Low Somatic Sodium Conductance Enhances Action Potential Precision in Time-Coding Auditory Neurons

Overview

Journal J Neurosci

Specialty Neurology

Date 2016 Nov 25

PMID 27881784

Citations 11

Authors

Yang Yang

Bina Ramamurthy

Andreas Neef

Matthew A Xu-Friedman

Affiliations

Soon will be listed here.

Abstract

Significance Statement: Proper hearing depends on analyzing temporal aspects of sounds with high precision. Auditory neurons that specialize in precise temporal information have a suite of unusual intrinsic properties, including nonovershooting action potentials and few sodium channels in the soma. However, it was not clear how low sodium channel availability in the soma influenced the temporal precision of action potentials initiated in the axon initial segment. We studied this using dynamic clamp to mimic sodium channels in the soma, which yielded normal, overshooting action potentials. Increasing somatic sodium conductance had major negative consequences: synaptic activity evoked action potentials with lower fidelity, and the precision of coincidence detection was degraded. Thus, low somatic sodium channel availability appears to enhance fidelity and temporal precision.

Citing Articles

Molecular logic for cellular specializations that initiate the auditory parallel processing pathways.

Jing J, Hu M, Ngodup T, Ma Q, Lau S, Ljungberg M Nat Commun. 2025; 16(1):489.

PMID: 39788966 PMC: 11717940. DOI: 10.1038/s41467-024-55257-z.

Revealing a hidden conducting state by manipulating the intracellular domains in K10.1 exposes the coupling between two gating mechanisms.

Abdelaziz R, Tomczak A, Neef A, Pardo L Elife. 2024; 12.

PMID: 39259196 PMC: 11390113. DOI: 10.7554/eLife.91420.

Fast Inhibition Slows and Desynchronizes Mouse Auditory Efferent Neuron Activity.

Fischl M, Pederson A, Voglewede R, Cheng H, Drew J, Torres Cadenas L J Neurosci. 2024; 44(33).

PMID: 38937103 PMC: 11326868. DOI: 10.1523/JNEUROSCI.0382-24.2024.

Molecular logic for cellular specializations that initiate the auditory parallel processing pathways.

Jing J, Hu M, Ngodup T, Ma Q, Lau S, Ljungberg C bioRxiv. 2023; .

PMID: 37293040 PMC: 10245571. DOI: 10.1101/2023.05.15.539065.

High-resolution volumetric imaging constrains compartmental models to explore synaptic integration and temporal processing by cochlear nucleus globular bushy cells.

Spirou G, Kersting M, Carr S, Razzaq B, Yamamoto Alves Pinto C, Dawson M Elife. 2023; 12.

PMID: 37288824 PMC: 10435236. DOI: 10.7554/eLife.83393.

References

Adam T, Schwarz D, Finlayson P . Firing properties of chopper and delay neurons in the lateral superior olive of the rat. Exp Brain Res. 1999; 124(4):489-502. DOI: 10.1007/s002210050645. View

Golding N, Ferragamo M, Oertel D . Role of intrinsic conductances underlying responses to transients in octopus cells of the cochlear nucleus. J Neurosci. 1999; 19(8):2897-905. PMC: 6782262. View

Burkitt A, Clark G . Analysis of integrate-and-fire neurons: synchronization of synaptic input and spike output. Neural Comput. 1999; 11(4):871-901. DOI: 10.1162/089976699300016485. View

Grigg J, Brew H, Tempel B . Differential expression of voltage-gated potassium channel genes in auditory nuclei of the mouse brainstem. Hear Res. 2000; 140(1-2):77-90. DOI: 10.1016/s0378-5955(99)00187-2. View

Gentet L, Stuart G, Clements J . Direct measurement of specific membrane capacitance in neurons. Biophys J. 2000; 79(1):314-20. PMC: 1300935. DOI: 10.1016/S0006-3495(00)76293-X. View

Oertel D, Bal R, GARDNER S, Smith P, Joris P . Detection of synchrony in the activity of auditory nerve fibers by octopus cells of the mammalian cochlear nucleus. Proc Natl Acad Sci U S A. 2000; 97(22):11773-9. PMC: 34348. DOI: 10.1073/pnas.97.22.11773. View

Taschenberger H, von Gersdorff H . Fine-tuning an auditory synapse for speed and fidelity: developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity. J Neurosci. 2000; 20(24):9162-73. PMC: 6773022. View

Xie X, Dale T, John V, Cater H, Peakman T, Clare J . Electrophysiological and pharmacological properties of the human brain type IIA Na+ channel expressed in a stable mammalian cell line. Pflugers Arch. 2001; 441(4):425-33. DOI: 10.1007/s004240000448. View

Futai K, Okada M, Matsuyama K, Takahashi T . High-fidelity transmission acquired via a developmental decrease in NMDA receptor expression at an auditory synapse. J Neurosci. 2001; 21(10):3342-9. PMC: 6762464. View

10.

Bal R, Oertel D . Potassium currents in octopus cells of the mammalian cochlear nucleus. J Neurophysiol. 2001; 86(5):2299-311. DOI: 10.1152/jn.2001.86.5.2299. View

11.

von Gersdorff H, Borst J . Short-term plasticity at the calyx of Held. Nat Rev Neurosci. 2002; 3(1):53-64. DOI: 10.1038/nrn705. View

12.

Colbert C, Pan E . Ion channel properties underlying axonal action potential initiation in pyramidal neurons. Nat Neurosci. 2002; 5(6):533-8. DOI: 10.1038/nn0602-857. View

13.

Brand A, Behrend O, Marquardt T, McAlpine D, Grothe B . Precise inhibition is essential for microsecond interaural time difference coding. Nature. 2002; 417(6888):543-7. DOI: 10.1038/417543a. View

14.

Burbidge S, Dale T, Powell A, Whitaker W, Xie X, Romanos M . Molecular cloning, distribution and functional analysis of the NA(V)1.6. Voltage-gated sodium channel from human brain. Brain Res Mol Brain Res. 2002; 103(1-2):80-90. DOI: 10.1016/s0169-328x(02)00188-2. View

15.

Meadows L, Chen Y, Powell A, Clare J, Ragsdale D . Functional modulation of human brain Nav1.3 sodium channels, expressed in mammalian cells, by auxiliary beta 1, beta 2 and beta 3 subunits. Neuroscience. 2002; 114(3):745-53. DOI: 10.1016/s0306-4522(02)00242-7. View

16.

Yu F, Catterall W . Overview of the voltage-gated sodium channel family. Genome Biol. 2003; 4(3):207. PMC: 153452. DOI: 10.1186/gb-2003-4-3-207. View

17.

Rothman J, Manis P . Differential expression of three distinct potassium currents in the ventral cochlear nucleus. J Neurophysiol. 2003; 89(6):3070-82. DOI: 10.1152/jn.00125.2002. View

18.

Rothman J, Manis P . The roles potassium currents play in regulating the electrical activity of ventral cochlear nucleus neurons. J Neurophysiol. 2003; 89(6):3097-113. DOI: 10.1152/jn.00127.2002. View

19.

Grothe B . New roles for synaptic inhibition in sound localization. Nat Rev Neurosci. 2003; 4(7):540-50. DOI: 10.1038/nrn1136. View

20.

Edwards C, Ottoson D . The site of impulse initiation in a nerve cell of a crustacean stretch receptor. J Physiol. 1958; 143(1):138-48. PMC: 1356716. DOI: 10.1113/jphysiol.1958.sp006049. View