Populations of GABAergic neurons and axons in layer I of rat auditory cortex

Abstract

Neurons and axon terminals (puncta) immunostained by an antibody against glutamic acid decarboxylase were studied in layer I of adult rats in architectonically identified area 41 of auditory cortex. The borders of area 41 and the laminar subdivisions of cortex were established in normal material and in other studies of cortical connections. Vibratomed or frozen sections were immunostained. The objectives of the study were to classify the types of (i) glutamic acid decarboxylase-positive neurons and (ii) puncta, and (iii) to examine their spatial distribution within layer I. Control sections were devoid of specific immunostaining. More than 90% of layer I cells are glutamic acid decarboxylase-positive. Four types of neuron were identified in Golgi material, including small neurons with stellate dendritic fields, horizontal cells with laterally projecting arbors, medium-sized neurons with stellate, widely ramifying dendritic fields, and large neurons with broad dendritic fields spanning the depth of layer I or branching laterally. In the glutamic acid decarboxylase material, examples with a somatodendritic shape matching each of these types were found. The average somatic diameter of glutamic acid decarboxylase-positive neurons ( X¯= 59μm 2, S.D. = 21μm 2) suggests that the small and medium-sized neurons predominate. Glutamic acid decarboxylase-positive neurons occur throughout the depth of layer I, but are far more numerous in the deeper half (68% in layer Ib) than in the superficial part (32% in layer Ia). Glutamic acid decarboxylase-positive neurons form small clusters of three to five cells across the cortical surface, with a range of 0–9/100 μm across the cortex. Most glutamic acid decarboxylase-positive neuronal perikarya were intensely immunostained, and the dendrites of the medium-sized and large neurons were traced as far as 50–75 μm beyond their initial branching point. Glutamic acid decarboxylase-positive puncta also had variable shapes. Both small, fine puncta (< 0.5 μm in diameter) and larger, coarser ones (>1.5 μm in diameter) were present, though the former were much more common. In traverses from the pia to the layer II border, the puncta average about 40/100 μm 2 (range: 20–80), and the shape of individual pia-layer II traverses is multipeaked, often with a slight trough at −80μm depth, then rising slowly in number toward layer II. These anatomical arrangements may have physiological consequences for cortical functional organization: (i) the GABAergic influences of layer I cells are directed laterally, toward other layer I neurons, or at the apical dendritic arbors of deep-lying commissural or corticofugal neurons, whose activity might be modulated by GABAergic layer I influences; (ii) the axons of layer II glutamic acid decarboxylase-positive neurons or of corticocortical interneurons may affect layer I. While many different transmitter molecules have been identified in layer I, it is probable that their activity influences a largely GABAergic neuronal population.