Different kinds of axon terminals forming symmetric synapses with the cell bodies and initial axon segments of layer II/III pyramidal cells. II. Synaptic junctions

Summary Four different types of axon terminals form symmetric synapses with the cell bodies and initial axon segments of pyramidal cells in layer II/III of rat visual cortex. One type belongs to chandelier cells, and the other three kinds of terminals have origins that have not been established yet. These latter are referred to as large, medium-sized and dense terminals. The purpose of the present study was to examine the synaptic junctions formed by all four types of terminal. The synapses formed by the chandelier cell terminals are readily recognized in thin sections because of the characteristic features of both the terminals and the initial axon segments, which are the neuronal elements postsynaptic to them. In en face views of these axo-axonal synapses the junctions can be seen to have presynaptic dense projections that form a grid in which they are triagonally spaced, and have an average centre-to-centre spacing of 84 nm. As an ensemble the projections form the presynaptic grid, which usually has an oval or round outline, but may be notched on one side where projections are absent. The synaptic junctions of the large, medium-sized and dense terminals were examined by making reconstructions of the terminals from serial thin sections. It was found that at the interfaces between the axon terminals and the cell bodies of pyramidal cells, several separate synaptic junctions may be present, in addition to a number of puncta adhaerentia. Thus, there may be as many as five separate synaptic junctions and as few as one. It was also found that while the proportion of the area of the synaptic interface occupied by synaptic junctions was between 12% and 26% for dense terminals, for medium sized terminals it was 10–15%, and for the one large terminal reconstructed it was only 8%. Thus, there can be multiple synaptic junctions between each of these types of axon terminals and a pyramidal cell, and because many of the terminals forming symmetric junctions are boutons en passant, a number of vesicle release sites exist between the presynaptic axon and its postsynaptic partner. The axon terminals forming symmetric synapses in the cerebral cortex are assumed to be inhibitory, and consequently it is suggested that this arrangement of multiple release sites is designed to ensure that stimulation of the presynaptic axon results in an effective level of hyperpolarization of the postsynaptic neuron.