Dynamics of retinotectal synaptogenesis in normal and 3-eyed frogs: evidence for the postsynaptic regulation of synapse number.

Abstract

Quantitative stereological methods were used to determine if the number, density, and types of synaptic connections formed during development are regulated by presynaptic input or by postsynaptic target cells in the optic tectum of normal and 3-eyed Rana pipiens tadpoles and frogs. Our analysis indicates that the number and size of synapses is approximately the same in both tecta of 3-eyed tadpoles and frogs, even though one tectal lobe is receiving input from twice the normal complement of retinal ganglion cells. Moreover, the number and size of synapses in the tectal lobes of 3-eyed animals did not differ significantly from values determined for normal tadpoles and frogs of the same developmental stage. These data suggest strongly that developing tectal cells regulate the number of synaptic contacts they will form. Differences in several morphological features between singly and doubly innervated tecta, however, including synapse density, distribution and complexity, amount of extracellular space, and number of myelin figures, suggest that the presence of supernumerary input retards tectal maturation. We propose that the noncorrelated activity of retinal ganglion cell terminals in the doubly innervated tectum results in fewer stabilized synapses per unit volume of neuropil and in the delayed maturation of the tectal neuropil. Taken together, our data suggest a complex dynamic interaction between retina and tectum during development.