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J Physiol Volume 562, Number 2, 421-437, January 15, 2005 DOI: 10.1113/jphysiol.2004.077032
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Subthreshold inactivation of voltage-gated K+ channels modulates action potentials in neocortical bitufted interneurones from rats

Alon Korngreen1,2, Katharina M. M. Kaiser1 and Yuri Zilberter1,3

1 Abteilung Zellphysiologie, Max-Planck-Institut für Medizinische Forschung, Jahnstrasse 29, D-69120 Heidelberg, Germany
2 Faculty of Life Sciences and The Leslie and Susan Gonda Interdisciplinary Brain Research Centre, Bar-Ilan University, Ramat-Gan 52900, Israel
3 Department of Neuroscience, Karolinska Institute, Retzius väg. 8, B2-2, S-17177 Stockholm, Sweden

Voltage-gated K+ channels perform many functions in integration of synaptic input and action potential (AP) generation. In this study we show that in bitufted interneurones from layer 2/3 of the somatosensory cortex, the height and width of APs recorded at the soma are sensitive to changes in the resting membrane potential, suggesting subthreshold activity of voltage-gated conductances. Attributes of K+ currents examined in nucleated patches revealed a fast subthreshold-inactivating K+ conductance (Kf) and a slow suprathreshold-inactivating K+ conductance (Ks). Simulations of these K+ conductances, incorporated into a Hodgkin–Huxley-type model, suggested that during a single AP or during low frequency trains of APs, subthreshold inactivation of Kf was the primary modulator of AP shape, whereas during trains of APs the shape was governed to a larger degree by Ks resulting in the generation of smaller and broader APs. Utilizing the facilitating function of unitary pyramidal-to-bitufted cell synaptic transmission, single back-propagating APs were initiated in a bitufted interneurone by repeated stimulation of a presynaptic pyramidal cell. Ca2+ imaging and dendritic whole-cell recordings revealed that modulation of APs, which also affect the shape of back-propagating APs, resulted in a change in dendritic Ca2+ influx. Compartmental simulation of the back-propagating AP suggested a mechanism for the modulation of the back-propagating AP height and width by subthreshold activation of Kf. We speculate that this signal may modulate retrograde GABA release and consequently depression of synaptic efficacy of excitatory input from neighbouring pyramidal neurones.

(Received 8 October 2004; accepted after revision 10 November 2004; first published online 11 November 2004)
Corresponding author A. Korngreen: Faculty of Life Sciences, Bar-Ilan University, Ramat-Gan 52900, Israel. Email: korngra{at}mail.biu.ac.il




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