Summary
Nerve cells of the human striatum were investigated with the use of a newly developed technique that reveals the pattern of pigmentation of individual nerve cells by means of transparent Golgi impregnations of their cell bodies and processes. Five types of neurons are distinguished:
Type I is a medium-sized spine-laden neuron with an axon giving off a great number of collateral branches. The vast majority of the cells in the striatum belong to this type. Numerous intensely stained lipofuscin granules are contained in one pole of the cell body and may also extend into adjacent portions of a dendrite.
Type II is a medium-sized to large neuron with long intertwining dendrites decorated with spines of uncommon shape. A distinguishing feature of this cell type is the presence of somal spines. This cell type is devoid of pigment or contains only a few tiny lipofuscin granules.
Type III is a large multipolar neuron. The cell body generates a few rather extended dendrites that are very sparsely spined. The finely granulated pigment is evenly dispersed within a large portion of the cytoplasm.
Type IV is a large aspiny neuron with rounded cell body and richly branching tortuous dendrites. The axon branches frequently in the vicinity of the parent soma. Large pigment granules are concentrated within a circumscribed part of the cell body close to the cell membrane.
Type V is a small to medium-sized aspiny neuron. The dendrites break up into a swirling mass of thin branches. More than one axon may be given off from the soma. The axons branch close to the soma into terminal twigs. Cells of this type contain numerous large and well-stained lipofuscin granules.
Each of the cell types has a characteristic pattern of pigmentation. The different varieties of nerve cells in the striatum can therefore be distinguished not only in Golgi impregnations but also in pigment-Nissl preparations.
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References
Adinolfi AM, Pappas GD (1968) The fine structure of the caudate nucleus of the cat. J Comp Neurol 133:167–184
Anderson CA, Westrum LE (1972) An electron microscopic study of the normal synaptic relationships and early degenerative changes in the rat olfactory tubercle. Z Zellforsch 127:462–482
Bak IJ, Markham CH, Cook ML, Stevens JG (1978) Ultrastructural and immunoperoxidase study of striatonigral neurons by means of retrograde axonal transport of Herpes simplex virus. Brain Res 143:361–369
Bolam JP, Somogyi P, Totterdell S, Smith AD (1981) A second type of striatonigral neuron: a comparison between retrogradely labelled and Golgi-stained neurons at the light and electron microscopic levels. Neuroscience 6:2141–2157
Braak H (1980) Architectonics of the human telencephalic cortex. In: Braitenberg V, Barlow HB, Florey E, Grüsser OJ, van der Loos H (eds) Studies of brain function. Vol 4. Springer, Berlin Heidelberg New York
Braak H Transparent Golgi impregnations: a way to examine both details of the cellular processes and components of the cell body. Stain Technol (in press)
Braak H, Braak E (1976) The pyramidal cells of Betz within the cingulate and precentral gigantopyramidal field in the human brain. A Golgi and pigmentarchitectonic study. Cell Tissue Res 172:103–119
Braak H, Braak E (1982) Neuronal types in the claustrum of man. Anat Embryol 163:447–460
Bradford R, Parnavelas JG, Lieberman AR (1977) Neurons in layer I of the developing occipital cortex of the rat. J Comp Neurol 176:121–132
Braitenberg V, Guglielmotti U, Sada E (1967) Correlation of crystal growth with the staining of axons by the Golgi procedure. Stain Technol 42:277–283
Brockhaus H (1942) Zur feineren Anatomie des Septum und des Striatum. J Psychol Neurol 51:1–56
Bunney BS, Aghajanian GK (1976) The precise localization of nigral afferents in the rat as determined by retrograde tracing technique. Brain Res 117:423–435
Chronister RB, Farnell KE, Marco LA, White LE (1976) The rodent neostriatum: A Golgi analysis. Brain Res 108:37–46
Chung JW, Hassler R, Wagner A (1976) Degenerated boutons in the fundus striati (nucleus accumbens septi) after lesion of the parafascicular nucleus in the cat. Cell Tissue Res 172:1–14
Chung JW, Hassler R, Wagner A (1977) Degeneration of two out of nine types of synapses in the putamen after center median coagulation in the cat. Exp Brain Res 28:345–361
Danner H, Pfister C (1981a) Spine-haltige Neurone im Caudatus-Putamen-Komplex der Ratte. J Hirnforsch 22:75–84
Danner H, Pfister C (1981b) Darstellung spine-haltiger Zwerg-Neurone im Caudatus-Putamen-Komplex der Ratte nach Pargylin-Applikation. Z Mikrosk Anat Forsch 95:210–216
Diaz-Cintra S, Cintra L, Kemper T, Resnick O, Morgane PJ (1981) Nucleus raphe dorsalis: A morphometric Golgi study in rats of three age groups. Brain Res 207:1–16
DiFiglia M, Pasik P, Pasik T (1976) A Golgi study of neuronal types in the neostriatum of monkeys. Brain Res 114:245–256
DiFiglia M, Pasik T, Pasik P (1980) Ultrastructure of Golgi-impregnated and gold-toned spiny and aspiny neurons in the monkey neostriatum. J Neurocytol 9:471–492
Dimova R, Vuillet J, Seite R (1980) Study of the rat neostriatum using a combined Golgi-electron microscope technique and serial sections. Neuroscience 5:1581–1596
Feremutsch K (1961) Basalganglien. In: Hofer H, Schultz AH, Starck D (eds) Primatologia. Vol II/2. Karger, Basel New York, pp 1–87
Fox CA, Andrade AN, Hellman DE, Schwyn RC (1971/72a) The spiny neurons in the primate striatum: A Golgi and electron microscopic study. J Hirnforsch 13:181–201
Fox CA, Andrade AN, Schwyn RC, Rafols JA (1971/72b) The aspiny neurons and the glia in the primate striatum: A Golgi and electron microscopic study. J Hirnforsch 13:341–362
Fox CA, LuQui IJ, Rafols JA (1974) Further observations on Ramón y Cajal's “dwarf” or “neurogliaform” neurons and the oligodendroglia in the primate striatum. J Hirnforsch 15:517–527
Frotscher M, Rinne U, Hassler R, Wagner A (1981) Termination of cortical afferents on identified neurons in the caudate nucleus of the cat. A combined Golgi-EM degeneration study. Exp Brain Res 41:329–337
Grofova I (1975) The identification of striatal and pallidal neurons projecting to the substantia nigra. An experimental study by means of retrograde axonal transport of horseradish peroxidase. Brain Res 91:286–291
Hassler R (1978) Striatal control of locomotion, intentional actions and of integrating and perceptive activity. J Neurol Sci 36:187–224
Hassler R, Usunoff KG, Wagner A, Bak IJ (1975) Über die doppelläufigen Verbindungen zwischen Striatum und Substantia nigra im licht-ubd elektronenmikroskopischen Bild bei der Katze. Anat Anz 137:357–368
Hassler R, Ahn ET, Wagner A, Kim JS (1978a) Experimenteller Nachweis von intrastriatalen Synapsentypen und Axon-Kollateralen durch Isolierung des Fundus striati von allen extrastriatalen Verbindungen. Anat Anz 143:413–436
Hassler R, Chung JW, Rinne U, Wagner A (1978b) Selective degeneration of two out of nine types of synapses in cat caudate nucleus after cortical lesions. Exp Brain Res 31:67–80
Hattori T, Fibiger HC, Mc Geer PL, Maler L (1973) Analysis of the fine structure of the dopaminergic nigrostriatal projection by electron microscopic autoradiography. Exp Neurol 41:599–611
Jacobson S (1967) Dimensions of the dendritic spine in the sensorimotor cortex of the rat, cat, squirrel monkey and man. J Comp Neurol 129:49–58
Jones EG, Powell TPS (1969) Morphological variations in the dendritic spines of the neocortex. J Cell Sci 5:509–529
Kemp JM (1968) Observations on the caudate nucleus of the cat impregnated with the Golgi method. Brain Res 11:467–470
Kemp JM, Powell TPS (1971a) The structure of the caudate nucleus of the cat: Light and electron microscopy. Phil Trans R Soc Lond B, 262:383–401
Kemp JM, Powell TPS (1971b) The site of termination of afferent fibres in the caudate nucleus. Phil Trans R Soc Lond B, 262:413–427
Kemp JM, Powell TPS (1971 c) The termination of fibres from the cerebral cortex and thalamus upon dendritic spines in the caudate nucleus: A study with the Golgi method. Phil Trans R Soc Lond B, 262:429–439
King JS, Schwyn RC, Fox CA (1971) The red nucleus in the monkey (Macaca mulatta): A Golgi and an electron microscopic study. J Comp Neurol 142:75–108
Kocsis JD, Sugimori M, Kitai ST (1977) Convergence of excitatory synaptic inputs to caudate spiny neurons. Brain Res 124:403–413
Koelliker A (1896) Handbuch der Gewebelehre des Menschen. Vol 2 (Aufl. 6) Engelmann, Leipzig
Laemle LK (1979) Neuronal populations of the human periaqueductal gray, nucleus lateralis. J Comp Neurol 186:93–108
Meller K, Breipohl W, Glees P (1969) Ontogeny of the mouse motor cortex. The polymorph layer or layer VI. A Golgi and electronmicroscopical study. Z Zellforsch 99:443–458
Mensah P, Deadwyler S (1974) The caudate nucleus of the rat: Cell types and the demonstration of a commissural system. J Anat (Lond) 117:281–293
Meyer G (1982) Short-axon neurons with two axon-like processes in the visual cortex of the cat. A Golgi study. Brain Res 232:455–459
Millhouse OE (1981) The Golgi methods. In: Heimer L, Robards MJ (eds) Neuroanatomical tracttracing methods. Plenum Press, New York London, pp 311–344
Nakamura Y (1975) An electron microscope study of the red nucleus in the cat, with special reference to the quantitative analysis of the axosomatic synapses. Brain Res 94:1–17
Namba M (1957) Cytoarchitektonische Untersuchungen am Striatum. J Hirnforsch 3:24–48
Norton S, Culver B (1977) A Golgi analysis of caudate neurons in rats exposed to carbon monoxide. Brain Res 132:455–465
Palay SL, Chan-Palay V (1974) Cerebellar cortex. Cytology and organization. Springer, Berlin Heidelberg New York
Pasik P, Pasik T, DiFiglia M (1979) The internal organization of the neostriatum in mammals. In: Divac I, Oberg RGE (eds) The neostriatum. Pergamon Press, Oxford New York, pp 5–36
Pasquier DA, Kemper TL, Forbes WB, Morgane PJ (1977) Dorsal raphe, substantia nigra and locus coeruleus: Interconnections with each other and the neostriatum. Brain Res Bull 2:323–339
Peters A, Kaiserman-Abramof IR (1970) The small pyramidal neuron of the rat cerebral cortex. The perikaryon, dendrites, and spines. Am J Anat 127:321–356
Pfister C, Danner H (1980) Fluoreszenzhistochemische und neurohistologische Untersuchungen am Nucleus raphes dorsalis der Ratte. Acta Histochem 66:253–261
Preston RJ, Bishop GA, Kitai ST (1980) Medium spiny neuron projection from the rat striatum: An intracellular horseradish peroxidase study. Brain Res 183:253–263
Rafols JA, Fox CA (1976) The neurons in the primate subthalamic nucleus: A Golgi and electron microscopic study. J Comp Neurol 168:75–111
Rafols JA, Fox CA (1979) Fine structure of the primate striatum. Appl Neurophysiol 42:13–16
Ramón y Cajal S (1891) Sur la structure de l'écorce cérébrale de quelques mammifères. Cellule 7:123–176
Ramón y Cajal S (1909) Histologie du système nerveux de l'homme et des vertébrés. Maloine, Paris. (Consejo superior de investigaciones cientificas, Madrid. Reprinted 1952 und 1955)
Reid JM, Gwyn DG, Flumerfelt BA (1975 a) A cytoarchitectonic and Golgi-study of the red nucleus in the rat. J Comp Neurol 162:337–362
Reid JM, Flumerfelt A, Gwyn DG (1975 b) An ultrastructural study of the red nucleus in the rat. J Comp Neurol 162:363–386
Retzius G (1893) Die Cajal'schen Zellen der Großhirnrinde beim Menschen und bei Säugetieren. Biol Unters 5:1–9
Ribak CE, Vaughn JE, Roberts E (1979) The GABA neurons and their axon terminals in rat corpus striatum as demonstrated by GAD immunocytochemistry. J Comp Neurol 187:261–283
Sadun AA, Pappas GD (1978) Development of distinct cell types in the feline red nucleus: A Golgi-Cox and electron microscopic study. J Comp Neurol 182:315–366
Schröder KF, Hopf A, Lange H, Thörner G (1975) Morphometrisch-statistische Strukturanalysen des Striatum, Pallidum und Nucleus subthalamicus beim Menschen. J Hirnforsch 16:333–350
Somogyi P, Smith AD (1979) Projection of neostriatal spiny neurons to the substantia nigra. Application of a combined Golgi-staining and horseradish peroxidase transport procedure at both light and electron microscopic levels. Brain Res 178:3–15
Somogyi P, Bolam JP, Smith AD (1981) Monosynaptic cortical input and local axon collaterals of identified striatonigral neurons. A light and electron microscopic study using the Golgi-peroxidase transport degeneration procedure. J Comp Neurol 195:567–584
Usunoff KG, Hassler R, Romansky K, Usunova P (1976) The nigrostriatal projection in the cat. Part I. Silver impregnation study. J Neurol Sci 28:265–288
Vogt C, Vogt O (1920) Zur Lehre der Erkrankungen des striären Systems. J Psychol Neurol 25:628–846
Wilson CJ, Groves PM (1980) Fine structure and synaptic connections of the common spiny neuron of the rat neostriatum: A study employing intracellular injection of horseradish peroxidase. J Comp Neurol 194:599–615
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Braak, H., Braak, E. Neuronal types in the striatum of man. Cell Tissue Res. 227, 319–342 (1982). https://doi.org/10.1007/BF00210889
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DOI: https://doi.org/10.1007/BF00210889