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The Journal of Neuroscience, August 13, 2003, 23(19):7358-7367

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Voltage- and Site-Dependent Control of the Somatic Impact of Dendritic IPSPs

Stephen R. Williams^1,2,3 and Greg J. Stuart^1,2

¹Division of Neuroscience, John Curtin School of Medical Research, Australian National University, Canberra, Australian Capital Territory 0200, Australia, ²Institute of Physiology, University of Freiburg, D-79104 Freiburg, Germany, and ³Neurobiology Division, Medical Research Council Laboratory of Molecular Biology, Cambridge CB2 2QH, United Kingdom

Inhibitory interneurons target specific subcellular compartments of cortical pyramidal neurons, where location-specific interactions of IPSPs with voltage-activated ion channels are likely to influence the inhibitory control of neuronal output. To investigate this, we simulated IPSPs as a conductance source at sites across the somato-apical dendritic axis (up to 750 µm) of neocortical layer 5 pyramidal neurons. Analysis revealed that the electrotonic architecture of cortical pyramidal neurons is highly voltage dependent, resulting in a significant site-dependent disparity between the amplitude, kinetics, and dendro-somatic attenuation of IPSPs generated from depolarized (-50 mV) and hyperpolarized (-80 mV) membrane potentials. At the soma, the time course of IPSPs evoked from depolarized potentials was greatest when generated from proximal dendritic sites and decreased as events were generated more distally, whereas the somatic time course of IPSPs evoked from hyperpolarized potentials was independent of the dendritic site of generation. This behavior resulted from the concerted actions of axo-somatic sodium channels that increased the duration of proximal dendritic IPSPs generated at depolarized potentials and distal dendritic hyperpolarization-activated channels that mediated site independence of somatic IPSP time course at hyperpolarized potentials. Functionally, this voltage-dependent control of IPSPs shaped the spatial and temporal profile of inhibition of axonal action potential firing and dendritic spike generation. Together, these findings demonstrate that the somatic impact of dendritic IPSPs is highly voltage dependent and controlled by classes of ion channels differentially distributed across axodendritic domains, directly revealing site-dependent inhibitory synaptic processing in cortical pyramidal neurons.

Key words: sodium channel; I_H channel; inhibition; patch clamp; action potential; neocortex; dendrite

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Received Apr. 8, 2003; revised Jun. 9, 2003; accepted Jun. 13, 2003.

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