Abstract
Motoneurons developmentally acquire appropriate cellular architectures that ensure connections with postsynaptic muscles and presynaptic neurons. In Drosophila, leg motoneurons are organized as a myotopic map, where their dendritic domains represent the muscle field. Here, we investigate mechanisms underlying development of aspects of this myotopic map, required for walking. A behavioral screen identified roles for Semaphorins (Sema) and Plexins (Plex) in walking behavior. Deciphering this phenotype, we show that PlexA/Sema1a mediates motoneuron axon branching in ways that differ in the proximal femur and distal tibia, based on motoneuronal birth order. Importantly, we show a novel role for glia in positioning dendrites of specific motoneurons; PlexB/Sema2a is required for dendritic positioning of late-born motoneurons but not early-born motoneurons. These findings indicate that communication within motoneurons and between glia and motoneurons, mediated by the combined action of different Plexin/Semaphorin signaling systems, are required for the formation of a functional myotopic map.
Highlights
Motoneurons are key elements in the neural networks that generate behavior in all nervous systems
Deciphering this phenotype, we show that PlexA/Sema1a mediates motoneuron axon branching in ways that differ in the proximal femur and distal tibia, based on motoneuronal birth order
These findings indicate that communication within motoneurons and between glia and motoneurons, mediated by the combined action of different Plexin/Semaphorin signaling systems, are required for the formation of a functional myotopic map
Summary
Motoneurons are key elements in the neural networks that generate behavior in all nervous systems. As final common output channels, they represent exclusive control elements of muscle effectors that mediate behavioral action For their correct function, motoneurons must acquire specific cellular architectures during development such that their input domains, usually manifest as dendrites, receive connections from appropriate pre-motor neurons, and their axonal output domains make connections to correct target muscle cells (Jessell et al 2011; Harris et al 2015; Arber 2012). In this system, the developmental processes involved in generating appropriate dendritic and axonal morphology of different types of larval (Landgraf & Thor 2006; Mauss et al 2009) and adult motoneurons have been studied extensively. The specific architecture of the motoneurons that innervate the adult leg has been shown to depend on their lineage and birth order, in that the majority of the leg motoneurons are postembryonic lineal descendants of neuroblast 15, and these motoneurons manifest a birth order-specific neuroanatomical organization
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