The pyramidal neurons in layer III of cat primary auditory cortex (AI)

Abstract

The neuronal architecture of pyramidal cells in layer III of the primary auditory cortex (AI) of adult cats was examined as a prelude to connectional and fine structural studies; in a further paper, the results of parallel studies of non-pyramidal layer III cells are presented. Layer III is about 400 m̈m thick, comprises about one-quarter of the thickness of AI, and lies some 400–800 m̈m deep to the pial surface. It is distinguished in Nissl, fiber, and Golgi preparations from layers II and IV, and also on connectional grounds, since its neurons are one of the principal inputs to the contralateral AI. Layer III may be divided into two roughly equal tiers on the basis of its neuronal and cytoarchitecture. Layer IIIa is populated by small cells with oval somata and many tiny pyramidal cells; the fiber architecture is dominated by radial bundles of medium-sized axons interspersed among columns of apical dendrites arising from deeper-lying pyramidal cells. In layer IIIb medium-sized and large pyramidal cells are more numerous, and the fiber architecture has a different, much denser texture, including extensive lateral components which invade layer IV, and large contingents of descending, probably corticofugal, axons. Five kinds of pyramidal neurons occur in Golgi preparations. Most numerous are the small, medium-sized, and large pyramidal cells; the two types of star pyramidal neurons are less common. The small pyramidal cell has a limited dendritic field and rather delicate dendrites; all but the apical one usually end in layer III. The medium-sized pyramidal cell is the most common neuron, and its rich basilar dendritic arbors are conspicuous, with their many dendritic appendages, in the layer III neuropil; their distal dendrites spread into layer IV. The largest pyramidal cells lie mainly in layer IIIb, and their lateral dendrites often mark the layer IIIb-IVa border. The apical dendrites of medium-sized and large pyramidal cells often extend to layer Ib, where they branch obliquely. The axons of these cells branch laterally after descending through layer III and toward the white matter. Often secondary or tertiary branches reascend to layer IV and more superficially; there is considerable stereotypy in this branching pattern. These numerous secondary branches contribute heavily to the layer IIIb-IVa lateral fiber plexus. The fourth variety of pyramidal cell has a round soma and a stellate dendritic field whose distal branches extend from layer V to layer I, but whose axon is chiefly in layer III. Finally, a star pyramidal cell with long lateral basilar arbors but rather smooth dendrites completes the picture. The basilar dendrites of most layer III pyramidal cells have their long axis parallel to the dorso-ventral orientation of isofrequency contours. A vertical, columnar organization is imposed by the plexus of thick and medium-sized, radially arranged ascending axons, the bundles of apical dendrites ascending from deeper layers in parallel with those of layer III pyramidal cells, and the axons of layer IV cells projecting toward these apical dendrites. Since many of the pyramidal cells project to the opposite AI in addition to having extensive local axonal ramifications, it is concluded that they may have a dual functional role in the organization of primary auditory cortex.