Synaptic specificity in frog sympathetic ganglia during reinnervation, sprouting, and embryonic development.

B cells and C cells in frog lumbar sympathetic ganglia are specifically innervated by preganglionic B fibers and C fibers, respectively. To explore the mechanisms underlying the formation of these specific synapses, electrophysiological studies were made of sprouting and regenerating synaptic connections following interruption of the preganglionic pathways. Studies were also made of developing connections in tadpole ganglia. After partial denervation (by selective interruption of B fibers), the C fibers sprouted and innervated B cells. When B fibers regenerated, they reinnervated B cells only, and within several weeks, C fiber synapses on B cells were no longer found. After complete denervation (by interruption of both B and C fibers) specific synaptic connections were eventually restored. At least 2 experimentally separable processes underlie this specificity: First, there is a preference for appropriate connections from the outset of reinnervation, seen even in the absence of competition between the 2 groups of preganglionic fibers. Despite this preference, however, some inappropriate synapses are formed. Second, those inappropriate synapses that do arise are eliminated when appropriate synapses are allowed to reform, as a result of competitive interactions between the 2 preganglionic fiber groups. In normally developing tadpole ganglia, B and C cells were not readily distinguishable. The great majority of tadpole neurons were found to be innervated exclusively by either B or C fibers. Some neurons were innervated by both preganglionic fiber groups, a situation virtually never found in adult ganglia. It thus appears that in normal development, as in reinnervation, innervation is by and large selective; inappropriate synapses may form, but they are eliminated during maturation, presumably through competitive interactions.