Intra-neuronal Competition for Synaptic Partners Conserves the Amount of Dendritic Building Material

• Published in: Neuron (Cambridge, Mass.) Mass.), 2017-02, Vol.93 (3), p.632-645.e6
• Main Authors: Ryglewski, Stefanie, Vonhoff, Fernando, Scheckel, Kathryn, Duch, Carsten
• Format: Article
• Language: English
• Subjects: acetylcholine; Acetylcholine - metabolism; Animals; Calcium Channels, T-Type - metabolism; Calcium Signaling; Chromosomes; competition; dendrite; Dendrites - metabolism; Dendrites - physiology; development; Drosophila; Drosophila Proteins - metabolism; excitation inhibition balance; flight; GABA; gamma-Aminobutyric Acid - metabolism; Genetic engineering; Insects; Morphology; motoneuron; Neuronal Plasticity; Neurons; Neurons - metabolism; Neurons - physiology; Presynaptic Terminals - metabolism; Presynaptic Terminals - physiology; Receptors, GABA-A - metabolism; Receptors, Nicotinic - metabolism; Software; synapse; Synapses - metabolism; Synapses - physiology; Transmitters
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2016.12.043

Brain development requires correct targeting of multiple thousand synaptic terminals onto staggeringly complex dendritic arbors. The mechanisms by which input synapse numbers are matched to dendrite size, and by which synaptic inputs from different transmitter systems are correctly partitioned onto a postsynaptic arbor, are incompletely understood. By combining quantitative neuroanatomy with targeted genetic manipulation of synaptic input to an identified Drosophila neuron, we show that synaptic inputs of two different transmitter classes locally direct dendrite growth in a competitive manner. During development, the relative amounts of GABAergic and cholinergic synaptic drive shift dendrites between different input domains of one postsynaptic neuron without affecting total arbor size. Therefore, synaptic input locally directs dendrite growth, but intra-neuronal dendrite redistributions limit morphological variability, a phenomenon also described for cortical neurons. Mechanistically, this requires local dendritic Ca2+ influx through Dα7nAChRs or through LVA channels following GABAAR-mediated depolarizations. [Display omitted] •Synaptic activity can direct postsynaptic arbor formation during dendritic growth•Competition of GABAergic and cholinergic synaptic inputs redistributes dendrites•Local dendritic calcium signaling is required for dendrite redistributions•Perturbations of correct input partitioning cause defects in fine motor control Ryglewski et al. report that competitive mechanisms are required to correctly partition synaptic inputs from different transmitter systems on the dendritic arbor of a Drosophila motoneuron. Perturbations cause dendrite shifts and result in defects of adaptive motor control.