Differential contributions of Shaker and Shab K+ currents to neuronal firing patterns in Drosophila

I-Feng Peng; Chun-Fang Wu

doi:10.1152/jn.01012.2006

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Differential contributions of Shaker and Shab K+ currents to neuronal firing patterns in Drosophila

Journal article

Peer reviewed

Differential contributions of Shaker and Shab K+ currents to neuronal firing patterns in Drosophila

I-Feng Peng and Chun-Fang Wu

Journal of neurophysiology, Vol.97(1), pp.780-794

01/2007

DOI: 10.1152/jn.01012.2006

PMID: 17079336

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Abstract

Different K(+) currents participate in generating neuronal firing patterns. The Drosophila embryonic "giant" neuron culture system has facilitated current- and voltage-clamp recordings to correlate distinct excitability patterns with the underlying K(+) currents and to delineate the mutational effects of identified K(+) channels. Mutations of Sh and Shab K(+) channels removed part of inactivating I(A) and sustained I(K), respectively, and the remaining I(A) and I(K) revealed the properties of their counterparts, e.g., Shal and Shaw channels. Neuronal subsets displaying the delayed, tonic, adaptive, and damping spike patterns were characterized by different profiles of K(+) current voltage dependence and kinetics and by differential mutational effects. Shab channels regulated membrane repolarization and repetitive firing over hundreds of milliseconds, and Shab neurons showed a gradual decline in repolarization during current injection and their spike activities became limited to high-frequency, damping firing. In contrast, Sh channels acted on events within tens of milliseconds, and Sh mutations broadened spikes and reduced firing rates without eliminating any categories of firing patterns. However, removing both Sh and Shal I(A) by 4-aminopyridine converted the delayed to damping firing pattern, demonstrating their actions in regulating spike initiation. Specific blockade of Shab I(K) by quinidine mimicked the Shab phenotypes and converted tonic firing to a damping pattern. These conversions suggest a hierarchy of complexity in K(+) current interactions underlying different firing patterns. Different lineage-defined neuronal subsets, identifiable by employing the GAL4-UAS system, displayed different profiles of spike properties and K(+) current compositions, providing opportunities for mutational analysis in functionally specialized neurons.

Shab Potassium Channels - genetics

Action Potentials - genetics

Electric Stimulation

Shaker Superfamily of Potassium Channels - genetics

Nervous System - metabolism

Shaker Superfamily of Potassium Channels - metabolism

Cells, Cultured

Cell Membrane - genetics

Drosophila Proteins - metabolism

Cell Lineage - physiology

Cell Differentiation - genetics

Patch-Clamp Techniques

Shab Potassium Channels - metabolism

Animals

Embryo, Nonmammalian

Cell Membrane - metabolism

Neurons - metabolism

Drosophila - metabolism

Drosophila Proteins - genetics

Potassium Channel Blockers - pharmacology

Details

Title: Subtitle: Differential contributions of Shaker and Shab K+ currents to neuronal firing patterns in Drosophila
Creators: I-Feng Peng - Department of Biological Sciences, University of Iowa, Iowa City, IA 52242, USA
Chun-Fang Wu
Resource Type: Journal article
Publication Details: Journal of neurophysiology, Vol.97(1), pp.780-794
Publisher: United States
DOI: 10.1152/jn.01012.2006
PMID: 17079336
ISSN: 0022-3077
eISSN: 1522-1598
Grant note: NS 26528 / NINDS NIH HHS HD 18577 / NICHD NIH HHS
Language: English
Date published: 01/2007
Academic Unit: Iowa Neuroscience Institute; Biology
Record Identifier: 9984070263002771

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