A quantitative study of synaptic contacts on interneurons and relay cells of the cat lateral geniculate nucleus

Summary

The relative proportions of synapses made by retinal and extraretinal terminals on interneurons and relay cells in lamina A of the dorsal lateral geniculate nucleus (LGN) of the cat were estimated quantitatively in a sample of 4003 synapses. Processes of interneurons or relay cells were identified by presence or absence of GABA immunoreactivity, respectively, in thin sections treated with post-embedding anti-GABA immunogold. On the basis of ultrastructural features, synaptic terminals were interpreted as belonging to retinal axons, cortical axons or axon collaterals of relay cells. GABAergic terminals were positively identified by being immunoreactive. GABA(-) terminals with heterogeneous and poorly defined characteristics, which could not be identified in the above classes, were grouped together in an “undetermined” category. Among the total synaptic inputs to interneurons, the following relative percentages of synapses from different terminals were obtained: retinal 25%, cortical 37%, GABAergic 26%, axon collaterals 2%, undetermined 6%. The vast majority of retinal terminals synapse on dendritic appendages of interneurons rather than on their dendritic trunks (about 20∶1). By contrast, the majority of cortical terminals synapse on dendrites rather than on dendritic appendages (about 5∶1). Virtually all axon-collaterals synapses were established on dendritic appendages. 17% of the dendritic profiles of interneurons contain synaptic vesicles; many of these profiles were seen in postsynaptic relation to cortical axons and in presynaptic relation with relay dendrites. Given the extensive electrotonic lengths of these cells observed by others, and the expected high electric resistance of the slender stalks that are known to connect the dendritic appendages to interneurons, these results suggest that microcircuits involving the interneuronal dendritic appendages with dendrites of relay cells are under predominantly retinal control. The microcircuits established by presynaptic dendritic trunks with relay dendrites, are under predominantly cortical control. The axonal (spiking) output of interneurons would be under control of the few retinal synapses on proximal dendrites of these cells. Among the total synaptic inputs to relay cells, the following relative percentages of different synapses were obtained: retinal 12%, cortical 58%, GABAergic 24%, axon collaterals 0.3%, undetermined 5%. Relay cells receive twice the number of cortical synapses than interneurons, suggesting that direct cortical excitatory influences on relay cells are more preponderant than cortico-interneuron mediated inhibition on these cells. The observed proportions of dendritic profiles of relay cells and interneurons (80% and 20%, respectively) in the geniculate neuropil are similar to the known proportions of somata of both types of cells in the A-laminae. This suggests a similarity in the average dendritic branching of relay cells and interneurons.