Evaluation of a model of the cochlear neural membrane. I. Physiological measurement of membrane characteristics in response to intrameatal electrical stimulation

Cartee, Lianne A.; Honert, Chris van den; Finley, Charles C.; Miller, Roger

doi:10.1016/s0378-5955(00)00109-x

Cited by 75 publications

(81 citation statements)

References 19 publications

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“…2) (Fig. 1) of our successful model (model II) and the brief estimates of the ARP and RRP agree very well with results of direct measurements after electrical stimulation of the AN (Brown, 1994;Dynes, 1996;Cartee et al, 2000;Miller et al, 2001;Shepherd et al, 2004;Morsnowski et al, 2006). Furthermore, our data and simulations suggest that the ARP and the time constant of the RRP might be similar for most fibers, despite anatomical variation (Liberman, 1982;Liberman and Oliver, 1984;Gleich and Wilson, 1993).…”

Section: The Refractory Functionsupporting

confidence: 84%

“…The estimates of the ARP and of the time constant of the RRP appear very plausible, in light of independent estimates available through other studies (Parkins, 1989;Brown, 1994;Dynes, 1996;Cartee et al, 2000;Miller et al, 2001;Shepherd et al, 2004;Morsnowski et al, 2006) and in addition were rather narrowly distributed. The estimates of the ARP, t D , had a median of 0.59 ms and an interquartile range of 0.40 -0.78 ms and a mean Ϯ SD of 0.65 Ϯ 0.62 ms.…”

Section: Estimates Of Parameters Returned By Model IIsupporting

confidence: 53%

“…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: 95%

“…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: The Refractory Functionsupporting

confidence: 84%

Section: Estimates Of Parameters Returned By Model IIsupporting

confidence: 53%

Section: Probing Model Ibmentioning

confidence: 92%

Section: Probing Model Iamentioning

confidence: 95%

Section: Introductionmentioning

confidence: 99%

See 3 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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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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Biophysics and Physiology

Abbas¹,

Miller²

2004

Cochlear Implants: Auditory Prostheses and Electric Hearing

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Evaluation of a model of the cochlear neural membrane. I. Physiological measurement of membrane characteristics in response to intrameatal electrical stimulation

Cited by 75 publications

References 19 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

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

Biophysics and Physiology

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