A Note on the Morphology of the Hypophysis in the Gymnophione Schistomepum thomense
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1 Okajimas Fol. anat. Op., 46: , 1970 A Note on the Morphology of the Hypophysis in the Gymnophione Schistomepum thomense By Hartwig Kuhlenbeck (Laboratory of Morphologic Brain Research, Prof. Dr. H. Kuhlenbeck, Woman's Medical College of Pennsylvania) Our recent communication on the morphology of the forebrain in Gymnophiona (Kuhlenbeck, M a I e w i t z and Beasley, 1966) dealt only with the significance of the topologically relevant fundamental longitudinal cell zones in telencephalon and diencephalon. Because some of our illustrations included the location of the hypophysis, we added a short reference to this structure, of which one component represents a hypothalamic neuraxial derivative. Yet, since both the subject matter of our presentation and the space available for our paper precluded any discussion of extraneous details, our reference had to remain necessarily sketchy. We merely stated that, adjacent to the parainfundibular part of the hypothalamus, the neurohypophysis with an anterior infundibular portion and a more posterior part may be recognized. The caudalward extension of the adenohypophysis to the base of the rhombencephalon was also mentioned. Moreover, those of our illustrations which adventitiously included outlines of the hypophysis (figs. 2, 5, 6, 1. c.), did not represent planes suitable for a visualization of the rather narrow caudal portion of neurohypophysis. However, seeing that relatively few data on the Caecilian hypophysis have been reported in the literature (S t end el 1, 1941 ; Laubmann, 1926; Pillay, 1957; Pasteels and Herlant, 1962 ; Wing s t r an d, 1966), it seemed therefore appropriate to add, while proceeding with further studies of the Gymnophione brain (K uhlenbec k, 1969), a few comments concerning our incidental observation on the configuration of the pituitary gland in this morphologically highly interesting vertebrate form. * Supported by U.S. N. I. H. Grant NB
2 308 H. Kuhlenbeck Gymnophiona (Coecilia, Caecilia, Apoda) are relatively rare, limbless, worm-like, burrowing tropical and subtropical amphibians with rudimentary tail and generally greatly reduced eyes. These animals, characteristically called in German, can be said to comprise the least known of the three extant orders pertaining to the class Amphibia. Until recently, no information concerning apodan fossil representatives was available, but two extinct species have now been reported, namely Ichthyophis muelleri Brunner (fragment of mandible, Riss-Wiirm IG-period, Pleistocene, Oberfranken, Germany), and Prohypogeophis tunariensis Marcus (two fairly large fragments from the Carboniferous, Bolivia). Relevant biological data on Gymnophiona have been concisely summarized by Noble (1931, 1954), and a detailed up-to-date taxonomic review concerning the Caecilians of the world was published by Taylor (1968). In 1913, only 19 genera, with 55 species, all included in a single family (Caeciliidae), were known. Taylor (1. c.) lists at present somewhat more than 160 species, distributed upon 34 genera and 3 families (Ichthyophiidae, Typhlonectidae, Caeciliidae). Our conclusion (K. et al., 1966) that the three extant recent orders of Amphibia, although easily comparable, show three conspicuously different transformations of the topologically invariant set of brain configurations, likewise seems applicable to an evaluation of the pituitary morphology in that class (Figure la-c). Competent students of phylogeny have justly expressed the opinion that origin and affinities of Dipnoi are still obscure (J a r v i k, 1968). Nevertheless, it can easily be seen that certain configurational similarities of lungfish brains (K u h 1 e n b e c k, 1929 ; G e r l a c h, 1933) with those of amphibians, notably urodeles, also include similarities displayed by morphologic features of the hypophysis (Figure 1, d). As regards its general morphology, the amphibian hypophysis can be easily compared with that of Amniota. It consists of the well-known two main subdivisions with essentially different origin, namely of adenohypophysis (lobus buccalis, lobus glandularis) and of neurohypophysis (lobus nervosus). The anlage of the adenohypophysis originates from the ectoderm of the stomodaeum by the infolding of an epithelial pocket known as Rathke's pouch. The neurohypophysis, on the other hand, develops as a derivative of the neuraxis, within the posterior inferior part of the hypothalamus, that is, from a neighborhood of hypothalamic floor caudal to the ridge of optic chiasma.
3 A note on the morphology of the hypophysis 309 Fig. 1. Median sections of the pituitary in amphibians and in a dipnoan. a: Bufo (anuran) ; b: Amblystoma (urodele); C: Hypogeophis (gymnophione); d: Protopterus (dipnoan); 1: saccus infundibuli ; 2: infundibular process (neurohypophysis) ; 3: pars intermedia (adenohypophysis); 4: median eminence (neurohypophysis) ; 5: zona tuberalis' (adenohypophysis); 6: portal vessels. Infundibular process, black ; eminentia medialis, vertical hatching ; infundibular stem, unmarked between 4 and 2; zona tuberalis ', crosses ; pars intermedia, stippled. From W i n g s t r an d, 1966 ; a, b and d are originals of that author, while c, redrawn after St e n d e 11, 1914, represents W i n g s t r an d's interpretation of S tendel diagram. The adenohypophysis differentiates further into pars distalis, pars intermedia, and pars tuberalis ( zona tuberalis '). Rathke's pouch may develop as an epithelial bud, which remains compact, or can display a lumen. This latter can either disappear or remain as a hypophysial cleft in the adult gland. The pars intermedia, contiguous with the distal portion (infundibular process) of the neurohypophysis, tends to be located dorsocaudally to, or even around the cleft, which, if present, represents the residual lumen of Rathke's pouch. The pars tuberalis may form more or less conspicuous paired outgrowths from the rostral portion of adenohypophysial anlage and is usually in close contact with the median eminence of neurohypophysis. Pars distalis constitutes the main portion. The neurohypophysis, again, displays the following three parts : median eminence, infundibular stem, and infundibular lobe. The median eminence (eminentia mediana) is that part of the neuro-
4 310 H. Kuhlenbeck hypophysis which is directly continuous with the non-hypophysial nervous parenchyma of the hypothalamus caudally or, respectively, caudo-basally to the chiasmatic ridge. In many Am niota, the median eminence forms a bulge on the brain surface, and is separated from the hypothalamus sensu stricto by a shallow groove (sulcus tuberoinfundibularis of Spat z, D i e p e n and Gaup p, 1948 ; sulcus hypophysio-hypothalamicus of K u h 1 e n b e c k and Ha y m a k e r, 1949, and of Kuhlenbeck, 1954). In some Amniota, including man, the eminentia medialis represents a more or less complete ring surrounding the entrance into the stalk made up by the infundibular stem. In a number of vertebrate forms, however, the eminentia medialis is restricted to the rostro-basal neighborhood of the proximal neurohypophysial complex. The infundibular stem is an often somewhat indistinctly delimited portion, which provides a stalk-like connection between eminentia medialis and infundibular process. This latter, also known as the neural lobe in the narrower sense, is the most distal part of the neurohypophysis. A vascular plexus (mantle plexus) between neurohypophysis and adenohypophysis, which is present in cyclostomes, selachians and osteichthyes, may, in various gnathostome fishes, display an arrangement characterized by a hypophysio-portal circulation. More or less distinctly differentiated hypophysio-portal vessels occur in amphibians and dipnoans. This portal system is still more complex in Amniota. Generally speaking, the primary net of the hypophysio-portal system seems to be located in the eminentia medialis, and the flow in the portal vessels is assumed to be directed toward the adenohypophysis. A portal circulation of this type appears to be a rather constant feature of vertebrates, establishing a link between neuraxis, of which the neurohypophysis is a part, and the adenohypophysis (cf. also Green, 1966). Since the present communication deals exclusively with some morphologic aspects of configuration, that is, with form in contradistinction to texture or structure, further comments or remarks on cytological, histological and functional details can be omitted. The relevant findings concerning these topics have been recently compiled, with respect to the entire vertebrate phylum, in three volumes of a publication on the pituitary edited by Harris and Donovan (1966). As seen in our material of the African Gymnophione Schisto-
5 A note on the morphology of the hypophysis 311 mepum thomense (family Caeciliidae), the Caecilian hypophysis displays, in regard to its anatomical components, the following subdivisions and form-relationships (Figures 2-5). Fig. 2. Semidiagrammatic midsagittal (A) and transverse (B) sections through the pituitary complex of Schistomepum thomense. 1-3: neurohypophysis ; 4-6 : adenohypophysis ; 1: eminentia medialis ; 2: infundibular stem ; 3: infundibular process ; 4: pars tuberalis ; 5: pars distalis ; 6: pars intermedia ; 7: ridge of supra- and postoptic commissures ( chiasmatic ridge ') ; 8: caudal portion of hypothalamic wall basal to mammillary region ; f: region of infundibular stem forming roof of hypothalamic infundibular recess ; p: hypophysio-portal system. The arrow points at sulcus hypophysio-hypothalamicus internus. Since the boundaries of the three subdivisions of adenohypophysis were indistinct in our material, only their location qua neighborhoods is indicated. The neurohypophysis consists of a median eminence, a very thin, membraneous infundibular stem, and a caudal infundibular lobe (infundibular process, ' neural lobe' sensu strictiori), contiguous with, and dorsally to, the caudal end of adenohypophysis. The median eminence appears in sagittal sections as a slight ventricular prominence of the ventricular floor in the posterior inferior part of the hypothalamus. It is caudally adjacent to the bulky ridge of supraoptic and allied commissures (' chiasmatic ridge '). A. transverse ventricular sulcus, which could be termed sulcus hypo-
6 312 H. Kuhlenbeck physio-hypothalamicus internus in analogy with the external sulcus mentioned above as described in man and other forms, approximately delimits eminentia medialis from hypothalamus proper (Figures 2-4). A rather shallow more caudal parallel accessory sulcus or depression within the median eminence may be faintly indicated in the midsagittal neighborhood (Figure 4). Scattered incidental observations which I made in the course of other studies on embryonic and adult amniote material seem to suggest that an internal (ventricular) hypophysio-hypothalamic sulcus may also occur, either as a transitory ontogenetic feature or as a persistent groove, in at least some higher vertebrates. The nucleated bodies of the cellular elements in the eminentia medialis of Schistomepum constitute a densely packed juxtaventricular layer, which is more compact and less wide than the periventricular cell layer of the rostrally adjoining hypothalamic neighborhood, and, together with the ventricular floor, tapers out caudalward toward the transition to infundibular stem. Externally to this juxtaventricular layer there is a vascular plexus, which extends into leptomeninx and rostral part of adenohypophysis and presumably represents the hypophysio-portal system, (Figures 2-4). Our material, processed for form-analytic investigations, and the purpose of our studies on the Caecilian neuraxis precluded further observations on structural or cytologic details concerning the portal vascular system and requiring a variety of different techniques. The infundibular stem is a conspicuously elongated membranous structure consisting of flattened neuroepithelial (ependymal) cells. It connects the infundibular lobe with hypothalamus dorsally, and with eminentia medialis basally. From infundibular lobe to level of eminentia medialis, the infundibular stem appears as a very thinwalled duct with collapsed lumen, located on the dorsal surface of adenohypophysis. The basal wall portion of this duct is continuous with the tapering caudal end of eminentia medialis, the transition being rather well demarcated. The dorsal wall portion of the duct flares out as a membrane forming the roof of the widening infundibular recess and attaches itself, with a sharp transition, to the thick hypothalamic wall basal to the mammillary region, which, in turn, lies basal to the neighborhood which we interpret as representing the rostral end of the deuterencephalic basal plate (K u h l e n b e c k et al., 1969, fig. 5). At this dorsal attachment, the flat neuroectodermal epithelium of infundibular stem is directly but abruptly
7 A note on the morphology of the hypophysis 313 continuous with the typical ependymal lining of hypothalamus. The infundibular lobe is a compact, roughly globular structure with vestiges of a partially obliterated residual lumen whose connection with that of infundibular stem is suggested by cellular traces (Figure 5), and could thus be described as a thick-walled pouch with collapsed lumen. It is located on the dorsal surface of the caudal end of adenohypophysis, in a pit-like median depression of this latter (Figure 2), and at transverse levels caudobasal to the prominent ventral rhombencephalic flexure (Figure 3). Since the transverse diameter of infundibular lobe is much shorter than that of the corresponding region of adenohypophysis, the caudal region of neurohypophysis represented by the infundibular lobe is not shown on most sagittal sections passing through the pituitary, with the exception of those which, in respect to the caudal hypophysial end, cut through the exact midline and its immediate vicinity (cf. Figure 3). Concerning the general structure of infundibular lobe, the cells which could be seen in our material comprised elements of glial, including pituicyte-like type, besides the cells resembling ependymal lining remnants. The adenohypophysis of Schistomepum can be described as a wedge-like cell plate whose dorsoventral thickness and transverse (right to left) width increase from rostral to caudal levels. In our specimens, its length measured approximately 1 mm, and its thickness from about 0.03 mm rostrally to circa 0.2 mm caudally. Its anterior width measured approximately 0.25 mm, while its caudal width expanded to about 1 mm, that is, roughly approximated the total length. At the rostral end of the adenohypophysis a pair of narrow, bar-like cell aggregations was noted bilaterally in close contiguity with the basal surface of eminentia medialis. These two strips of cells converge caudalward toward the rostral extremity of the main. glandular portion with which they seem to be continuous, but observations in different specimens suggest that one or both of these rostraiward protruding paired cell aggregates may also assume the aspect of detached individual structures. Although, as mentioned above, our material was not suited for detailed structural and cytologic studies, the well-known three subdivisions of the adenohypophysis could be roughly identified. Pars tuberalis or zona tuberalis located rostrally, is directly related to the hypophysio-portal system, and, moreover, includes the abovementioned protruding pair of bar- or tongue-like processes. Caudalward follows the main part or pars distalis, which constitutes the
8 314 H. Kuhlenbeck bulk of the adenohypophysis. At posterior levels of this latter, a region, contiguous with the infundibular process of neurohypophysis, corresponds to the pars intermedia. Clearly outlined cleft formations representing the residual lumen of Rathke's pouch could not be seen in our specimens. Summary The hypophysis of the African Gymnophione Schistomepum displays a configuration essentially corresponding to that obtaining in the very few (apparently only three) other species of Gymnophiones whose pituitary has been studied by previous authors. On the basis of these scant, but perhaps sufficiently suggestive data it can be presumed that the Gymnophione hypophysis, although easily comparable with that in the two other extant orders of Amphibia, represents a strikingly different transformation of a common, topologically invariant morphologic pattern. The characteristics of the Gymnophione pituitary seem to be the membranous structure of the long infundibular stem, the globular aspect of the relatively small infundibular lobe embedded in a median and dorsal pit provided by the caudal end of adenohypophysis, and the rather conspicuous flatness of this latter. The caudal extension of the hypophysial complex toward the base of the rhombencephalon in correlation with the pronounced ventrally directed flexure of that brain subdivision may likewise be considered to represent a Caecilian pattern-peculiarity. References G e r la c h, J.: Uber das Gehirn von Protopterus annectens. Ein Beitrag zur Marphologie des Dipnoerhirnes. Anat. Anz. 75 : (1933). G r e e n, J. D.: The comparative anatomy of the portal vascular system and of the innervation of the hypophysis. In : The Pituitary Gland, Ha r r i s, G. W. and D o n o v a n, B. T. eds., vol. 1, pp (Univ. of California Press, Berkeley 1966). H a r r i s, G. W. and D ono v a n, B. T., eds. : The Pituitary Gland. 3 vols. (Univ. of California Press, Berkeley 1966). Jar vi k, E.: Aspects of vertebrate phylogeny. Nobel Symposium 4. Current problems of lower vertebrate phylogeny, Orvig, T., ed., p (Almquist & Wiksell, Stockholm 1968). Kuhlenbec k, H.: Uber die Grundbestandteile des Zwischenhirnbauplans der Anamnier. Morphol. Jahrb. 63: (1929). : The human diencephalon. A summary of development, structure, function, and pathology (S. Karger, Basel 1954).
9 A note on the morphology of the hypophysis 315 : Observations on the rhombencephalon in the gymnophione Siphonops annulatus. (Abstract). Anat. Rec. 163: 311 (1969). K u h 1 e n b e c k, H. and Hay m a k e r, W.: The derivatives of the hypothalamus in the human brain: their relation to the extrapyramidal and autonomic systems. Milit. Surg. 105: (1949). Ku h 1 e n b e c k, H., M a l e w it z, T. D. and B e a s l e y, A. B. : Further observations on the morphology of the forebrain in Gymnophiona, with reference to the topologic vertebrate forebrain pattern. In: Evolution of the Forebrain. Phylagenesis and Ontogenesis of the Forebrain. Hassle r, R. and St e p h a n, H., eds., pp (Thieme, Stuttgart 1966). L a u b m a n n, W.: Die Entwicklung der Hypophyse bei Hypogeophis rostratus. Z. f. Anat. Entw. Gesch. 80 : (1926). N o b 1 e, G. K.: The Biology of the Amphibia (McGraw-Hill, New York 1931; Dover, New York 1954). P a s t e el s, J. L. et Her I an t, M.: Les differentes categories de cellules chrornophiles de l'hypophyse d'amphibiens. Verb. I. europ. anat. Kongr. Strassburg 1960, Erg. H. anat. Anz. 109: (1962). Pilla y, K. V.: The hypothalamo-hypophyseal neurosecretory system of Gegeneophis carnosus Beddome. Z. Zellforsch. mikr. Anat. 46 : (1957). Spat z, H., D i e p e n, R. und Gaup p, V.: Zur Anatomie des Infundibulum und des Tuber cinereum beim Kaninchen. D. Z. Nervenheilk. 159: (1948). S t e n d e 11, W.: Die Hypophysis cerebri. Oppels Lehrb. d. vergl. mikr. Anat. d. Wirbelt. 8. Teil (Fischer, Jena 1914). Taylo r, E. H.: The Caecilians of the World. A taxonomic review (Univ. of Kansas Press, Lawrence 1968). W i n g s t r a n d, K. G.: Comparative anatomy and evolution of the hypophysis. In : The Pituitary Gland, H a r r i s, G. W. and D o n o v a n, B. T. eds, vol. 1, p (Univ. of California Press, Berkeley 1966).
10 316 Explanation of Figures Figure 3 (Plate I). A series of sagittal section (A-D) showing the pituitary complex in Schistomepum and cutting through the vicinity of the midline plane (hematoxylin-eosin, approx. x 40). 1: eminentia medialis ; 2: infundibular stem ; 3: infundibular process ; 4: pars tuberalis ; 5: pars distalis ; 6: pars intermedia ; 7: ridge of supra- and postoptic commissures ( chiasmatic ridge ') ; 8: caudal portion of hypothalamic wall basal to mammillary region ; 9: commissural plate of lamina terminalis with commissura pallii (above) and commissura anterior (below) ; 10 : recessus praeopticus ; b: approximate end of deuterencephalic basal cell plate ; f: region of infundibular stem forming roof of hypothalamic infundibular recess ; p: hypophysio-portal system. It will be noted that sections A and B do not show the infundibular process, which is plainly displayed in section D, while its lateral surface is barely reached in section C.
11 317 Plate H. Kuhlenbeck I
12 318 Figure 4 (Plate II). Sagittal sections through anterior (A) and posterior (B) part of pituitary complex in Schistomepum. Arrow x accessory groove in eminentia mediana ; other abbreviations as in fig. 3 (hematoxylin-eosin, approx. x 80). Section A is lateral to caudal portion of infundibular stem. Figure 5 (Plate II). Sagittal sections through posterior part of pituitary complex in Schistomepum. d: cellular traces indicating connection of infundibular lobe lumen with infundibular stem ; other abbreviations as in fig. 3 (hematoxylin-eosin, approx. x 80).
13 319 Plate II 4A 4B 5A 5B H. Kuhlenbeck
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