Summary
Labelled neurons were identified by autoradiography following tangential intracortical injection of [3H]-γ-aminobutyrate (GABA).The addition of cis-1,3-aminocyclohexane carboxylic acid to the GABA solution prevented perikaryal labelling. Labelled neurons were found in each injected layer and in addition they were always present directly above the injection track. The labelling of neurons in layer II. and upper III. following injections in layers V. and VI. can be explained by retrograde axonal transport and indicates that some GABA-ergic neurons project vertically.
Ninety neurons of different types were Golgi impregnated and examined for selective [3H]-GABA uptake. Sixteen of these were labelled. On the basis of dendritic characteristics they were classified as aspiny multipolar neurons with small, medium or large dendritic fields, sparsely spiny multipolar neurons and one neuron was a bipolar cell. Thus Golgi impregnation of their processes reveals that cortical GABA-ergic neurons are a heterogeneous population.
A [3H]-GABA accumulating, aspiny neuron with profoundly branching, “bushy” dendrites and locally arborizing axon in layer VI. was studied in the electron microscope. Its fine structural characteristics were similar to those of other identified non-pyramidal neurons. The existence of several types of cortical GABA-ergic neurons differing in their synaptic connections is discussed.
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Bolam JP, Clarke DJ, Smih AD, Somogyi P (1983) A type of aspiny neuron in the rat neostriatum accumulates 3H-γ-aminobutyric acid: combination of Golgi-staining, autoradiography and electron microscopy. J Comp Neurol 213: 121–134
Bowery NG, Jones GP, Neal MJ (1976) Selective inhibition of neuronal GABA uptake by cis-1,3-aminocyclohexane carboxylic acid. Nature 264: 281–284
Chronwall BM, Wolff JR (1980) Prenatal and postnatal development of GABA-accumulating cells in the occipital neocortex of rat. J Comp Neurol 190: 187–298
Curtis DR, Duggan AW, Johnston FD, McLennan GAR (1971) Antagonism between bicuculline and GABA in the cat brain. Brain Res 33: 57–73
Fairén A, Valver de F (1980) A specialized type of neuron in the visual cortex of cat: a Golgi and electron microscope study of chandelier cells. J Comp Neurol 194: 761–780
Fairén A, DeFelipe J, Martinez-Ruiz R (1981) The Golgi-EM procedure: a tool to study neocortical interneurons. Glial and neuronal cell biology (11th Int Cong Anat) AR Liss, NewYork, pp 291–301
Feldman ML, Peters A (1978) The forms of non-pyramidal neurons in the visual cortex of the rat. J Comp Neurol 179: 761–793
Freund TF, Somogyi P (1983) The section-Golgi impregnation procedure. I. Description of the method and its combination with histochemistry after intracellular iontophoresis or retrograde transport of horseradish peroxidase. Neuroscience 9: 463–474
Garey LJ (1976) Synaptic organization of afferent fibres and intrinsic circuits in the neocortex. In: Rémond A (ed) Handbook of electroencephalography and clinical neurophysiology, vol 2A. Elsevier, Amsterdam, pp 57–85
Halász N, Ljungdahl Å, Hökfelt T (1979) Transmitter histochemistry of the rat olfactory bulb. III. Autoradiographic localization of [3H]-GABA. Brain Res 167: 221–240
Hedlich A, Winkelmann E (1982) Neuronentypen des visuellen Cortex der adulten und juvenilen Ratte. J Hirnforsch 23: 353–373
Hendrickson AE, Hunt SP, Wu JY (1981) Immunocytochemical localisation of glutamic acid decarboxylase in monkey striate cortex. Nature 292: 605–607
Hendry SHC, Jones EG (1981) Sizes and distributions of intrinsic neurons incorporating tritiated GABA in monkey sensory-motor cortex. J Neurosci 1: 390–408
Hökfelt T, Ljungdahl Å (1972) Autoradiographic identification of cerebral and cerebellar cortical neurons accumulating labeled gamma-aminobutyric acid (3H-GABA). Exp Brain Res 14: 354–362
Hornung JP, Garey LJ (1981) The thalamic projection to cat visual cortex: Ultrastructure of neurons identified by Golgi impregnation or retrograde horseradish peroxidase transport. Neuroscience 6: 1053–1068
Hunt SP, Künzle H (1976) Selective uptake and transport of label within three identified neuronal systems after injection of 3H-GABA into the pigeon optic tectum: an autoradiographic and Golgi study. J Comp Neurol 170: 173–190
Iversen LL, Mitchell JF, Srinivasan V (1971) The release of γ-aminobutyric acid during inhibition in the cat visual cortex. J Physiol (Lond) 212: 519–534
Krnjevic K, Schwartz S (1967) The action of γ-aminobutyric acid on cortical neurones. Exp Brain Res 3: 320–336
Lund JS (1973) Organization of neurons in the visual cortex, area 17, of the monkey (Macaca mulatta). J Comp Neurol 147: 455–496
Lund JS, Henry GH, Macqueen CL, Harvey AR (1979) Anatomical organization of primary visual cortex (area 17) of the cat. A comparison with area 17 of the Macaque monkey. J Comp Neurol 184: 599–618
Martin KAC, Somogyi P, Whitteridge D (1983) Physiological and morphological properties of identified basket cells in the cat's visual cortex. Exp Brain Res 50: 193–200
Parnavelas JG, Lieberman AR, Webster KE (1977) Organization of neurons in the visual cortex, area 17, of the rat. J Anat 124: 305–322
Peters A, Fairén A (1978) Smooth and sparsely-spined stellate cells in the visual cortex of the rat: a study using a combined Golgi-electron microscope technique. J Comp Neurol 181: 129–172
Peters A, Proskauer CC (1980) Synaptic relationships between a multipolar stellate cell and a pyramidal neuron in the rat visual cortex — a combined Golgi-electron microscope study. J Neurocytol 9: 163–184
Peters A, Proskauer CC, Ribak CE (1982) Chandelier cells in rat visual cortex. J Comp Neurol 206: 397–416
Ribak CE (1978) Aspinaous and sparsely-spinous stellate neurons in the visual cortex of rats contain glutamic acid decarboxylase. J Neurocytol 7: 461–478
Ribak CE, Vaughn JE, Saito K, Barber R, Roberts E (1977) Glutamate decarboxylase localization in neurons of the olfactory bulb. Brain Res 126: 1–18
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: 261–284
Rose D, Blakemore C (1974) Effects of bicuculline on functions of inhibition in visual cortex. Nature 249: 375–377
Saito K, Barber R, Wu J-Y, Matsuda T, Roberts E, Vaughn JE (1974) Immunohistochemical localization of glutamic acid decarboxylase in rat cerebellum. Proc Natl Acad Scid USA 71: 269–273
Schober W, Winkelmann E (1975) Der visuelle Kortex der Ratte. Cytoarchitektonik and stereotaktische Parameter. Z Mikrosk-Anat Forsch 89: 431–446
Schon F, Iversen LL (1972) Selective accumulation of (3H) GABA by stellate cells in rat cerebellar cortex in vivo. Brain Res 42: 503–507
Sillito AM (1975) The effectiveness of bicuculline as an antagonist of GABA and visually evoked inhibition in cat's striate cortex. J Physiol (Lond) 250: 287–304
Somogyi P (1977) A specific axo-axonal interneuron in the visual cortex of the rat. Brain Res 136: 345–350
Somogyi P, Cowey A, Halász N, Freund TF (1981a) Vertical organization of neurons accumulating 3H-GABA in the visual cortex of the rhesus monkey. Nature 294: 761–763
Somogyi P, Freund TF, Halász N, Kisvárday ZF (1981b) Selectivity of neuronal 3H-GABA accumulation in the visual cortex as revealed by Golgi staining of the labelled neurons. Brain Res 225: 431–436
Somogyi P, Cowey A, Kisvárday ZF, Freund TF, Szentágothai J (1983a) Retrograde transport of 3H-GABA reveals specific interlaminar connections in the striate cortex of monkey. Proc Natl Acad Sci USA 80: 2385–2389
Somogyi P, Freund TF, Cowey A (1982) The axo-axonic interneuron in the cerebral cortex of the rat, cat and monkey. Neuroscience 7: 2577–2608
Somogyi P, Freund TF, Wu J-Y, Smith AD (1983b) The section Golgi impregnation procedure. II. Immunocytochemical demonstration of glutamate decarboxylase in Golgi-impregnated neurons and in their afferent synaptic boutons in the visual cortex of the cat. Neuroscience 9: 475–490
Somogyi P, Smith AD, Nunzi MG, Gorio A, Takagi H, Wu J-Y (1983c) Glutamate decarboxylase immunoreactivity in the hippocampus of the cat. Distribution of immunoreactive synaptic terminals with special reference to the axon initial segment of pyramidal neurons. J Neurosci (in press)
Streit P, Knecht E, Cuénod M (1979) Transmitter-specific retrograde labeling in the striato-nigral and raphe-nigral pathways. Science 205: 306–307
Szentágothai J (1973) Synaptology of the visual cortex. In: Jung R (ed) Handbook of sensory physiology, central processing of visual information, vol VII/3B. Springer, Berlin Heidelberg New York, pp 269–324
Tömböl T, Madarász M, Hajdu F, Somogyi Gy (1976) Some data on the Golgi architecture of visual areas and suprasylvian gyrus in the cat. Verh Anat Ges 70: 271–275
Tsumoto T, Eckart W, Creutzfeldt OD (1979) Modification of orientation sensitivity of cat visual cortex neurons by removal of GABA-mediated inhibition. Exp Brain Res 34: 351–365
Valverde F (1971) Short axon neuronal subsystems in the visual cortex of the monkey. Int J Neurosci 1: 181–197
Werner L, Hedlich A, Winkelmann E, Brauer K (1979) Versuch einer Identifizierung von Nervenzellen des Visuellen Kortex der Ratte nach Nissl- und Golgi-Kopsch Darstellung. J Hirnforsch 20: 121–139
Wolff JR, Chronwall BM (1982) Axosomatic synapses in the visual cortex of adult rat — a comparison between GABA-accumulating and other neurons. J Neurocytol 11: 409–426
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Financially supported by the Hungarian Academy of Sciences, the International Cultural Institute of Budapest, the Wellcome Trust, the Royal Society, and the E. P. Abraham Cephalosporin Trust
During part of this project P. Somogyi was supported by the Wellcome trust at Dept. of Pharmacology, Oxford University
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Somogyi, P., Freund, T.F. & Kisvárday, Z.F. Different types of 3H-GABA accumulating neurons in the visual cortex of the rat. Characterization by combined autoradiography and Golgi impregnation. Exp Brain Res 54, 45–56 (1984). https://doi.org/10.1007/BF00235817
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DOI: https://doi.org/10.1007/BF00235817