Synaptic Hierarchy A Putative Mechanism for Determining Synapse Specificity

During early synapse formation, target cell contact is known to bring about specific changes in presynaptic transmitter release, and these changes can range from coupling of the secretory machinery to action potentials in snails16, to switching of transmitter phenotype in rats17. The Lymnaea model has uncovered yet another novel interaction that occurs between reciprocally connected neurons during early synapse formation. Specifically, the two respiratory neurons visceral dorsal 4 (VD4) and RPeD1 paired in culture establish mutual inhibitory synaptic connections within 24 h. However, when examined during early stages of synapse formation (12-18 h), the cell VD4 wins over RPeD1 by being the first to establish inhibitory synapses with RPeD1. This is achieved through VD4-induced suppression of transmitter release from RPeD1. This suppression is transient and it involves peptide release from the VD418. Once VD4 has fully established synapses with RPeD1, its suppressive control over RPeD1's secretory machinery is lifted, thus enabling RPeD1 to release transmitter and hence establish its inhibitory synapses with VD4. This study provides a unique example of "synaptic hierarchy" whereby neurons such as VD4 which control higher order behaviors (such as cardio-respiratory) outcompete other neurons for target occupancy. Together, these studies from Lymnaea show that transmitter-receptor interactions can serve many important developmental roles in mollusks, ranging from target cell selection, synapse formation, to establishing the synaptic hierarchy.

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