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 micron in diameter), endings in layers II-IV were coarser and more globular (larger than 1 micron), 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 sometimes 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. Since puncta are believed to be the light microscopic correlate of synaptic terminals, they can suggest how inhibitory circuits are organized. Even within an area, the laminar puncta patterns may reflect different inhibitory arrangements. Thus, in layer I the fine, granular endings could contact preferentially the distal dendrites of pyramidal cells in deeper layers. The remoteness of such terminals from the spike initiation zone contrasts with the many puncta on all pyramidal cell perikarya and the large globular endings on basket cell somata. Basket cells might receive feed-forward disinhibition, pyramidal cells feed-forward inhibition, and GABAergic non-basket cells would be the target of only sparse inhibitory axosomatic input. Such arrangements imply that the actions of GABA on AI neurons are neither singular nor simple and that the architectonic locus, laminar position, and morphological identity of a particular neuron must be integrated for a more refined view of its role in cortical circuitry.