Paper - The nerve as a formative influence in the development of taste-buds (1920)
Olmsted JMD. The nerve as a formative influence in the development of taste-buds. (1920) J Comp. Neurol. 465- Template:Historic disclaimer
The Nerve As A Formative Influence In The Development Of Taste-Buds
J. M. D. Olmsted
Department of Physiology and Physiological Chemistry, College of Medicine, University of Illinois, Chicago, Illinois
- From the Department of Physiology and Physiological Chemistry, College of Medicine, University of Illinois, Chicago, Illinois.
The influence of one organ upon the development of another is a fundamental problem in morphogenesis. Embryologists have rather taken for granted that the differentiation of specialized organs, such as the transformation of epithelial cells into taste-buds, is due to the growth of the appropriate nerve into the region concerned. Hermann ('84), who first described the development of taste-buds in the dog, seems toholdthis view, though he states that one sees the embryonic nerve beneath the germinative layer of the epidermis after the dermal papilla appears. The nerve then passes up to the forming taste-bud, and finally the characteristic spindle-shaped taste-cells become differentiated.
Marchand ('02), who studied the developing papillae in the human foetus, states: "Vers le cinquieme mois, certaines cellules de la couche generatrice commencent alors a se differencier pour donner naissance aux borgeous gustatifs. Les nerfs gustatifs qui commandent la differentiation sont arrives au contact de Perithelium."
Landacre ('07), in his paper on the place of origin and distribution of taste-buds in Amiurus melas, says, in regard to the question whether the taste-buds appear fortuitously and are later connected with their gustatory nerves or whether the nerve fibers take the initiative and produce a bud on the surface, that the evidence is much more in accord with the latter view. His best proof is that the smaller subdivisions of the groups of tastebuds are determined by the number of nerves supplying these subdivisions, and that buds and nerves appear practically simultaneously. "The assumption . . . that the appearance of the taste-bud indicates the time at which the nerve supplying it reaches the surface needs verification for taste-buds in Amiurus."
There are two cases in which it seems to have been proved that differentiation of sense organs is dependent upon the nerve, namely, the formation of the tactile corpuscles of Merkel (Szymonowicz, '95) and of Grandry's and Herbst's corpuscles (Szymonowicz, '96).
The growth of such organs as teeth, however, is claimed to be absolutely independent of the nervous system (Moral and Hoseman, '19). But the nerve does exert a regulating influence, either increasing or decreasing the rate of growth, or causing changes in color of the tooth.
In another paper (to appear shortly) I have described the degeneration of taste-buds which occurs after severing the branches of the seventh cranial nerve leading to the barbels of the catfish, Amiurus nebulosus, and also the reappearance of taste-buds directly attendant upon the regeneration of the nerve. The present paper affords additional evidence that the presence of the nerve is the formative influence in the development of taste-buds.
Materials and Methods
When the end of a barbel (0.5 to 1 cm.) of Amiurus is cut off, sufficient regeneration takes place under normal circumstances to become evident to the eye at the end of two weeks. The regenerated portion appears as a colorless finger-like projection, having less than half the diameter of the stump from which it springs. "When prepared withMallory's phosphotungstic haematoxylin, according to the directions given on page 369 of Mallory and Wright's " Pathological Technique," the cartilage, pigment cells, and connective tissue stain a brilliant red ; the nuclei of epidermal cells and of the nervous tissue stain a brilliant blue; while the nerve fibrils and cytoplasm of the epidermis, especially the cytoplasm of the sense cells of the taste-buds, take on a characteristic lilac hue.
Such preparations show that regeneration is more rapid in the region near the old stump of cartilage. It is rapid growth in this region that causes the finger-like appearance of the new part.
A column of large hyaline cells extends from the old cartilage nearly to the basement membrane of the epidermis at the very tip of the new portion of the barbel. In the younger specimen with a regenerated end, i.e., 2 to 3 mm. in length, these precartilage cells stain a light blue, but in later stages of regeneration they take the typical brilliant red of the old cartilage. These cells are readily distinguishable by their form and staining properties. Along the anterior border of this column of precartilage is always seen, even in the shortest regenerated pieces, a small amount of fibrous material which stains the characteristic lilac hue, and which when traced to its origin is always found to be continuous with the old nerve trunk. Certain sagittal sections bring out this relationship most favorably in a single section, and the connection can be readily traced in a series of transverse crosssections. These fibers extend in bundles between the rod of precartilage and the germinative layer of the epidermis throughout practically the whole length of the regenerated tip of any barbel.
When the regenerated end of a barbel is less than 2 or 3 mm. in length, the germinative layer of the epidermis extends in a smooth unbroken sheet around the entire new end. Both transverse and sagittal sections show this unbroken line, and yet the nerve extends practically throughout the length of the new piece. But when a length of 3 to 4 mm. is reached, one can see several indentations in the germinative layer. These appear first in the region near the junction between the old and new tissue, and particularly along the anterior border of the new nerve. These indentations are the beginnings of the dermal papillae, the invariable forerunners of the taste-buds. Each papilla is filled with a small bundle of nerve fibers which stands out from the nerve trunk like a small button, almost as if they had exerted such force in their growth out from the nerve that they had indented the germinative layer at that spot.
Later stages of regeneration showed the presence of fully developed taste-buds along the whole length of the regenerated end, mainly concentrated, however, along the edge nearest the nerve. The development of mature taste-buds after the formation of the dermal papillae is to be described in a later paper.
It is evident, therefore, that the growth of the nerve into the appropriate region precedes the appearance of taste-buds, and that the formation of dermal papillae, the immediate forerunners of the taste-buds, is most intimately connected with the growth into it of the particular branch of the nerve trunk which is to innervate it.
- The nerve and cartilage in all stages of regenerating ends of barbels of the catfish, Amiurus nebulosus, extend practically the complete distance from the old stump to the basement membrane of the epidermis at the very tip.
- Short regenerated pieces, though possessing cartilage and nerve, show no trace of taste-buds.
- The formation of dermal papillae, the invariable forerunners of taste-buds, takes place at the base of longer regenerated pieces as if the germinative layer of the epidermis were indented by the growth into it of a small branch from the nerve trunk.
- Since taste-buds degenerate in a barbel whose nerve is cut and reappear when the nerve regenerates, and since the nerve appears in the appropriate region before there is any evidence of a developing taste-bud, the presence of the nerve may be said to be the causative factor in the formation of taste-buds.
Hermann, F. 1884 Beitrag zur Entwicklungsgeschichte des Geschmacksorgans beim Kaninchen. Arch. f. mikr. Anat., Bd. 24, S. 216-229.
Land acre, F. L. 1907 On the place of origin and method of destribution of tastebuds in Amiurus melas. Jour. Comp. Neur., vol. 17, pp. 1-67.
Mallory, F. B., and Wright, J. H. 1915 Pathological Technique. Phila. A) pp.
Marchand, M. L. 1902 Developpement des papilles gustatives chez de foetus humain. Cont. Rend. Soc. Biol. Paris, T. 54, pp. 910 912.
Moral, II., dnd Hoseman, (1. 1919 Uber den Einflusa der Nerven auf das Wachstum der Zahne. Anal. Hefte, Bd. 57, S. 201-250.
Szymonowicz, W. 1895 Beitrage zur Kenntniss der Nervenendigungen in Hautgebilden. Arch. f. mikr. Anat., Bd. 15, S. 624 654. 1896 I Clicr lien l',:ni mid die Knt wickelung der Nervenendigungen in Entenschnabel. [bid., Bd. 48, S. 329-358.
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