Transmitter release at the hair cell ribbon synapse

Glowatzki, Elisabeth; Fuchs, Paul

doi:10.1038/nn796

Cited by 524 publications

(700 citation statements)

References 40 publications

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“…In contrast, the RRP estimate from ⌬C m measurements in mouse inner hair cells is Ϸ53-64 SVs per synapse, whereas the morphologically docked SV pool contains only [16][17][18][19][20][21][22][23][24][25][26][27][28][29][30]. Some of this difference may be due to the fact that synaptic exocytosis had not been inhibited before fixation, which in frog saccular hair cells reduced the number of docked SVs per synapse from 43 to 32 (11).…”

Section: Discussionmentioning

confidence: 99%

Frequency selectivity of synaptic exocytosis in frog saccular hair cells

Rutherford

Roberts

2006

Proc. Natl. Acad. Sci. U.S.A.

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The ability to respond selectively to particular frequency components of sensory inputs is fundamental to signal processing in the ear. The frog (Rana pipiens) sacculus, which is used for social communication and escape behaviors, is an exquisitely sensitive detector of sounds and ground-borne vibrations in the 5-to 200-Hz range, with most afferent axons having best frequencies between 40 and 60 Hz. We monitored the synaptic output of saccular sensory receptors (hair cells) by measuring the increase in membrane capacitance (⌬Cm) that occurs when synaptic vesicles fuse with the plasmalemma. Strong stepwise depolarization evoked an exocytic burst that lasted 10 ms and corresponded to the predicted capacitance of all docked vesicles at synapses, followed by a 20-ms delay before additional vesicle fusion. Experiments using weak stimuli, within the normal physiological range for these cells, revealed a sensitivity to the temporal pattern of membrane potential changes. Interrupting a weak depolarization with a properly timed hyperpolarization increased ⌬Cm. Small sinusoidal voltage oscillations (؎5 mV centered at ؊60 mV) evoked a ⌬Cm that corresponded to 95 vesicles per s at each synapse at 50 Hz but only 26 vesicles per s at 5 Hz and 27 vesicles per s at 200 Hz (perforated patch recordings). This frequency selectivity was absent for larger sinusoidal oscillations (؎10 mV centered at ؊55 mV) and was largest for hair cells with the smallest sinusoidal-stimulievoked Ca 2؉ currents. We conclude that frog saccular hair cells possess an intrinsic synaptic frequency selectivity that is saturated by strong stimuli.afferent ͉ synaptic vesicle pool ͉ ribbon synapse ͉ capacitance ͉ tuning T he auditory and vestibular systems in the ear and the related mechanosensory and electrosensory organs of the lateral line employ a remarkable variety of mechanical and neural mechanisms to distinguish frequency components of sensory signals from Ͻ10 Hz to nearly 100 kHz (1, 2). In each of these organs, a sensory stimulus passes through one or more stages of mechanical or electrical filtering (3), leading to graded changes in the sensory receptor cell's membrane potential, V m . Oscillatory sensory stimuli usually produce oscillations in V m , with the greatest amplitude occurring at a preferred frequency. Hair cells in the frog sacculus possess a broadly tuned electrical filter that causes V m to oscillate preferentially at frequencies between 35 and 75 Hz (4), as well as spontaneous oscillations of the mechanosensory apparatus at frequencies between 5 and 50 Hz (5).At the hair cells' output synapses, the information contained in V m is transmitted by a chemical neurotransmitter (glutamate) to postsynaptic terminals and encoded as a train of action potentials that travel to the brain. Each of these afferent synapses contains a presynaptic dense body [also known as the synaptic body (SB) or synaptic ribbon] (Fig. 1a) similar to ribbon synapses in the retina. As at other chemical synapses, V m controls calcium influx through voltage-gated cal...

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Section: Discussionmentioning

confidence: 99%

Frequency selectivity of synaptic exocytosis in frog saccular hair cells

Rutherford

Roberts

2006

Proc. Natl. Acad. Sci. U.S.A.

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“…2D). Compound vesicles have been observed in non-neuronal secretory cells (e.g., Alvarez de Toledo and Fernandez, 1990) and could potentially underlie the multivesicular release reported in bipolar cells (Singer et al, 2004) and cochlear hair cells (Glowatzki and Fuchs, 2002;Edmonds et al, 2004). On the other hand, it is difficult to reconcile the fusion of compound vesicles with the rise in membrane capacitance evoked by the rapid, global elevation of calcium, which is best described by a smooth, single exponential function indicative of the fusion of a small, homogeneous class of vesicle (Heidelberger et al, 1994).…”

Section: Fusion Scenarios and Ribbon Functionmentioning

confidence: 99%

Synaptic transmission at retinal ribbon synapses

Heidelberger

Thoreson

Witkovsky

2005

Progress in Retinal and Eye Research

208

231

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The molecular organization of ribbon synapses in photoreceptors and ON bipolar cells is reviewed in relation to the process of neurotransmitter release. The interactions between ribbon synapseassociated proteins, synaptic vesicle fusion machinery and the voltage-gated calcium channels that gate transmitter release at ribbon synapses are discussed in relation to the process of synaptic vesicle exocytosis. We describe structural and mechanistic specializations that permit the ON bipolar cell to release transmitter at a much higher rate than the photoreceptor does, under in vivo conditions. We also consider the modulation of exocytosis at photoreceptor synapses, with an emphasis on the regulation of calcium channels.

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“…In the healthy acoustically driven ear, spikes are initiated at the peripheral terminal aided by a dense population of Nav1.6 channels (Hossain et al 2005). The spike timing of the SGN inherits variability from the synaptic transmission process between an IHC that is characterized by probabilistic release of vesicles (Glowatzki and Fuchs 2002;Heil et al 2007;Safieddine et al 2012). However, the spike timing of the SGN is known to have intrinsic variability due to the inherent stochasticity of voltage-gated ion channel fluctuations (Verveen and Derksen 1968;Sigworth 1981).…”

Section: Spatial Effects Of CI Stimulation Related To Temporal Interamentioning

confidence: 99%

“…As such, these neurons act as crucial contributors to the auditory system since they serve as the first layer of auditory neurons encoding afferent spiking information. Inner hair cells release synaptic vesicle packets in a probabilistic nature (Glowatzki and Fuchs 2002;Heil et al 2007;Safieddine et al 2012) which could be responsible for the high variability of SGN firing rates in acoustic stimulation. In contrast, when electrically stimulated with a cochlear implant, SGNs are directly excited by voltage-gated ion channel activity.…”

Section: Introductionmentioning

confidence: 99%

Temporal Considerations for Stimulating Spiral Ganglion Neurons with Cochlear Implants

Boulet

White

Bruce

2015

JARO

103

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A wealth of knowledge about different types of neural responses to electrical stimulation has been developed over the past 100 years. However, the exact forms of neural response properties can vary across different types of neurons. In this review, we survey four stimulus-response phenomena that in recent years are thought to be relevant for cochlear implant stimulation of spiral ganglion neurons (SGNs): refractoriness, facilitation, accommodation, and spike rate adaptation. Of these four, refractoriness is the most widely known, and many perceptual and physiological studies interpret their data in terms of refractoriness without incorporating facilitation, accommodation, or spike rate adaptation. In reality, several or all of these behaviors are likely involved in shaping neural responses, particularly at higher stimulation rates. A better understanding of the individual and combined effects of these phenomena could assist in developing improved cochlear implant stimulation strategies. We review the published physiological data for electrical stimulation of SGNs that explores these four different phenomena, as well as some of the recent studies that might reveal the biophysical bases of these stimulus-response phenomena.

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Transmitter release at the hair cell ribbon synapse

Cited by 524 publications

References 40 publications

Frequency selectivity of synaptic exocytosis in frog saccular hair cells

Frequency selectivity of synaptic exocytosis in frog saccular hair cells

Synaptic transmission at retinal ribbon synapses

Temporal Considerations for Stimulating Spiral Ganglion Neurons with Cochlear Implants

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