Synaptic organization of anomalous retinal projections to the somatosensory and auditory thalamus: target-controlled morphogenesis of axon terminals and synaptic glomeruli.

These experiments examine which morphological features of axon terminals and their synaptic glomeruli are determined by afferent axons, and which by their targets. In normal, adult hamsters, electron microscopy reveals that, with respect to multiple ultrastructural features, the terminals and synaptic glomeruli of retinal afferent axons in the dorsal lateral geniculate nucleus differ from those of ascending auditory and somatosensory afferents in the medial geniculate and ventrobasal nuclei, respectively. These features include: (1) the location of specific sensory axon terminals on the somata and dendrites of their targets neurons, (2) the constitutents of the glomeruli and their synaptic relationships, (3) the number of specific sensory terminal boutons per glomerulus, (4) bouton size, (5) the number of dendritic and somatic appendages contacted by each bouton, and (6) the mitochondrial morphology of the specific sensory afferent boutons. In order to ascertain which of these features are determined by afferent axons and which by their targets, we subjected newborn Syrian hamsters to surgical procedures known to produce permanent, abnormal retinal projections to the main thalamic auditory (medial geniculate) and somatosensory (ventrobasal) nuclei. When the animals were adults, we examined the terminals and synaptic glomeruli of abnormal retino-auditory and retino-somatosensory axons that were anterogradely labeled by intraocular injection of horseradish peroxidase. With respect to all of the preceding features except mitochondrial morphology, the terminals and synaptic glomeruli of retino-medial geniculate and retino-ventrobasal axons more nearly resembled those of normal, auditory and somatosensory afferent axons, respectively, than they did those of normal, retino-lateral geniculate axons. These results demonstrate that the differentiation of all the features that we have examined, except mitochondrial morphology, is determined by factors in target neurons or their environment. This finding suggests that the differentiation of morphological features involved in contacts among neurons (including the type, number and size of interconnected neuronal elements and the loci at which they contact each other) is responsive to interactions among the connected elements, or between neural elements and their environment (e.g., glia, extracellular matrix), whereas the differentiation of structures reflecting intrinsic functions of individual neuronal elements is not responsive to such interactions.