Small conductance Ca2+-activated K+ channels induce the firing pause periods during the activation of Drosophila nociceptive neurons

Abstract

In Drosophila larvae, Class IV sensory neurons respond to noxious thermal stimuli and provoke heat avoidance behavior. Previously, we showed that the activated neurons displayed characteristic fluctuations of firing rates, which consisted of repetitive high-frequency spike trains and subsequent pause periods, and we proposed that the firing rate fluctuations enhanced the heat avoidance (Terada et al., 2016). Here, we further substantiate this idea by showing that the pause periods and the frequency of fluctuations are regulated by small conductance Ca2+-activated K+ (SK) channels, and the SK knockdown larvae display faster heat avoidance than control larvae. The regulatory mechanism of the fluctuations in the Class IV neurons resembles that in mammalian Purkinje cells, which display complex spikes. Furthermore, our results suggest that such fluctuation coding in Class IV neurons is required to convert noxious thermal inputs into effective stereotyped behavior as well as general rate coding.

DeTerm: Software for automatic detection of neuronal dendritic branch terminals via an artificial neural network

“…sensory neurons with extensive dendritic arbors that cover the body wall and function in thermal, light and mechanical sensation (Chin & Tracey, 2017;Hwang et al, 2007;Onodera, Baba, Murakami, Uemura, & Usui, 2017;Tracey, Wilson, Laurent, & Benzer, 2003;Walcott, Mauthner, Tsubouchi, Robertson, & Tracey, 2018;Xiang et al, 2010). da neurons elaborate their dendritic arbors two dimensionally between the epidermis and the muscles, and they are easily visualized at high resolution by whole-mount imaging using cell-specific transgenic GFP markers (Grueber, Ye, Moore, Jan, & Jan, 2003;Sugimura et al, 2003).…”

The Drosophila Small Conductance Calcium-Activated Potassium Channel Negatively Regulates Nociception

“…Additionally, an “unconventional spike” that is triggered by a large dendritic calcium transient has been proposed to be important ( Terada et al, 2016 ). Indeed, a recent study also provided evidence that SK channels could regulate firing, because RNAi against SK was found to cause increases in the firing frequency of nociceptive neurons ( Onodera et al, 2017 ). That study proposed that dendritically localized SK channels might respond to a dendritic Ca 2+ transient.…”

Loss of Pseudouridine Synthases in the RluA Family Causes Hypersensitive Nociception inDrosophila

“…It is noteworthy that prior studies have noted a potential link between the degree of dendrite branching and the sensitivity of nociception behaviors (Honjo et al 2016). In other cases, axonal factors such as the ion channel SK have been found to be important in regulating the cIVda neuron excitability (Walcott et al 2018;Onodera et al 2017).…”