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Control of submillisecond synaptic timing in binaural coincidence detectors by Kv1 channels

Nature Neuroscience volume 13, pages 601–609 (2010)Cite this article

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Abstract

Neurons in the medial superior olive process sound-localization cues via binaural coincidence detection, in which excitatory synaptic inputs from each ear are segregated onto different branches of a bipolar dendritic structure and summed at the soma and axon with submillisecond time resolution. Although synaptic timing and dynamics critically shape this computation, synaptic interactions with intrinsic ion channels have received less attention. Using paired somatic and dendritic patch-clamp recordings in gerbil brainstem slices together with compartmental modeling, we found that activation of Kv1 channels by dendritic excitatory postsynaptic potentials (EPSPs) accelerated membrane repolarization in a voltage-dependent manner and actively improved the time resolution of synaptic integration. We found that a somatically biased gradient of Kv1 channels underlies the degree of compensation for passive cable filtering during propagation of EPSPs in dendrites. Thus, both the spatial distribution and properties of Kv1 channels are important for preserving binaural synaptic timing.

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Figure 1: Propagation of simulated EPSPs from the dendrites to the soma in MSO neurons.
Figure 2: The shape of EPSPs is stable regardless of propagation distance.
Figure 3: A DTX-sensitive conductance mediates EPSP sharpening.
Figure 4: Characterization of IK-LVA in outside-out patches.
Figure 5: Relative timing of IK-LVA and sEPSPs in whole-cell recordings at 35 °C.
Figure 6: VDS for dendritic and somatic EPSC injection in a compartmental model of the MSO.
Figure 7: Spatial effects of VDS in an MSO neuron model.
Figure 8: Spatio-temporal dynamics of membrane potential and IK-LVA for bilateral ITD-like distal inputs (750 Hz).

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Acknowledgements

We thank D. Johnston and A. Reyes for their comments on a previous version of the manuscript. This work was supported by grants from the US National Institutes of Health (DC006877 to N.L.G. and DC008543 to J.R.) and Ruth Kirschstein National Research Service Awards to P.J.M and L.L.S.

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Author notes

  1. Paul J Mathews and Pablo E Jercog: These authors contributed equally to this work.

Authors and Affiliations

  1. Section of Neurobiology and Institute for Neuroscience, University of Texas at Austin, Austin, Texas, USA

    Paul J Mathews, Luisa L Scott & Nace L Golding

  2. Center for Neural Science, New York University, New York, New York, USA

    Pablo E Jercog & John Rinzel

  3. Courant Institute of Mathematical Sciences, New York University, New York, New York, USA

    John Rinzel

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  1. Paul J Mathews
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Contributions

P.J.M. performed all of the voltage-clamp experiments characterizing IK-LVA in patches and whole cells. N.L.G. conducted dual somatic and dendritic current-clamp recordings. L.L.S. performed some of the experiments from older animals and also made some of the initial observations on voltage-dependent sharpening. P.E.J. performed all of the simulations. N.L.G. and J.R. helped design and supervise the experiments and simulations, respectively. N.L.G. wrote the manuscript, with contributions from P.J.M., P.E.J. and J.R.

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Correspondence to Nace L Golding.

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Mathews, P., Jercog, P., Rinzel, J. et al. Control of submillisecond synaptic timing in binaural coincidence detectors by Kv1 channels. Nat Neurosci 13, 601–609 (2010). https://doi.org/10.1038/nn.2530

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