Specific muscle contacts induce increased transmitter release and neuritic arborization in motoneuronal cultures

Identified buccal motoneuron 19 (B19), isolated from the nervous system of Helisoma and plated into cell culture, is selective in synapse formation and requires contact with appropriate muscle targets before acquiring secretory competence. Action potential-regulated transmitter release was elevated specifically at neuritic arbors in contact with appropriate muscle fibers. In contrast, contact between B19 and inappropriate muscle targets failed to induce changes in presynaptic secretory properties. Spontaneous transmitter release rate was elevated globally across neuritic arbors of B19 in appropriate muscle cocultures, including arbors without direct muscle contact. In addition, dual contacts formed between B19 and two different muscle targets resulted in significant elevations in excitation-secretion coupling only at neuritic sites of appropriate muscle contact and not at sites of contact with mismatched targets. Image analyses of presynaptic neuronal architecture revealed that appropriate, but not novel, muscle targets elicited increased arborization of neurites at sites of neuron-muscle contact. In contrast to results with neuron B19, secretory properties of buccal neuron 5 (B5), a neuron capable of forming inappropriate chemical synapses with a number of novel targets in culture, were not enhanced by inappropriate muscle contact. We conclude that muscle targets vary in their ability to induce presynaptic modifications (e.g., excitation-secretion coupling, spontaneous transmitter release, and neuritic arborization) in identified motoneurons of Helisoma. These results imply that separate molecular pathways exist which control each of these events during synaptic differentiation. The differential potency of muscle targets for induction of presynaptic changes indicates the existence of a cellular mechanism of target recognition. We hypothesize that such a mechanism underlies the ability of neuron B19 to discriminate between potential postsynaptic partners in cell culture.