Refractoriness Enhances Temporal Coding by Auditory Nerve Fibers

Avissar, Michael; Wittig, John H.; Saunders, James C.; Parsons, Thomas D.

doi:10.1523/jneurosci.3405-12.2013

Cited by 31 publications

(35 citation statements)

References 56 publications

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“…In healthy SGNs, refractoriness is actually a feature which enhances spike timing precision (Avissar et al 2013). Yet, even though SGNs have one of the fastest post-spike recoveries Miller et al 2001;Cartee et al 2006;Rattay et al 2013), when CIs are involved, refractoriness can be perceived as a limitation of the maximum firing rate in response to pulse rates of 2000 pulses/s or higher.…”

Section: Refractorinessmentioning

confidence: 99%

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: Refractorinessmentioning

confidence: 99%

Temporal Considerations for Stimulating Spiral Ganglion Neurons with Cochlear Implants

Boulet

White

Bruce

2015

JARO

103

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“…Phase locking can also be quantified by measures of entrainment, the extent to which spikes are generated in each and every stimulus period. Avissar et al () defined entrainment as the ratio of the number of stimulus cycles eliciting exactly 1 spike to the total number of cycles. Joris et al () defined entrainment as the ratio of the number of ISIs falling into a bin of duration T and centered on T to the total number of ISIs within their analysis window.…”

Section: Phase Lockingmentioning

confidence: 99%

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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“…To simulate refractory periods of AN fibers (Avissar et al, 2013), generated spikes that are closer to the preceding spike by T ref ϭ 1.5 ms were discarded. Because of the refractoriness, simulated spike rates of AN fibers were generally lower than the intensity .…”

Section: Computational Modelingmentioning

confidence: 99%

Tonotopic Optimization for Temporal Processing in the Cochlear Nucleus

Oline

Ashida

Burger

2016

Journal of Neuroscience

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In the auditory system, sounds are processed in parallel frequency-tuned circuits, beginning in the cochlea. Auditory nerve fibers reflect this tonotopy and encode temporal properties of acoustic stimuli by "locking" discharges to a particular stimulus phase. However, physiological constraints on phase-locking depend on stimulus frequency. Interestingly, low characteristic frequency (LCF) neurons in the cochlear nucleus improve phase-locking precision relative to their auditory nerve inputs. This is proposed to arise through synaptic integration, but the postsynaptic membrane's selectivity for varying levels of synaptic convergence is poorly understood. The chick cochlear nucleus, nucleus magnocellularis (NM), exhibits tonotopic distribution of both input and membrane properties. LCF neurons receive many small inputs and have low input thresholds, whereas high characteristic frequency (HCF) neurons receive few, large synapses and require larger currents to spike. NM therefore presents an opportunity to study how small membrane variations interact with a systematic topographic gradient of synaptic inputs. We investigated membrane input selectivity and observed that HCF neurons preferentially select faster input than their LCF counterparts, and that this preference is tolerant of changes to membrane voltage. We then used computational models to probe which properties are crucial to phase-locking. The model predicted that the optimal arrangement of synaptic and membrane properties for phase-locking is specific to stimulus frequency and that the tonotopic distribution of input number and membrane excitability in NM closely tracks a stimulus-defined optimum. These findings were then confirmed physiologically with dynamic-clamp simulations of inputs to NM neurons.

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Refractoriness Enhances Temporal Coding by Auditory Nerve Fibers

Cited by 31 publications

References 56 publications

Temporal Considerations for Stimulating Spiral Ganglion Neurons with Cochlear Implants

Temporal Considerations for Stimulating Spiral Ganglion Neurons with Cochlear Implants

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

Tonotopic Optimization for Temporal Processing in the Cochlear Nucleus

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