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The Journal of Neuroscience, October 21, 2009, 29(42):13353-13364; doi:10.1523/JNEUROSCI.1463-09.2009

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Cellular/Molecular
Kv7/KCNQ Channels Control Action Potential Phasing of Pyramidal Neurons during Hippocampal Gamma Oscillations In Vitro

Richardson N. Leão, Hui Min Tan, and André Fisahn

Neuronal Oscillations Laboratory, Department of Neuroscience, Karolinska Institute, 17177 Stockholm, Sweden

Correspondence should be addressed to Dr. André Fisahn, Nobel Institute for Neurophysiology, Department of Neuroscience, Retzius väg 8, A3:5, Karolinska Institute, 17177 Stockholm, Sweden. Email: andre.fisahn{at}ki.se

While the synaptic mechanisms involved in the generation of in vitro network oscillations have been widely studied, little is known about the importance of voltage-gated currents during such activity. Here we study the role of the M-current (I_M) in the modulation of network oscillations in the gamma-frequency range (20–80 Hz). Kv7/KCNQ subunits, the molecular correlates of I_M, are abundantly expressed in CA1 and CA3 pyramidal neurons, and I_M is an important modulator of pyramidal neuron firing. Using hippocampal slices, we recorded field activity and pyramidal neuron action potential timing during kainate-induced gamma oscillations. Application of the specific I_M blocker XE991 causes a significant reduction of gamma oscillation amplitude with no significant change in oscillation frequency. Concomitant CA3 pyramidal neuron recordings show a significant increase in action potential frequency during ongoing gamma oscillations after the application of XE991. This increase is associated with a significant loss of periodicity of pyramidal neuron action potentials relative to the phase of the gamma oscillations. Using dynamic clamp, we show that I_M acts to improve the periodicity of action potential timing and to decrease action potential frequency. We further validate these results in a compartmental model of a pyramidal neuron. Our work suggests that I_M modulates gamma oscillations by regulating the phasing of action potential firing in pyramidal neurons.

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Received March 27, 2009; revised Aug. 7, 2009; accepted Aug. 11, 2009.

Correspondence should be addressed to Dr. André Fisahn, Nobel Institute for Neurophysiology, Department of Neuroscience, Retzius väg 8, A3:5, Karolinska Institute, 17177 Stockholm, Sweden. Email: andre.fisahn{at}ki.se

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