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The Journal of Neuroscience, April 6, 2005, 25(14):3489-3498; doi:10.1523/JNEUROSCI.0597-05.2005

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Cellular/Molecular
A Functional Role for Small-Conductance Calcium-Activated Potassium Channels in Sensory Pathways Including Nociceptive Processes

Parmvir K. Bahia,¹ Rie Suzuki,¹ David C. H. Benton,¹ Amanda J. Jowett,² Mao Xiang Chen,² Derek. J. Trezise,² Anthony H. Dickenson,¹ and Guy W. J. Moss¹

¹Department of Pharmacology, University College London, London WC1E 6BT, United Kingdom, and ²GlaxoSmithKline Research and Development, Stevenage SG1 2NY, United Kingdom

We investigated the role of small-conductance calcium-activated potassium (SK) and intermediate-conductance calcium-activated potassium channels in modulating sensory transmission from peripheral afferents into the rat spinal cord. Subunit-specific antibodies reveal high levels of SK3 immunoreactivity in laminas I, II, and III of the spinal cord. Among dorsal root ganglion neurons, both peripherin-positive (C-type) and peripherin-negative (A-type) cells show intense SK3 immunoreactivity. Furthermore, dorsal root-stimulated sensory responses recorded in vitro are inhibited when SK channel activity is increased with 1-ethyl-2-benzimidazolinone (1-EBIO). In vivo electrophysiological recordings show that neuronal responses to naturally evoked nociceptive and nonnociceptive stimuli increase after application of the selective SK channel blocker 8,14-diaza-1,7(1,4)-diquinolinacyclotetradecaphanedium di-trifluoroacetate (UCL 1848), indicating that SK channels are normally active in moderating afferent input. Conversely, neuronal responses evoked by mechanical stimuli are inhibited when SK channel activity is increased with 1-EBIO. These effects are reversed by the subsequent application of UCL 1848. Our data demonstrate that SK channels have an important role in controlling sensory input into the spinal cord.

Key words: apamin; dorsal root ganglion; sensory transmission; afterhyperpolarization; C-fiber; K⁺ channel

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Received Aug 20, 2004; revised February 14, 2005; accepted February 15, 2005.

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