Tiling among stereotyped dendritic branches in an identified Drosophila motoneuron

Abstract

Different types of neurons can be distinguished by the specific targeting locations and branching patterns of their dendrites, which form the blueprint for wiring the brain. Unraveling which specific signals control different aspects of dendritic architecture, such as branching and elongation, pruning and cessation of growth, territory formation, tiling, and self-avoidance requires a quantitative comparison in control and genetically manipulated neurons. The highly conserved shapes of individually identified Drosophila neurons make them well suited for the analysis of dendritic architecture principles. However, to date it remains unclear how tightly dendritic architecture principles of identified central neurons are regulated. This study uses quantitative reconstructions of dendritic architecture of an identified Drosophila flight motoneuron (MN5) with a complex dendritic tree, comprising more than 4,000 dendritic branches and 6 mm total length. MN5 contains a fixed number of 23 dendritic subtrees, which tile into distinct, nonoverlapping volumes of the diffuse motor neuropil. Across-animal comparison and quantitative analysis suggest that tiling of the different dendritic subtrees of the same neuron is caused by competitive and repulsive interactions among subtrees, perhaps allowing different dendritic compartments to be connected to different circuit elements. We also show that dendritic architecture is similar among different wildtype and GAL4 driver fly lines. Metric and topological dendritic architecture features are sufficiently constant to allow for studies of the underlying control mechanisms by genetic manipulations. Dendritic territory and certain topological measures, such as tree compactness, are most constant, suggesting that these reflect the intrinsic molecular identity of the neuron. INDEXING TERMSdendrite; dendritic arborization; repulsion; motoneuron; tiling; topology; avoidance The remarkably diverse dendritic architectures of different types of neurons determine the types and numbers of inputs a neuron receives (Connors and Regehr, 1996; Cory et al., 2009). Furthermore, dendritic structure can affect the integration and computation of synaptic input information (Single and Borst, 1998; Häusser et al., 2000, Koch andSegev, 2000; London and Häusser, 2005 Additional supporting information may be found in the online version of this article. HHS Public Access Author ManuscriptAuthor Manuscript Author Manuscript Author ManuscriptStrikingly similar morphologies exist for the same types of vertebrate (e.g., pyramidal, Purkinje, or basket cells) and invertebrate neurons. In fact, dendritic morphology is a major criterion for the classification of neurons. Moreover, individually identified neurons with distinct morphologies exist in many invertebrate preparations (Mendenhall and Murphey, 1974;Ikeda et al., 1980;Thomas and Wyman, 1984; Levine, 2000, Libersat andDuch, 2002). These neurons can be unambiguously identified in different animals of the same species, only one such neuron exists per n...

Dendrites are dispensable for basic motoneuron function but essential for fine tuning of behavior

“…1B). MN5 can be unambiguously identified from animal to animal and displays a stereotyped dendritic morphology comprising a total length of 6,500 μm and >4,000 branches (13). Dendritic architecture is tightly regulated during development by steroid hormones (24), calcium signaling (25), neural activity (19,20), and cell surface signals (26).…”

“…This study uses the Drosophila genetic model system to selectively abolish dendrites from a subset of identified wing muscle motoneurons that have well-described and stereotyped dendritic morphologies (13) and firing patterns during flight (14) and courtship song (15,16). Surprisingly, we find that motoneurons that lack 90% of their dendrites are still contacted by appropriate synaptic partners and produce qualitatively normal firing patterns and wing movements during flight and courtship song.…”

Temporal coherency between receptor expression, neural activity and AP-1-dependent transcription regulatesDrosophilamotoneuron dendrite development

“…7B,C). In all 11 preparations, MN5 was lacking multiple dendritic sub-trees (Vonhoff and Duch, 2010), and neither posterior nor anterior dendrites reached their normal territory boundaries. Dendritic defects as induced by premature activity (Fig.…”

“…Drosophila melanogaster were reared as previously described (Vonhoff and Duch, 2010;Vonhoff et al, 2012). Motoneuron GAL4 driver lines were: (1) w; P103.3-GAL4, UAS-mCD8-GFP;+, (2) C380-GAL4, UAS-mCD8-GFP;; Cha-GAL80 and (3) w;UAS-mCD8-GFP; D42-GAL4, Cha-GAL80.…”

“…It innervates the contralateral, dorsal-most two fibers of the dorsolongitudinal flight muscle (DLM) (Ikeda and Koenig, 1988), which produces the power for wing downstroke during Drosophila flight. MN5 has a stereotyped dendritic structure comprising a total length of 6500 µm and >4000 branches (Vonhoff and Duch, 2010). Although MN5 is born during embryonic development, it is developmentally arrested during larval life, and all dendrites develop de novo during pupal life (Fig.…”