563

J. Anat. (1977), 123, 3, pp. 563-577 With 15 figures Printed in Great Britain

The early innervation of the developing deciduous teeth* ANTHONY A. PEARSON

Department of Anatomy, School of Medicine, University of Oregon Health Sciences Center, Portland, Oregon 97201

(Accepted 27 April 1976) INTRODUCTION

There is still much speculation about the initial innervation of developing teeth, and the factors concerned. Routine histological stains do not usually show the ultimate destination of individual nerve fibres and this has led to uncertainty as to when a particular tooth first receives its innervation. Since there is no evidence that nerve fibres or their endings enter the epithelium of the dental (enamel) organ, the problem is to determine when nerve fibres penetrate the dental papilla and the dental sac, or enter the mesenchyme which contributes to the formation of these structures. The present study is concerned with the ingrowth of nerve fibres into tooth-bearing areas of the mouth in human embryos and fetuses. MATERIALS AND METHODS

This study is based on serial sections of human embryos and fetuses stained for nerve fibres by the protargol method of Bodian (1936) and the silver gelatin method of Pearson & Whitlock (1949). This study also includes observations on the collection of human embryos in the Carnegie Embryological Laboratories at the University of California in Davis. The ages of the embryos are calculated from the time-table of human development formulated by Streeter (1951) and summarized by Davies (1963). OBSERVATIONS

Embryos of 5 and 6 weeks Before there is histological evidence of tooth development the maxillary nerve has grown into the maxillary process and the inferior alveolar nerve into the mandibular process. This can be demonstrated in human embryos of about 5 weeks (Fig. 1). At this stage there are slight thickenings of the ectodermal epithelium lining the front part of the oral cavity: in older embryos the epithelial thickenings are more pronounced in areas where the alveolar arches will develop. These thickened areas of the epithelium are called the 'primary epithelial bands' (Gaunt, Osborn & Ten Cate, 1967). The course of the maxillary nerves closely parallels these epithelial bands in the upper jaw and the inferior alveolar nerves have a similar relation in the lower jaw. As these epithelial bands thicken they push deeper into the underlying mesenchyme. * Supported by U.S.P.H.S. Research Grant HD-07277 from the National Institute for Child Health and Human Development.

564

ANTHONY A. PEARSON

Fig. 1. A drawing of a frontal section of the head region of a 10 mm human embryo about 33-35 days ± 1 of age. Bodian method. x 30. Abbreviations for the figures are given on p. 577.

Fig. 2. A drawing of a frontal section of a 19 mm human embryo almost 6 weeks of age showing the rostral portion of the superior dental lamina. Bodian method. x 35.

Innervation of developing teeth

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Fig. 3. A drawing of a frontal section of the same 19 mm human embryo (Fig. 2) showing the relation of the anterior superior alveolar nerves to the superior dental lamina. Bodian method. x 35.

Two parallel epithelial ridges are formed: the one on the buccal side is the vestibular, or labial lamina, while that on the lingual side is the dental lamina which gives rise to the tooth buds (Figs. 2-6). The thickened epithelia forming the dental laminae in the roof and floor of the front of the oral cavity first appear in the regions where incisor and canine tooth buds will develop. Subsequently, the thickening process which forms the dental laminae extends caudad into the molar tooth-bearing areas. The formation of the dental laminae in the lower jaw appears to be slightly more advanced than that in the upper jaw. The thickenings which will give rise to the incisor tooth buds appear to be slightly better developed than those in the canine regions. However, when the tooth buds have definitely begun to form, the canine tooth buds appear to be somewhat more advanced. The thickened epithelium constituting the dental laminae extends to the midline and the dental laminae of the two sides become united (Figs. 2, 4). This coalescence was described by Nery, Kraus & Croup (1970). The dental laminae are well shown in human embryos of about 6 weeks of age (19-23 mm crown-rump length). At this time a branch of the inferior alveolar nerve can be seen penetrating the mesenchyme adjacent to the dental lamina of the lower jaw. This branch is the incisive nerve, and its fibres leave the inferior alveolar nerve in the region adjoining that portion of the dental lamina where the canine tooth bud

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ANTHONY A. PEARSON

Fig. 4. A drawing of a frontal section of the same 19 mm human embryo showing the rostral portion of the inferior dental lamina. Bodian method. x 35.

will develop. The continuation of the inferior alveolar nerve beyond this point of branching is the mental nerve. The main components of the trigeminal nerve can be demonstrated easily in sagittal sections of human embryos as early as 5 weeks. The course of the maxillary and the inferior alveolar nerves is prominent and the main sensory components of the trigeminal nerve within the brain stem can be demonstrated. Thus the mesencephalic root of V can be seen extending into the mesencephalon, while other root fibres pass to the main sensory nucleus of V, and the descending root extends into the medulla oblongata. Certain aspects of the developing dental lamina are well shown in the sixth week of human development (Figs. 2-6). In the sections of a 19 mm CR human embryo cut in the frontal plane, the rostral portion of the superior dental lamina is shown as a thickened part of the oral epithelium in the centre of the roof of the mouth (Fig. 2). A groove (G) or a thinning of the epithelium indicates the margins of the dental lamina. The superior dental laminae are now fused and extend across the midplane. The epithelium in the floor of the mouth is somewhat thickened but the inferior dental lamina is not included in the section shown in Figure 2. It is in this thickened

Innervation of developing teeth

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Fig. 5. A drawing of a frontal section of the same 19 mm human embryo showing the relation of the incisive nerves to the inferior dental lamina. Bodian method. x 35.

epithelium of the superior dental lamina that the upper incisor tooth buds will develop. However, the individual tooth buds of the upper incisor teeth could not be recognized in this embryo. In slightly older embryos, thickened portions of the superior dental lamina indicate the regions where the primordia of the lateral and medial incisor tooth buds will develop. A medial branch of the anterior superior alveolar nerve distributes its fibres to the thickened mesenchyme which is closely adjacent to this part of the dental lamina. These fibres fan out in the mesenchyme adjacent to that part of the dental lamina where the primordia of the upper incisor tooth buds will develop (Figs. 2, 3 and 10). This branch corresponds to the incisive nerve in the lower jaw. The thickened oral epithelium in the front of the lower jaw shown in Figure 4 is the rostral portion of the inferior dental lamina. The further localized thickenings in this rostral portion of the inferior dental lamina indicate the positions of the primordia of the lower incisor tooth buds, but again the individual tooth buds are not sharply defined (Figs. 4, 5). A branch of the inferior alveolar nerve, the incisive nerve, distributes its fibres to the thickened mesenchyme adjacent to this medial part of the inferior dental lamina (Figs. 5, 11 and 12). The nerve fans out into the mesenchyme,

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Fig. 6. A drawing of a frontal section of the same 19 mm human embryo showing the anterior and posterior superior alveolar nerves. The section was cut in a slightly oblique plane and the right side of the section is slightly anterior to the left side. Bodian method. x 35.

but it has not yet divided into separate branches for the two incisor tooth buds. The portion of the inferior dental lamina shown on the right side of Figure 4 includes the anlagen of the two inferior incisor tooth germs on that side. The thickened portion of the inferior dental lamina near the midline on the left side is in the region where the lower medial incisor tooth bud will develop. The primordium of the lower lateral incisor tooth bud is not included in the left side of this section. Fibres of the incisive nerves of the two sides extend close to the midline; however, they were not observed to cross the midline as they occasionally do in the adult (Durward, 1964). When such a crossing is present it probably dates from an early stage in development. At about the level where the upper canine tooth bud will develop (Fig. 6, right) the maxillary nerve gives off a branch, the anterior superior alveolar nerve. This nerve in turn gives off a smaller branch to the thickened mesenchyme adjacent to the superior dental lamina where the canine tooth bud will develop. The remainder of the superior alveolar nerve continues forward and medially to be distributed to the mesenchyme adjacent to the dental lamina where the- primordia of the incisor tooth buds will develop. Caudal to the level of the primordium of the canine tooth bud, the maxillary nerve gives off the posterior superior alveolar branches which distribute fibres to the mesenchyme adjacent to the caudal portion of the superior dental lamina (Fig. 6, left). On this side there is a middle superior alveolar nerve which supplies the mesenchyme adjacent to that portion of the dental lamina lying between the areas supplied by the anterior and posterior superior alveolar nerves. All three superior alveolar nerves contribute to a plexus of nerves closely associated with the thickened mesenchyme adjacent to the superior dental lamina. Branches extend

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medially and laterally as well as rostrally and caudally. The general plan of the superior dental plexus has begun to take form by the time the human embryo is 6 weeks of age. The caudal portions of the superior dental laminae are not as well developed as the more rostral portions, and the sites where the individual molar tooth buds will develop could not be recognized with any certainty in human embryos of less than 20 mm CR length. The inferior alveolar nerve gives off several small branches to the thickened mesenchyme lying adjacent to that portion of the dental lamina which lies caudal to the developing incisor teeth. The most rostral of these branches is given off from the inferior alveolar nerve in the region where it divides into its terminal branches, namely, the incisive and the mental nerves. This may be a separate branch, or it may be a branch of the incisive nerve. It is distributed to the mesenchyme adjacent to that portion of the dental lamina where the canine tooth bud will develop. Branches caudal to this go to the region where the molar tooth buds will develop (Fig. 6). The exact number of these small branches is difficult to determine at this age. In human embryos, in the latter part of the sixth week (23 mm CR length), the dental laminae show further signs of development. The caudal portion of each dental lamina is well shown in sagittal sections, where it appears like a ledge or a shelf of 36

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Fig. 8. A drawing from sagittal sections of the same 23 mm human embryo closer to the median plane. Bodian method. x 61.

epithelium. In an embryo cut in a favourable plane, a major portion of the course and distribution of the superior alveolar nerves can be demonstrated in a few sections (Fig. 7). The posterior superior alveolar nerve is formed by several branches which contribute to the caudal portion of the superior dental plexus. This plexus lies close to the thickened mesenchyme adjacent to the superior dental lamina. A middle superior alveolar nerve could be recognized on both sides of some embryos as a small branch of the maxillary nerve. The anterior superior alveolar nerve (Fig. 8) is a large bundle of fibres whose branches are distributed to the rostral portion of the developing superior dental plexus. This plexus is made up of a few small bundles of fibres which lie close to the mesenchyme adjacent to the rostral and medial portions of the superior dental lamina. Regional enlargements of the dental lamina indicate the positions of the developing tooth buds of the upper canine and incisor teeth. However, in sagittal sections their individual identities are more difficult to determine. The inferior alveolar nerve (Fig. 8) divides into its terminal branches, the incisive nerve and the mental nerve, in the region just caudal to the developing canine tooth bud. The incisive nerve can be followed rostrally and medially close to the thickened mesenchyme adjacent to the developing tooth buds of the lower canine and incisor

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teeth. The incisive nerve has divided into a branch to the mesenchyme related to the canine tooth bud and a branch which is distributed to the mesenchyme adjacent to the region of the developing incisor tooth buds. Branches of the inferior alveolar nerve caudal to its division into its terminal branches are small and more difficult to follow. They are lost in the mesenchyme adjacent to the caudal portion of the inferior dental lamina.

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The early innervation of the developing deciduous teeth.

563 J. Anat. (1977), 123, 3, pp. 563-577 With 15 figures Printed in Great Britain The early innervation of the developing deciduous teeth* ANTHONY A...
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