Cell Tiss. Res. 183, 541-552 (1977)

Cell and Tissue Research 9 by Springer-Verlag 1977

Special Dendritic and Axonal Endings Formed by the Cerebrospinal Fluid Contacting Neurons of the Spinal Cord B. Vigh, I. Vigh-Teichmann and B. Aros 2nd Department of Anatomy, Histology and Embryology,SemmelweisUniversity Medical School, Budapest, Hungary

Summary. The cerebrospinal fluid (CSF) contacting neurons have a dendritic process which protrudes into the central canal, and is provided with one long kinocilium and many shorter stereocilia (about 80 in the turtle) as revealed by scanning electron microscopy. The shape, number and arrangement of the cilia are similar to those of known receptor endings. The silver impregnated axons of these cells converge to a paired centrosuperficial tract forming terminal enlargements at the ventrolateral surface of the spinal cord. Lying among glial endfeet these terminals are ultrastructurally similar to those present in known neurosecretory areas. The nerve endings are attached to the basal lamina, and they comprise many synaptic vesicles (200 to 400A in diameter), as well as granular vesicles of different sizes (diameter 600 to 1800 A). The axons may lie within finger-like protrusions on the surface of the spinal cord, or they may terminate around vessels. Morphological evidence suggests that these nerve terminals and the corresponding CSF contacting perikarya represent a spinal neurosecretory system possibly influenced by information taken up by its special dendrites protruding into the inner CSF space.

Key words: Cerebrospinal fluid contacting neurons - Spinal cord - Dendrites - Receptor endings - Neurosecretory axon terminals - Various vertebrates.

Introduction The neurosensory cells of the central canal described by Kolmer in 1921 and called spinal CSF contacting neurons by us, have been studied by several authors (Agduhr, 1922; Kolmer, 1925, 1931; Leonhardt, 1967; Vigh-Teichmann and Vigh, 1969, 1970; Arnold, 1970; Baumgarten et al., 1970; Vigh et al., 1970 a, b, 1971 a, b, c; Vigh, 1971; Vigh and Vigh-Teichmann, 1971, 1973). Dr. B. Vigh, 2nd Department of Anatomy, Histology and Embryology, Semmelweis University Medical School, Budapest, Hungary

Send offprint requests to:

542

B. Vigh et al.

The most characteristic part of these cells is the dendritic ending that protrudes into the central canal. In the rabbit, these terminals were studied with the scanning electron microscope by Lindemann and Leonhardt (1973). In the present paper, we report on the scanning electron microscopy of these CSF contacting endings in the turtle. Concerning the axons of these cells already Agduhr (l 922) mentioned that they may reach the outermost zone of the spinal cord, or terminate on other spinal neurons, but a detailed study on this problem has not yet been made. Recently, we found nerve terminals on the surface of the terminal filum in the carp and the cervical spinal cord in Triturus cristatus and the axolotl (Vigh, 1974; Vigh et al., 1974) and we have suggested that these terminals may be formed by the axons of the CSF contacting neurons. Ochi and Hosoya (1975) also described superficial nerve terminals in the spinal cord of Lampetra japonica which originate from CSF contacting neurons. Starting from these data, in the present work we repeated the silver impregnation studies of Kolmer and Agduhr in order to follow the path of the axons of the CSF contacting neurons. Further, we investigated the superficial terminals of these axons with the electron microscope in various vertebrates.

Material and Methods Segments of the cervical, thoracal, lumbar, sacral and caudal spinal cord, oblongate medulla and terminal ilium (the latter only in fishes and anurans) of a total of 136 submammalian vertebrates were studied light- and electron microscopically. The following species were examined: Cyprinus carpio,

Anguilla anguilla, Cichlasoma nigrofasciatum, Misgurnus fossilis, Phoxinus laevis, Triturus cristatus et vulgaris, Pleurodeles waltlii, Amblystoma mexicanum, Rana esculenta, tigrina et arvalis, Bombinator igneus, Xenopus laevis, Emys orbicularis, Pseudemys scripta elegans, Testudo hermanni, Lacerta agilis, viridis et muralis, Elaphe longissima, Gallus domesticus, Turdus merula, Melopsittacus undulatus, Taeniopiga castanotis, Serinus canarinus. For light microscopic demonstration of the perikarya and processes the rapid Golgi and the GolgiKopsch impregnation methods were applied. The materials embedded in celloidin were sectioned at 60120 lam in the transverse or longitudinal planes. Semithin sections of the materials embedded for electron microscopy were stained with toluidine blue azure II and used for light microscopy. For scanning and transmission electron microscopy animals were anaesthetized in ether and perfused through the aortic bulb with 5 or 6 ~ glutaraldehyde dissolved in Millonig phosphate buffer, for 15 to 20 rain. For further details concerning the preparation for transmission electron microscopy see Vigh-Teichmann et al. (1976). The materials for scanning electron microscopy were dehydrated in ethanol and amylacetate and dried by the critical point method using CO 2. The specimens were coated with carbon and gold and examined in a JEOL 100 B electron microscope equipped with a scanning adapter. The transmission electron microscopic sections were photographed in a JEM 6C and JEOL 100C electron microscopes 1.

Results

The spinal CSF contacting neurons have a dendritic terminal that protrudes into the lumen of the central canal (Fig. I a). It is known that this terminal possesses a kinocilium and many stereocilia (lit. in: Vigh and Vigh-Teichmann, 1973). As 1 We wish to thank for the working facilities at the Morphological Department of the Institute of Public Health (OKI) and the 2nd Electron Microscopic Laboratory of the Semmelweis University, Budapest. We are grateful to Mr. A. Werglesz for his help in the preparation and photography of the scanning electron microscopic material

Cerebrospinal Fluid Contacting N e u r o n s of Spinal Cord

543

Fig. 1 a-e. CSF contacting dendritic terminals of the central canal, a Ultrastructure o f a neuronal perikaryon (plasmalemma dotted) and its CSF contacting terminal in the cervical region of the spinal cord ofLacerta agilis. CC central canal; R Reissner's fiber. At arrow stereocilia of the terminal, x 6000. b and e Scanning electron microscopic view of the CSF contacting terminals (large arrows) at the cranial end o f the central canal in Pseudemys scripta elegans. Ependyma/microvilli in hexagonal arrangement (dotted line in the upper right corner), in the middle a single kinocilium (small arrows), x 2000 and x 3000. d and e N u m e r o u s (about 80) stereocilia on the CSF contacting terminals. C kinocilium; M ependymal microvilli, x 9000

Fig. 2 a-f. Demonstration of the dendrites and the axons of the CSF contacting neurons in the turtle (Emys orbicularis) by Golgi impregnation, a A CSF contacting perikaryon (P), its dendrite and stereocilia (large arrow) in the lumen of the central canal (dottedline). The varicose axon (small arrows) runs ventrolaterally. Photomontage, x 1200. b Circular arrangement of the CSF contacting neurons around the central canal (CC). x 480. e The axon of the CSF contacting neuron (large arrow) runs to the ventrolateral surface of the spinal cord (smallarrows). Dottedcentral canal (CC) and surface of the cord; FM fissura mediana anterior. Photomontage, • 200. d Axons of CSF contacting neurons (arrows) converge laterally of the central canal (CC) to form an unmyelinated centrosuperficial tract. Photomontage, x 720. e and f Terminal part of the centrosuperficial tract (CST). At arrows terminal enlargements on the surface of the spinal cord (dotted line). Photomontages, x 650, x 300

Cerebrospinal Fluid Contacting Neurons of Spinal Cord

545

revealed by the s c a n n i n g electron microscope, in the turtle (Pseudernys scripta elegans) these terminals are scattered o n the surface o f the central canal lying a m o n g e p e n d y m a l cells (Fig. I b). The surfaces o f the e p e n d y m a l cells form hexagonal areas with microvilli at the cell b o r d e r a n d a k i n o c i l i u m in the centre. The C S F c o n t a c t i n g terminals c a n be recognized b y their stereocilia being longer a n d thicker t h a n e p e n d y m a l microvilli, b u t shorter t h a n kinocilia (Fig. 1 c, d). The n u m b e r o f the stereocilia o n one C S F c o n t a c t i n g t e r m i n a l is a b o u t 80 (Fig. 1 d, e). The perikarya a n d the C S F c o n t a c t i n g dendrites (Fig. 2 a, b) c a n be easily d e m o n s t r a t e d with silver i m p r e g n a t i o n techniques as described by K o l m e r (1921, 1925, 1931) a n d A g d u h r (1922). I n some cases, the stereocilia of the dendritic terminals are also visible (Fig. 2 a). The axons c o u l d be traced for a longer distance i n reptiles a n d birds only. I n fishes a n d a m p h i b i a n s , the axons were n o t well stained in o u r material. I n birds, the diameter of the spinal cord is rather large w h e n c o m p a r e d with that o f lower vertebrates because of the higher n u m b e r o f t r a n s i t o r y nerve fibers. Therefore, we were u n a b l e to follow the axons of the C S F c o n t a c t i n g n e u r o n s a l o n g their course even in sections o f 120 m i c r o n thickness. O n the contrary, in reptiles, especially in the turtle E m y s orbicularis, the axons were easier to follow a l o n g their whole p a t h (Fig. 2 c). Starting from the basal part o f the nerve cell, the axons first converge at b o t h sides of the central canal a n d form a thin tract Fig. 3 a-I~ The axon terminal area on the ventrolateral surface of the spinal cord in fishes and urodeles, a The zone of the distribution of the nerve endings on the spinal surface(identifiedby electron microscope) at the border of the anterior and lateral fascicles (arrows) in Phoxinus laevis, x 170. lnset the area of the axon terminals (dotted line between arrows) with higher magnification. Anguilla anguilla, x 420. Semithin sections stained with toluidine blue azure II. b and e Axons (A) and terminals (dotted) containing granular vesicles(V) of 800, or 1400/~ in diameter and synaptic vesicles (at arrows) in the caudal spinal cord of the carp. BL basal lamina; GE glial endfoot, x 25,500. d Large nerve terminal (dotted) on the basal lamina (BL) of the surface of the caudal spinal cord. Cyprinus carpio. At arrow dense projections at the basal lamina and accumulations of synaptic vesicles. M mitochondrium; V granular vesicles(800A in diameter), x 25,500.e and fAxons containing large (about 1600A in diameter) granular vesiclesnear and on the surface of the cervical spinal cord of Arnblystoma mexicanum. Arrow indicates accumulation of small vesiclesand electron density at the basal lamin~ MFmyelinatedfiber of the anterior fascicle. • 25,500. g Axon terminal containing granular vesicleson the basal lamina (BL) of the surface of the cervical spinal cord of Pleurodeles wattlii. A t arrow accumulation of synaptic vesicles. x 25,500. h Axon terminal (plasmalemma dotted) containing many synaptic vesicles and granular vesicles (1200A in diameter), on the surface of the thoracal spinal cord of Triturus vulgaris. A t arrows electron density near the basal lamina, x 25,500 Fig. 4 a-h. The superficial axon terminal area of the spinal cord in the frog, Lacertilians and chicken, a Axonterminalinfrontofavessel(VE)penetratingtheterminalfilumofXenopuslaevis. x 4000. The inset shows the terminal with higher magnification, x 26,600. BL basal lamina, b Axon terminal containing synaptic vesicles and granular vesicles of 600,3, in diameter at the surface of the proximal part of the terminal ilium in ~Yenopus laevis. BL basal lamina, x 31,500. c Axon terminal containing granular vesiclesof 1000A, at the surface of the conus terminalis (conus medullaris) of Xenopus laevis. BL basal lamina, x 27,600. d Axon terminal (plasmalemma dotted) at the surface of the cervical spinal cord of Lacerta muralis. M myelinated fibers of the anterior fascicle, x 25,000.eAxon terminal containing many synaptic vesicleson the surface of the distal medulla oblongata of Lacerta agilis. C collagenous fibrils. x 37,200. f Finger-like protrusions (P) in front of the ligamentum denticulatum in the sacral spinal cord of the chicken.Vgranular vesiclesin the axons lyingwithin the protrusions, x 25,500. g Accumulation of synaptic vesicles of an axon on the basal lamina (arrow) of the surface of the finger-like protrusion. x 25,500. h Axon terminal forming the tip of a finger-likeprotrusion of the surface of the spinal cord in the chicken. BL basal lamina. • 37,200

B. VI@

546

3 Caption

see p. 545

ct al.

Cerebrospindl

Fluid

4 Caption

see p. 545

Contacting

Neurons

of Spinal

Cord

547

NTA

Fig. 5. Schematic drawing of the spinal cord demonstrating the organization of the spinal CSF contacting neuronal system. The CSF contacting nerve cells receiving synapses on their perikarya (perhaps formed by axon collaterals of neighbouring cells of a similar type) have a receptor dendritic ending in the internal CSF space and a neurosecretory axon terminal on the basal lamina of the surface of the nervous tissue. CST centrosuperficial tract formed by the axons of the CSF contacting neurons; E ependymal cells; F ilia radicularia motorica; Ft filum terminale; Mo medulla oblongata; N CSF contacting neuron; NTA nerve terminal area formed by the axons of the CSF contacting neurons; R Reissner's fiber; S different types of synaptic hemidesmosomes on the basal lamina of the surface of the spinal cord; Ve meningeal vessel

Cerebrospinal Fluid Contacting Neurons of Spinal Cord

549

at the border of the central grey matter (Fig. 2d). The tract then turns ventrolaterally and runs diagonally across the grey substance to the end of the ventral column (Fig. 2 c, e, f). Here, the fibers diverge and enter the white matter to terminate in small enlargements at the ventrolateral surface of the spinal cord (Fig. 2 e, f). This surface zone lies lateral from the motoric fila radicularia. Some axons may terminate more medially or laterally from this main area of nerve endings. We found side branches on axons only in the close vicinity of the basal part of the CSF contacting neurons. We could not find any termination of axons along the course of this "centrosuperficial" tract in the turtle. Examining the superficial area of nerve terminals of the spinal cord with the transmission electron microscope we found unlnyelinated axons running to the outer surface and terminating there at the border of the nervous and meningeal tissues. Light microscopically, in sections stained with routine histological techniques, this zone is not visible. In semithin sections of various vertebrates we could identify the zone of nerve terminals by comparing it with the same area of ultrathin sections in the electron microscope. In lower vertebrates, this zone is located in the vicinity of a triangle-shaped area which consists of unmyelinated fibers and lies between the large myelinated fibers of the ventral fascicle and the smaller myelinated fibers of the lateral fascicle (Fig. 3 a). In birds, this area is situated in front of the ligamentum denticulatum. The axons terminating at the surface reach the external basal lamina, where they lie between glial endfeet (Fig. 3 b, c). Here, they form terminal enlargements which are sometimes rather long in fishes (Fig. 3 d). The terminals may lie side by side, but in general they are scattered over a wide area. In one ultrathin cross section we counted 1 to 15 axons on each side of the spinal cord. Generally, these axons are more electron dense than other unmyelinated fibers in the cord. Different kinds of granular vesicles were present in these axons: a smaller sized type (600 to 1000N in diameter, Figs. 3 b, d, 4 b, c, e) and a larger one (Figs. 3 c, e, f, g, h, 4 d) measuring 1200 to 1800N in diameter. The terminals o f these axons are attached to the external basal lamina by hemidesmosome-like structures (Fig. 3 c, d., f, g). Synaptic vesicles of 200 to 400 A in diameter are accumulated at these contact sites. The terminals also contain some mitochondria. With the exception of fishes and birds we found no major segmental differences in the structures described at the cervical, thoracal, lumbar, sacral or caudal levels studied, or at the levels of the distal oblongate medulla and of the proximal part of the terminal filum. In fishes, the terminals are more numerous in the neighbourhood of the urophysis. In birds, we observed numerous terminals at the level of the fissura lumbosacralis. In urodeles, thin nerve-like processes were seen which contain some axons and protrude from the surface of the spinal cord into the meningeal tissue. These processes seem to ramify and terminate after a short course among vessels of the unfenestrated type. In anurans, nerve endings lying on the basal lamina were also found around vessels entering the terminal filum (Fig. 4 a). Here, axons containing granular vesicles may contact infoldings of the basal lamina which lie inside the nervous tissue. In birds, the axon terminals may enter the protrusions of the surface of the cord (Fig. 4 f, g, h). Finally, it is worth mentioning that we observed CSF contacting neurons at the

550

B. Vigh et al.

level of the proximal filum terminale not only in fishes (Vigh, 1974; Vigh et al., 1974) but also in the anurans studied. Our findings are summarized in a schematic drawing (Fig. 5).

Discussion The axon terminals, described in an earlier publication, which lie on the external surface o f the terminal ilium of the carp were found to be similar to known neurohormonal nerve terminals of neurosecretory cells (Vigh, 1974; Vigh et al., 1974). In the present study, we could establish that nerve endings formed by the axons of the CSF contacting neurons of the central canal build up a paired longitudinal zone extending from the oblongate medulla to the terminal ilium (Fig. 5). Lying among glial endfeet these axon endings contain synaptic vesicles and granular vesicles of different sizes. The terminals are attached to the basal lamina of the external surface of the nervous tissue by hemidesmosomes and the synaptic vesicles are accumulated here ("synaptic hemidesmosome"). We regard this special type of axon ending present in all neurosecretory areas (neurohypophysis, median eminence, urophysis, etc.) as the most characteristic structure of neurosecretory cells (Vigh et al., 1974; Vigh, 1975). We therefore believe that these spinal axon terminals and the corresponding p e r i k a r y a - t h e CSF contacting n e u r o n s - r e p r e s e n t a spinal neurosecretory system. On the basis of the fine structure of the perikarya and the presence of granular vesicles also Leonhardt (1967) ascribed a secretory function to these cells which according to him may release their product by means of their "Mitochondrienkolben", i.e. dendritic terminals contacting the internal CSF. In our opinion, the different types of granular vesicles may carry some hypothetical biologically active material which is released from the described axon endings to the surface of the brain. From here, the substances may reach the external CSF space and/or the meningeal vessels. As fenestrae are lacking in the endothelia of the vessels fast penetration of secreted materials into the blood stream is not very likely. Therefore, also a direct effect on the vessels must be taken into consideration. It should be mentioned that already Agduhr (1922) has suggested a regulatory function for these cells which he considered as neurosensory cells. The information required for the regulatory function mentioned by Agduhr (1922) was supposed to reach the receptor endings penetrating the central canal. As our earlier results have shown, these dendritic CSF contacting terminals are similar to those of known receptor cells, especially mechanoreceptors of the lateral line organ, or the inner ear (lit. in Vigh an:l Vigh-Teichmann, 1973; Vigh et al., 1976). Moreover, our present scanning electron microscopical findings show that the CSF contacting dendrites resemble the receptor endings of some mechanoreceptors, e.g. those of the hair cells of the inner ear, also with regard to the appearance and number of the stereocilia (about 80). Kolmer (1921) suggested a connection in the receptor mechanism between Reissner's fiber and the neurosensory cells of the central canal. We found a morphological relation between Reissner's fiber and the CSF contacting neurons similar to that between the tectorial membrane and the hair cells of the organon of Corti (Vigh et al., 1976). Perhaps, by monitoring some parameters of the CSF

Cerebrospinal Fluid Contacting Neurons of Spinal Cord

551

(intensity o f flow?) these C S F contacting neurons m a y play a role in the regulation o f the leptomeningeal vessels and in turn the circulation in the nervous tissue and o f the CSF. A t present, we c a n n o t exclude a chemosensory function for the special dendrites o f the neurons. Differences a m o n g species must also be taken into consideration as the dendritic terminals are somewhat different in the various species investigated. In higher vertebrates, they f o r m bulbous enlargements and their stereocilia are thin (Vigh et al., 1971 a; Vigh and Vigh-Teichmann, 1973). L e o n h a r d t (1967) and L i n d e m a n n and L e o n h a r d t (1973) did n o t find cilia on these terminals in the rabbit. The above mentioned suppositions concerning the role o f this system a r e calling for further strengthening, or substitution by better ones. Finally, we would like to mention that K o l m e r (1921, 1925, 1931) postulated a peculiar m e c h a n o r e c e p t o r function for these neurons: perceiving the m o v e m e n t o f the spinal c o l u m n these cells, via their axons, might inform, m o t o r i c neurons o f the spinal cord. Terminations o f such axons on cells o f the spinal grey matter were f o u n d by A g d u h r (1922). In our silver impregnated material in the turtle, we could however n o t observe similar connections. N e a r the perikarya o f the C S F contacting neurons, only some a x o n collaterals were seen, perhaps running to other C S F contacting nerve cells (see also: Vigh et al., 1974). However, connections between these axons and other nerve cells o f the spinal grey matter m a y also exist. In this context we refer to the fact that, in addition to n e u r o h o r m o n a l endings, cell to cell "peptidergic" synapses occur in other neurosecretory systems as well ( B a r g m a n n et al., 1967; Scharrer, 1974; Vigh-Teichmann et al., 1976). Therefore, in our further investigations we are planning to study this question by means o f lesioning experiments in higher vertebrates first o f all. A t the same time we intend to clarify whether also perikarya other than C S F contacting neurons f o r m terminals on the surface o f the spinal cord.

References Agduhr, E.: lAber ein zentrales Sinnesorgan (?) bei den Vertebraten. Z. Anat. Entwickl.-Gesch. 66, 223-360 (1922) Arnold, W.: lJber eigentiimliche neuronale Zellelemente des Zentralkanals von Salamandra maculosa. Z. Zellforsch. 105, 176-187 (1970) Bargmann, W., Lindner, E., Andres, K.H.: l~ber Synapsen an endocrinen Epithelzellen und die Definition sekretorischer Neurone. Untersuchungen am Zwischenlappen der Katzenhypophyse. Z. Zellforsch. 77, 282-298 (1967) Baumgarten, H.G., Falck, B., Wartenberg, H.: Adrenergic neurons in the lower spinal cord of the pike (Esox lucius) and their relation to the neurosecretory system of the neurohypophysis spinalis caudatis. Z. Zellforsch. 107, 479-498 (1970) Kolmer, W. : Das "Sagittalorgan" der Wirbeltiere. Z. Anat. Entwickl.-Oesch. 60, 652-717 (1921) Kolmer, W.: Weitere Beitr/ige zur Kenntnis des Sagittalorgans der Wirbeltiere. Verh. anat. Ges. (Jena) 60, 252-257 (1925) Kolmer, W.: IJber das Sagittalorgan, ein zentrales Sinnesorgan der Wirbeltiere, insbesondere beim Affen. Z. ZeUforsch. 13, 236-248 (1931) Leonhardt, H.: Zur Frage einer intraventrikul/iren Neurosekretion. Eine bisher unbekannte nerv6se Struktur im IV. Ventrikel des Kaninchens. Z. Zellforsch. 79, 172-184 (1967) Lindemann, B., Leonhardt, H.: Supraependymale Neuriten, Gliazellen und Mitochondrienkolben im caudalen Abschnitt des Bodens der Rautengrube. Z. Zellforsch. 140, 401-412 (1973) Ochi, J., Hosoya, Y.: Monoamine neurons in the brain and spinal cord of the lamprey, Lampetra

552

B. Vigh et al.

japonica. A fluorescence and electron microscopic study (E. Yamada, ed.), p. 141. Tokyo: Proc. 10th Int. Congre. Anat. 1975 Scharrer, B.: New trends in invertebrate neurosecretion. In: Neurosecretion. The final neuroendocrine pathway (F. Knowles and L. Vollrath, eds.), pp. 285-287. Berlin-Heidelberg-New York: Springer 1974 Vigh, B.: Das Paraventrikularorgan und das zirkumventrikul~ire System. Studia biol. hung. 10. Budapest: Akad6mia Kiad6 1971 Vigh, B.: Ultrastructural studies on the caudal neurosecretory system, spinal CSF contacting neurons and ilium terminale. In: Neurosecretion. The final neuroendocrine pathway (F. Knowles and L. Vollrath, eds.), p. 324. Berlin-Heidelberg-New York: Springer 1974 Vigh, B.: The synaptic semidesmosome as special neurosecretory structure (In Hungarian). MTA Biol. Oszt. K6zl. 18, 301-306 (1975) Vigh, B., Vigh-Teichmann, I.: Structure of the medullo-spinal liquor contacting neuronal system. Acta biol. Acad. Sci. hung. 22, 227-243 (1971) Vigh, B., Vigh-Teichmann, I.: Comparative ultrastructure of the CSF contacting neurons. In: Int. Rev. Cytol. 35, (G.H. Bourne and J.F. Danielli, eds.), pp. 189-251. New York: Academic Press 1973 Vigh, B., Vigh-Teichmann, I., Aros, B.: Ultrastructure of the CSF contacting neurons of the spinal cord in the newt (Triturus cristatus). Acta morph. Acad. Sci. hung. 18, 369-383 (1970) Vigh, B., Vigh-Teichmann, I., Aros, B.: Ultrastruktur der spinalen Liquorkontaktneurone beim Krallenfrosch (Xenopus laevis). Z. Zellforsch. 112, 201-211 (1971 a) Vigh, B.; Vigh-Teichmann, I., Aros, B.: Ultrastruktur der Liquorkontaktneurone des Zentralkanals des Rtickenmarkes beim Karpfen (Cyprinus carpio). Z. Zellforsch. 122, 301-309 (1971 b) Vigh, B., Vigh-Teichmann, I., Aros, B.: Intraependymal cerebrospinal fluid contacting neurons and axon terminals on the external surface in the filum terminale of the carp (Cyprinus carpio). Cell Tiss. Res. 148, 359-370 (1974) Vigh, B., Vigh-Teichmann, I., Aros, B.: Today's outlines of neurosecretory phenomena (In Hungarian). In: Recent Problems of Biology (Gy. Csaba, ed,). Budapest: Medicina K6nyvkiad6 1976 Vigh, B., Vigh-Teichmann, I., Korits/mszky, S., Aros, B.: Ultrastruktur der Liquorkontaktneurone des Rtickenmarkes yon Reptilien. Z. Zellforsch. 109, 180-194 (1970) Vigh, B., Vigh-Teichmann, I., Korits/mszky, S., Aros, B.: Ultrastructure of the spinal CSF contacting neuronal system in the white leghorn chicken. Acta morph. Acad. Sci. hung. 19, 9-24 (1971) Vigh-Teichmann, I., Vigh, B.: Liquor contacting neuronal areas in the periventricular gray substance of the central nervous system. Gen. comp. Endocr. 13, 537 (1969) Vigh-Teichmann, I., Vigh, B.: Structure and function of the liquor contacting neurosecretory system. In: Aspects of Neuroendocrinology (W. Bargmann and B. Scharrer, eds.), pp. 329-337. BerlinHeidelberg-New York: Springer 1970 Vigh-Teichmann, I., Vigh, B., Aros, B.: Ciliated neurons and different types of synapses in anterior hypothalamic nuclei of reptiles. Cell Tiss. Res. 174, 139-160 (1976)

Accepted May 10, 1977

Special dendritic and axonal endings formed by the cerebrospinal fluid contacting neurons of the spinal cord.

Cell Tiss. Res. 183, 541-552 (1977) Cell and Tissue Research 9 by Springer-Verlag 1977 Special Dendritic and Axonal Endings Formed by the Cerebrospi...
3MB Sizes 0 Downloads 0 Views