Acoustic trauma slows AMPA receptor‐mediated EPSCs in the auditory brainstem, reducing GluA4 subunit expression as a mechanism to rescue binaural function

Lateral superior olive (LSO) principal neurons receive AMPA receptor (AMPAR) ‐ and NMDA receptor (NMDAR)‐mediated EPSCs and glycinergic IPSCs. Both EPSCs and IPSCs have slow kinetics in prehearing animals, which during developmental maturation accelerate to sub‐millisecond decay time‐constants. This correlates with a change in glutamate and glycine receptor subunit composition quantified via mRNA levels. The NMDAR‐EPSCs accelerate over development to achieve decay time‐constants of 2.5 ms. This is the fastest NMDAR‐mediated EPSC reported. Acoustic trauma (AT, loud sounds) slow AMPAR‐EPSC decay times, increasing GluA1 and decreasing GluA4 mRNA. Modelling of interaural intensity difference suggests that the increased EPSC duration after AT shifts interaural level difference to the right and compensates for hearing loss. Two months after AT the EPSC decay times recovered to control values. Synaptic transmission in the LSO matures by postnatal day 20, with EPSCs and IPSCs having fast kinetics. AT changes the AMPAR subunits expressed and slows the EPSC time‐course at synapses in the central auditory system.

• Publication year

  2016

• Venue

  Journal of Physiology

• Publication date

  2016-06-09

• Fields of study

  Biology, Medicine, Chemistry

• Identifiers
  DOI 10.1113/JP271929PMID 27104476PMCID 4929335
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Excitation by Axon Terminal GABA Spillover in a Sound Localization Circuit

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• Principles and standards for reporting animal experiments in The Journal of Physiology and Experimental Physiology

  2015cited by this paper
• The precise temporal pattern of prehearing spontaneous activity is necessary for tonotopic map refinement.

  2014cited by this paper
• Inhibitory glycinergic neurotransmission in the mammalian auditory brainstem upon prolonged stimulation: short-term plasticity and synaptic reliability

  2014cited by this paper
• Glycinergic transmission modulates GABAergic inhibition in the avian auditory pathway

  2014cited by this paper
• Mechanisms contributing to central excitability changes during hearing loss

  2012cited by this paper
• Comparative posthearing development of inhibitory inputs to the lateral superior olive in gerbils and mice.

  2011cited by this paper
• Phosphorylation of AMPA Receptors Is Required for Sensory Deprivation-Induced Homeostatic Synaptic Plasticity

  2011cited by this paper
• Genetic analysis of neuronal ionotropic glutamate receptor subunits

  2011cited by this paper
• GluA4 is indispensable for driving fast neurotransmission across a high‐fidelity central synapse

  2011influential reference
• Low‐voltage activated Kv1.1 subunits are crucial for the processing of sound source location in the lateral superior olive in mice

  2011cited by this paper
• Modulation and control of synaptic transmission across the MNTB.

  2011influential reference
• Pre- and postsynaptic properties of glutamatergic transmission in the immature inhibitory MNTB-LSO pathway.

  2011cited by this paper
• It's About Time: How Input Timing Is Used and Not Used To Create Emergent Properties in the Auditory System

  2011cited by this paper
• Varying overall sound intensity to the two ears impacts interaural level difference discrimination thresholds by single neurons in the lateral superior olive.

  2010cited by this paper
• Triheteromeric NR1/NR2A/NR2B Receptors Constitute the Major N-Methyl-d-aspartate Receptor Population in Adult Hippocampal Synapses

  2010cited by this paper
• Lateral olivocochlear (LOC) neurons of the mouse LSO receive excitatory and inhibitory synaptic inputs with slower kinetics than LSO principal neurons.

  2010cited by this paper
• NMDAR‐mediated EPSCs are maintained and accelerate in time course during maturation of mouse and rat auditory brainstem in vitro

  2010cited by this paper
• Synaptic changes underlying the strengthening of GABA/glycinergic connections in the developing lateral superior olive.

  2010cited by this paper
• The impact of synaptic conductance on action potential waveform: evoking realistic action potentials with a simulated synaptic conductance.

  2009cited by this paper
• Adding Insult to Injury: Cochlear Nerve Degeneration after “Temporary” Noise-Induced Hearing Loss

  2009cited by this paper
• Cochlear nucleus neurons redistribute synaptic AMPA and glycine receptors in response to monaural conductive hearing loss.

  2009cited by this paper
• Native glycine receptor subtypes and their physiological roles.

  2009cited by this paper
• PKA has a critical role in synaptic delivery of GluR1- and GluR4-containing AMPARs during initial stages of acquisition of in vitro classical conditioning.

  2009cited by this paper
• Tonotopic reorganization of developing auditory brainstem circuits

  2009influential reference
• Maturation of excitatory synaptic transmission of the rat nucleus accumbens from juvenile to adult.

  2009cited by this paper
• Involvement of AMPA receptor desensitization in short‐term synaptic depression at the calyx of Held in developing rats

  2008cited by this paper
• Initial segment Kv2.2 channels mediate a slow delayed rectifier and maintain high frequency action potential firing in medial nucleus of the trapezoid body neurons

  2008cited by this paper
• Initial segment Kv2.2 channels mediate a slow delayed rectifier and maintain high frequency action potential firing in MNTB neurons

  2008cited by this paper
• Acceleration of AMPA receptor kinetics underlies temperature‐dependent changes in synaptic strength at the rat calyx of Held

  2007cited by this paper
• GABA and glycine as neurotransmitters: a brief history

  2006cited by this paper
• Multiple polymorphic loci determine basal hepatic and splenic iron status in mice

  2006cited by this paper
• Deafness‐related decreases in glycine‐immunoreactive labeling in the rat cochlear nucleus

  2005cited by this paper
• Postsynaptic Expression of Homeostatic Plasticity at Neocortical Synapses

  2005cited by this paper
• Hearing Loss Raises Excitability in the Auditory Cortex

  2005cited by this paper
• Shift from depolarizing to hyperpolarizing glycine action occurs at different perinatal ages in superior olivary complex nuclei

  2005cited by this paper
• Inhibitory synapses in the developing auditory system are glutamatergic

  2005cited by this paper
• Neural population coding of sound level adapts to stimulus statistics

  2005cited by this paper
• Developmental refinement of inhibitory sound-localization circuits.

  2005cited by this paper
• Maturation of glycinergic inhibition in the gerbil medial superior olive after hearing onset

  2005cited by this paper
• Differences in glycinergic mIPSCs in the auditory brain stem of normal and congenitally deaf neonatal mice.

  2004cited by this paper
• Kv1 currents mediate a gradient of principal neuron excitability across the tonotopic axis in the rat lateral superior olive

  2004cited by this paper
• Developmental switch from GABA to glycine release in single central synaptic terminals

  2004cited by this paper
• The Role of AMPA Receptor Gating in the Development of High-Fidelity Neurotransmission at the Calyx of Held Synapse

  2004cited by this paper
• Inhibitory Control at a Synaptic Relay

  2004cited by this paper
• The Synaptic Vesicle Protein CSPα Prevents Presynaptic Degeneration

  2004cited by this paper
• Unilateral cochlear ablation produces greater loss of inhibition in the contralateral inferior colliculus

  2004cited by this paper
• Interaural level difference processing in the lateral superior olive and the inferior colliculus.

  2004cited by this paper
• The synaptic vesicle protein CSP alpha prevents presynaptic degeneration.

  2004cited by this paper
• Decreased Temporal Precision of Auditory Signaling in Kcna1-Null Mice: An Electrophysiological Study In Vivo

  2003cited by this paper
• Developmental Increase in Vesicular Glutamate Content Does Not Cause Saturation of AMPA Receptors at the Calyx of Held Synapse

  2003cited by this paper
• The Lateral Superior Olive: A Functional Role in Sound Source Localization

  2003cited by this paper
• Expression and Function of Chloride Transporters during Development of Inhibitory Neurotransmission in the Auditory Brainstem

  2003cited by this paper
• Elimination and strengthening of glycinergic/GABAergic connections during tonotopic map formation

  2003cited by this paper
• The Coding of Spatial Location by Single Units in the Lateral Superior Olive of the Cat. II. The Determinants of Spatial Receptive Fields in Azimuth

  2002cited by this paper
• Localization of rat glycine receptor α1 and α2 subunit transcripts in the developing auditory brainstem

  2001cited by this paper
• High-Fidelity Transmission Acquired via a Developmental Decrease in NMDA Receptor Expression at an Auditory Synapse

  2001cited by this paper
• A new mathematical model for relative quantification in real-time RT-PCR.

  2001cited by this paper
• Localization of rat glycine receptor alpha1 and alpha2 subunit transcripts in the developing auditory brainstem.

  2001cited by this paper
• NMDAR EPSC kinetics do not regulate the critical period for LTP at thalamocortical synapses

  2001cited by this paper
• Correlation of AMPA Receptor Subunit Composition with Synaptic Input in the Mammalian Cochlear Nuclei

  2001cited by this paper
• The glycinergic inhibitory synapse

  2001cited by this paper
• Delay analysis in the auditory brainstem of the rat: comparison with click latency.

  2001cited by this paper
• Latency as a function of intensity in auditory neurons: influences of central processing.

  2000cited by this paper
• Fine-Tuning an Auditory Synapse for Speed and Fidelity: Developmental Changes in Presynaptic Waveform, EPSC Kinetics, and Synaptic Plasticity

  2000cited by this paper
• GABA mediates presynaptic inhibition at glycinergic synapses in a rat auditory brainstem nucleus

  2000cited by this paper
• Synaptic activity at calcium-permeable AMPA receptors induces a switch in receptor subtype

  2000cited by this paper
• Status epilepticus decreases glutamate receptor 2 mRNA and protein expression in hippocampal pyramidal cells before neuronal death.

  2000cited by this paper
• Diversity and plasticity in amino acid receptor subunits in the rat auditory brain stem.

  2000cited by this paper
• Development and influence of inhibition in the lateral superior olivary nucleus.

  2000cited by this paper
• Characterisation of inhibitory and excitatory postsynaptic currents of the rat medial superior olive

  2000cited by this paper
• Expression of AMPA receptor subunit flip/flop splice variants in the rat auditory brainstem and inferior colliculus

  2000cited by this paper
• Developmental Profile of the Changing Properties of NMDA Receptors at Cerebellar Mossy Fiber–Granule Cell Synapses

  2000cited by this paper
• Differential Distribution of Intracellular Glutamate Receptors in Dendrites

  1999cited by this paper
• Time Course and Permeation of Synaptic AMPA Receptors in Cochlear Nuclear Neurons Correlate with Input

  1999cited by this paper
• Synaptic mechanisms for coding timing in auditory neurons.

  1999cited by this paper
• A Developmental Shift from GABAergic to Glycinergic Transmission in the Central Auditory System

  1998cited by this paper
• Neuron types in the rat lateral superior olive and developmental changes in the complexity of their dendritic arbors

  1998cited by this paper
• Corelease of two fast neurotransmitters at a central synapse.

  1998cited by this paper
• Development of adult‐type inhibitory glycine receptors in the central auditory system of rats

  1997cited by this paper
• Processing of interaural intensity differences in the LSO: role of interaural threshold differences.

  1997cited by this paper
• Correlation between kinetics and RNA splicing of alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptors in neocortical neurons.

  1996cited by this paper
• Neural Delays Shape Selectivity to Interaural Intensity Differences in the Lateral Superior Olive

  1996cited by this paper
• Synaptic NMDA receptors in developing mouse hippocampal neurones: functional properties and sensitivity to ifenprodil.

  1996cited by this paper
• Recordings from slices indicate that octopus cells of the cochlear nucleus detect coincident firing of auditory nerve fibers with temporal precision

  1995cited by this paper
• Pre‐ and postsynaptic glutamate receptors at a giant excitatory synapse in rat auditory brainstem slices.

  1995cited by this paper
• Inhibition in the superior olivary complex: pharmacological evidence from mouse brain slice.

  1995cited by this paper
• Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS.

  1995cited by this paper
• Development of glycinergic and glutamatergic synaptic transmission in the auditory brainstem of perinatal rats

  1995cited by this paper
• Envelope coding in the lateral superior olive. I. Sensitivity to interaural time differences.

  1995cited by this paper
• AMPA receptors with high Ca2+ permeability mediate synaptic transmission in the avian auditory pathway.

  1995cited by this paper
• Pathway-specific variants of AMPA receptors and their contribution to neuronal signaling

  1994cited by this paper
• A characterization of excitatory postsynaptic potentials in the avian nucleus magnocellularis.

  1994cited by this paper
• A molecular determinant for submillisecond desensitization in glutamate receptors.

  1994cited by this paper
• Development of hearing in neonatal rats: air and bone conducted ABR thresholds.

  1993cited by this paper
• Activity‐dependent Refinement of Inhibitory Connections

  1993cited by this paper
• The kinetics of the response to glutamate and kainate in neurons of the avian cochlear nucleus.

  1992cited by this paper
• Functional correlation of fetal and adult forms of glycine receptors with developmental changes in inhibitory synaptic receptor channels.

  1992cited by this paper
• The influence of inhibitory afferents on the development of postsynaptic dendritic arbors

  1992cited by this paper
• Physiological properties of neurons in the mouse superior olive: membrane characteristics and postsynaptic responses studied in vitro.

  1991cited by this paper

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• Noise-Induced Hearing Loss Enhances Ca2+-Dependent Electrical Activity in Lateral Cochlear Efferents

  2025cites this paper
• Cellular and synaptic specializations for sub-millisecond precision in the mammalian auditory brainstem

  2025cites this paper
• Conditional mGluR5 Knockout in Glutamatergic Pathways Disrupts the Development of Excitatory Synaptic Transmission onto Mouse MNTB Neurons.

  2025cites this paper
• Synaptic Drive onto Inhibitory and Excitatory Principal Neurons of the Mouse Lateral Superior Olive

  2025cites this paper
• Hearing loss-related altered neuronal activity in the inferior colliculus.

  2024cites this paper
• Molecular and functional profiling of cell diversity and identity in the lateral superior olive, an auditory brainstem center with ascending and descending projections

  2024cites this paper
• Sensorineural hearing loss and cognitive impairment: three hypotheses

  2024cites this paper
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• Development of synaptic fidelity and action potential robustness at an inhibitory sound localization circuit: effects of otoferlin‐related deafness

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  2022cites this paper
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  2021cites this paper
• Why is the perceptual octave stretched? An account based on mismatched time constants within the auditory brainstem

  2021cites this paper
• Ambient noise exposure induces long-term adaptations in adult brainstem neurons

  2021cites this paper
• Specific loss of neural sensitivity to interaural time difference of unmodulated noise stimuli following noise-induced hearing loss.

  2020cites this paper
• Activity-Dependent Calcium Signaling in Neurons of the Medial Superior Olive during Late Postnatal Development

  2020influential citation
• Kv3.1 and Kv3.3 subunits differentially contribute to Kv3 channels and action potential repolarization in principal neurons of the auditory brainstem

  2020cites this paper
• Physiological and anatomical development of glycinergic inhibition in the mouse superior paraolivary nucleus following hearing onset.

  2020cites this paper
• Auditory brainstem development and plasticity.

  2020cites this paper
• The Superior Olivary Complex

  2020cites this paper
• GABA is a modulator, rather than a classical transmitter, in the medial nucleus of the trapezoid body–lateral superior olive sound localization circuit

  2019cites this paper
• The ion channels and synapses responsible for the physiological diversity of mammalian lower brainstem auditory neurons

  2019cites this paper
• Topographic map refinement and synaptic strengthening of a sound localization circuit require spontaneous peripheral activity

  2019cites this paper
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  2019cites this paper
• Intrinsic and miniature postsynaptic current changes in rat principal neurons of the lateral superior olive after unilateral auditory deprivation at an early age.

  2019cites this paper
• Pre‐ and postsynaptic ionotropic glutamate receptors in the auditory system of mammals

  2018cites this paper
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  2018cites this paper
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  2018cites this paper
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  2018cites this paper
• Precisely timed inhibition facilitates action potential firing for spatial coding in the auditory brainstem

  2018cites this paper
• Glycinergic Inhibitory Plasticity in Binaural Neurons Is Cumulative and Gated by Developmental Changes in Action Potential Backpropagation.

  2018influential citation
• Impaired auditory processing and altered structure of the endbulb of Held synapse in mice lacking the GluA3 subunit of AMPA receptors

  2017cites this paper
• Physiological models of the lateral superior olive

  2017cites this paper
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  2016cites this paper