Human Palate, Arch Oral Biol 7:137-150. 1962. Downloaded from jdr.sagepub.com at PENNSYLVANIA STATE UNIV on March 4, 2014 For personal use only. No other uses without permission. 752 TONGE 19. BURDI, A.R., and FAIST, K. Morphogenesis of the Palate in Normal Human Embryos with Special Emphasis on the Mechanisms Involved, Amer J Anat 120:149-160, 1967. 20. COSLET, J.G., and COHEN, D.W. The Basal Cell Layer of the Developing Oral Mucosa in the Human Fetus, J Periodont Res 2: 297-316, 1967. 21. DAMOvA, N. Sur l'Histochemie de 1'Epithelium de la Cavit6 Buccale des Embryons Humains en vue de la Keratinisation, Bull Inst Morphol (Acad Bulg des Sci), 11:2132, 1965. 22. DAMOvA, N.: Contribution 'a 'Etude de l'Hemopoiese Dans la Muqueuse Buccale Chez des Embryons Humains Mesurant d'un a Cinquante-Deux Centimetres de Long, Bull Inst Morphol Acad Bulg des Sci, 6:29-38, 1962. 23. GASSER, R.F.: The Development of the Facial Nerve in Man, Ann Otol 76:37-57, 1967. 24. GASSER, R.F.: The Development of the Facial Muscles in Man, Am J Anat 120:357376, 1967. 25. HUMPHREY, T.: The Relation of Nerve Fibers to the Developing Enamel Organs and Dental Papillae of Human Fetuses of 7.5 to 12 Weeks of Menstrual Age, Ala J Med Sci 2:137-148, 1965. 26. HUMPHREY, T.: The Development of Trigeminal Nerve Fibers to the Oral Mucosa, Compared with Their Development to Cutaneous Surfaces, J Comp Neurology 126: 91-108, 1966. 27. BLECHSCHMIDT, E., and DAIKOKU, S.: Die Entotehung der Motorischen Innervation in der Menschlichen Zungenmuskulatur, Acta Anat 63:179-198, 1966. 28. YOUSSEF, E.H.: The Development of the Skull in a 34 Mm. Human Embryo, Acta Anat 57:72-90, 1964. 29. SOLIMAN, A.H., and YOUSSEF, E.H.: The Development of the Mandible in a 34 mm Human Embryo, Egypt Med Assoc 36: 575-581, 1963. J Dent Res Supplement to No. 5 30. KANAGASUNTHERAM, R.: A Note on the Development of the Tubotympanic Recess in the Human Embryo, J Anat 101:4, 731741, 1967. 31. BoSSEY, J., and GAILLARD, L.: Les Vestiges Ligamentaires du Cartilage de Meckel, Acta Anat 52:282-290, 1963. 32. YUODELIS, R.A.: The Morphogenesis of the Human Temporomandibular Joint and Its Associated Structures, J Dent Res 45:182191, 1966. 33. YUODELIS, R.A.: Ossification of the Human Temporomandibular Joint, J Dent Res 45: 192-198, 1966. 34. KNOBLICH, R.: Accessory Thyroid in the Lateral Floor of the Mouth, Oral Surg 19: 234-238, 1965. 35. YOKOH, Y.: Development of the Third Branchial Duct in the Human Embryo, Okajimas Fol Anat Jap 40:531-563, 1965. 36. LITTLE, J.W., and RiCKLES, N.H.: The Histogenesis of the Branchial Cyst, Amer J Path 50:533-547, 1967. 37. RICKLES, N.H., and LITTLE, J.W.: The Histogenesis of the Branchial Cyst: II. A Study of the Lining Epithelium, Amer J Path 50:765-777, 1967. 38. STREETER, G.L.: Developmental Horizons in Human Embryos, Contrib Embryol Carneg Inst vol 30-34, 1942-195 1. 39. KRAus, B.S., KITAMURA, H., and LATHAM, R.A.: Atlas of Developmental Anatomy of the Face, New York: Harper & Row, 1966. 40. SPEMANN, H. Embryonic Development and Induction, chap 17, New Haven: Yale University Press, 1938, pp 346-366. 41. PAUL, J.: Cell Biology, chaps 9, 10, London: Heinemann, 1965, pp 132-153. 42. WADDINGTON, C.H.: Principles of Embryology, chaps 1, 10, 15, 20, London: Allen and Unwin, 1956, pp 3-28, 173-222, 329347, 415-468. 43. TONGE, C.H.: The Development and Arrangement of the Dental Follicle, Trans Eur Orth Soc 39:1-9, 1963. Downloaded from jdr.sagepub.com at PENNSYLVANIA STATE UNIV on March 4, 2014 For personal use only. No other uses without permission.