Distribution and ultrastructure of neurons in opossum piriform cortex displaying immunoreactivity to GABA and GAD and high‐affinity tritiated GABA uptake

Abstract

GABAergic neurons have been identified in the piriform cortex of the opossum at light and electron microscopic levels by immunocytochemical localization of GABA and the GABA‐synthesizing enzyme glutamic acid decarboxylase and by autoradiographic visualization of high‐affinity ³H‐GABA uptake. Four major neuron populations have been distinguished on the basis of soma size, shape, and segregation at specific depths and locations: large horizontal cells in layer Ia of the anterior piriform cortex, small globular cells with thin dendrites concentrated in layers Ib and II of the posterior piriform cortex, and multipolar and fusiform cells concentrated in the deep part of layer III in anterior and posterior parts of the piriform cortex and the subjacent endopiriform nucleus. All four populations were well visualized with both antisera, but the large layer Ia horizontal cells displayed only very light ³H‐GABA uptake, thus suggesting a lack of local axon collaterals or lack of high‐affinity GABA uptake sites. The large, ultrastructurally distinctive somata of layer Ia horizontal cells receive a very small number of symmetrical synapses; the thin, axonlike dendrites of small globular cells are exclusively postsynaptic and receive large numbers of both symmetrical and asymmetrical synapses, in contrast to somata which receive a small number of both types; and the deep multipolar and fusiform cells receive a highly variable number of symmetrical and asymmetrical synapses on somata and proximal dendrites.Labeled puncta of axon terminal dimensions were found in large numbers in the neuropil surrounding pyramidal cell somata in layer II and in the endopiriform nucleus. Moderately large numbers of labeled puncta were found in layer I at the depth of pyramidal cell apical dendrites with greater numbers in layer Ia at the depth of distal apical segments than in layer Ib.High‐affinity GABA uptake was demonstrated in the termination zone of the projection from the anterior olfactory nucleus to the anterior piriform cortex. Cell bodies of origin of this projection displayed heavy retrograde labeling with ³H‐GABA. Matching neuropil and cellular labeling was demonstrated with the GABA‐BSA antiserum but not with the GAD antiserum, thus suggesting that GABA is normally present in these cells but is taken up from the neuropil rather than synthesized. No comparable high‐affinity GABA uptake was demonstrated in the association fiber systems that originate in the piriform cortex.The functional significance of the present results is discussed with respect to: feedback and feedforward inhibitory circuits, a possible role of the GABAergic neurons distinguished in generation of a slow inhibitory process mediated by GABA_B receptors in addition to the well‐known fast inhibitory process mediated by GABA_A receptors, autoregulation of excitability level by inhibitory processes vs. participation in integrative processes, and the role of inhibitory processes in epileptogenesis. Special features of the piriform cortex that make it well suited as a model for analysis of inhibitory processes in cerebral cortex are described.