Active dendrites support efficient initiation of dendritic spikes in hippocampal CA3 pyramidal neurons

Abstract

CA3 pyramidal neurons are important for memory formation and pattern completion in the hippocampal network. It is generally thought that proximal synapses from the mossy fibers activate these neurons most efficiently, whereas distal inputs from the perforant path have a weaker modulatory influence. We used confocally targeted patch-clamp recording from dendrites and axons to map the activation of rat CA3 pyramidal neurons at the subcellular level. Our results reveal two distinct dendritic domains. In the proximal domain, action potentials initiated in the axon backpropagate actively with large amplitude and fast time course. In the distal domain, Na+ channel–mediated dendritic spikes are efficiently initiated by waveforms mimicking synaptic events. CA3 pyramidal neuron dendrites showed a high Na+-to-K+ conductance density ratio, providing ideal conditions for active backpropagation and dendritic spike initiation. Dendritic spikes may enhance the computational power of CA3 pyramidal neurons in the hippocampal network.

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Figure 1: Subcellular patch-clamp recording from dendrites and axons of CA3 pyramidal neurons.
Figure 2: Action potentials backpropagate into the dendrites of CA3 pyramidal neurons with large amplitude and fast time course.
Figure 3: Dendritic action potential backpropagation in CA3 pyramidal cells shows only moderate activity dependence.
Figure 4: High Na+-to-K+ conductance ratio and distinct conductance gradients in CA3 pyramidal neuron dendrites.
Figure 5: Efficient initiation of dendritic Na+ spikes in CA3 pyramidal neurons.
Figure 6: Dendritic spikes are mediated by voltage-gated Na+ channels.
Figure 7: Dendritic spikes increase the efficacy of axosomatic action potential initiation.

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Acknowledgements

We thank G. Buzsáki and J. Lisman for critically reading previous manuscript versions. We also thank F. Marr and I. Koeva for technical assistance and E. Kramberger for perfect editorial support. This work was supported by the Deutsche Forschungsgemeinschaft (TR 3/B10) and the European Union (European Research Council Advanced grant to P.J.).

Author information

S.K. performed the experiments and analyzed the data. H.H. and S.J.G. contributed to initial experiments. P.J. analyzed data and wrote the paper. All of the authors revised the paper.

Correspondence to Peter Jonas.

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Kim, S., Guzman, S., Hu, H. et al. Active dendrites support efficient initiation of dendritic spikes in hippocampal CA3 pyramidal neurons. Nat Neurosci 15, 600–606 (2012). https://doi.org/10.1038/nn.3060

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