Measuring the Refractoriness of the Electrically Stimulated Auditory Nerve

Morsnowski, A.; Charasse, Basile; Collet, Lionel; Killian, Matthijs; Müller-Deile, J.

doi:10.1159/000095966

Cited by 58 publications

(60 citation statements)

References 25 publications

(23 reference statements)

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“…Hence, the refractory period has a random, exponential distribution with a mean duration of (t D ϩ 1/ R ). This refractory function has been implemented in many previous modeling studies (Schroeder and Hall, 1974;Lütkenhöner et al, 1980;Young and Barta, 1986;Li and Young, 1993;Prijs et al, 1993;Schoonhoven et al, 1997;Meddis and O'Mard, 2005;Meddis, 2006), and its shape is in excellent agreement with recent physiological data (Brown, 1994;Miller et al, 2001;Morsnowski et al, 2006); it is also illustrated in Figure 1. In this scenario, the ISIs should be distributed according to a general-gamma distribution (Young and Barta, 1986;Li and Young, 1993;Lehmann, 2002), the CDF of which is given by the following:…”

Section: Variant Asupporting

confidence: 80%

“…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: 92%

“…The estimates of the ARP appeared too short, and in most cases were even negative (mean t D across the 186 estimates, Ϫ0.041 ms; median, Ϫ0.001 ms). The estimates of the RRP (mean 1/ R , 2.77 ms; median, 2.45 ms), in contrast, appeared too long in light of the results of direct measurements after electrical stimulation of the AN, which indicate values in the range of 0.2-1.5 ms (Parkins, 1989;Brown, 1994;Dynes, 1996;Cartee et al, 2000;Miller et al, 2001;Shepherd et al, 2004;Morsnowski et al, 2006). Such long estimates of the RRP are also incompatible with the ability of AN fibers to follow high rates of electrical stimulation with 1 spike per pulse, up to at least 800/s (Javel and Shepherd, 2000), which requires the mean refractory period to be Յ1.25 ms.…”

Section: Probing Model Iamentioning

confidence: 94%

“…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). These data, therefore, question the common notion that the excitation of AN fibers is provided by a Poisson process.…”

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: Variant Asupporting

confidence: 80%

Section: Probing Model Ibmentioning

confidence: 92%

Section: Probing Model Iamentioning

confidence: 94%

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

“…RPS-IPG is similar to the RPS stimulus but with a long IPG of 6 ms. This long IPG was added to allow recordings of EABR responses to the last phase of the stimuli with little effect of the initial low phase (e.g., Cohen 2009;Miller et al 2001;Morsnowski et al 2006). Since the more prominent EABR peaks are normally within the first 5 ms after the onset of a stimulus, this IPG is long enough to prevent possible effects of responses elicited by the first phase, under the assumption that the short phase would be able to stimulate the AN.…”

Section: Eabr Stimulimentioning

confidence: 99%

The Polarity Sensitivity of the Electrically Stimulated Human Auditory Nerve Measured at the Level of the Brainstem

Undurraga

Carlyon

Wouters

et al. 2013

JARO

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Recent behavioral studies have suggested that the human auditory nerve of cochlear implant (CI) users is mainly excited by the positive (anodic) polarity. Those findings were only obtained using asymmetric pseudomonophasic (PS) pulses where the effect of one phase was measured in the presence of a counteracting phase of opposite polarity, longer duration, and lower amplitude than the former phase. It was assumed that only the short high-amplitude phase was responsible for the excitation. Similarly, it has been shown that electrically evoked compound action potentials could only be obtained in response to the anodic phases of asymmetric pulses. Here, experiment 1 measured electrically evoked auditory brainstem responses to standard symmetric, PS, reversed pseudomonophasic, and reversed pseudomonophasic with inter-phase gap (6 ms) pulses presented for both polarities. Responses were time locked to the short high-amplitude phase of asymmetric pulses and were smaller, but still measurable, when that phase was cathodic than when it was anodic. This provides the first evidence that cathodic stimulation can excite the auditory system of human CI listeners and confirms that this stimulation is nevertheless less effective than for the anodic polarity. A second experiment studied the polarity sensitivity at different intensities by means of a loudness balancing task between pseudomonophasic anodic (PSA) and pseudomonophasic cathodic (PSC) stimuli. Previous studies had demonstrated greater sensitivity to anodic stimulation only for stimuli producing loud percepts. The results showed that PSC stimuli required higher amplitudes than PSA stimuli to reach the same loudness and that this held for current levels ranging from 10 to 100 % of the dynamic range.

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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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Measuring the Refractoriness of the Electrically Stimulated Auditory Nerve

Cited by 58 publications

References 25 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

The Polarity Sensitivity of the Electrically Stimulated Human Auditory Nerve Measured at the Level of the Brainstem

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

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