Neural Masking by Sub-threshold Electric Stimuli: Animal and Computer Model Results

Miller, Charles A.; Woo, Jeong-Soo; Abbas, Paul J.; Hu, Ning; Robinson, Barbara K.

doi:10.1007/s10162-010-0249-9

Cited by 28 publications

(83 citation statements)

References 40 publications

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“…More specifically, spike rate adaptation is a neuron's tendency to lower its excitability in response to ongoing action potentials. This is generally observed across timescales on the order of 10 to 100 ms (Zhang et al 2007;Heffer et al 2010;Miller et al 2011) or even minutes (Litvak et al 2003) but typically greater than those for refractoriness, facilitation, and accommodation. For example, one trial of a neuron's response to high-rate stimulation in Figure 2D shows that initially, the neuron fires multiple consecutive action potentials, then later in the pulse train, the occurrence of spikes diminishes.…”

Section: Spike Rate Adaptation and Interacting Phenomenamentioning

confidence: 98%

“…In a follow-up study, Miller et al (2011) investigated both the buildup of and the recovery from adaptation. The stimulation paradigm involved applying a "masker" pulse train to induce adaptation and immediately after the cessation of the masker to switch to a low-rate "probe" pulse train, in order to observe the recovery from adaptation.…”

Section: Spike Rate Adaptation and Interacting Phenomenamentioning

confidence: 99%

“…In their model, the principle ionic currents were formed by the fast sodium and delayed rectifier potassium voltage-gated ion channels. To this day, these channels are central to explaining the biophysical underpinnings of neural excitation in the SGN and thus are used in many computational models (Phan et al 1994;Rubinstein 1995;Matsuoka et al 2001;Mino et al 2004;Imennov and Rubinstein 2009;Chow and White 1996;Negm and Bruce 2014;Negm and Bruce 2008;Woo et al 2009b;Woo et al 2009a;Woo et al 2009c;Miller et al 2011;Smit et al 2008;Cartee 2000Cartee , 2006Rattay 2000;Rattay et al 2001;Rattay et al 2013;Rattay and Danner 2014). However, the ion channels of the Hodgkin-Huxley model alone cannot explain long relative refractoriness, long-term accommodation, and spike rate adaptation.…”

Section: Mechanisms and Modelsmentioning

confidence: 99%

“…A rather salient example of this issue is depicted in Fig. 6 of Miller et al (2011). It shows that even after varying the densities of two unique potassium ion channel types, the model cannot successfully predict one ratio of densities that can simultaneously and accurately quantify refractoriness and spike rate adaptation in electrically stimulated SGNs.…”

Section: Refractorinessmentioning

confidence: 99%

“…An effort to explicitly model spike rate adaptation for CI stimulation was developed in a series of papers by Miller et al (2011) and Woo et al (2009aWoo et al ( , 2009bWoo et al ( , 2009c. The idea was that during the repolarization of an action potential, K + ion efflux contributed to incrementally increasing the extracellular K + ion concentration.…”

Section: Spike Rate Adaptationmentioning

confidence: 99%

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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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Section: Spike Rate Adaptation and Interacting Phenomenamentioning

confidence: 98%

Section: Spike Rate Adaptation and Interacting Phenomenamentioning

confidence: 99%

Section: Mechanisms and Modelsmentioning

confidence: 99%

Section: Refractorinessmentioning

confidence: 99%

Section: Spike Rate Adaptationmentioning

confidence: 99%

See 3 more Smart Citations

Temporal Considerations for Stimulating Spiral Ganglion Neurons with Cochlear Implants

Boulet

White

Bruce

2015

JARO

103

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Predictions of the Contribution of HCN Half-Maximal Activation Potential Heterogeneity to Variability in Intrinsic Adaptation of Spiral Ganglion Neurons

Boulet

Bruce

2016

JARO

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Spiral ganglion neurons (SGNs) exhibit a wide range in their strength of intrinsic adaptation on a timescale of 10s to 100s of milliseconds in response to electrical stimulation from a cochlear implant (CI). The purpose of this study was to determine how much of that variability could be caused by the heterogeneity in half-maximal activation potentials of hyperpolarization-activated cyclic nucleotide-gated cation (HCN) channels, which are known to produce intrinsic adaptation. In this study, a computational membrane model of cat type I SGN was developed based on the Hodgkin-Huxley model plus HCN and low-threshold potassium (KLT) conductances in which the half-maximal activation potential of the HCN channel was varied and the response of the SGN to pulse train and paired-pulse stimulation was simulated. Physiologically plausible variation of HCN half-maximal activation potentials could indeed determine the range of adaptation on the timescale of 10s to 100s of milliseconds and recovery from adaptation seen in the physiological data while maintaining refractoriness within physiological bounds. This computational model demonstrates that HCN channels may play an important role in regulating the degree of adaptation in response to pulse train stimulation and therefore contribute to variable constraints on acoustic information coding by CIs. This finding has broad implications for CI stimulation paradigms in that cell-to-cell variation of HCN channel properties are likely to significantly alter SGN excitability and therefore auditory perception.

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Forward Masking in Cochlear Implant Users: Electrophysiological and Psychophysical Data Using Pulse Train Maskers

Adel

Hilkhuysen

Noreña

et al. 2017

JARO

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Electrical stimulation of auditory nerve fibers using cochlear implants (CI) shows psychophysical forward masking (pFM) up to several hundreds of milliseconds. By contrast, recovery of electrically evoked compound action potentials (eCAPs) from forward masking (eFM) was shown to be more rapid, with time constants no greater than a few milliseconds. These discrepancies suggested two main contributors to pFM: a rapid-recovery process due to refractory properties of the auditory nerve and a slow-recovery process arising from more central structures. In the present study, we investigate whether the use of different maskers between eCAP and psychophysical measures, specifically single-pulse versus pulse train maskers, may have been a source of confound.In experiment 1, we measured eFM using the following: a single-pulse masker, a 300-ms low-rate pulse train masker (LTM, 250 pps), and a 300-ms high-rate pulse train masker (HTM, 5000 pps). The maskers were presented either at same physical current (Φ) or at same perceptual (Ψ) level corresponding to comfortable loudness. Responses to a single-pulse probe were measured for masker-probe intervals ranging from 1 to 512 ms. Recovery from masking was much slower for pulse trains than for the single-pulse masker. When presented at Φ level, HTM produced more and longer-lasting masking than LTM. However, results were inconsistent when LTM and HTM were compared at Ψ level. In experiment 2, masked detection thresholds of single-pulse probes were measured using the same pulse train masker conditions. In line with our eFM findings, masked thresholds for HTM were higher than those for LTM at Φ level. However, the opposite result was found when the pulse trains were presented at Ψ level.Our results confirm the presence of slow-recovery phenomena at the level of the auditory nerve in CI users, as previously shown in animal studies. Inconsistencies between eFM and pFM results, despite using the same masking conditions, further underline the importance of comparing electrophysiological and psychophysical measures with identical stimulation paradigms.

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Neural Masking by Sub-threshold Electric Stimuli: Animal and Computer Model Results

Cited by 28 publications

References 40 publications

Temporal Considerations for Stimulating Spiral Ganglion Neurons with Cochlear Implants

Temporal Considerations for Stimulating Spiral Ganglion Neurons with Cochlear Implants

Predictions of the Contribution of HCN Half-Maximal Activation Potential Heterogeneity to Variability in Intrinsic Adaptation of Spiral Ganglion Neurons

Forward Masking in Cochlear Implant Users: Electrophysiological and Psychophysical Data Using Pulse Train Maskers

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