Laminar distribution and neuronal targets of GABAergic axon terminals in cat primary auditory cortex (AI)

The form, density, and neuronal targets of presumptive axon terminals (puncta) that were immunoreactive for gamma‐aminobutyric acid (GABA) or its synthesizing enzyme, glutamic acid decarboxylase (GAD), were studied in cat primary auditory cortex (AI) in the light microscope. High‐resolution, plastic‐embedded material and frozen sections were used. The chief results were: (1) There was a three‐tiered numerical distribution of puncta, with the highest density in layer Ia, an intermediate number in layers Ib–IVb, and the lowest concentration in layers V and VI, respectively. (2) Each layer had a particular arrangement: layer I puncta were fine and granular (less than 1 μm), and layer V and VI puncta were mixed in size and predominantly small. (3) The form and density of puncta in every layer were distinctive. (4) Immunonegative neurons received, in general, many more axosomatic puncta than immunopositive cells, with the exception of the large multipolar (presumptive basket) cells, which invariably had many puncta in layers II–VI. (5) The number of puncta on the perikarya of GABAergic neurons was sometines related to the number of puncta in the layer, and in other instances it was independent of the layer. Thus, while layer V had a proportion of GABAergic neurons similar to layer IV, it had only a fraction of the number of puncta: perhaps the intrinsic projections of supragranular GABAergic cells are directed toward layer IV, as those of infragranular GABAergic neurons may be.

[1]  A. Hendrickson,et al.  Immunocytochemical localization of glutamic acid decarboxylase in monkey striate cortex , 1981, Nature.

[2]  A Keller,et al.  Synaptic organization of GABAergic neurons in the mouse SmI cortex , 1987, The Journal of comparative neurology.

[3]  P. Somogyi,et al.  Identified axo-axonic cells are immunoreactive for GABA in the hippocampus visual cortex of the cat , 1985, Brain Research.

[4]  P S Goldman-Rakic,et al.  Quantitative autoradiography of major neurotransmitter receptors in the monkey striate and extrastriate cortex , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  J. E. Vaughn,et al.  Synaptic organization of immunocytochemically identified GABA neurons in the monkey sensory-motor cortex , 1983, Journal of neurocytology.

[6]  Kisou Kubota,et al.  Morphological differences between fast and slow pyramidal tract neurons in the monkey motor cortex as revealed by intracellular injection of horseradish peroxidase by pressure , 1981, Neuroscience Letters.

[7]  J. E. Vaughn,et al.  GABA Neurons in the Cerebral Cortex , 1984 .

[8]  J. Winer,et al.  Populations of GABAergic neurons and axons in layer I of rat auditory cortex , 1989, Neuroscience.

[9]  C. Ribak,et al.  Aspinous and sparsely-spinous stellate neurons in the visual cortex of rats contain glutamic acid decarboxylase , 1978, Journal of neurocytology.

[10]  M. Konishi,et al.  Calcium binding protein-like immunoreactivity labels the terminal field of nucleus laminaris of the barn owl , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  M. Ahissar,et al.  Encoding of sound-source location and movement: activity of single neurons and interactions between adjacent neurons in the monkey auditory cortex. , 1992, Journal of neurophysiology.

[12]  J. DeFelipe,et al.  The pyramidal neuron of the cerebral cortex: Morphological and chemical characteristics of the synaptic inputs , 1992, Progress in Neurobiology.

[13]  A. Peters,et al.  Different kinds of axon terminals forming symmetric synapses with the cell bodies and initial axon segments of layer II/III pyramidal cells. I. Morphometric analysis , 1990, Journal of neurocytology.

[14]  M. Descheˆnes,et al.  Morphological characterization of slow and fast pyramidal tract cells in the cat , 1979, Brain Research.

[15]  J. Winer,et al.  Structure of layer II in cat primary auditory cortex (AI) , 1985, The Journal of comparative neurology.

[16]  F. Wörgötter,et al.  Topographical Aspects of Intracortical Excitation and Inhibition Contributing to Orientation Specificity in Area 17 of the Cat Visual Cortex , 1991, The European journal of neuroscience.

[17]  J. Winer,et al.  The pyramidal neurons in layer III of cat primary auditory cortex (AI) , 1984, The Journal of comparative neurology.

[18]  M. Marín‐padilla Double origin of the pericellular baskets of the pyramidal cells of the human motor cortex: a Golgi study. , 1969, Brain research.

[19]  S. W. Jaslove The integrative properties of spiny distal dendrites , 1992, Neuroscience.

[20]  D. Schmechel,et al.  Variability in the terminations of GABAergic chandelier cell axons on initial segments of pyramidal cell axons in the monkey sensory‐motor cortex , 1985, The Journal of comparative neurology.

[21]  Lynn J. Bindman,et al.  The neurophysiology of the cerebral cortex , 1981 .

[22]  P. Somogyi,et al.  Immunogold demonstration of GABA in synaptic terminals of intracellularly recorded, horseradish peroxidase-filled basket cells and clutch cells in the cat's visual cortex , 1986, Neuroscience.

[23]  J. Winer,et al.  Morphology and spatial distribution of GABAergic neurons in cat primary auditory cortex (AI) , 1994, The Journal of comparative neurology.

[24]  M Marín-Padilla,et al.  Three‐dimensional structural organization of layer I of the human cerebral cortex: A golgi study , 1990, The Journal of comparative neurology.

[25]  J. Winer,et al.  Layer V in rat auditory cortex: Projections to the inferior colliculus and contralateral cortex , 1988, Hearing Research.

[26]  J. Lund,et al.  Distribution of GABAergic neurons and axon terminals in the macaque striate cortex , 1987, The Journal of comparative neurology.

[27]  W. Oertel,et al.  Production of a specific antiserum to rat brain glutamic acid decar☐ylase by injection of an antigen-antibody complex , 1981, Neuroscience.

[28]  I. Törk,et al.  Serotoninergic innervation of the cat cerebral cortex , 1988, The Journal of comparative neurology.

[29]  M. Wong-Riley,et al.  Correlation between cytochrome oxidase staining and the uptake and laminar distribution of tritiated aspartate, glutamate, γ-aminobutyrate and glycine in the striate cortex of the squirrel monkey , 1985, Neuroscience.

[30]  P. Somogyi,et al.  Glutamate decarboxylase‐immunoreactive terminals of Golgi‐impregnated axoaxonic cells and of presumed basket cells in synaptic contact with pyramidal neurons of the cat's visual cortex , 1983, The Journal of comparative neurology.

[31]  A. Peters,et al.  Enigmatic bipolar cell of rat visual cortex , 1988, The Journal of comparative neurology.

[32]  I Fariñas,et al.  Patterns of synaptic input on corticocortical and corticothalamic cells in the cat visual cortex. II. The axon initial segment , 1991, The Journal of comparative neurology.

[33]  T. P. S. Powell,et al.  An electron microscopic study of the termination of thalamocortical fibres in areas 3b, 1 and 2 of the somatic sensory cortex in the monkey , 1981, Brain Research.

[34]  J. Winer The Functional Architecture of the Medial Geniculate Body and the Primary Auditory Cortex , 1992 .

[35]  J. Winer,et al.  Patterns of GABAergic immunoreactivity define subdivisions of the mustached bat's medial geniculate body , 1992, The Journal of comparative neurology.

[36]  W. Oertel,et al.  Immunocytochemical localization of glutamate decar☐ylase in rat cerebellum with a new antiserum , 1981, Neuroscience.

[37]  P. Somogyi,et al.  Targets and Quantitative Distribution of GABAergic Synapses in the Visual Cortex of the Cat , 1990, The European journal of neuroscience.

[38]  R. Porter,et al.  Morphology of neurons in area 4γ of the cat's cortex studied with intracellular injection of HRP , 1988 .

[39]  J. E. Vaughn,et al.  A comparison of the localization of choline acetyltransferase and glutamate decarboxylase immunoreactivity in rat cerebral cortex , 1988, Neuroscience.

[40]  M. Colonnier,et al.  A laminar analysis of the number of round‐asymmetrical and flat‐symmetrical synapses on spines, dendritic trunks, and cell bodies in area 17 of the cat , 1985, The Journal of comparative neurology.

[41]  I Fariñas,et al.  Patterns of synaptic input on corticocortical and corticothalamic cells in the cat visual cortex. I. The cell body , 1991, The Journal of comparative neurology.

[42]  J. Bolz,et al.  Morphological types of projection neurons in layer 5 of cat visual cortex , 1990, The Journal of comparative neurology.

[43]  Enrico Mugnaini,et al.  Comparative study of glutamate decarboxylase immunoreactive boutons in the mammalian inferior olive , 1989, The Journal of comparative neurology.

[44]  E. White,et al.  Intrinsic circuitry: Synapses involving the local axon collaterals of corticocortical projection neurons in the mouse primary somatosensory cortex , 1990, The Journal of comparative neurology.

[45]  J. Winer,et al.  The non‐pyramidal cells in layer III of cat primary auditory cortex (AI) , 1984, The Journal of comparative neurology.

[46]  U. Eysel,et al.  Network of GABAergic large basket cells in cat visual cortex (area 18): Implication for lateral disinhibition , 1993, The Journal of comparative neurology.

[47]  J. Winer,et al.  Anatomy of layer IV in cat primary auditory cortex (AI) , 1984, The Journal of comparative neurology.

[48]  E. G. Jones,et al.  Varieties and distribution of non‐pyramidal cells in the somatic sensory cortex of the squirrel monkey , 1975, The Journal of comparative neurology.

[49]  J. Matsubara,et al.  Local, horizontal connections within area 18 of the cat. , 1988, Progress in brain research.

[50]  D. Oliver,et al.  EM autoradiographic study of the projections from the dorsal nucleus of the lateral lemniscus: A possible source of inhibitory inputs to the inferior colliculus , 1989, The Journal of comparative neurology.

[51]  F. Valverde,et al.  Development, morphology and topography of chandelier cells in the auditory cortex of the cat. , 1985, Brain research.

[52]  D. Oliver,et al.  Fine structure of GABA-labeled axonal endings in the inferior colliculus of the cat: Immunocytochemistry on deplasticized ultrathin sections , 1992, Neuroscience.

[53]  E. White Cortical Circuits: Synaptic Organization of the Cerebral Cortex , 1989 .

[54]  R. L. Marie,et al.  The form and distribution of GABAergic synapses on the principal cell types of the ventral cochlear nucleus of the cat , 1989, Hearing Research.

[55]  J. DeFelipe,et al.  A correlative electron microscopic study of basket cells and large gabaergic neurons in the monkey sensory-motor cortex , 1986, Neuroscience.

[56]  J. E. Rose,et al.  The cellular structure of the auditory region of the cat , 1949, The Journal of comparative neurology.