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Spatial compartmentalization and functional impact of conductance in pyramidal neurons

Nature Neuroscience volume 7, pages 961–967 (2004)Cite this article

Abstract

Dendritic spikes signal synaptic integration at remote apical dendritic sites in neocortical pyramidal neurons in vitro. Do dendritic spikes have a salient signaling role under in vivo conditions, where neocortical pyramidal neurons are bombarded with synaptic input? In the present study, levels of synaptic conductance apparent during active network states in vivo were emulated in vitro. Pronounced enhancement of somatic or apical dendritic conductance was spatially compartmentalized and 'visible' over a dendritic length (∼200 μm) on the order of half the voltage length constant, as predicted by passive cable models. The spatial compartmentalization of conductance allowed independent subthreshold synaptic integration at axo-somatic and apical dendritic sites. Furthermore, spikes generated at distal apical dendritic sites efficiently propagated to the axon to initiate action potentials under high synaptic conductance states. The dendritic arborization and voltage-activated channel complement of rat neocortical pyramidal neurons are therefore optimized to allow distributed processing under realistic conductance states.

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Figure 1: Compartmentalization of conductance in pyramidal neurons.
Figure 2: Conductance compartmentalization is independent of magnitude.
Figure 3: Impact of conductance on dendritic stimulated EPSPs.
Figure 4: Independence of distal dendritic synaptic integration.
Figure 5: Control of dendritic excitation by simulated synaptic bombardment.
Figure 6: Dendritic synaptic conductance controls action potential back-propagation.

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Acknowledgements

I am grateful to S. Atkinson, L. Gentet, B. Khakh and L. Lagnado for helpful comments on the manuscript.

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  1. Medical Research Council (MRC) Laboratory of Molecular Biology, Hills Road, Cambridge, CB2 2QH, UK

    Stephen R Williams

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Correspondence to Stephen R Williams.

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Supplementary information

Supplementary Fig. 1

Control of apical dendritic spikes. (a) Quadruple somato-dendritic recording of dendritic spikes evoked by a threshold current step (green) under control (upper traces) and in the presence of a somatic conductance source (90 nS). (b) In conductance-insensitive neurons (n = 29) incremental increases of somatic conductance failed to alter the amplitude of dendritic spikes at site of generation (red), at proximal apical dendritic loci (blue) or the initiation of axonal action potentials (black). (c) In a conductance-sensitive neuron enhanced somatic conductance (90 nS) broke the link between dendritic spike generation and axonal action potential initiation. (d) Pooled data demonstrating the independence of dendritic spike generation, but the conductance-dependent disruption of axonal action potential firing (n = 16) in conductance-sensitive neurons. (GIF 34 kb)

Supplementary Fig. 2

Properties of conductance-sensitive and conductance-insensitive neurons. (a) In conductance-sensitive and -insensitive neurons enhanced somatic conductance (90 nS) decreased the somatic peak apparent input resistance to a similar degree. (b) Distribution of the maximal rate of rise of dendritic spikes recorded at distal (right data cluster) and proximal apical dendritic sites. (c) Pooled analysis describing the maximal rate of rise of dendritic spikes and somatic action potentials in the two classes of neurons (conductance-insensitive: site of generation 25.6 ± 2.1 Vs−1 (567 ± 13 μm), proximal-apical 68.0 ± 6.5 Vs−1 (250 ± 9 μm), soma 381.6 ± 9.1 Vs−1; conductance-sensitive: site of generation 17.7 ± 2.0 Vs−1, P < 0.005 (Students' T-test) (587 ± 17 μm), proximal-apical 34.3 ± 4.9 Vs−1, P < 0.001 (225 ± 12 μm), soma 370.1 ± 11.7 Vs−1 (not different)). (GIF 28 kb)

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Williams, S. Spatial compartmentalization and functional impact of conductance in pyramidal neurons. Nat Neurosci 7, 961–967 (2004). https://doi.org/10.1038/nn1305

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