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Primary and secondary motoneurons use different calcium channel types to control escape and swimming behaviors in zebrafish

, , , , and . Proceedings of the National Academy of Sciences, 117 (42): 26429--26437 (2020)
DOI: 10.1073/pnas.2015866117

Abstract

Genetic manipulations, functional imaging, and patch-clamp electrophysiology provide new insights into the roles played by the P/Q and N calcium channel types in zebrafish neuromuscular transmission. These two channel types are the mainstay of synaptic transmission among vertebrates and their functional distinctions likely form the basis of their synapse-specific expression. We show that the primary and secondary motoneurons differ in these two calcium channel types, providing independent control over escape and rhythmic swimming behaviors. The control over separate behaviors occurs despite their sharing of the same synapses and postsynaptic receptors. This synapse sharing by presynaptic terminals with functionally distinct calcium channel types calls for investigations into similar processes at other synapses.The escape response and rhythmic swimming in zebrafish are distinct behaviors mediated by two functionally distinct motoneuron (Mn) types. The primary (1°Mn) type depresses and has a large quantal content (Qc) and a high release probability (Pr). Conversely, the secondary (2°Mn) type facilitates and has low and variable Qc and Pr. This functional duality matches well the distinct associated behaviors, with the 1°Mn providing the strong, singular C bend initiating escape and the 2°Mn conferring weaker, rhythmic contractions. Contributing to these functional distinctions is our identification of P/Q-type calcium channels mediating transmitter release in 1°Mns and N-type channels in 2°Mns. Remarkably, despite these functional and behavioral distinctions, all \~15 individual synapses on each muscle cell are shared by a 1°Mn bouton and at least one 2°Mn bouton. This blueprint of synaptic sharing provides an efficient way of controlling two different behaviors at the level of a single postsynaptic cell.All study data are included in the article.

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