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Investigations on the Regional Determination of the Central Nervous System

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Investigations on the Regional Determination of the Central Nervous System INVESTIGATIONS ON THE REGIONAL DETERMINATION OF THE CENTRAL NERVOUS SYSTEM BY P. D. NIEUWKOOP From the Zoological Laboratory of the State University, Utrecht (Received 3 May 1946) (With Seventeen Text-figures) INTRODUCTION Among the experiments to elucidate the origin of the germ cells in the Urodeles (Nieuwkoop, 1946), one experimental series was investigated, in which the dorsal blastoporal lip of one embryo was transplanted to the presumptive ventral lip of another (cf. Spemann, 1918, 1931a). In order to investigate the development of the germ cells, experimental animals must be reared to an age at which the germ cells are localized in the germ ridges, and show definite differentiation; in the present case, therefore, they have been allowed to develop until they reached an age of about 4 weeks, and all their yolk had been absorbed, which corresponds to about stage 43 (Glaesner). At this stage all the tissues showed complete differentiation. Most of the embryos could not be reared longer, as they could not take food in consequence of abnormalities in head and trunk (mouth, intestinal tube and anus). In various experiments by other authors, almost all preparations have been fixed at a very early developmental stage (tail-bud stages) in order to prevent mortality. My own experiments demonstrate that this mortality must be ascribed almost completely to extraneous infection. With an accurate sterile working method (described by Woerdeman, 1930), the mortality can be reduced to nil if the egg material is good. The primary as well as the secondary embryonic rudiments of these duplicitas showed well-differentiated nervous systems. Their structure, especially that of the secondary rudiments, was very interesting (they varied between a complete nervous system and a small fragment of the spinal cord only). The analysis of the structure of these incomplete nervous systems forms the subject of this paper. RELATIVE POSITION OF PRIMARY AND SECONDARY EMBRYONIC RUDIMENTS (a) Method of transplantation Early gastrulae of Triturus taeniatus were used. The dorsal blastoporal lip was isolated as follows. Two sagittal cuts were made along meridians of the egg, to the right and left sides of the dorsal median line, from about the animal border of the marginal zone up the blastoporal margin. Then a transverse cut was made along the JEB.24, I & 2 10 146 P. D. NlEUWKOOP animal border of the marginal zone, and the graft was bent outwards. Attached vegetative blastomeres, recognizable by their light colour, were removed from the inner side, after which the graft was completely isolated by a fourth cut along the blastoporal margin (cf. Fig. 1 a). The same operation was performed in the host, but on the opposite, ventral, side of the marginal zone. The graft was placed in the wound field in a normal orientation, viz. with its vegetative border against the vegetative field of the host and its median line coinciding with the ventral meridian of the host (cf. Fig. 1 b). d. Fig. 1. Diagram of transplantation of dorsal blastoporal lip of early gastrula (a) in the place of ventral blastoporal lip of early gastrula (b). d. dorsal; v. ventral; veg.f. vegetative field. (b) Differences in the character of the graft An accurate determination of the stage of operation was not of much importance for the original purpose of this transplantation experiment. The operation was, therefore, performed on embryos, ranging from very early (first indication of the dorsal blastoporal lip) to middle (horseshoe-shaped blastopore) gastrula stages. In the first case the graft consisted of presumptive notochord, prechordal plate and perhaps small parts of the cephalic entoderm. In the second case, however, in which external and any already invaginated marginal zone were transplanted together, cephalic entoderm and prechordal plate cell material probably formed no part of the graft. It is therefore clear that the character of the graft varied in individual cases. Unfortunately, individual data are not available. In a number of cases the graft had been reduced in size by loss of blastomeres, probably owing to damage during the operation. In some cases, therefore, only a small part of the original graft remained, and later invaginated. (c) Description of the early development of experimental animals* The first effect of the operation was a marked elongation of the embryo. In comparison with a control which showed a similar deformation after removal of the yolk membrane, elongation was much greater in the experimental animals. These • In this second series in which the embryos are early fixed, T. alpestris was used. Regional determination of the central nervous system 147 became pear-shaped, the blastopore being situated on the stalk. Two points of invagination were present, giving rise to two archenteron roofs and two neural plates (Fig. 2a, b). In many cases the secondary neural plate was smaller—shorter and narrower—than the primary one. Both became visible, however, at the same moment. In the embryos examined, I could find only one archenteron, viz. in the primary embryonic rudiment. pr.embr.r. (a) sec.embr.r. pr.arch.r. sec.arch.r. Fig. 2. Duplicitas larva, T. alpestris 254 at early neurula stage. (a)External view. (6) Medial section (left half). Originally most caudal parts of entoderm stained before operation (dark dotted). Enlarge- ment + 40 X . B. blastopore; pr. and sec.arch.r. primary and secondary archenteron roof; pr. and sec.embr.r. primary and secondary embryonic rudiment. The two embryonic rudiments were situated exactly opposite each other in T. alpestris 254 (Fig. 2 a, b) and 132 (Fig. 3). In Fig. 3 a, b the notochord and spinal cord of the primary and of the secondary embryo remained separated throughout their lengths. The entoderm mass, on the other hand, was situated chiefly in the anterior part of the trunk. Only a very thin column of entodermal cells was present in the middle trunk region, whereas the caudal part of the trunk was completely free of entoderm. The secondary embryonic rudiment, being shorter than the primary one, was microcephalic. The external form of the duplicitas differed very much from 148 P. D. NlEUWKOOP that of controls of the same age. In T. alpestris 141 (Fig. 4a) the secondary neural plate was much smaller than the primary one. It was situated somewhat to the right of the ventral median line. In the older embryo (Fig. 46) this secondary rudiment had been displaced far to the lateral and even to the dorsal side. The caudal part of its spinal cord was united with the primary cord. The external form of the embryo was, in contradistinction to T. alpestris 132 (Fig. 3), scarcely different from a normal embryo of the same age. pr.embr.r. (a) sec.embr.r. Fig. 3. Duplicitas larva, T. alpestris 132 at tail-bud stage, (a) External view (embryo attached to cellophane membrane), (b) Medial section through primary and secondary rudiments (most caudal entoderm stained as in T. alpestris 254); separate primary and secondary notochords, neural tubes and tail-buds. Enlargement ± 30 x . Abbreviations as in Fig. 2. (d) General remarks The object of all the operations was to obtain two embryonic rudiments, similarly directed and situated exactly opposite each other. The first requirement was fulfilled in all cases, the direction of gastrulation of primary and secondary rudiment being the same and extending from the vegetative to the animal side. In respect to the second requirement the individual cases diverged greatly. It is of interest to con- sider the causes of this variability. Sources of errors in the orientation of the graft (1) In early gastrulae the dorsal median line is difficult to determine. Theoreti- cally, it runs through the middle of the dorsal blastoporal lip. Considerable deviations could be observed, however, in individual eggs. Regional determination of the central nervous system 149 (2) The graft was intended to consist of the median part of the dorsal blastoporal lip. Small deviations to the right and left could, however, not be avoided. (3) The wound field was not always exactly opposite the dorsal median line. Here the same errors as in (1) may be expected. (4) Finally, in the greater number of cases, the orientation of the graft did not entirely coincide with that of the host. The direction of invagination often showed small lateral deviations. (a) pr.embr.r. sec.embr.r. sec.embr.r. pr.embr.r. B. Fig. 4. Duplicitas larva, T. alpestris 141. (a) External view of primary and secondary neural plates; asymmetrical, lateroventral position of secondary neural plate. (6) External view of normal primary and irregular rudimentary secondary rudiment at tail-bud stage; lateral to dorsolateral position of secondary rudiment (most caudal entoderm stained as in T. alpestris 254). Enlargement (a) + 35 x, (6) + 20 x. Abbreviations as in Fig. 2. Significance of these deviations in the final position of the graft The external displacements and those which occur during the first phase of the invagination take place along the meridians (Vogt, 19296; Nieuwkoop, 1946); existing deviations do not increase during this period. After passing the blastoporal lip, however, movements of dorsal convergence arise in the primary and secondary embryonic rudiments. In a normal embryo they extend over the whole of the mesoderm (and ectoderm), except in its medioventral region, where the attractive forces from the right and left sides counterbalance each other. On the left or the right side, the lateral and ventral mesoderm and ectoderm are under the influence of one attractive centre only, viz. the corresponding half of the axial system of the embryo. The greater the distance of a point from the axial system, the weaker is the action of the dorsal median line, andthe later its action begins (Vogt, 19296; Yamada, 1938).
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