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The Journal of Neuroscience, March 2, 2005, 25(9):2348-2358; doi:10.1523/JNEUROSCI.4384-04.2005

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Cellular/Molecular
Shal and Shaker Differential Contribution to the K⁺ Currents in the Drosophila Mushroom Body Neurons

Gabriel Gasque,¹ Pedro Labarca,² Enrique Reynaud,¹ and Alberto Darszon¹

¹Departamento de Genética del Desarrollo y Fisiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos 62210, México, and ²Centro de Estudios Científicos, Casilla 1469, Valdivia, Chile

Shaker, a voltage-dependent K⁺ 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 (28%) 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 (24%) 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.

Key words: learning; memory; mushroom bodies; Shaker; K⁺ channels; Drosophila

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Received June 18, 2004; revised December 27, 2004; accepted January 20, 2005.

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