Physiology, pharmacology and plasticity at the inner hair cell synaptic complex

Ruel, Jérôme; Wang, Jing; Rebillard, Guy; Eybalin, Michel; Lloyd, Ruth; Pujol, Rémy; Puel, Jean–Luc

doi:10.1016/j.heares.2006.08.017

Cited by 179 publications

(136 citation statements)

References 65 publications

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“…It is also unlikely that the gamma component is caused by activity of lateral olivocochlear efferent neurons. Although their activity can suppress (but also increase) the firing rates of AN fibers (Guinan, 1996(Guinan, , 2006Ruel et al, 2001Ruel et al, , 2007Oestreicher et al, 2002;Puel et al, 2002;Le Prell et al, 2003), the detailed anatomy of this system (Warr, 1992) rules it out as a candidate.…”

Section: Discussionmentioning

confidence: 99%

Spontaneous Activity of Auditory-Nerve Fibers: Insights into Stochastic Processes at Ribbon Synapses

Heil¹,

Neubauer²,

Irvine³

et al. 2007

J. Neurosci.

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In several sensory systems, the conversion of the representation of stimuli from graded membrane potentials into stochastic spike trains is performed by ribbon synapses. In the mammalian auditory system, the spiking characteristics of the vast majority of primary afferent auditory-nerve (AN) fibers are determined primarily by a single ribbon synapse in a single inner hair cell (IHC), and thus provide a unique window into the operation of the synapse. Here, we examine the distributions of interspike intervals (ISIs) of cat AN fibers under conditions when the IHC membrane potential can be considered constant and the processes generating AN fiber activity can be considered stationary, namely in the absence of auditory stimulation. Such spontaneous activity is commonly thought to result from an excitatory Poisson point process modified by the refractory properties of the fiber, but here we show that this cannot be the case. Rather, the ISI distributions are one to two orders of magnitude better and very accurately described as a result of a homogeneous stochastic process of excitation (transmitter release events) in which the distribution of interevent times is a mixture of an exponential and a gamma distribution with shape factor 2, both with the same scale parameter. Whereas the scale parameter varies across fibers, the proportions of exponentially and gamma distributed intervals in the mixture, and the refractory properties, can be considered constant. This suggests that all of the ribbon synapses operate in a similar manner, possibly just at different rates. Our findings also constitute an essential step toward a better understanding of the spike-train representation of time-varying stimuli initiated at this synapse, and thus of the fundamentals of temporal coding in the auditory pathway.

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Section: Discussionmentioning

confidence: 99%

Spontaneous Activity of Auditory-Nerve Fibers: Insights into Stochastic Processes at Ribbon Synapses

Heil¹,

Neubauer²,

Irvine³

et al. 2007

J. Neurosci.

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“…The evidence for regeneration includes (1) the observation of growth cone-like structure(s) in electron micrographs of AMPA-treated ears, (2) the presence of normalappearing synapses in the recovered ear despite widespread severe swelling in the acute condition, and (implicitly) (3) the apparent recovery of thresholds for the cochlear compound action potential (Puel et al 1998;Ruel et al 2007).…”

Section: Degeneration Vs Regeneration After Excitotoxicitymentioning

confidence: 99%

“…These observations have suggested there is degeneration, followed by regeneration, of auditory nerve terminals in the adult guinea pig ear. However, until recently, virtually all of the morphological analysis of this afferent neuronal excitotoxicity in the inner ear has been at the ultrastructural level (Puel et al 1998;Pujol and Puel 1999;Ruel et al 2007), where quantification is extremely labor-intensive and thus essentially absent from the published record.…”

Section: Introductionmentioning

confidence: 99%

Primary Neural Degeneration in the Guinea Pig Cochlea After Reversible Noise-Induced Threshold Shift

Lin

Furman

Kujawa

et al. 2011

JARO

478

446

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Recent work in mouse showed that acoustic overexposure can produce a rapid and irreversible loss of cochlear nerve peripheral terminals on inner hair cells (IHCs) and a slow degeneration of spiral ganglion cells, despite full recovery of cochlear thresholds and no loss of inner or outer hair cells (Kujawa and Liberman, J Neurosci 29:14077-14085, 2009). This contrasts with earlier ultrastructural work in guinea pig suggesting that acute noise-induced neural degeneration is followed by full regeneration of cochlear nerve terminals in the IHC area (Puel et al., Neuroreport 9:2109-2114, 1998 Pujol and Puel, Ann N Y Acad Sci 884:249-254, 1999). Here, we show that the same patterns of primary neural degeneration reported for mouse are also seen in the noiseexposed guinea pig, when IHC synapses and cochlear nerve terminals are counted 1 week post-exposure in confocal images from immunostained whole mounts and that the same slow degeneration of spiral ganglion cells occurs despite no loss of IHCs and apparent recovery of cochlear thresholds. The data cast doubt on prior claims that there is significant neural regeneration and synaptogenesis in the adult cochlea and suggest that denervation of the inner hair cell is an important sequela of "reversible" noiseinduced hearing loss, which likely applies to the human ear as well.

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“…Thus, conventional synaptic transmission may take place at the OHC/type-II contact. There is ample pharmacological evidence that IHC/type-I synapses are glutamatergic and that type-I terminals express AMPAtype receptors (Ruel et al 2007). In vitro, neonatal typeIIs show a glutamate response that is enhanced by cyclothiazide (Jagger and Housley 2003), consistent with AMPA-type transmission; however, this response appears to be from somatic receptors and may represent a transient developmental stage.…”

Section: Type-ii Responses and Synaptic Transmission At Their Recipromentioning

confidence: 99%

Reciprocal Synapses Between Outer Hair Cells and their Afferent Terminals: Evidence for a Local Neural Network in the Mammalian Cochlea

Thiers

Nadol

Liberman

2008

JARO

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Cochlear outer hair cells (OHCs) serve both as sensory receptors and biological motors. Their sensory function is poorly understood because their afferent innervation, the type-II spiral ganglion cell, has small unmyelinated axons and constitutes only 5% of the cochlear nerve. Reciprocal synapses between OHCs and their type-II terminals, consisting of paired afferent and efferent specialization, have been described in the primate cochlea. Here, we use serial and semi-serial-section transmission electron microscopy to quantify the nature and number of synaptic interactions in the OHC area of adult cats. Reciprocal synapses were found in all OHC rows and all cochlear frequency regions. They were more common among third-row OHCs and in the apical half of the cochlea, where 86% of synapses were reciprocal. The relative frequency of reciprocal synapses was unchanged following surgical transection of the olivocochlear bundle in one cat, confirming that reciprocal synapses were not formed by efferent fibers. In the normal ear, axo-dendritic synapses between olivocochlear terminals and type-II terminals and/or dendrites were as common as synapses between olivocochlear terminals and OHCs, especially in the first row, where, on average, almost 30 such synapses were seen in the region under a single OHC. The results suggest that a complex local neuronal circuitry in the OHC area, formed by the dendrites of type-II neurons and modulated by the olivocochlear system, may be a fundamental property of the mammalian cochlea, rather than a curiosity of the primate ear. This network may mediate local feedback control of, and bidirectional communication among, OHCs throughout the cochlear spiral.

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Physiology, pharmacology and plasticity at the inner hair cell synaptic complex

Cited by 179 publications

References 65 publications

Spontaneous Activity of Auditory-Nerve Fibers: Insights into Stochastic Processes at Ribbon Synapses

Spontaneous Activity of Auditory-Nerve Fibers: Insights into Stochastic Processes at Ribbon Synapses

Primary Neural Degeneration in the Guinea Pig Cochlea After Reversible Noise-Induced Threshold Shift

Reciprocal Synapses Between Outer Hair Cells and their Afferent Terminals: Evidence for a Local Neural Network in the Mammalian Cochlea

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