Summary
GABAergic neurons have been identified in monkey sensory-motor cerebral cortex by light microscopic, immunocytochemical localization of the GABA synthesizing enzyme, glutamic acid decarboxylase (GAD). All GAD-positive neurons are non-pyramidal cells. Their somata are present in all layers and are evenly distributed across layers II-VI of the motor cortex (area 4), but are found in greater concentrations in layers II, IV and VI of all areas of first somatic sensory cortex (SI; areas 3a, 3b and 1–2). GAD-positive puncta (putative axon terminals) are present throughout the sensory-motor cortex, and they are found immediately adjacent to the somata, dendrites and presumptive axon initial segments of GAD-negative pyramidal cells. In addition, they are observed in close approximation to the somata of both large and small GAD-positive neurons. In area 4, the density of puncta is highest in the superficial cortical layers (layers I-III) and gradually declines throughout the deeper layers. In SI, the highest densities of puncta are present in layer IV, while moderately high densities are found in layers I-III and VI. In areas 3a and 3b, the puncta in layers IV and VI are particularly numerous and form foci that exhibit greater density than adjacent regions.
GAD-positive neurons withlarge somata, 15–33 μ in diameter, are present in layers IIIB-VI of all areas. Such cells have many primary dendrites that radiate in all directions. In addition they have axons that ascend either from the superficial aspect of the somata or from primary dendrites, and that exhibit horizontal collateral branches. These neurons closely resemble the large basket cells (Marin-Padilla, 1969; Jones, 1975), and they may give rise to many of the GAD-positive endings surrounding the somata and proximal dendrites of pyramidal cells in layers III-VI. In addition,small GAD-positive somata are present in all layers, but they are most numerous in layers II and IIIA of all areas and in layer IV of SI. The somata and proximal dendrites of these cells vary from a multipolar shape with small, beaded dendrites, found primarily in layer IV, to bitufted and multipolar shapes with larger, smooth dendrites. The diversity of somal sizes and locations, the variety of dendritic patterns, and the different distributions of GAD-positive puncta, all combine to suggest that several different morphological classes of intrinsic comprise the GABA neurons of monkey cerebral cortex.
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References
Barber, R. &Saito, K. (1976) Light microscopic visualization of GAD and GABA-T in immunocytochemical preparations of rodent C.N.S. InGABA in Nervous System Function (edited byRoberts, E., Chase, T. N. andTower, D. B.), pp. 113–32. New York: Raven Press.
Cajal, S., Ramón, Y. (1911)Histologie du Système Nerveux de l'Homme et des Vertébrés Vol. 2 (translated byAzoulay, S.). Paris: Maloine.
Chronwall, B. M. &Wolff, J. R. (1978) Classification and location of neurons taking up [3H]-GABA in the visual cortex of rats. InAmino Acids as Chemical Transmitters (edited byFonnum, F.), pp. 297–303. New York: Plenum Press.
Emson, P. C. &Hunt, S. P. (1981) Anatomical chemistry of the cerebral cortex. InThe Organization of the Cerebral Cortex (edited bySchmitt, F. O., Worden, F. G., Adelman, G. andDennis, S. G.), pp. 325–45. Cambridge: MIT Press.
Emson, P. C. &Lindvall, O. (1979) Distribution of putative neurotransmitters in the neocortex.Neuroscience 4, 1–30.
Fairén, A. &Valverde, F. (1980) A specialized type of neuron in the visual cortex of the cat: a Golgi and electron microscopic study of chandelier cells.Journal of Comparative Neurology 194, 761–80.
Hendrickson, A. E., Hunt, S. P. &Wu, J. -Y. (1981) Immunocytochemical localization of glutamic acid decarboxylase in monkey striate cortex.Nature 292, 605–7.
Hendry, S. H. C., Houser, C. R., Jones, E. G. &Vaughn, J. E. (1983) Synaptic organization of immunocytochemically identified GABA neurons in the monkey sensory-motor cortex.Journal of Neurocytology 12, 639–660.
Hendry, S. H. C. &Jones, E. G. (1981) Sizes and distributions of intrinsic neurons incorporating tritiated GABA in monkey sensory-motor cortex.Journal of Neuroscience 1, 390–408.
Hirsch, H. &Robins, E. (1962) Distribution of γ-aminobutyric acid in the layers of the cerebral and cerebellar cortex. Implications for its physiological role.Journal of Neurochemistry 9, 63–70.
Hökfelt, T. &Ljungdahl, Å. (1972) Autoradiographic identification of cerebral and cerebellar cortical neurons accumulating labelled gamma-aminobutyric acid (3H-GABA).Experimental Brain Research 14, 354–62.
Houser, C. R., Vaughn, J. E., Jones, E. G. &Hendry, S. H. C. (1980) GABA neurons of monkey motor and sensory cortex: An immunocytochemical study.Abstracts of the Society for Neuroscience 6, 159.
Jones, E. G. (1975) Varieties and distribution of non-pyramidal cells in the somatic sensory cortex of the squirrel monkey.Journal of Comparative Neurology 160, 205–68.
Jones, E. G. (1981) Anatomy of cerebral cortex: columnar input-output organization. InThe Organization of the Cerebral Cortex (edited bySchmitt, F. O., Worden, F. G., Adelman, G. andDennis, S. G.), pp. 199–235. Cambridge, MA: MIT Press.
Jones, E. G. &Wise, S. P. (1977) Size, laminar and columnar distribution of efferent cells in the sensory-motor cortex of monkeys.Journal of Comparative Neurology 175, 391–438.
Krnjević, K. (1974) Chemical nature of synaptic transmission in vertebrates.Physiological Reviews 54, 418–540.
Marin-Padilla, M. (1969) Origin of the pericellular baskets of the pyramidal cells of the human motor cortex: a Golgi study.Brain Research 14, 633–46.
Marin-Padilla, M. (1972) Double origin of the pericellular baskets of the pyramidal cells of the human motor cortex: a Golgi study.Brain Research 38, 1–12.
Marin-Padilla, M. (1974) Three-dimensional reconstruction of the pericellular nests (baskets) of the motor (area 4) and visual (area 17) areas of the human cerebral cortex. A Golgi study.Zeitschrift für Anatomie und Entwicklungsgeschichte 144, 123–35.
McLaughlin, B. J., Wood, J. G., Saito, K., Barber, R., Vaughn, J. E., Roberts, E. &Wu, J. -Y. (1974) The fine structural localization of glutamate decarboxylase in synaptic terminals of rodent cerebellum.Brain Research 76, 377–91.
Mountcastle, V. B. (1979) An organizing principle for cerebral function: the unit module and the distributed system. InThe Neurosciences: Fourth Study Program (edited bySchmitt, F. O. andWorden, F. G.), pp. 21–42. Cambridge: MIT Press.
Oertel, W. H., Schmechel, D. E., Mugnaini, E., Tappaz, M. L. &Kopin, I. J. (1981) Immunocytochemical localization of glutamate decarboxylase in rat cerebellum with a new antiserum.Neuroscience 6, 2715–35.
Pérez de la Mora, M., Passani, L. D., Tapia, R., Teran, L., Palacios, R., Fuxe, K., Hökfelt, T. &Ljungdahl, Å. (1981) Demonstration of central γ-aminobutyrate-containing nerve terminals by means of antibodies against glutamate decarboxylase.Neuroscience 6, 875–95.
Peters, A. &Proskauer, C. C. (1980) Smooth or sparsely spined cells with myelinated axons in rat visual cortex.Neuroscience 5, 2079–92.
Peters, A., Proskauer, C. C. &Ribak, C. E. (1982) Chandelier cells in rat visual cortex.Journal of Comparative Neurology 206, 397–416.
Peters, A. &Regidor, J. (1981) A reassessment of the forms of nonpyramidal neurons in area 17 of cat visual cortex.Journal of Comparative Neurology 203, 685–716.
Ribak, C. E. (1978) Aspinous and sparsely spinous stellate neurons in the visual cortex of rats contain glutamic acid decarboxylase.Journal of Neurocytology 7, 461–78.
Ribak, C. E., Harris, A. B., Vaughn, J. E. &Roberts, E. (1979) Inhibitory, GABAergic nerve terminals decrease at sites of focal epilepsy.Science 205, 211–4.
Ribak, C. E., Vaughn, J. E. &Saito, K. (1978) Immunocytochemical localization of glutamic acid decarboxylase in neuronal somata following colchicine inhibition of axonal transport.Brain Research 140, 315–32.
Saito, K., Wu, J. -Y., Matsuda, T. &Roberts, E. (1974) Immunochemical comparisons of vertebrate glutamic acid decarboxylase.Brain Research 65, 277–85.
Sillito, A. M. (1975) The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat.Journal of Physiology 250, 305–29.
Slemmon, J. R., Salvaterra, P. M. &Saito, K. (1980) Preparation and characterization of peroxidase: antiperoxidase-Fab complex.Journal of Histochemistry and Cytochemistry 28, 10–5.
Sloper, J. J., Johnson, P. &Powell, T. P. S. (1980) Selective degeneration of interneurons in the motor cortex of infant monkeys following controlled hypoxia: a possible cause of epilepsy.Brain Research 198, 204–9.
Somogyi, P. (1977) A specific ‘axo-axonal’ interneuron in the visual cortex of the rat.Brain Research 136, 345–50.
Sternberger, L. A. (1979)Immunocytochemistry 2nd edn. pp. 104–69. New York: Wiley and Sons.
Szentágothai, J. (1979) Local neuron circuits of the neocortex. InThe Neurosciences: Fourth Study Program (edited bySchmitt, F. O. andWorden, F. G.), pp. 399–415. Cambridge: MIT Press.
Szentágothai, J. &Arbib, M. A. (1974) Conceptual models of neural organization.Neurosciences Research Program Bulletin 12, 307–510.
Tsumoto, T., Eckhart, W. &Creutzfeldt, O. D. (1979) Modification of orientation sensitivity of cat visual cortex neurons by removal of GABA-mediated inhibition.Experimental Brain Research 34, 351–63.
Ulmar, G., Ljungdahl, Å. &Hökfelt, T. (1975) Enzyme changes after undercutting of cerebral cortex in the rat.Experimental Neurology 46, 199–208.
Ulmar, G. &Neuhoff, V. (1980) Free amino acids in the isolated cortex of the rat determined by the Dns microassay.Experimental Neurology 69, 99–109.
Valverde, F. (1971) Short axon neuronal subsystems in the visual cortex of the monkey.International Journal of Neuroscience 1, 181–97.
Vaughn, J. E., Barber, R. P., Ribak, C. E. &Houser, C. R. (1981) Methods for the immunocytochemical localization of proteins and peptides involved in neurotransmission. InCurrent Trends in Morphological Techniques Vol. III (edited byJohnson, J. E.), pp. 33–70. Boca Raton: CRC Press Inc.
Wood, J. G., McLaughlin, B. J. &Vaughn, J. E. (1976) Immunocytochemical localization of GAD in electron microscopic preparations of rodent C.N.S. InGABA in Nervous System Function (edited byRoberts, E., Chase, T. N. andTower, D. B.), pp. 133–48. New York: Raven Press.
Wu, J. -Y., Matsuda, T. &Roberts, E. (1973) Purification and characterization of glutamate decarboxylase from mouse brain.Journal of Biological Chemistry 248, 3029–34.
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Houser, C.R., Hendry, S.H.C., Jones, E.G. et al. Morphological diversity of immunocytochemically identified GABA neurons in the monkey sensory-motor cortex. J Neurocytol 12, 617–638 (1983). https://doi.org/10.1007/BF01181527
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DOI: https://doi.org/10.1007/BF01181527