Sequential acquisition of cacophony calcium currents, sodium channels and voltage-dependent potassium currents affects spike shape and dendrite growth during postembryonic maturation of an identified Drosophila motoneuron

• Published in: The European journal of neuroscience 2014-05, Vol.39 (10), p.1572-1585
• Main Authors: Ryglewski, Stefanie, Kilo, Lukas, Duch, Carsten
• Format: Article
• Language: English
• Subjects: Action Potentials - physiology; Animals; Biological and medical sciences; Calcium - metabolism; Cell Enlargement; Dendrites - physiology; differentiation; Drosophila; Drosophila melanogaster; Fundamental and applied biological sciences. Psychology; Immunohistochemistry; ion channel; ionic current; Membrane Potentials - physiology; Metamorphosis, Biological - physiology; Microscopy, Confocal; Motor Neurons - cytology; Motor Neurons - physiology; Optical Imaging; patch-clamp; Patch-Clamp Techniques; Potassium - metabolism; Potassium Channels, Voltage-Gated - metabolism; Sodium Channels - metabolism; Vertebrates: nervous system and sense organs
• ISSN: 0953-816X; 1460-9568
• DOI: 10.1111/ejn.12517

During metamorphosis the CNS undergoes profound changes to accommodate the switch from larval to adult behaviors. In Drosophila and other holometabolous insects, adult neurons differentiate either from respecified larval neurons, newly born neurons, or are born embryonically but remain developmentally arrested until differentiation during pupal life. This study addresses the latter in the identified Drosophila flight motoneuron 5. In situ patch‐clamp recordings, intracellular dye fills and immunocytochemistry address the interplay between dendritic shape, excitability and ionic current development. During pupal life, changes in excitability and spike shape correspond to a stereotyped, progressive appearance of voltage‐gated ion channels. High‐voltage‐activated calcium current is the first current to appear at pupal stage P4, prior to the onset of dendrite growth. This is followed by voltage‐gated sodium as well as transient potassium channel expression, when first dendrites grow, and sodium‐dependent action potentials can be evoked by somatic current injection. Sustained potassium current appears later than transient potassium current. During the early stages of rapid dendritic growth, sodium‐dependent action potentials are broadened by a calcium component. Narrowing of spike shape coincides with sequential increases in transient and sustained potassium currents during stages when dendritic growth ceases. Targeted RNAi knockdown of pupal calcium current significantly reduces dendritic growth. These data indicate that the stereotyped sequential acquisition of different voltage‐gated ion channels affects spike shape and excitability such that activity‐dependent calcium influx serves as a partner of genetic programs during critical stages of motoneuron dendrite growth. During development neurons are equipped with a specific set of ion channels to accommodate their function in adult behavior. Here we show that structural and electrophysiological development of an identified Drosophila flight motoneuron, MN5, are accompanied by the sequential acquisition of voltage gated Ca2+, Na+ and K+ currents. Targeted RNAi knock down of Ca2+ channels causes impaired dendrite growth, thus showing distinct mechanistic interactions of structural and physiological development.