Neurons accumulating [ 3Hgamma-aminobutyric acid (GABA) in supragranular layers of cat primary auditory cortex (AI)

Abstract

The classes of neurons accumulating exogenously injected, tritiated gamma-aminobutyric acid ([ 3HGABA) were studied in the supragranular layers in the primary auditory field of the adult cat. The size, laminar locus, and somatodendritic profiles of labeled neurons were studied light microscopically in frozen- or Vibratome-sectioned, 30 μm thick material, and in semithin, 1–2 μm thick, plastic-embedded high-resolution autoradiographic preparations. The chief goals of the study were to determine which types of cells could be identified as accumulating [ 3HGABA in layers I, II and III, and to establish possible relationships between these cells and (i) neurons described in Golgi studies of these layers, and (ii) the neurons found, in parallel investigations of the connections of the primary auditory field, to participate as ipsilateral corticocortical and commissural cells of origin. The principal findings are: that neurons in every layer in the primary auditory field take up tritiated gamma-aminobutyric acid; that their Nissl-counterstained somata have a smaller average area, and a smaller range of areas, than do the unlabeled cells; that more than one type of labeled neuron—as defined by somatic size and shape, height : width ratios, and nuclear membrane morphology—could be identified in each layer; that none of the labeled neurons had a soma with a pyramidal configuration; that the labeled cells are comparable in size, shape, and laminar distribution to some populations of non-pyramidal ipsilateral corticocortical cells of origin in layers II and III, and perhaps to certain classes of commissurally projecting, layer III non-pyramidal neurons; and finally, that only a rather small proportion—perhaps 10% or less, except in layer I—of the supragranular cells appear to accumulate labeled material. With regard to the identity of particular classes of neurons accumulating silver grains above background in the individual layers, in layer I, 2 of the 4 types of neurons characterized in Golgi preparations take up gamma-aminobutyric acid and the remaining 2 types may also, and the relative number of labeled cells appears to be higher than in the other layers; in layer II, 2 of the 9 varieties are labeled, and 4 other types may also be; and in layer III, 2 of the 11 types take up gamma-aminobutyric acid, and 5 other varieties may as well. Three types of non-pyramidal layer II cells that project ipsilaterally from AI to the second auditory cortical field, AII, possibly accumulate gamma-aminobutyric acid; 3 types of commissural non-pyramidal cells of origin linking AI to AI appear to be labeled by gamma-aminobutyric acid. Thus, of the total of 24 types of neurons characterized in previous morphological and connectional studies of layers I–III in AI, 6 are likely candidates for a gamma-aminobutyric acid-modulated inter- or intracortical role, 11 others may be, while 7 others are unlikely to be. The neurons in AI which are positive for gamma-aminobutyric acid are characterized by their somatodendritic heterogeneity, broad laminar distribution, and distinctive patterns of cortical connectivity. Somata accumulating gamma-aminobutyric acid are probably intermingled among ipsilateral corticocortical and commissural cells of origin in AI. These differences imply that more than one cortical pathway or local circuit arising in AI may use gamma-aminobutyric acid as a neurotransmitter, although its precise functional role remains to be demonstrated physiologically in auditory cortex.