Responses to sound of the basilar membrane of the mammalian cochlea

doi:10.1016/0959-4388(92)90179-O

Current Opinion in Neurobiology

Volume 2, Issue 4, August 1992, Pages 449-456

https://doi.org/10.1016/0959-4388(92)90179-O Get rights and content

Abstract

Recent evidence shows that the frequency-specific non-linear properties of auditory nerve and inner hair cell responses to sound, including their sharp frequency tuning, are fully established in the vibration of the basilar membrane. In turn, the sensitivity, frequency selectivity and non-linear properties of basilar membrane responses probably result from an influence of the outer hair cells.

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Citation Excerpt :
The first mechanism is via activation of the cochlear outer hair cells, which in turn move the inner hair cells to produce an auditory percept. The outer hair cells are highly nonlinear mechanical amplifiers that provide as much as 1000-fold gain for low-level sounds but no gain for high-level sounds (Ruggero, 1992). The outer hair cells can respond to electric stimulation (Le Prell et al., 2006; Ren et al., 1995) and their nonlinearity is likely responsible for the pitch distortion, especially by the ear canal stimulation in the present study.
While noninvasive brain stimulation is convenient and cost effective, its utility is limited by the substantial distance between scalp electrodes and their intended neural targets in the head. The tympanic membrane, or eardrum, is a thin flap of skin deep in an orifice of the head that may serve as a port for improved efficiency of noninvasive stimulation. Here we chose the cochlea as a target because it resides in the densest bone of the skull and is adjacent to many deep-brain-stimulation structures. We also tested the hypothesis that noninvasive electric stimulation of the cochlea may restore neural activities that are missing in acoustic stimulation. We placed an electrode in the ear canal or on the tympanic membrane in 25 human adults (10 females) and compared their stimulation efficiency by characterizing the electrically-evoked auditory sensation. Relative to ear canal stimulation, tympanic membrane stimulation was four times more likely to produce an auditory percept, required eight times lower electric current to reach the threshold and produced two-to-four times more linear suprathreshold responses. We further measured tinnitus suppression in 14 of the 25 subjects who had chronic tinnitus. Compared with ear canal stimulation, tympanic membrane stimulation doubled both the probability (22% vs. 55%) and the amount (−15% vs. −34%) of tinnitus suppression. These findings extended previous work comparing evoked perception and tinnitus suppression between electrodes placed in the ear canal and on the scalp. Together, the previous and present results suggest that the efficiency of conventional scalp-based noninvasive electric stimulation can be improved by at least one order of magnitude via tympanic membrane stimulation. This increased efficiency is most likely due to the shortened distance between the electrode placed on the tympanic membrane and the targeted cochlea. The present findings have implications for the management of tinnitus by offering a potential alternative to interventions using invasive electrical stimulation such as cochlear implantation, or other non-invasive transcranial electrical stimulation methods.
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The auditory system relies on local and global representations to discriminate sounds. This study investigated whether vision influences the development and functioning of these fundamental sound computations. We employed a computational approach to control statistical properties embedded in sounds and tested samples of sighted controls (SC) and congenitally (CB) and late-onset (LB) blind individuals in two experiments. In experiment 1, performance relied on local features analysis; in experiment 2, performance benefited from computing global representations. In both experiments, SC and CB performance remarkably overlapped. Conversely, LB performed systematically worse than the other groups when relying on local features, with no alterations on global representations. Results suggest that auditory computations tested here develop independently from vision. The efficiency of local auditory processing can be hampered in case sight becomes unavailable later in life, supporting the existence of an audiovisual interplay for the processing of auditory details, which emerges only in late development.
A simplified physiological model of rate-level functions of auditory-nerve fibers
2021, Hearing Research
Citation Excerpt :
Where needed, the values were derived by linear interpolation of the log(b(A)/bref) versus stimulus level functions. These data show that the nonlinearities are most pronounced at CF, reminiscent of the nonlinearities in the vibrations of the basilar membrane and other cochlear structures (e.g., Ruggero, 1992; Robles and Ruggero, 2001; Olson and Strimbu, 2020). These data also show that the nonlinearities can be present at rather low stimulus levels (e.g., 30 dB SPL), consistent with basilar membrane nonlinearities measured in cat by Cooper and Rhode (1992) but lower than the basilar membrane compression thresholds assumed or estimated in previous studies of cat ANF rate-level functions (Sachs and Abbas, 1974; Sachs et al., 1989).
Several approaches have been used to describe the rate-level functions of auditory-nerve fibers (ANFs). One approach uses descriptive models that can be fitted easily to data. Another derives rate-level functions from comprehensive physiological models of auditory peripheral processing. Here, we seek to identify the minimal set of components needed to provide a physiologically plausible account of rate-level functions. Our model consists of a first-order Boltzmann mechanoelectrical transducer function relating the instantaneous stimulus pressure to an instantaneous output, followed by a lowpass filter that eliminates the AC component, followed by an exponential synaptic transfer function relating the DC component to the mean spike rate. This is perhaps the simplest physiologically plausible model capable of accounting for rate-level functions under the assumption that the model parameters for a given ANF and stimulus frequency are level-independent. We find that the model typically accounts well for rate-level functions from cat ANFs for all stimulus frequencies. More complicated model variants having saturating synaptic transfer functions do not perform significantly better, implying the system operates far away from synaptic saturation. Rate saturation in the model is caused by saturation of the DC component of the filter output (e.g., the receptor potential), which in turn is due to the saturation of the transducer function. The maximum mean spike rate is approximately constant across ANFs, such that the slope parameter of the exponential synaptic transfer function decreases with increasing spontaneous rate. If the synaptic parameters for a given ANF are assumed to be constant across stimulus frequencies, then frequency- and level-dependent input nonlinearities are derived that are qualitatively similar to those reported in the literature. Contrary to assumptions in the literature, such nonlinearities are obtained even for ANFs having high spontaneous rates. Finally, spike-rate adaptation is examined and found to be accounted for by a decrease in the slope parameter of the synaptic transfer function over time following stimulus onset.
Genetic and functional diversity of primary auditory afferents
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Type I spiral ganglion neurons (I-SGNs) of the mammalian cochlea convey all acoustic information from the sensory hair cells to second order neurons in the brainstem. Despite evidence supporting physiological diversity of I-SGNs and of its importance for encoding the various features of sounds, knowledge of their molecular diversity is only emerging. In this review, we outline the recent efforts in the identification of mammalian I-SGN types and summarize how genetic and anatomical features of each individual neuron type relate to functional aspects that characterize sound information processing in the primary auditory afferent system.
Noise-induced Cochlear Synaptopathy with and Without Sensory Cell Loss
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Citation Excerpt :
Both exposures produced acute threshold elevations localized to the region just above the noise band. This pattern of shift relative to the exposure spectrum is consistent with nonlinearities of the cochlear mechanical response (Ruggero, 1992). The higher level, shorter duration exposure produced about 20–25 dB maximum shifts at 24 h (Fig. 5A, B), whereas shifts for the lower-level, 8 h exposure were <10 dB at the same post-exposure time (Fig. 5F, G), and all recovered by 2 wks.
Prior work has provided extensive documentation of threshold sensitivity and sensory hair cell losses after noise exposure. It is now clear, however, that cochlear synaptic loss precedes such losses, at least at low-moderate noise doses, silencing affected neurons. To address questions of whether, and how, cochlear synaptopathy and underlying mechanisms change as noise dose is varied, we assessed cochlear physiologic and histologic consequences of a range of exposures varied in duration from 15 min to 8 h and in level from 85 to 112 dB SPL. Exposures delivered to adult CBA/CaJ mice produced acute elevations in hair cell- and neural-based response thresholds ranging from trivial (∼5 dB) to large (∼50 dB), followed by varying degrees of recovery. Males appeared more noise vulnerable for some conditions of exposure. There was little to no inner hair cell (IHC) loss, but outer hair cell (OHC) loss could be substantial at highest frequencies for highest noise doses. Synapse loss was an early manifestation of noise injury and did not scale directly with either temporary or permanent threshold shift. With increasing noise dose, synapse loss grew to ∼50%, then declined for exposures yielding permanent hair cell injury/loss. All synaptopathic, but no non-synaptopathic exposures produced persistent neural response amplitude declines; those additionally yielding permanent OHC injury/loss also produced persistent reductions in OHC-based responses and exaggerated neural amplitude declines. Findings show that widespread cochlear synaptopathy can be present with and without noise-induced sensory cell loss and that differing patterns of cellular injury influence synaptopathic outcomes.
A Novel Ergodic Discrete Difference Equation Cochlear Model: Theoretical Analyses, Reproduction of Mammalian Nonlinear Sound Processing, and Comparison of Implementation
2024, IEEE Transactions on Circuits and Systems II: Express Briefs

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Responses to sound of the basilar membrane of the mammalian cochlea

Abstract

Curr Opin Neurobiol

Trends Neurosci

J Acoust Soc Am

J Acoust Soc Am

J Acoust Soc Am

J Neuropbysiol

Science

Hear Res

Phil Trans R Soc Lond [Biol]

Hear Res

J Acoust Soc Am

Nature

Hear Res

Auditory Physics. Physical Principles in Hearing Theory. III

Physics Reports

Cochlear Partition Vibration — Recent Views

J Acoust Soc Am

Cochlear Tuning Properties: Concurrent Basilar Membrane and Single Nerve Fiber Measurements

Science

Measurement of Basilar Membrane Motion in the Guinea Pig Using the Mossbauer Technique

J Acoust Soc Am

Comparison Between the Tuning Properties of Inner Hair Cells and Basilar Membrane Motion

Hear Res

The Influence of Mossbauer Source Size and Position on Phase and Amplitude Measurements of the Guinea Pig Basilar Membrane

Hear Res

Transient Response of the Basilar Membrane Measured in Squirrel Monkey Using the Mossbauer Effect

J Acoust Soc Am

Heterodyne Interferometer for Cellular Vibration Measurement

Acta Otolaryngol [Suppl]

Laser Doppler Velocimetry of Basilar Membrane Vibration

Hear Res

Application of a Commercially-Manufactured Doppler-Shift Laser Velocimeter to the Measurement of Basilar-Membrane Vibration

Hear Res

Furosemide Alters Organ of Corti Mechanics: Evidence for Feedback of Outer Hair Cells Upon the Basilar Membrane

J Neurosci

A Model Describing Nonlinearities in Hearing by Active Processes with Saturation at 40 dB

Biol Cybern

An Active Process in Cochlear Mechanics

Hear Res