Local Control of Postinhibitory Rebound Spiking in CA1 Pyramidal Neuron Dendrites
Open Access
- 5 May 2010
- journal article
- Published by Society for Neuroscience in Journal of Neuroscience
- Vol. 30 (18), 6434-6442
- https://doi.org/10.1523/jneurosci.4066-09.2010
Abstract
Postinhibitory rebound spiking is characteristic of several neuron types and brain regions, where it sustains spontaneous activity and central pattern generation. However, rebound spikes are rarely observed in the principal cells of the hippocampus under physiological conditions. We report that CA1 pyramidal neurons support rebound spikes mediated by hyperpolarization-activated inward current (Ih), and normally masked by A-type potassium channels (KA). In both experiments and computational models,KAblockage or reduction consistently resulted in a somatic action potential upon release from hyperpolarizing injections in the soma or main apical dendrite. Rebound spiking was systematically abolished by the additional blockage or reduction ofIh. Since the density of bothKAandIhincreases in these cells with the distance from the soma, such “latent” mechanism may be most effective in the distal dendrites, which are targeted by a variety of GABAergic interneurons. Detailed computer simulations, validated against the experimental data, demonstrate that rebound spiking can result from activation of distal inhibitory synapses. In particular, partialKAreduction confined to one or few branches of the apical tuft may be sufficient to elicit a local spike following a train of synaptic inhibition. Moreover, the spatial extent and amount ofKAreduction determines whether the dendritic spike propagates to the soma. These data suggest that the plastic regulation ofKAcan provide a dynamic switch to unmask postinhibitory spiking in CA1 pyramidal neurons. This newly discovered local modulation of postinhibitory spiking further increases the signal processing power of the CA1 synaptic microcircuitry.Keywords
This publication has 70 references indexed in Scilit:
- Kv4.2 is a locus for PKC and ERK/MAPK cross-talkBiochemical Journal, 2009
- Interneurons hyperpolarize pyramidal cells along their entire somatodendritic axisNature Neuroscience, 2008
- Functional significance of axonal Kv7 channels in hippocampal pyramidal neuronsProceedings of the National Academy of Sciences of the United States of America, 2008
- Long-Term Potentiation in Rat Hippocampal Neurons Is Accompanied by Spatially Widespread Changes in Intrinsic Oscillatory Dynamics and ExcitabilityNeuron, 2007
- Regulation of Dendritic Excitability by Activity-Dependent Trafficking of the A-Type K+ Channel Subunit Kv4.2 in Hippocampal NeuronsNeuron, 2007
- Associative pairing enhances action potential back‐propagation in radial oblique branches of CA1 pyramidal neuronsThe Journal of Physiology, 2007
- Differences between the scaling of miniature IPSCs and EPSCs recorded in the dendrites of CA1 mouse pyramidal neuronsThe Journal of Physiology, 2006
- Distinct timing in the activity of cannabinoid-sensitive and cannabinoid-insensitive basket cellsNature Neuroscience, 2006
- Quantitative Analysis and Subcellular Distribution of mRNA and Protein Expression of the Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels throughout Development in Rat HippocampusCerebral Cortex, 2006
- Neural signatures of cell assembly organizationNature Reviews Neuroscience, 2005