Two Components of the Pineal Organ in the Mink (Mustela Vison) : Their Structural Similarity to Submammalian Pineal Complexes and Calcification*

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Two Components of the Pineal Organ in the Mink (Mustela Vison) : Their Structural Similarity to Submammalian Pineal Complexes and Calcification* Arch. Histol. Cytol., Vol. 55, No. 5 (1992) p. 477-489 Two Components of the Pineal Organ in the Mink (Mustela vison) : Their Structural Similarity to Submammalian Pineal Complexes and Calcification* Bela VIGH and Ingeborg VIGH-TEICHMANN Photoneuroendocrine Laboratory of the Second Department of Anatomy, Histology and Embryology, Semmelweis University Medical School; and Neuroendocrine Section of the Hungarian Academy of Sciences, Semmelweis Medical University Joint Research Organization, Budapest, Hungary Received August 25, 1992 Summary. The pineal complex in the mink (Mustela The forerunner of vertebrates is believed to have vison) consists of a larger ventral and a smaller dorsal been four-eyed: two eyes looking laterally as locators pineal. Both organs contain pinealocytes, neurons, glial for perceiving the reflected light from objects in the cells, nerve fibers and synapses in an organization environment, and two eyes looking toward the sky characteristic of nervous tissue. The cellular elements as primitive pineal organs to perceive modifications are arranged circularly around strait lumina. These lumina correspond to the photoreceptor spaces of sub- of solar radiation (see Fig. 10, in VIGH and VIGH- mammalian pineals. A 9+0-type cilium marks the recep- TEICHMANN, 1988). Accordingly, two organs form a tory pole of the pinealocytes which may form an inner- pineal complex in some cyclostomes, teleosts, anur- segment-like dendrite terminal in the pineal lumina. ans and reptiles, while in other vertebrates they are The cilia correspond to outer segments which form photo- represented by a single organ or two anlages which receptor membrane multiplications in the pineal of sub- unite during ontogeny, as do the human pineal (MOL- mammalians and in certain insectivorous and mustelid LER, 1974). Several mammals have both deep and mammals (bat, hedgehog, ferret). Axonal processes of superficial parts of the pineal. The incidence of two the pinealocytes contain synaptic ribbons and terminate pineals lying in parallel has not yet been registered in on intrapineal neurons of both organs. This pattern adult mammals. represents a neural efferentation of the pineal nervous The mink (Mustela vison) is a member of the tissue The axonal processes of pinealocytes also form neurohormonal endings which pierce the perivascular mustelids, which are ancient carnivorous animals. limiting glial membrane in the ventral as well as in the Our examination of the mink aimed to gain further dorsal pineal. The upper pineal ("epipineal") of the mink data on the organization of the pineal in this mam- may correspond to the parapineal, frontal, or parietal malian group as it differs from those generally stud- organs of submammalian pineal complexes. ied. Recently, we have found outer-segment-like cilia Both pineals are encapsulated by the meningeal tissue of photoreceptor cells in the pineal organ of the of the brain stem. Afferent vasomotor axons of the ferret, another mustelid (VIGH and VIGH-TEICHMANN, meninges innervate smooth muscle cells of pineal arter- 1991b). It is already known that the pineal of the ioles. There are corpora arenacea in the pineal arach- mink plays a role in the seasonal timing of gonadal noid and in the pineal nervous tissue, primarily in the activity, moulting periods, pelage composition, etc. ventral pineal. The localization of calcium ions detected around the membrane of pineal cells by pyroantimonate (MARTINET and ALLAIN, 1985). The structure of the cytochemistry suggests membrane activity as the source pineal was investigated by WEMAN and NOBIN (1979), of the calcium ions. The accumulation of calcium by the ROUVET (1982), and TILLET and coworkers (1989). pinealocytes may be due to their neurosensory character. The localization of biogenic amines and melatonin The mink is the first animal described to have both intra- was described by these authors, and the fine structure pineal and meningeal concrements like the human pineal. of the mink pineal was found to be similar to that of This investigation was supported by the Hungarian OTKA grant No. 1109. 477 478 B. VIGH and I. VIGH-TEICHMANN: the ferret except that intrapineal neurons were not desmosomes. The upper pineal is in close contact detected in the mink. with the choroid plexus of the suprapineal recess. Our interest in studying the mink was strengthened Both organs contain a small lumen in the center of when we found a double pineal, with both sections the follicular tissue units (Fig. la, c-e). These are containing neuronal perikarya. There were also cal- more prominent in young animals than in adults. cified concretions and meningeal axons innervating Bundles of axons run in these microlumina formed by pineal arterioles in this mustelid. ependymal cells bearing microvilli and a kinocilium and connected by cell binding structures. Dendritic processes of pinealocytes also border these lumina MATERIALS AND METHODS and often form inner segment-like thickenings (Fig. id, e) which contain microtubules, basal bodies and Twenty-seven minks (Mustela visors) aged from new- striated ciliary rootlet fibers. Solitary 9 + 0-type (Fig. born to one year old (sexually matured) and one id, inset) cilia emerge from pinealocytes into the micro- and-a-half year olds of both sexes were received from lumina and/or the intercellular space. The cytoplasm the Maxima stock-farm in Vaskut, Hungary. After of the pinealocytes is characterized by an abundance hexobarbital natrium (AWD Dresden, FRG) narcosis, of ribosomes and mitochondria which are larger than 14 animals were perfused intracardially with 1-4% those of the pineal neurons. An axonal process of the glutaraldehyde; the pineals of the others were im- pinealocytes which contains parallel microtubules mersed in a fixative of 3-5% glutaraldehyde dis- and mitochondria runs to the pineal neurons and/or solved in phosphate or cacodylate buffer (pH 7.2; 300 (their collaterals ?) crosses the limiting glial mem- mosm). The best fixation was obtained with 4% brane (Fig. 2a) to form ribbon-type neurohormonal glutaraldehyde. For the localization and ultrastruc- terminals (Fig. 2a, b) in both the ventral and the tural visualization of calcium ions, the potassium dorsal pineal. Mitoses were often found in the pineals pyroantimonate (PPA) method was used as described of one to four week-old minks. earlier (VIGH et al., 1989b). The material was washed There is a high number of neuronal perikarya in in a buffer, dehydrated in ethanol, and embedded in both pineals. The nerve cells are larger and more Polybed 812 or LR-White (Polyscience, St. Goar, electron lucent than pinealocytes (Fig. 2c), and con- FRG). One micron thick sections were stained with tain small mitochondria, rough surfaced endoplasmic toluidine blue-azure II for light microscopic examina- reticulum and Golgi-areas. Axons presumably emerg- tion. Ultrathin sections stained with uranyl acetate ing from intra-and/or extrapineal neurons form and lead citrate were examined and photographed in synapses on the neuronal perikarya and their den- JEM 6C and OPTON 902 electron microscopes. drites. Some of the axon terminals contain synaptic vesicles and a few granular vesicles; other terminals formed by pinealocytic processes also contain vesi- cle-crowned rodlets (Fig. 2d). A few electron lucent RESULTS profiles (of pinealocytic or neuronal processes ?) con- tain synaptic spherules (Fig. 2e). Myelinated and Structure of the pineal organs unmyelinated nerve fibers are present intrapineally The mink has a pineal complex located below the and perivascularly. splenium of the corpus callosum. It is composed of a Both pineal organs are covered by a leptomenin- smaller upper, and a larger ventral organ separated geal tissue (Figs. la, b, 3a), the continuation of the from each other by a meningeal layer (Fig. la, b). The corresponding diencephalic meningeal layers. They two pineals are separately connected to the habenu- consist of a stratified arachnoid and the cell layers of lar area of the epithalamus. The dorsal pineal is not the pia mater. Axons of the perivasal nerve bundles a diverticlulum of the ventral one as indicated in (Fig. 3b, c) form synapses on the smooth muscle cells serial sections. Both organs contain pinealocytes, of pineal arterioles (Fig. 3d). glial cells, nerve cells, unmyelinated and myelinated nerve fibers and synapses. The tissue of the pineals is Pineal calcification separated from the pial/perivascular spaces by a basal lamina. Intermediate filament-containing processes There are numerous corpora arenacea in the pineal of glial cells run to the perivascular and outer sur- complex of the mink. They occur predominantly in faces and form a limiting membrane with their end- the ventral pineal organ and its arachnoid; however, feet. The latter are connected by junctional struc- they are absent in the arachnoid of the surrounding tures and are attached to the basal lamina by hemi- brain tissue (Fig. 3a). meningeal acervuli are larger Pineal Organs in the Mink 479 b a C d e Fig. 1 a-e. Light- and electron-microscopic structure of the pineal complex of the mink. a and b. The dorsal (DP) and ventral (VP) pineal separated by a meningeal layer (M). Arrow: Lumen of a follicular tissue unit sectioned through its center. x250. c. Pineal lumen (L) of the ventral pineal of an adult animal. D pinealocytic dendrite, E ependymal cells bearing microvilli and connected by zonulae adherentes. X 18,800. d. Innersegment- like protrusion (IS) bearing a cilium (C) at the end of a pinealocytic dendrite (D) in a photoreceptor lumen (L) of the ventral pineal of a two-week-old animal. E ependymal cells, asterisk ciliary pit. X45,600. Inset: Cross section of a 9+0 cilium. Asterisk ciliary pit. X 51,400. e. Dendritic process (D) of a pinealocyte of an adult animal. E ependymal cells connected to the pinealocytic dendrite by cell-binding structures, IS inner segment-like enlargement, L pineal lumen. X 38,000 480 B. VIGH and I. VIGH-TEICHMANN: than intrapineal ones: most of the latter are only and glial cells, even in young animals where concre- visible with the electron microscope (Fig.
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