Auditory Hair Cell-Afferent Fiber Synapses Are Specialized to Operate at Their Best Frequencies

Schnee, Michael; Lawton, D.M.; Furness, David N.; Benke, Tim A.; Ricci, Anthony J.

doi:10.1016/j.neuron.2005.06.004

Cited by 119 publications

(172 citation statements)

References 51 publications

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“…However, even after removing desensitization in CTZ, the AF response still depressed. Steady-state release was 11.0 Ϯ 2.4% (n ϭ 9) of the initial peak, not significantly different from control, thus confirming that synaptic depression is likely caused by presynaptic mechanisms such as vesicle depletion, as inferred previously from capacitance recordings (9)(10)(11)(12)(13)(14).…”

Section: Resultssupporting

confidence: 82%

“…3C) and 1.4 for the integral of the AF response (data not shown). A similar linear relation has been shown before at the hair cell synapse (11,(14)(15)(16) and explained by a ''nanodomain model,'' where opening of one Ca 2ϩ channel activates release of only very nearby vesicles (15,17). Thus, as open probability rises with depolarization, each Ca 2ϩ channel's ''cluster'' of vesicles sums to produce a linear dependence on Ca 2ϩ current.…”

Section: Resultssupporting

confidence: 75%

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Time course and calcium dependence of transmitter release at a single ribbon synapse

Goutman

Glowatzki

2007

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

222

322

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At the first synapse in the auditory pathway, the receptor potential of mechanosensory hair cells is converted into a firing pattern in auditory nerve fibers. For the accurate coding of timing and intensity of sound signals, transmitter release at this synapse must occur with the highest precision. To measure directly the transfer characteristics of the hair cell afferent synapse, we implemented simultaneous whole-cell recordings from mammalian inner hair cells (IHCs) and auditory nerve fiber terminals that typically receive input from a single ribbon synapse. During a 1-s IHC depolarization, the synaptic response depressed >90%, representing the main source for adaptation in the auditory nerve. Synaptic depression was slightly affected by ␣-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor desensitization; however, it was mostly caused by reduced vesicular release. When the transfer function between transmitter release and Ca 2؉ influx was tested at constant open probability for Ca 2؉ channels (potentials >0 mV), a super linear relation was found. This relation is presumed to result from the cooperative binding of three to four Ca 2؉ ions at the Ca 2؉ sensor. However, in the physiological range for receptor potentials (؊50 to ؊30 mV), the relation between Ca 2؉ influx and afferent activity was linear, assuring minimal distortion in the coding of sound intensity. Changes in Ca 2؉ influx caused an increase in release probability, but not in the average size of multivesicular synaptic events. By varying Ca 2؉ buffering in the IHC, we further investigate how Ca 2؉ channel and Ca 2؉ sensor at this synapse might relate.hearing ͉ exocytosis ͉ hair cell ͉ synaptic transmission ͉ auditory nerve fiber M echanosensory hair cells of the inner ear release neurotransmitter continuously and with high temporal precision onto dendrites of auditory nerve fibers (AFs) (1); therefore, availability of releasable synaptic vesicles is critical. Synaptic ribbons, presynaptic structures presenting a halo of tethered vesicles, also found in retinal photoreceptors and bipolar cells (2), are thought to facilitate accumulation of vesicles presynaptically (3). Postsynaptically, ␣-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors mediate fast synaptic transmission (4). The response of the cochlea to sound has been investigated in great detail: prolonged sound stimulation produces an increase in the firing activity of the auditory nerve that adapts on a milliseconds time scale (5). However, direct demonstration of the synaptic processes underlying adaptation and sustained release is still missing. Heretofore, hair cell exocytosis has been measured by changes in membrane capacitance that sum activity from all of the dozens of ribbon synapses in each cell (3). Capacitance measurements therefore cannot distinguish properties of individual ribbons and are limited in temporal resolution, requiring extrapolation for the earliest components. Nor does this approach reveal what role postsynaptic desensitization might play.I...

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Section: Resultssupporting

confidence: 82%

Section: Resultssupporting

confidence: 75%

Time course and calcium dependence of transmitter release at a single ribbon synapse

Goutman

Glowatzki

2007

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

222

322

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“…Numerous physiological investigations have sought to understand the function of the SB (7-9, 11, 12, 16-22). The predominant hypothesis is that the SB facilitates high rates of sustained transmission by capturing and͞or transporting SVs to release sites, although other functions have been proposed (23), including frequency selectivity (24).…”

Section: Discussionmentioning

confidence: 99%

“…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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“…The IHC-AN synapse complex is believed to be mainly responsible for this adaptation. Although the mechanism that gives rise to synaptic adaptation is not completely understood, it could be caused either by the depletion of neurotransmitter from a readily releasable presynaptic pool of neurotransmitter ͑Moser and Beutner, 2000; Schnee et al, 2005;Goutman and Glowatzki, 2007͒ or by the desensitization of post-synaptic receptors ͑Raman et al, 1994͒. Modeling the adaptation in the IHC-AN synapse has been a focus of extensive research over the last several decades. Early attempts employed a single-reservoir system with loss and replenishment of transmitter quanta ͑Schroeder and Hall, 1974;Sujaku, 1974, 1975͒, and later models added extra reservoirs ͑or sites͒ or more complex principles of transmitter flow control ͑Furukawa and Matsuura, 1978;Furukawa et al, 1982;Ross, 1982Ross, , 1996Schwid and Geisler, 1982;Smith and Brachman, 1982;Cooke, 1986;Meddis, 1986Meddis, , 1988Westerman and Smith, 1988͒.…”

Section: Introductionmentioning

confidence: 99%

A phenomenological model of the synapse between the inner hair cell and auditory nerve: Long-term adaptation with power-law dynamics

Zilany

Bruce²,

Nelson³

et al. 2009

The Journal of the Acoustical Society of America

318

346

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There is growing evidence that the dynamics of biological systems that appear to be exponential over short time courses are in some cases better described over the long-term by power-law dynamics. A model of rate adaptation at the synapse between inner hair cells and auditory-nerve ͑AN͒ fibers that includes both exponential and power-law dynamics is presented here. Exponentially adapting components with rapid and short-term time constants, which are mainly responsible for shaping onset responses, are followed by two parallel paths with power-law adaptation that provide slowly and rapidly adapting responses. The slowly adapting power-law component significantly improves predictions of the recovery of the AN response after stimulus offset. The faster power-law adaptation is necessary to account for the "additivity" of rate in response to stimuli with amplitude increments. The proposed model is capable of accurately predicting several sets of AN data, including amplitude-modulation transfer functions, long-term adaptation, forward masking, and adaptation to increments and decrements in the amplitude of an ongoing stimulus.

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Auditory Hair Cell-Afferent Fiber Synapses Are Specialized to Operate at Their Best Frequencies

Cited by 119 publications

References 51 publications

Time course and calcium dependence of transmitter release at a single ribbon synapse

Time course and calcium dependence of transmitter release at a single ribbon synapse

Frequency selectivity of synaptic exocytosis in frog saccular hair cells

A phenomenological model of the synapse between the inner hair cell and auditory nerve: Long-term adaptation with power-law dynamics

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