In order to describe the circuitry of a single retinal X-cell axon in the lateral geniculate nucleus, we physiologically characterized such an axon in the optic tract and injected it intra-axonally with horseradish peroxidase. Subsequently, we recovered the axon and employed electron microscopic techniques to examine the distribution of synapses from 18% of its labeled terminals by reconstructing the unlabeled postsynaptic neurons through a series of 1,200 consecutive thin sections. We found remarkable selectivity for the axon's output, since only four of the 43 available neurons in a limited portion of the terminal arbor receive synapses from labeled terminals. Moreover, the distribution of these synapses on the four neurons, which we term cells 1 through 4, varies with respect to synapses from other classes of terminals that contact the same cells, including synapses from unlabeled retinal terminals. For cells 1 and 3, the labeled terminals provide 49% and 33%, respectively, of their retinal synapses, and these are located on both dendritic shafts and appendages. Synapses from the injected axon to these cells are thus integrated with those from other retinal axons. For cell 2, the labeled terminals provide 100% of its retinal synapses, but these synapses converge on clusters of dendritic appendages where they are integrated with convergent inhibitory inputs. Finally, for cell 4, the labeled terminals provide less than 2% of its retinal inputs, and these are distally located; we suggest that these synapses are remnants of physiologically inappropriate miswiring that occurs during development. The findings from this study support a concept of selectivity in neuronal circuitry in the mammalian central nervous system and also reveal some of the diverse integrative properties of neurons in the lateral geniculate nucleus.