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The Journal of Neuroscience, November 22, 2006, 26(47):12325-12338; doi:10.1523/JNEUROSCI.3521-06.2006

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Cellular/Molecular
Somatodendritic Kv7/KCNQ/M Channels Control Interspike Interval in Hippocampal Interneurons

J. Josh Lawrence,^1 * Fernanda Saraga,^2,3,4 * Joseph F. Churchill,¹ Jeffrey M. Statland,¹ Katherine E. Travis,¹ Frances K. Skinner,^2,3,4,5 and Chris J. McBain¹

¹Laboratory of Cellular and Synaptic Neurophysiology, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892, ²Toronto Western Research Institute, University Health Network, ³Department of Physiology, ⁴Department of Medicine (Neurology), and ⁵Institute of Biomaterials and Biomedical Engineering, University of Toronto, Toronto, Ontario, Canada M5T 2S8

Correspondence should be addressed to either of the following: Josh Lawrence at the above address, Email: lawrenjo{at}mail.nih.gov; or Fernanda Saraga, Department of Zoology, Room 303, University of Toronto, 25 Harbord Street, Toronto, Canada M5S 3G5, Email: fernanda.saraga{at}utoronto.ca

The M-current (I_M), comprised of Kv7 channels, is a voltage-activated K⁺ conductance that plays a key role in the control of cell excitability. In hippocampal principal cells, I_M controls action potential (AP) accommodation and contributes to the medium-duration afterhyperpolarization, but the role of I_M in control of interneuron excitability remains unclear. Here, we investigated I_M in hippocampal stratum oriens (SO) interneurons, both from wild-type and transgenic mice in which green fluorescent protein (GFP) was expressed in somatostatin-containing interneurons. Somatodendritic expression of Kv7.2 or Kv7.3 subunits was colocalized in a subset of GFP+ SO interneurons, corresponding to oriens-lacunosum moleculare (O-LM) cells. Under voltage clamp (VC) conditions at –30 mV, the Kv7 channel antagonists linopirdine/XE-991 abolished the I_M amplitude present during relaxation from –30 to –50 mV and reduced the holding current (I_hold). In addition, 0.5 mM tetraethylammonium reduced I_M, suggesting that I_M was composed of Kv7.2-containing channels. In contrast, the Kv7 channel opener retigabine increased I_M amplitude and I_hold. When strongly depolarized in VC, the linopirdine-sensitive outward current activated rapidly and comprised up to 20% of the total current. In current-clamp recordings from GFP+ SO cells, linopirdine induced depolarization and increased AP frequency, whereas retigabine induced hyperpolarization and arrested firing. In multicompartment O-LM interneuron models that incorporated I_M, somatodendritic placement of Kv7 channels best reproduced experimentally measured I_M. The models suggest that Kv3- and Kv7-mediated channels both rapidly activate during single APs; however, Kv3 channels control rapid repolarization of the AP, whereas Kv7 channels primarily control the interspike interval.

Key words: antiepileptic; action potential; hippocampus; interneuron; M-current; neuromodulation; potassium channel

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Received March 17, 2006; revised Oct. 12, 2006; accepted Oct. 14, 2006.

Correspondence should be addressed to either of the following: Josh Lawrence at the above address, Email: lawrenjo{at}mail.nih.gov; or Fernanda Saraga, Department of Zoology, Room 303, University of Toronto, 25 Harbord Street, Toronto, Canada M5S 3G5, Email: fernanda.saraga{at}utoronto.ca

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