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Synaptic plasticity in the auditory system: a review

Abstract

Synaptic transmission via chemical synapses is dynamic, i.e., the strength of postsynaptic responses may change considerably in response to repeated synaptic activation. Synaptic strength is increased during facilitation, augmentation and potentiation, whereas a decrease in synaptic strength is characteristic for depression and attenuation. This review attempts to discuss the literature on short-term and long-term synaptic plasticity in the auditory brainstem of mammals and birds. One hallmark of the auditory system, particularly the inner ear and lower brainstem stations, is information transfer through neurons that fire action potentials at very high frequency, thereby activating synapses >500 times per second. Some auditory synapses display morphological specializations of the presynaptic terminals, e.g., calyceal extensions, whereas other auditory synapses do not. The review focuses on short-term depression and short-term facilitation, i.e., plastic changes with durations in the millisecond range. Other types of short-term synaptic plasticity, e.g., posttetanic potentiation and depolarization-induced suppression of excitation, will be discussed much more briefly. The same holds true for subtypes of long-term plasticity, like prolonged depolarizations and spike-time-dependent plasticity. We also address forms of plasticity in the auditory brainstem that do not comprise synaptic plasticity in a strict sense, namely short-term suppression, paired tone facilitation, short-term adaptation, synaptic adaptation and neural adaptation. Finally, we perform a meta-analysis of 61 studies in which short-term depression (STD) in the auditory system is opposed to short-term depression at non-auditory synapses in order to compare high-frequency neurons with those that fire action potentials at a lower rate. This meta-analysis reveals considerably less STD in most auditory synapses than in non-auditory ones, enabling reliable, failure-free synaptic transmission even at frequencies >100 Hz. Surprisingly, the calyx of Held, arguably the best-investigated synapse in the central nervous system, depresses most robustly. It will be exciting to reveal the molecular mechanisms that set high-fidelity synapses apart from other synapses that function much less reliably.

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Abbreviations

AMPA:

α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid

ANF:

Auditory nerve fiber

AP:

Action potential

AVCN:

Anteroventral cochlear nucleus

BC:

Bushy cell

CB1R:

Cannabinoid receptors

CNC:

Cochlear nuclear complex

CTZ:

Cyclothiazide

DCN:

Dorsal cochlear nucleus

DGG:

γ-D-glutamylglycine

DNLL:

Dorsal nucleus of the lateral lemniscus

EGTA-AM:

Ethylene glycol tetraacetic acid-acetoxymethyl ester

EPSC:

Excitatory postsynaptic current

EPSP:

Excitatory postsynaptic potential

GABA:

γ-aminobutyric acid

GC:

Granule cells in the DCN

IC:

Inferior colliculus

IpCa :

Presynaptic calcium current

IPSC:

Inhibitory postsynaptic current

IPSP:

Inhibitory postsynaptic potential

ISI:

Inter-stimulus interval

KO:

Knockout

LSO:

Lateral superior olive

mGluRs:

Metabotropic glutamate receptors

MNTB:

Medial nucleus of the trapezoid body

MSO:

Medial superior olive

NA:

Nucleus angularis

NL:

Nucleus laminaris

NLL:

Nuclei of the lateral lemniscus

nMAG:

Nucleus magnocellularis

NMDA:

N-methyl-D-aspartate

P:

Postnatal day

PDs:

Prolonged depolarizations

PF:

Parallel fibers (from GCs)

PPD:

Paired-pulse depression

PPF:

Paired-pulse facilitation

PPR:

Paired-pulse ratio

Pr :

Release probability

PTH:

Posttetanic hyperpolarization

PTP:

Posttetanic potentiation

PVCN:

Posteroventral cochlear nucleus

RRP:

Readily releasable pool

SOC:

Superior olivary complex

STD:

Short-term depression

STDP:

Spike-time dependent plasticity

STP:

Short-term plasticity

STF:

Short-term facilitation

τdep :

Time constant for depression

τfast :

Time constant for fast recovery phase

τslow :

Time constant for slow recovery phase

TVC:

Tuberculo-ventral cell

VCN:

Ventral cochlear nucleus

WT:

Wild-type

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Acknowledgment

This work was supported by the Priority Program 1608 “Ultrafast and temporally precise information processing: normal and dysfunctional hearing” of the Deutsche Forschungsgemeinschaft (grant FR-1784/17-1).

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Correspondence to Eckhard Friauf.

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Friauf, E., Fischer, A.U. & Fuhr, M.F. Synaptic plasticity in the auditory system: a review. Cell Tissue Res 361, 177–213 (2015). https://doi.org/10.1007/s00441-015-2176-x

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Keywords

  • Short-term plasticity
  • Auditory brainstem
  • Calyx of Held
  • Endbulb of Held
  • Long-term plasticity