Shal and Shaker Differential Contribution to the K⁺Currents in theDrosophilaMushroom Body Neurons

Abstract

Shaker, a voltage-dependent Kϩ channel, is enriched in the mushroom bodies (MBs), the locus of olfactory learning in Drosophila. Mutations in the shaker locus are known to alter excitability, neurotransmitter release, synaptic plasticity, and olfactory learning. However, a direct link of Shaker channels to MB intrinsic neuron (MBN) physiology has not been documented. We found that transcripts for shab, shaw, shaker, and shal, among which only Shaker and Shal have been reported to code for A-type currents, are present in the MBs. The electrophysiological data showed that the absence of functional Shaker channels modifies the distribution of half-inactivation voltages (V i1/2 ) in the MBNs, indicating a segregation of Shaker channels to only a subset (ϳ28%) of their somata. In harmony with this notion, we found that approximately one-fifth of MBNs lacking functional Shaker channels displayed dramatically slowed-down outward current inactivation times and reduced peak-current amplitudes. Furthermore, whereas all MBNs were sensitive to 4-aminopyridine, a nonspecific A-type current blocker, a subset of neurons (ϳ24%) displayed little sensitivity to a Shal-specific toxin. This subset of neurons displaying toxin-insensitive outward currents had more depolarized V i1/2 values attributable to Shaker channels. Our findings provide the first direct evidence that altered Shaker channel function disrupts MBN physiology in Drosophila. To our surprise, the experimental data also indicate that Shaker channels segregate to a minor fraction of MB neuronal somata (20 -30%), and that Shal channels contribute the somatic A-type current in the majority of MBNs.

Drosophila cacophonyChannels: A Major Mediator of Neuronal Ca2+Currents and a Trigger for K+Channel Homeostatic Regulation

“…6) and suggest the possibility that I A is upregulated in adult cac neurons as well. It is worth noting that Shal mRNA level was not altered in cac neurons, although Shal, rather than Sh, channels are considered to be the dominant contributor to I A in the neuronal soma Baro et al, 1997;Gasque et al, 2005;Peng and Wu, 2007). These data suggest an interesting possibility that Sh plays a role in neuronal plasticity for upregulation and downregulation of neuronal excitability during environmental challenges or behavioral conditioning.…”

H+ pump-dependent changes in membrane voltage are an early mechanism necessary and sufficient to induceXenopustail regeneration

“…This technique has uncovered transporters involved in morphogenetic events in both vertebrates and invertebrates (Duboc et al, 2005;Etter et al, 1999;Gasque et al, 2005;Hibino et al, 2006;Pyza et al, 2004;Shimeld and Levin, 2006).…”

Bridging behavior and physiology: Ion‐channel perspective on mushroom body‐dependent olfactory learning and memory in Drosophila

“…Since Wu et al (1983) first reported that dissociated Drosophila larval neurons could be maintained in culture for more than a week, larval brain dispersions, from which MBNs can be identified by tissue-restricted expression of a reporter protein, have been used for the study of VDICs (Wright and Zhong, 1995;Delgado et al, 1998;Gasque et al, 2005). Olfactory learning is not an adult specific trait.…”