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J Neurophysiol (February 8, 2006). doi:10.1152/jn.01083.2005
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Submitted on October 13, 2005
Accepted on February 2, 2006

KCNQ/Kv7 channel regulation of hippocampal gamma frequency firing in the absence of synaptic transmission

Sonia Piccinin1, Andrew D. Randall1, and Jon T. Brown2*

1 Neurology and GI CEDD, GlaxoSmithKline, Harlow, ESSEX, United Kingdom; MRC Centre for Synaptic Plasticity, University of Bristol, Bristol, United Kingdom
2 Neurology and GI CEDD, GlaxoSmithKline, Harlow, ESSEX, United Kingdom

* To whom correspondence should be addressed. E-mail: Jon.2.Brown{at}gsk.com.

Synchronous neuronal firing can be induced in hippocampal slices in the absence of synaptic transmission by lowering extracellular Ca2+ and raising extracellular K+. However, the ionic mechanisms underlying this non-synaptic synchronous firing are not well understood. In this study we have investigated the role of KCNQ/Kv7 channels in regulating this form of non-synaptic bursting activity. Incubation of rat hippocampal slices in reduced (0.2 mM) [Ca2+]O and increased (6.3 mM) [K+]O, blocked synaptic transmission, increased neuronal firing, and led to the development of spontaneous periodic non-synaptic epileptiform activity. This activity was recorded extracellularly as large (4.7 ± 1.9 mV) depolarising envelopes with superimposed high frequency synchronous population spikes. These intraburst population spikes initially occurred at a high frequency (~120 Hz) which decayed throughout the burst stabilising in the gamma frequency band (30-80 Hz). Further increasing [K+]O resulted in an increase in the interburst frequency without altering the intraburst population spike frequency. Application of retigabine (10 µM), a Kv7 channel modulator, completely abolished the bursts, in an XE-991 sensitive manner. Furthermore, application of the Kv7 channel blockers, Linopirdine (10 µM) or XE-991 (10 µM) alone, abolished the gamma frequency, but not the higher frequency population spike firing observed during low Ca2+/high K+ bursts. These data suggest that Kv7 channels are likely to play a role in the regulation of synchronous population firing activity.




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