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

Neuron. 2017 Feb 8;93(3):632-645.e6. doi: 10.1016/j.neuron.2016.12.043. Epub 2017 Jan 26.

Abstract

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. VIDEO ABSTRACT.

Keywords: Drosophila; GABA; acetylcholine; competition; dendrite; development; excitation inhibition balance; flight; motoneuron; synapse.

Publication types

  • Video-Audio Media

MeSH terms

  • Acetylcholine / metabolism*
  • Animals
  • Calcium Channels, T-Type / metabolism*
  • Calcium Signaling*
  • Dendrites / metabolism*
  • Dendrites / physiology
  • Drosophila
  • Drosophila Proteins / metabolism*
  • Neuronal Plasticity*
  • Neurons / metabolism
  • Neurons / physiology
  • Presynaptic Terminals / metabolism
  • Presynaptic Terminals / physiology
  • Receptors, GABA-A / metabolism*
  • Receptors, Nicotinic / metabolism*
  • Synapses / metabolism*
  • Synapses / physiology
  • gamma-Aminobutyric Acid / metabolism*

Substances

  • Calcium Channels, T-Type
  • Drosophila Proteins
  • Receptors, GABA-A
  • Receptors, Nicotinic
  • nicotinic acetylcholine receptor alpha-subunits, Drosophila
  • gamma-Aminobutyric Acid
  • Acetylcholine