Summary
Within the suprachiasmatic nucleus (SCN) of the rat the fine structure of the synapses and some features of their topological arrangement were studied. Five types of synapses could be distinguished with certainty:
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A.
Two types of Gray-type-I (GTI) or asymmetrical synapses (∼33%). The presynaptic elements contain strikingly different types of mitochondria. Size of clear vesicles: ∼ 450 Å. Synapses with subjunctional bodies often occur, among these also “crest synapses”. Localization: dendritic shafts and spines, rarely somata.
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B.
Three types of Gray-type-2 (GTII) or symmetrical synapses (∼66%)∶:1) Axo-dendritic and -somatic (=AD) synapses. Size of clear vesicles: ∼500 Å. 2) Invaginated axo-dendritic and -somatic (=IAD) synapses with club-like postsynaptic protrusions within the presynaptic elements (PreEl). Size of clear vesicles is very variable: ∼ 400–1,000 Å. 3) Dendro-dendritic, -somatic and somato-dendritic (=DD) synapses occurring at least partly in reciprocal arrangements. They represent an intrinsic system.
Shape of clear vesicles: often oval; sucrose treatment partly produces flattening.
Dense core-vesicles (dcv) are found in all GTII- and most of the GTI-synapses after three-dimensional reconstruction. All types of synapses (mostly GTII-synapses) can be enclosed by multilamellar astroglial formations. The synapses often occur in complex synaptic arrangements.
Dendrites and somata of females show significantly more multivesiculated bodies than those of males. Further pecularities of presynaptic (PreEls) and postsynaptic elements (PostEls) within the SCN are described and discussed.
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Abbreviations
- AD synapse:
-
axo-dendritic (+somatic) GTII synapse
- dcv:
-
dense core vesicle
- DD synapse:
-
dendro-dendritic/dendro-somatic/somato-dendritic synapse
- GTI synapse:
-
Gray-Type-I synapse
- GTII synapse:
-
Gray-Type-II synapse
- IAD synapse:
-
invaginated axodendritiċ (+somatic) GTII synapse
- PreEl(s):
-
presynaptic element(s)
- PostEl(s):
-
postsynaptic element(s)
- sb:
-
subjunctional body(ies)
- SCN:
-
suprachiasmatic nucleus
References
Adinolfi, A.M.: The fine structure of neurons and synapses in the entopeduncular nucleus of the cat. J. comp. Neurol. 135, 225–248 (1969)
Adinolfi, A.M.: The organization of synaptic junctions in cat putamen. Brain Res. 32, 53–67 (1971)
Aghajanian, G.K., Bloom, F.E.: Electron-microscope localization of tritiated norepinephrine in rat brain: effect of drugs. J. Pharmacol. exp. Ther. 156, 407–416 (1967)
Akert, K., Pfenninger, K., Sandri, C., Moor, H.: Freeze etching and cytochemistry of vesicles and membrane complexes in synapses of the central nervous system. In: Structure and function of synapses (G.D. Pappas and D.P. Purpura, eds.), p. 67–86. New York: Raven Press 1972
Andres, K.H.: Morphological criteria for the differentiation of synapses in vertebrates. J. Neur. Transm. Suppl. XII, 1–37 (1975)
Anzil, A.P., Blinzinger, K., Matsushima, A.: Dark cisternal fields: specialized formations of the endoplasmic reticulum in striated neurons of a rat. Z. Zellforsch. 113, 553–557 (1971)
Bak, I.J., Choi, W.B.: Electron microscopic investigation of synaptic organization of the trochlear nucleus in cat. I. Normal ultrastructure. Cell Tiss. Res. 150, 409–423 (1974)
Baumgarten, H.G., Lachenmayer, L.: 5,7-dihydroxytryptamine: improvement in chemical lesioning of indoleamine neurons in the mammalian brain. Z. Zellforsch. 135, 399–414 (1972)
Baylor, D.A., Nicholls, J.G.: Changes in extracellular potassium concentrations produced by neuronal activity in the central nervous system of the leech. J. Physiol. (Lond.) 203, 555–569 (1969)
Birks, R.J., Mackey, M.C., Weldon, P.R.: Organelle formation from pinocytotic elements in neurites of cultured sympathetic ganglia. J. Neurocytol. 1, 311–340 (1972)
Bloom, F.E., Hoffer, B.J., Siggins, G.R., Barker, J.L., Nicoll, R.A.: Effects of serotonin on central neurons. Microiontophoretic administration. Fed. Proc. 31, 97–106 (1972)
Bodian, D.: An electron microscopic characterization of classes of synaptic vesicles by means of controlled aldehyde fixation. J. Cell Biol. 44, 115–124 (1970)
Brightman, M.W., Reese, T.S.: Junctions between intimately apposed cell membrane in the vertebrate brain. J. Cell Biol. 40, 648–661 (1969)
Calas, A.: L'innervation monoaminergique de l'éminence médiane — étude radiautographique et pharmacologique chez le canard Anas platyrhynchos. I. L'innervation catécholaminergique. Z. Zellforsch. 138, 503–522 (1973)
Chiba, T., Doba, N.: The synaptic structure of catecholaminergic axon varicosities in the dorsomedial portion of the nucleus tractus solitarii of the cat: possible roles in the regulation of cardiovascular reflexes. Brain Res. 84, 31–46 (1975)
Clattenburg, R.E., Singh, R.P., Montemurro, D.G.: Post-coital ultrastructural changes in neurons of the suprachiasmatic nucleus of the rabbit. Z. Zellforsch. 125, 448–459 (1972)
Colonnier, M.: Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscopic study. Brain Res. 9, 268–287 (1968)
Conrad, C.D., Stumpf, W.E.: Retinal projections traced with thaw-mount autoradiography and multiple injections of tritiated precursor or precursor cocktail. Cell Tiss. Res. 155, 283–290 (1974)
Creutzfeldt, O.D.: Reciprocal lateral inhibition of on-and-off-center neurons in the lateral geniculate body of the cat. Exp. Brain Res. 10, 311–330 (1970)
Critchlow, V.: The role of light in the neuroendocrine system. In: Advances in neuroendocrinology (A.W. Nalbankov, ed.), p. 377–426. Urbana: Univ. of Illinois Press 1963
Fuxe, K.: Distribution of monoamine nerve terminals in the central nervous system. Acta physiol. scand. 64, Suppl. 247, 37–85 (1965)
Gray, E.G.: Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscopic study. J. Anat. (Lond.) 93, 420–432 (1959)
Gray, E.G.: Round and flat vesicles in the fish central nervous system. In: Cellular dynamics of the neuron (S.H. Barondes, ed.). Symp. Int. Soc. Cell Biol. 8, 211–227 (1969)
Gray, E.G.: The cytonet, plain and coated vesicles, reticulosomes, multivesicular bodies and nuclear pores. Brain Res. 62, 329–335 (1973)
Gray, E.G.: Synaptic fine structure and nuclear, cytoplasmic and extracellular networks. J. Neurocytol. 4, 315–339 (1975)
Güldner, F.-H., Wolff, J.R.: Multi-lamellar astroglial wrapping of neuronal elements in the hypothalamus of rat. Experientia (Basel) 29, 1355–1356 (1973)
Güldner, F.-H., Wolff, J.R.: Dendro-dendritic synapses in the suprachiasmatic nucleus of the rat hypothalamus. J. Neurocytol. 3, 245–250 (1974)
Hartwig, H.G.: Electron microscopic evidence for a retinohypothalamic projection to the suprachiasmatic nucleus of Passer domesticus. Cell Tiss. Res. 153, 89–99 (1974)
Hendrickson, A.E., Wagoner, N., Cowan, W.M.: An autoradiographic and electron microscopic study of retino-hypothalamic connections. Z. Zellforsch. 135, 1–26 (1972)
Heuser, J.E., Reese, T.S.: Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J. Cell Biol. 57, 315–344 (1973)
King, J.C., Williams, T.H., Gerall, A.A.: Transformations of hypothalamic arcuate neurons. I. Changes associated with stages of the estrous cycle. Cell Tiss. Res. 153, 497–515 (1974)
Krieg, W.J.S.: The hypothalamus of the albino rat. J. comp. Neurol. 55, 19–89 (1932)
Kuffler, S.W., Nicholls, J.G.: The physiology of neuroglial cells. Ergebn. Physiol. 57, 1–90 (1966)
Le Beux, Y.J.: An ultrastructural study of the neurosecretory cells of the medial vascular prechiasmatic gland, the preoptic recess and the anterior part of the suprachiasmatic area. Z. Zellforsch. 114, 404–440 (1971)
Lenn, N.J.: Localization of uptake of tritiated norepinephrine by rat brain in vivo and in vitro using electron microscopic autoradiography. Amer. J. Anat. 120, 377–390 (1967)
Lieberman, A.R., Webster, K.E.: Aspects of the synaptic organization of intrinsic neurons in the dorsal lateral geniculate nucleus. J. Neurocytol. 3, 677–710 (1974)
Makara, G.B., Hodács, L.: Rostral projections from the hypothalamic arcuate nucleus. Brain Res. 84, 23–29 (1975)
Makara, G.B., Rappay, Gy., Stark, E.: Autoradiographic localization of 3H-gamma-aminobutyric acid in the medial hypothalamic hypothalamus. Exp. Brain Res. 22, 229–455 (1975)
Moore, R.Y.: Retinohypothalamic projection in mammals: a comparative study. Brain Res. 49, 403–409 (1973)
Moore, R.Y., Eichler, V.B.: Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Res. 42, 201–206 (1972)
Moore, R.Y., Klein, D.C.: Visual pathways and the central neural control of a circadian rhythm in pineal serotonin N-acetyltransferase activity. Brain Res. 71, 17–34 (1974)
Moore, R.Y., Lenn, N.J.: A retinohypothalamic projection in the rat. J. comp. Neurol. 146, 1–14 (1972)
Morris, J.F., Cannata, M.A.: A possible origin of pale neurosecretory granules in the neurohypophysis. J. Anat. (Lond.) 111, 345–347 (1972)
Morris, J.F., Cannata, M.A.: Ultrastructural preservation of the dense core of posterior pituitary neurosecretory granules and its implications for hormone release. J. Endocr. 57, 517–529 (1973)
Némeček, St.: Principles of synaptic ultrastructure in the central nervous system. In: Collection of Scientific Works of the Faculty of Medicine, Charles University, Hradec Králové, vol. 15, no. 3, p. 221–361 (1972)
Palay, S.L., Chan-Palay, V.: Cerebellar cortex. Cytology and organization. Berlin-Heidelberg-New York: Springer 1974
Párducz, A., Joó, F., Fehér, O.: The role of choline in maintaining the fine structure of nerve terminals in the superior cervical ganglion of cat. J. Neur. Transm. Suppl. 11, 299–314 (1974)
Peters, A., Kaiserman-Abramof, J.R.: The small pyramidal neuron of the rat cerebral cortex. The synapses upon dendritic spines. Z. Zellforsch. 100, 487–506 (1969)
Peters, A., Palay, S.L., Webster, W. de F.: The fine structure of the nervous system. New York-Evanston-London: Hoeber Med. Div., Harper and Row, Publ. 1970
Price, J.L., Powell, T.P.S.: The synaptology of the granule cells of the olfactory bulb. J. Cell Sci. 7, 125–156 (1970)
Prince, F.P., Jones-Witters, P.H.: The ultrastructure of the medial preoptic area of the rat. Cell Tiss. Res. 153, 517–530 (1974)
Reese, T.S., Shepherd, G.M.: Dendro-dendritic synapses in the central nervous system. In: Structure and function of synapses (Pappas G.D., Purpura, E.P., eds.), p. 121–136. New York: Raven Press Publishers; Amsterdam: North-Holland Publishing Company, 1972
Ribak, C.E., Peters, A.: An autoradiographic study of the projections from the lateral geniculate body of the rat. Brain Res. 92, 341–368 (1975)
Saavedra, J.M., Palkovits, M., Brownstein, M.J., Axelrod, J.: Serotonin distribution in the nuclei of the rat hypothalamus and preoptic region. Brain Res. 77, 157–165 (1974)
Spiegel, E.A., Zweig, H.: Zur Cytoarchitektonik des Tuber cinereum. Arb. neurol. Inst. Wien. Univ. 22, 278–312 (1917)
Stephan, F.H., Zucker, I.: Circadian rhythms in drinking behaviour and locomotor activity of rats are eliminated by hypothalamic lesions. Proc. nat. Acad. Sci. (Wash.) 69, 1583–1586 (1972)
Suburo, A.M., Pellegrino de Iraldi, A.: An ultrastructural study of the rat's suprachiasmatic nucleus. J. Anat. (Lond.) 105, 439–446 (1969)
Swanson, L.W., Cowan, W.M.: The efferent connections of the suprachiasmatic nucleus of the hypothalamus. J. comp. Neurol. 160, 1–12 (1975)
Swanson, L.W., Cowan, W.M., Jones, E.G.: An autoradiographic study of the afferent connections of the ventral lateral geniculate nucleus in the albino rat and the cat. J. comp. Neurol. 156, 143–163 (1974)
Szentágothai, J.: Neuronal and synaptic architecture of the lateral geniculate nucleus. Handbook of sensory physiology VII/3. Central Processing of Visual Information, vol. B. In: Visual centers in the brain (R. Jung, ed.), p. 141–176 (1973)
Szentágothai, J., Flerkó, B., Mess, Z., Halász, B.: The hypothalamic control of the anterior pituitary, 3rd ed. Budapest: Akadémiai 1968
Thorpe, P.A.: The presence of a retinohypothalamic projection in the ferret. Brain Res. 85, 343–346 (1975)
Tigges, J., O'Steen, W.K.: Termination of retinofugal fibers in squirrel monkey: a re-investigation using autoradiographic methods. Brain Res. 79, 489–495 (1974)
Tigges, M., Tigges, J., Lange, R.H.: Tilt analysis of pleomorphic vesicles in the superficial layers of the superior colliculus of Galago and chimpanzee. J. Neurocytol. 4, 289–300 (1975)
Uchizono, K.: Characteristics of excitatory and inhibitory synapses in the central nervous system. Nature (Lond.) 207, 642–643 (1965)
Valdivia, O.: Methods of fixation and the morphology of synaptic vesicles. Anat. Rec. 166, 392 (1970)
Vandesande, F., Mey, J. De, Dierickx, K.: Identification of neurophysin producing cells. I. The origin of the neurophysin-like substance-containing nerve fibers of the external region of the median eminence of the rat. Cell Tiss. Res. 151, 187–200 (1974)
Van Harreveld, A., Trubatch, J.: Synaptic changes in frog brain after stimulation with potassium chloride. J. Neurocytol. 4, 33–46 (1975)
Wakefield, C., Hall, E.: Some observations on the ultrastructure of the central amygdaloid nucleus in the cat. Cell Tiss. Res. 151, 489–498 (1974)
Waxman, S.G., Pappas, G.D.: An electron microscopic study of synaptic morphology in the oculomotor nuclei of three inframammalian species. J. comp. Neurol. 143, 41–72 (1971)
Whittaker, V.P., Zimmermann, H., Dowdall, M.J.: The biochemistry of cholinergic synapses as exemplified by the electric organ of Torpedo. J. Neur. Transm., Suppl. XII, 39–60 (1975)
Wolff, J.R., Schieweck, Ch., Emmenegger, H., Meier-Ruge, W.: Cerebrovascular ultrastructural alterations after intraarterial infusions of ouabain, scilla-glycosides, heparin and histamine. Acta neuropath. (Berl.) 31, 45–58 (1975)
Wurtman, R.J.: Effects of light and visual stimuli on endocrine function. In: Neuroendocrinology, vol. II (L. Martini and W.F. Ganong, eds.), pp. 19–59. New York: Academic Press 1967
Záborszky, L., Léránth, C.S., Marton, J., Palkovits, M.: Afferent brainstem pathways to hypothalamus and to limbic system in the rat. In: Hormones and brain function, Budapest 1971, p. 449–457. Budapest: Akadémiai Kiadó, Publishing House of the Hungarian Acad. Sci. 1973
Zimmermann, H., Whittaker, V.P.: Effect of electrical stimulation on the yield and composition of synaptic vesicles from the cholinergic synapses of the electric organ of Torpedo: A combined biochemical, electrophysiological and morphological study. J. Neurochem. 22, 435–450 (1974a)
Zimmermann, H., Whittaker, V.P.: Different recovery rates of the electrophysiological biochemical and morphological parameters in the cholinergic synapses of the Torpedo electric organ after stimulation. J. Neurochem. 22, 1109–1114 (1974b)
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Dedicated to Prof. Dr. Drs. h.c. Wolfgang Bargmann on the occasion of his 70th birthday.
The author wishes to thank Mrs. Ingrid Kräft, Mrs. Annelies Wolff, Mrs. Bassirat Pirouzmandi and Miss Lisa Hildebrandt for excellent technical assistance and Miss Gisela Kotte for preparing the manuscript.
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Güldner, FH. Synaptology of the rat suprachiasmatic nucleus. Cell Tissue Res. 165, 509–544 (1976). https://doi.org/10.1007/BF00224478
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DOI: https://doi.org/10.1007/BF00224478