Chordotonal neurons have dendritic spike initiation zones that are controlled by Para, the Drosophila sodium channel
Authors: Thomas A. Ravenscroft 1,2; Ashleigh Jacobs 3; Mingxue Gu 1,2; Daniel F. Eberl 3; Hugo J. Bellen 1,2,4
Affiliations: 1) Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX; 2) Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital, Houston, TX; 3) Department of Biology, University of Iowa, Iowa City, IA; 4) Department of Neuroscience, Baylor College of Medicine, Houston, TX
Keywords: b. dendrites; j. ion channels
The fruit fly Drosophila melanogaster has provided important insights into how sensory information is transduced by Transient Receptor Potential (TRP) channels in the Peripheral Nervous System (PNS). In bipolar chordotonal neurons (CN), TRP channels alone are not sufficient for the transduction of mechanical stimuli. We use an intronic Minos-mediated integration cassette to show that the sole voltage-gated sodium channel (NaV) in Drosophila, Para, is localized to the dendrites of these bipolar neurons. Para is localized to the distal tip of the dendrites in all CN and is colocalized with the mechanosensitive TRP channel NompC, distal to the mechanosensitive TRP channel Inactive. This localization is unique to bipolar CNs as we do not observe dendritic localization of Para in other peripheral neurons. Reducing para expression using RNAi in chordotonal neurons of the adult Johnston’s organ severely affects sound-evoked potentials. However, in addition to the dendritic localization, Para also localizes to a proximal spike initiation zone (SIZ) at an axonal initial segment-like region in axons of both bipolar and multidendritic PNS neurons. Therefore, to determine the dendritic specific role of para in CN neurons, we expressed a genetically encoded calcium indicator in CNs and recorded the fluorescence spike changes in dendrites upon mechanical stimuli. We show that the observed spikes in dendrites are nearly completely abolished by exposure to the NaV inhibitor Tetrodotoxin (TTX). We conclude that NaV channels are essential for mechanosensation in CN dendrites and that Para localization marks a dendritic SIZ in the distal dendrite as well as a SIZ in axons near the cell body. Hence, the TRP channels present in the dendrite of chordotonal neurons must cooperate with Para to trigger a neuronal response.