Electrically Evoked Motile Responses of Mammalian Type I Vestibular Hair Cells

Vestibular hair cells, type I and II, with membrane potentials around -64 mV were prepared from guinea pig ampullar cristae and maculae. In type I cells, current injection, application of voltage steps during membrane patch-clamping, or extracellular alternating current (ac) fields evoked fast length changes of 50 nm to 500 nm of the cell “neck”. Mechanical responses were determined by computerized video techniques with contrast-enhanced digital image subtraction (DIS) and interpeak pixel counts (IPPC) or by double photodiode measurements. These techniques allowed spatial resolutions of 300 nm, 120 nm, and 50 nm, respectively. In contrast to measurements of high-frequency movements of auditory outer hair cells (OHCs), the mechanical responses of type I VHCs were restricted to low frequencies below 85 Hz. In addition to recently reported slow motility of VHCs, the present results suggest that fast mechanical VHC responses could significantly influence macular and cupular mechanics. Isometric and isotonic variants are discussed. The observed frequency maxima gap between VHCs and OHCs is suggested to contribute to a clear separation of the auditory and the vestibular sensory modality.

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Ionic Currents and Electromotility in Inner Ear Hair Cells From Humans

Journal of Neurophysiology ◽

10.1152/jn.1998.79.4.2235 ◽

1998 ◽

Vol 79 (4) ◽

pp. 2235-2239 ◽

Cited By ~ 22

Author(s):

John S. Oghalai ◽

Jeffrey R. Holt ◽

Takashi Nakagawa ◽

Thomas M. Jung ◽

Newton J. Coker ◽

...

Keyword(s):

Inner Ear ◽

Hair Cells ◽

Ionic Currents ◽

Sensory Epithelium ◽

Outer Hair Cells ◽

Sensory Receptor ◽

Surgical Removal ◽

Type I ◽

Vestibular Hair Cells ◽

Sensory Receptor Cells

Oghalai, John S., Jeffrey R. Holt, Takashi Nakagawa, Thomas M. Jung, Newton J. Coker, Herman A. Jenkins, Ruth Anne Eatock, and William E. Brownell. Ionic currents and electromotility in inner ear hair cells from humans. J. Neurophysiol. 79: 2235–2239, 1998. The upright posture and rich vocalizations of primates place demands on their senses of balance and hearing that differ from those of other animals. There is a wealth of behavioral, psychophysical, and CNS measures characterizing these senses in primates, but no prior recordings from their inner ear sensory receptor cells. We harvested human hair cells from patients undergoing surgical removal of life-threatening brain stem tumors and measured their ionic currents and electromotile responses. The hair cells were either isolated or left in situ in their sensory epithelium and investigated using the tight-seal, whole cell technique. We recorded from both type I and type II vestibular hair cells under voltage clamp and found four voltage-dependent currents, each of which has been reported in hair cells of other animals. Cochlear outer hair cells demonstrated electromotility in response to voltage steps like that seen in rodent animal models. Our results reveal many qualitative similarities to hair cells obtained from other animals and justify continued investigations to explore quantitative differences that may be associated with normal or pathological human sensation.

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Static length changes of cochlear outer hair cells can tune low-frequency hearing

10.1101/228353 ◽

2017 ◽

Author(s):

Nikola Ciganović ◽

Rebecca L. Warren ◽

Batu Keçeli ◽

Stefan Jacob ◽

Anders Fridberger ◽

...

Keyword(s):

Inner Ear ◽

Hair Cells ◽

Organ Of Corti ◽

Outer Hair Cells ◽

Frequency Selectivity ◽

Apical Region ◽

Low Frequencies ◽

Inner Hair Cells ◽

Length Changes ◽

The Brain

AbstractThe cochlea not only transduces sound-induced vibration into neural spikes, it also amplifies weak sound to boost its detection. Actuators of this active process are sensory outer hair cells in the organ of Corti, whereas the inner hair cells transduce the resulting motion into electric signals that propagate via the auditory nerve to the brain. However, how the outer hair cells modulate the stimulus to the inner hair cells remains unclear. Here, we combine theoretical modeling and experimental measurements near the cochlear apex to study the way in which length changes of the outer hair cells deform the organ of Corti. We develop a geometry-based kinematic model of the apical organ of Corti that reproduces salient, yet counter-intuitive features of the organ’s motion. Our analysis further uncovers a mechanism by which a static length change of the outer hair cells can sensitively tune the signal transmitted to the sensory inner hair cells. When the outer hair cells are in an elongated state, stimulation of inner hair cells is largely inhibited, whereas outer hair cell contraction leads to a substantial enhancement of sound-evoked motion near the hair bundles. This novel mechanism for regulating the sensitivity of the hearing organ applies to the low frequencies that are most important for the perception of speech and music. We suggest that the proposed mechanism might underlie frequency discrimination at low auditory frequencies, as well as our ability to selectively attend auditory signals in noisy surroundings.Author summaryOuter hair cells are highly specialized force producers inside the inner ear: they can change length when stimulated electrically. However, how exactly this electromotile effect contributes to the astonishing sensitivity and frequency selectivity of the inner ear has remained unclear. Here we show for the first time that static length changes of outer hair cells can sensitively regulate how much of a sound signal is passed on to the inner hair cells that forward the signal to the brain. Our analysis holds for the apical region of the inner ear that is responsible for detecting the low frequencies that matter most in speech and music. This shows a mechanisms for how frequency-selectivity can be achieved at low frequencies. It also opens a path for the efferent neural system to regulate hearing sensitivity.

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The location and mechanism of electromotility in guinea pig outer hair cells

Journal of Neurophysiology ◽

10.1152/jn.1993.70.2.549 ◽

1993 ◽

Vol 70 (2) ◽

pp. 549-558 ◽

Cited By ~ 38

Author(s):

R. Hallworth ◽

B. N. Evans ◽

P. Dallos

Keyword(s):

Guinea Pig ◽

Hair Cells ◽

Outer Hair Cell ◽

Length Change ◽

Opposite Polarity ◽

Outer Hair Cells ◽

Response Amplitude ◽

Change Function ◽

Length Changes ◽

Diameter Change

1. The microchamber method was used to examine the motile responses of isolated guinea pig outer hair cells to electrical stimulation. In the microchamber method, an isolated cell is drawn partway into a suction pipette and stimulated transcellularly. The relative position of the cell in the microchamber is referred to as the exclusion fraction. 2. The length changes of the included and excluded segments were compared for constant sinusoidal stimulus amplitude as functions of the exclusion fraction. Both included and excluded segments showed maximal responses when the cell was excluded approximately halfway. Both segments showed smaller or absent responses when the cell was almost fully excluded or almost fully included. 3. When the cell was near to, but not at, the maximum exclusion, the included segment response amplitude was zero, whereas the excluded segment response amplitude was nonzero. In contrast, when the cell was nearly fully included, the excluded segment response amplitude was zero, but the included segment response amplitude was still detectable. A simple model of outer hair cell motility based on these results suggests that the cell has finite-resistance terminations and that the motors are restricted to a region above the nucleus and below its ciliated apex (cuticular plate). 4. The function describing length change as a function of command voltage was measured for each segment as the exclusion fraction was varied. The functions were similar at midrange exclusions (i.e., when the segments were about equal length), showing nonlinearity and saturability. The functions were strikingly different when the segment lengths were different. The effects of exclusion on the voltage to length-change functions suggested that the nonlinearity and saturability are local properties of the motility mechanism. 5. The diameter changes of both segments were examined. The segment diameter changes were always antiphasic to the length changes. This finding implies that the motility mechanism has an active antiphasic diameter component. The diameter change amplitude was a monotonically increasing function of exclusion for the included segment, and a decreasing function for the excluded segment. 6. The voltage to length-change and voltage to diameter-change functions were measured for the same cell and exclusion fraction. The voltage to diameter-change function was smaller in amplitude than the voltage to length-change function. The functions were of opposite polarity to each other, but were otherwise similar in character. Thus it is likely that the same motor mechanism is responsible for both axial and diameter deformations.

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Guinea Pig Vestibular Type I Hair Cells Can Show Reversible Shortening

Journal of Vestibular Research ◽

10.3233/ves-1991-1303 ◽

1991 ◽

Vol 1 (3) ◽

pp. 241-250

Author(s):

Pascale N.M. Lapeyre ◽

Yves Cazals

Keyword(s):

Guinea Pig ◽

Hair Cells ◽

Neck Region ◽

Outer Hair Cells ◽

Test Solution ◽

Induced Response ◽

Type I ◽

Hypotonic Solution ◽

Bathing Medium ◽

Water Influx

Guinea pig isolated vestibular type I hair cells (VIHCs) were recently reported by our group to respond to high [KCl] solutions by an irreversible tilt of their neck region and sometimes by a sustained shortening and swelling. A possible osmotic contribution to these shape changes was investigated by substituting gluconate (G) for chloride in the test solution, so as to minimize water influx, and also by changing the osmotic pressure of the extracellular solution. For comparison, similar experiments were also undertaken on cochlear outer hair cells (OHCs). Utricular and ampullar type I hair cells were more difficult to isolate than OHCs and, like them, responded to an isotonic high [KCl] solution by a sustained shortening and widening, which were found to be reversible for most cells when rinsed with the control solution. In a high [KG] solution, all OHCs showed a shortening reversible in the test solution; among the VIHCs tested, two-thirds presented a slight sustained shortening without widening and a third showed a spontaneously reversible shortening, particularly at the neck level. VIHCs exposed to a high [N-methyl-D-glucamine chloride] solution, this impermeant cation replacing K+ for control, presented only a slight sustained shortening. In response to osmotic changes of the bathing medium, both VIHCs and OHCs showed a sustained shortening or elongation (the latter to a lesser degree) for hypo- and hyperosmotic solutions, respectively. The VIHCs and OHCs that presented a reversible shortening in a high [KG] solution widened concomitantly with their shortening, but to a smaller extent compared with what was observed in a high [KCl] solution, and this diameter increase was reversible in the test solution, unlike the widening observed in a hypotonic solution. These results show that a reversible shortening occurred for some VIHCs; they also indicate the involvement of two components in the KCl-induced response: one osmotic and another potassium-dependent.

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Molecular characterization of an inward rectifier channel (IKir) found in avian vestibular hair cells: cloning and expression of pKir2.1

Physiological Genomics ◽

10.1152/physiolgenomics.00096.2004 ◽

2004 ◽

Vol 19 (2) ◽

pp. 155-169 ◽

Cited By ~ 11

Author(s):

Manning J. Correia ◽

Thomas G. Wood ◽

Deborah Prusak ◽

Tianxiang Weng ◽

Katherine J. Rennie ◽

...

Keyword(s):

Hair Cells ◽

Cho Cells ◽

Dwell Time ◽

Single Channel ◽

Cloning And Expression ◽

Single Type ◽

Type I ◽

Type Ii ◽

Vestibular Hair Cells ◽

Inwardly Rectifying

A fast inwardly rectifying current has been observed in some of the sensory cells (hair cells) of the inner ear of several species. While the current was presumed to be an IKir current, contradictory evidence existed as to whether the cloned channel actually belonged to the Kir2.0 subfamily of potassium inward rectifiers. In this paper, we report for the first time converging evidence from electrophysiological, biochemical, immunohistochemical, and genetic studies that show that the Kir2.1 channel carries the fast inwardly rectifying currents found in pigeon vestibular hair cells. Following cytoplasm extraction from single type II and multiple pigeon vestibular hair cells, mRNA was reverse transcribed, amplified, and sequenced. The open reading frame (ORF), consisting of a 1,284-bp nucleotide sequence, showed 94, 85, and 83% identity with Kir2.1 subunit sequences from chick lens, Kir2 sequences from human heart, and a mouse macrophage cell line, respectively. Phylogenetic analyses revealed that pKir2.1 formed an immediate node with hKir2.1 but not with hKir2.2–2.4. Hair cells (type I and type II) and supporting cells in the sensory epithelium reacted positively with a Kir2.1 antibody. The whole cell current recorded in oocytes and CHO cells, transfected with pigeon hair cell Kir2.1 (pKir2.1), demonstrated blockage by Ba2+ and sensitivity to changing K+ concentration. The mean single-channel linear slope conductance in transfected CHO cells was 29 pS. The open dwell time was long (∼300 ms at −100 mV), and the closed dwell time was short (∼34 ms at −100 mV). Multistates ranging from 3–6 were noted in some single-channel responses. All of the above features have been described for other Kir2.1 channels. Current clamp studies of native pigeon vestibular hair cells illustrated possible physiological roles of the channel and showed that blockage of the channel by Ba2+ depolarized the resting membrane potential by ∼30 mV. Negative currents hyperpolarized the membrane ∼20 mV before block but ∼60 mV following block. RT-PCR studies revealed that the pKir2.1 channels found in pigeon vestibular hair cells were also present in pigeon vestibular nerve, vestibular ganglion, lens, neck muscle, brain (brain stem, cerebellum and optic tectum), liver, and heart.

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Axodendritic versus axosomatic cochlear efferent termination is determined by afferent type in a hierarchical logic of circuit formation

Science Advances ◽

10.1126/sciadv.abd8637 ◽

2021 ◽

Vol 7 (4) ◽

pp. eabd8637

Author(s):

Jemma L. Webber ◽

John C. Clancy ◽

Yingjie Zhou ◽

Natalia Yraola ◽

Kazuaki Homma ◽

...

Keyword(s):

Hair Cells ◽

Fiber Type ◽

Afferent Fiber ◽

Outer Hair Cells ◽

Type I ◽

Type Ii ◽

Efferent Neurons ◽

Distinct Pair ◽

Mechanosensory Hair Cells ◽

Circuit Formation

Hearing involves a stereotyped neural network communicating cochlea and brain. How this sensorineural circuit assembles is largely unknown. The cochlea houses two types of mechanosensory hair cells differing in function (sound transmission versus amplification) and location (inner versus outer compartments). Inner (IHCs) and outer hair cells (OHCs) are each innervated by a distinct pair of afferent and efferent neurons: IHCs are contacted by type I afferents receiving axodendritic efferent contacts; OHCs are contacted by type II afferents and axosomatically terminating efferents. Using an Insm1 mouse mutant with IHCs in the position of OHCs, we discover a hierarchical sequence of instructions in which first IHCs attract, and OHCs repel, type I afferents; second, type II afferents innervate hair cells not contacted by type I afferents; and last, afferent fiber type determines if and how efferents innervate, whether axodendritically on the afferent, axosomatically on the hair cell, or not at all.

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Temporal Bone Studies of the Human Peripheral Vestibular System

Annals of Otology Rhinology & Laryngology ◽

10.1177/00034894001090s504 ◽

2000 ◽

Vol 109 (5_suppl) ◽

pp. 20-25 ◽

Cited By ~ 38

Author(s):

Kojiro Tsuji ◽

Steven D. Rauch ◽

Conrad Wall ◽

Luis Velázquez-Villaseñor ◽

Robert J. Glynn ◽

...

Keyword(s):

Hair Cell ◽

Hair Cells ◽

Ganglion Cells ◽

Significant Loss ◽

Small Sample ◽

Type I ◽

Type Ii ◽

Vestibular Hair Cells ◽

Scarpa's Ganglion ◽

Temporal Bones

Quantitative assessments of vestibular hair cells and Scarpa's ganglion cells were performed on 17 temporal bones from 10 individuals who had well-documented clinical evidence of aminoglycoside ototoxicity (streptomycin, kanamycin, and neomycin). Assessment of vestibular hair cells was performed by Nomarski (differential interference contrast) microscopy. Hair cell counts were expressed as densities (number of cells per 0.01 mm2 surface area of the sensory epithelium). The results were compared with age-matched normal data. Streptomycin caused a significant loss of both type I and type II hair cells in all 5 vestibular sense organs. In comparing the ototoxic effect on type I versus type II hair cells, there was greater type I hair cell loss for all 3 cristae, but not for the maculae. The vestibular ototoxic effects of kanamycin appeared to be similar to those of streptomycin, but the small sample size precluded definitive conclusions from being made. Neomycin did not cause loss of vestibular hair cells. Within the limits of this study (maximum postototoxicity survival time of 12 months), there was no significant loss of Scarpa's ganglion cells for any of the 3 drugs. The findings have implications in several clinical areas, including the correlation of vestibular test results to pathological findings, the rehabilitation of patients with vestibular ototoxicity, the use of aminoglycosides to treat Meniere's disease, and the development of a vestibular prosthesis.

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