Response of cochlear nerve fibers to brief acoustic stimuli: Role of discharge-history effects

Gaumond, R.P.; Kim, Duck O.; Molnar, Charles E.

doi:10.1121/1.390164

Cited by 50 publications

(35 citation statements)

References 11 publications

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“…fibers (Kiang et al, 1965;Gaumond et al, 1983;Young and Barta, 1986;Carney, 1993;Li and Young, 1993;Miller and Wang, 1993;Zhang et al, 2001) and modeled, for example, by a second, very long, time constant for the recovery process during the RRP (Carney, 1993;Miller and Wang, 1993;Zhang et al, 2001). Such refractory properties, however, are not supported by the direct measurements (Brown, 1994;Dynes, 1996;Cartee et al, 2000;Miller et al, 2001;Shepherd et al, 2004;Morsnowski et al, 2006).…”

Section: Probing Model Ibmentioning

confidence: 87%

“…2d, 3d). The latter phenomenon has been reported widely in the literature (Gray, 1967;Gaumond et al, 1982Gaumond et al, , 1983Young and Barta, 1986;Li and Young, 1993;Prijs et al, 1993;Johnson, 1996), and the failure of the model to capture this phenomenon has already been pointed out by Young and Barta (1986) and Li and Young (1993).…”

Section: Probing Model Iamentioning

confidence: 92%

“…The mean ISI is given by the following: (Gray, 1967;Gaumond et al, 1982Gaumond et al, , 1983Li and Young, 1993) [Prijs et al (1993), their Fig. 7] originates from the fraction of gamma-distributed IEIs of the stochastic process providing the excitation (Fig.…”

Section: Probing Model Ibmentioning

confidence: 99%

“…The observed deviations from strictly exponential ISI distributions are therefore commonly attributed to the refractoriness of AN fibers. By the same rationale, the slow recovery (over tens of milliseconds) of the discharge probability with time since the last spike (Gray, 1967;Gaumond et al, 1982Gaumond et al, , 1983Li and Young, 1993;Johnson, 1996) has also been attributed to the refractory properties (Kiang et al, 1965;Gaumond et al, 1983;Young and Barta, 1986;Carney, 1993;Li and Young, 1993;Miller and Wang, 1993;Zhang et al, 2001). However, direct studies of the refractory properties of AN fibers by means of electrical stimulation have shown that refractory periods are very short, Ͻ1 or 2 ms (Brown, 1994;Dynes, 1996;Cartee et al, 2000;Miller et al, 2001;Shepherd et al, 2004;Morsnowski et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

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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: Probing Model Ibmentioning

confidence: 87%

Section: Probing Model Iamentioning

confidence: 92%

Section: Probing Model Ibmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

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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show abstract

“…In models of ANF spike patterns, the excitatory (release) events are commonly thought to be produced by a Poisson point process that is homogeneous during spontaneous activity (Kiang et al, 1965;Gaumond et al, 1983;Young and Barta, 1986;Carney, 1993;Li and Young, 1993;Miller and Wang, 1993;Johnson, 1996;Zhang et al, 2001). A fractal doubly stochastic point process has also been proposed to account for rate trends over longer timescales (Ͼ100 ms; Lowen andTeich, 1991, 1992;Delgutte, 1996;Jackson and Carney, 2005).…”

Section: Introductionmentioning

confidence: 99%

A Model of Synaptic Vesicle-Pool Depletion and Replenishment Can Account for the Interspike Interval Distributions and Nonrenewal Properties of Spontaneous Spike Trains of Auditory-Nerve Fibers

2014

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In mammalian auditory systems, the spiking characteristics of each primary afferent (type I auditory-nerve fiber; ANF) are mainly determined by a single ribbon synapse in a single receptor cell (inner hair cell; IHC). ANF spike trains therefore provide a window into the operation of these synapses and cells. It was demonstrated previously (Heil et al., 2007) that the distribution of interspike intervals (ISIs) of cat ANFs during spontaneous activity can be modeled as resulting from refractoriness operating on a non-Poisson stochastic point process of excitation (transmitter release events from the IHC). Here, we investigate nonrenewal properties of these cat-ANF spontaneous spike trains, manifest as negative serial ISI correlations and reduced spike-count variability over short timescales. A previously discussed excitatory process, the constrained failure of events from a homogeneous Poisson point process, can account for these properties, but does not offer a parsimonious explanation for certain trends in the data. We then investigate a three-parameter model of vesicle-pool depletion and replenishment and find that it accounts for all experimental observations, including the ISI distributions, with only the release probability varying between spike trains. The maximum number of units (single vesicles or groups of simultaneously released vesicles) in the readily releasable pool and their replenishment time constant can be assumed to be constant (ϳ4 and 13.5 ms, respectively). We suggest that the organization of the IHC ribbon synapses not only enables sustained release of neurotransmitter but also imposes temporal regularity on the release process, particularly when operating at high rates.

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Spike timing in auditory‐nerve fibers during spontaneous activity and phase locking

Heil

Peterson

2016

Synapse

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In vertebrates, all acoustic information transmitted from the inner ear to the central auditory system is relayed by primary auditory afferents (auditory-nerve fibers; ANFs). These neurons are also the most peripheral elements to use action potentials (spikes) to encode the acoustic information. Here, we review what is known about the spiking of ANFs during spontaneous activity, when spike timing might be regarded as largely random, and during stimulation by low-frequency sounds, when spikes are phase locked to the stimulus waveform, a phenomenon generally considered a hallmark of temporal precision and speed in the auditory system. We focus on mammals, in which each ANF is driven by a single ribbon synapse in a single receptor cell, but also cover relevant research on ANFs of vertebrates from other classes. For spontaneous activity, we highlight several spike-history effects in interspike interval distributions, hazard-rate functions, serial interval correlations, and spike-count statistics. We also review models that have attempted to account for these properties. For phase locking, we focus on the responses to low-frequency tones, rather than to low-frequency components of broadband signals such as noise or clicks. We critically review the measures commonly used to quantify phase locking and urge caution when interpreting such measures with respect to spike-timing precision. We also review the dependence of phase locking on stimulus amplitude and frequency. Finally, we identify some open questions.

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Response of cochlear nerve fibers to brief acoustic stimuli: Role of discharge-history effects

Cited by 50 publications

References 11 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

A Model of Synaptic Vesicle-Pool Depletion and Replenishment Can Account for the Interspike Interval Distributions and Nonrenewal Properties of Spontaneous Spike Trains of Auditory-Nerve Fibers

Spike timing in auditory‐nerve fibers during spontaneous activity and phase locking

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