Connectivity and convergence of single corticostriatal axons

Abstract

The distribution of synapses formed by corticostriatal neurons was measured to determine the average connectivity and degree of convergence of these neurons and to search for spatial inhomogeneities. Two kinds of axonal fields, focal and extended, and two striatal tissue compartments, the patch (striosome) and matrix, were analyzed separately. Electron microscopic examination revealed that both kinds of corticostriatal axons made synapses at varicosities that could be identified in the light microscope, and each varicosity made a single synapse. Thus, the distribution of varicosities was a good estimate of the spatial distribution of synapses. The distance between axonal varicosities was measured to determine the density of synaptic connections formed by one axon within the volume occupied by a striatal neuron. Intersynaptic distances were distributed exponentially, except that synapses were rarely located <4 μm apart. The mean distance between synapses was ~10 μm, so axons made a maximum of 40 synapses within the dendritic volume of a spiny neuron. There are ~2840 spiny neurons located within the volume of the dendrites of one spiny cell (Oorschot, 1996), so each axon must contact ≤1.4% of all cells in its axonal arborization. Within the same volume there are ~30.5 million asymmetric synapses (Ingham et al., 1996), approximately half of which are cortical in origin. Thus, ~380,000 cortical axons innervate the volume of the dendritic tree of one spiny cell. Striatal neurons with totally overlapping dendritic volumes have few presynaptic cortical axons in common, and cortical cells with overlapping axons have few striatal target neurons in common. These results explain the absence of redundancy in the responses of neurons located near each other in the striatum.