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The Journal of Neuroscience, February 8, 2006, 26(6):1677-1687; doi:10.1523/JNEUROSCI.3664-05.2006
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Cellular/Molecular
Single Ih Channels in Pyramidal Neuron Dendrites: Properties, Distribution, and Impact on Action Potential Output
Maarten H. P. Kole,1 * Stefan Hallermann,2 * andGreg J. Stuart1 1Division of Neuroscience, John Curtin School of Medical Research, Australian National University, Canberra 0200, Australian Capital Territory, Australia, and 2Physiologisches Institut I, Universität Freiburg, D-79104 Freiburg, Germany
Correspondence should be addressed to Maarten H. P. Kole at the above address. Email: maarten.kole{at}anu.edu.au
The hyperpolarization-activated cation current (Ih) plays an important role in regulating neuronal excitability, yet its native single-channel properties in the brain are essentially unknown. Here we use variance-mean analysis to study the properties of single Ih channels in the apical dendrites of cortical layer 5 pyramidal neurons in vitro. In these neurons, we find that Ih channels have an average unitary conductance of 680 ± 30 fS (n = 18). Spectral analysis of simulated and native Ih channels showed that there is little or no channel flicker below 5 kHz. In contrast to the uniformly distributed single-channel conductance, Ih channel number increases exponentially with distance, reaching densities as high as
550 channels/µm2 at distal dendritic sites. These high channel densities generate significant membrane voltage noise. By incorporating a stochastic model of Ih single-channel gating into a morphologically realistic model of a layer 5 neuron, we show that this channel noise is higher in distal dendritic compartments and increased threefold with a 10-fold increased single-channel conductance (6.8 pS) but constant Ih current density. In addition, we demonstrate that voltage fluctuations attributable to stochastic Ih channel gating impact on action potential output, with greater spike-timing precision in models with the experimentally determined single-channel conductance. These data suggest that, in the face of high current densities, the small single-channel conductance of Ih is critical for maintaining the fidelity of action potential output.
Key words: HCN; nonstationary fluctuation analysis; spike timing; noise; cortex; gain
Received Aug. 30, 2005; revised Dec. 21, 2005; accepted Dec. 21, 2005.
Correspondence should be addressed to Maarten H. P. Kole at the above address. Email: maarten.kole{at}anu.edu.au
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