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Research Articles, Systems/Circuits

Arrangement of Excitatory Synaptic Inputs on Dendrites of the Medial Superior Olive

Alexander R. Callan, Martin Heß, Felix Felmy and Christian Leibold
Journal of Neuroscience 13 January 2021, 41 (2) 269-283; DOI: https://doi.org/10.1523/JNEUROSCI.1055-20.2020
Alexander R. Callan
1Department Biology II, Ludwig-Maximilians-Universität München, München, Germany, 82152
2Graduate School of Systemic Neurosciences, Ludwig-Maximilians-Universität München, München, Germany, 82152
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Martin Heß
1Department Biology II, Ludwig-Maximilians-Universität München, München, Germany, 82152
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Felix Felmy
3Zoologisches Institut, Stiftung Tierärztliche Hochschule Hannover, Hannover, Germany, 30559
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Christian Leibold
1Department Biology II, Ludwig-Maximilians-Universität München, München, Germany, 82152
4Bernstein Center for Computational Neuroscience, München, Germany, 82152
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Abstract

Neurons in the medial superior olive (MSO) detect 10 µs differences in the arrival times of a sound at the two ears. Such acuity requires exquisitely precise integration of binaural synaptic inputs. There is substantial understanding of how neuronal phase locking of afferent MSO structures, and MSO membrane biophysics subserve such high precision. However, we still lack insight into how the entirety of excitatory inputs is integrated along the MSO dendrite under sound stimulation. To understand how the dendrite integrates excitatory inputs as a whole, we combined anatomic quantifications of the afferent innervation in gerbils of both sexes with computational modeling of a single cell. We present anatomic data from confocal and transmission electron microscopy showing that single afferent fibers follow a single dendrite mostly up to the soma and contact it at multiple (median 4) synaptic sites, each containing multiple independent active zones (the overall density of active zones is estimated as 1.375 per μm2). Thus, any presynaptic action potential may elicit temporally highly coordinated synaptic vesicle release at tens of active zones, thereby achieving secure transmission. Computer simulations suggest that such an anatomic arrangement boosts the amplitude and sharpens the time course of excitatory postsynaptic potentials by reducing current sinks and more efficiently recruiting subthreshold potassium channels. Both effects improve binaural coincidence detection compared with single large synapses at the soma. Our anatomic data further allow for estimation of a lower bound of 7 and an upper bound of 70 excitatory fibers per dendrite.

SIGNIFICANCE STATEMENT Passive dendritic propagation attenuates the amplitude of postsynaptic potentials and widens their temporal spread. Neurons in the medial superior olive, with their large bilateral dendrites, however, can detect coincidence of binaural auditory inputs with submillisecond precision, a computation that is in stark contrast to passive dendritic processing. Here, we show that dendrites can counteract amplitude attenuation and even decrease the temporal spread of postsynaptic potentials, if active subthreshold potassium conductances are triggered in temporal coordination along the whole dendrite. Our anatomic finding that axons run in parallel to the dendrites and make multiple synaptic contacts support such coordination since incoming action potentials would depolarize the dendrite at multiple sites within a brief time interval.

  • binaural hearing
  • coincidence detection
  • dendritic computation
  • innervation pattern
  • ITD
  • MSO

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The Journal of Neuroscience: 41 (2)
Journal of Neuroscience
Vol. 41, Issue 2
13 Jan 2021
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Arrangement of Excitatory Synaptic Inputs on Dendrites of the Medial Superior Olive
Alexander R. Callan, Martin Heß, Felix Felmy, Christian Leibold
Journal of Neuroscience 13 January 2021, 41 (2) 269-283; DOI: 10.1523/JNEUROSCI.1055-20.2020

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Arrangement of Excitatory Synaptic Inputs on Dendrites of the Medial Superior Olive
Alexander R. Callan, Martin Heß, Felix Felmy, Christian Leibold
Journal of Neuroscience 13 January 2021, 41 (2) 269-283; DOI: 10.1523/JNEUROSCI.1055-20.2020
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Keywords

  • binaural hearing
  • coincidence detection
  • dendritic computation
  • innervation pattern
  • ITD
  • MSO

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