Tuning of synapse number, structure and function in the cochlea

Meyer, Alexander; Frank, Tom; Khimich, Darina; Hoch, Gerhard; Riedel, Dietmar; Chapochnikov, Nikolai M.; Yarin, Yury M.; Harke, Benjamin; Hell, Stefan W.; Egner, Alexander; Moser, Tobias

doi:10.1038/nn.2293

Cited by 303 publications

(356 citation statements)

References 50 publications

(91 reference statements)

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“…Since ANFs with different spontaneous rates likely innervate the same IHC (Liberman, 1982), the effective local [Ca 2ϩ ] in at individual active zones of a given IHC must differ. In line with this suggestion, Frank et al (2009) and Meyer et al (2009) reported a substantial variability in the magnitude of submicrometer, transient Ca 2ϩ hotspots at the base of individual IHCs. The authors interpret these hotspots as Ca 2ϩ microdomains associated with presynaptic active zones and argue that their variability, which was similar to that of the effective local [Ca 2ϩ ] in estimated here, is due to differences in the number or density of Ca V 1.3 channels near the different ribbon synapses of an individual IHC.…”

supporting

confidence: 63%

An Improved Model for the Rate–Level Functions of Auditory-Nerve Fibers

Heil

Neubauer

Irvine³

2011

J. Neurosci.

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Acoustic information is conveyed to the brain by the spike patterns in auditory-nerve fibers (ANFs). In mammals, each ANF is excited via a single ribbon synapse in a single inner hair cell (IHC), and the spike patterns therefore also provide valuable information about those intriguing synapses. Here we reexamine and model a key property of ANFs, the dependence of their spike rates on the sound pressure level of acoustic stimuli (rate-level functions). We build upon the seminal model of Sachs and Abbas (1974), which provides good fits to experimental data but has limited utility for defining physiological mechanisms. We present an improved, physiologically plausible model according to which the spike rate follows a Hill equation and spontaneous activity and its experimentally observed tight correlation with ANF sensitivity are emergent properties. We apply it to 156 cat ANF rate-level functions using frequencies where the mechanics are linear and find that a single Hill coefficient of 3 can account for the population of functions. We also demonstrate a tight correspondence between ANF rate-level functions and the Ca 2ϩ dependence of exocytosis from IHCs, and derive estimates of the effective intracellular Ca 2ϩ concentrations at the individual active zones of IHCs. We argue that the Hill coefficient might reflect the intrinsic, biochemical Ca 2ϩ cooperativity of the Ca 2ϩ sensor involved in exocytosis from the IHC. The model also links ANF properties with properties of psychophysical absolute thresholds.

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supporting

confidence: 63%

An Improved Model for the Rate–Level Functions of Auditory-Nerve Fibers

Heil

Neubauer

Irvine³

2011

J. Neurosci.

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“…In contrast, the auditory system is unique in its organizational simplicity. Acoustic information is transmitted into the brain by a single class of primary afferents that make one-to-one connections with inner hair cell sensory receptors (Spoendlin, 1973;Liberman, 1982;Meyer et al, 2009). This organization, which appears at face value to severely limit coding capacity, prompts the question of how the richness and precision of auditory information is sent to the CNS to process the frequency, intensity, timbre, and location of sound that is ultimately perceived (Bizley and Walker, 2010).…”

Section: Introductionmentioning

confidence: 99%

Unmasking of Spiral Ganglion Neuron Firing Dynamics by Membrane Potential and Neurotrophin-3

Crozier

Davis

2014

J. Neurosci.

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Type I spiral ganglion neurons have a unique role relative to other sensory afferents because, as a single population, they must convey the richness, complexity, and precision of auditory information as they shape signals transmitted to the brain. To understand better the sophistication of spiral ganglion response properties, we compared somatic whole-cell current-clamp recordings from basal and apical neurons obtained during the first 2 postnatal weeks from CBA/CaJ mice. We found that during this developmental time period neuron response properties changed from uniformly excitable to differentially plastic. Low-frequency, apical and high-frequency basal neurons at postnatal day 1 (P1)-P3 were predominantly slowly accommodating (SA), firing at low thresholds with little alteration in accommodation response mode induced by changes in resting membrane potential (RMP) or added neurotrophin-3 (NT-3). In contrast, P10 -P14 apical and basal neurons were predominately rapidly accommodating (RA), had higher firing thresholds, and responded to elevation of RMP and added NT-3 by transitioning to the SA category without affecting the instantaneous firing rate. Therefore, older neurons appeared to be uniformly less excitable under baseline conditions yet displayed a previously unrecognized capacity to change response modes dynamically within a remarkably stable accommodation framework. Because the soma is interposed in the signal conduction pathway, these specializations can potentially lead to shaping and filtering of the transmitted signal. These results suggest that spiral ganglion neurons possess electrophysiological mechanisms that enable them to adapt their response properties to the characteristics of incoming stimuli and thus have the capacity to encode a wide spectrum of auditory information.

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“…In the past decade, the analysis of excitotoxic synaptic damage has been greatly facilitated by quantitative light microscopy 120 . Counting immunolabeled IHC ribbon synapses in wholemounted mouse organs of Corti 116 , Kujawa and Liberman demonstrated a massive loss of ribbonoccupied IHC synapses in the highfrequency cochlea of rodents, even as a result of sound exposures that do not cause a permanent increase in hearing thresholds 116 (FIG.…”

mentioning

confidence: 99%