scholarly journals K+ Accumulation and Clearance in the Calyx Synaptic Cleft of Type I Mouse Vestibular Hair Cells

Neuroscience ◽  
2020 ◽  
Vol 426 ◽  
pp. 69-86 ◽  
Author(s):  
P. Spaiardi ◽  
E. Tavazzani ◽  
M. Manca ◽  
G. Russo ◽  
I. Prigioni ◽  
...  
Keyword(s):  
Hair Cells ◽  
Synaptic Cleft ◽  
Type I ◽  
Vestibular Hair Cells

scholarly journals A Biophysical Model of Nonquantal Transmission at the Vestibular Hair Cell-Calyx Synapse: KLV currents Modulate Fast Electrical and Slow K+ potentials in the Synaptic Cleft

2021 ◽  
Author(s):  
Aravind Chenrayan Govindaraju ◽  
Imran H Quraishi ◽  
Anna Lysakowski ◽  
Ruth Anne Eatock ◽  
Robert M Raphael
Keyword(s):  
Hair Cell ◽  
Hair Cells ◽  
Low Voltage ◽  
Electrical Potential ◽  
Synaptic Cleft ◽  
Biophysical Model ◽  
Afferent Neuron ◽  
Type I ◽  
Significant Finding ◽  
Vestibular Hair Cells

Vestibular hair cells transmit information about head position and motion across synapses to primary afferent neurons. At some of these synapses, the afferent neuron envelopes the hair cell, forming an enlarged synaptic terminal referred to as a calyx. The vestibular hair cell-calyx synapse supports nonquantal transmission (NQT), a neurotransmitter-independent mechanism that is exceptionally fast. The underlying biophysical mechanisms that give rise to NQT are not fully understood. Here we present a computational model of NQT that integrates morphological and electrophysiological data. The model predicts that NQT involves two processes: changes in cleft K+ concentration, as previously recognized, and very fast changes in cleft electrical potential. A significant finding is that changes in cleft electrical potential are faster than changes in [K+] or quantal transmission. The electrical potential mechanism thus provides a basis for the exceptional speed of neurotransmission between type I hair cells and primary neurons and explains experimental observations of fast postsynaptic currents. The [K+] mechanism increases the gain of NQT. Both processes are mediated by current flow through low-voltage-activated K+ (KLV) channels located in both pre-synaptic (hair cell) and post-synaptic (calyx inner face) membranes. The model further demonstrates that the calyx morphology is necessary for NQT; as calyx height is increased, NQT increases in size, speed and efficacy at depolarizing the afferent neuron. We propose that the calyx evolved to enhance NQT and speed up signals that drive vestibular reflexes essential for stabilizing the eyes and neck and maintaining balance during rapid and complex head motions.

Ionic Currents and Electromotility in Inner Ear Hair Cells From Humans

1998 ◽  
Vol 79 (4) ◽  
pp. 2235-2239 ◽  
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.

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

2004 ◽  
Vol 19 (2) ◽  
pp. 155-169 ◽  
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.

Electrically Evoked Motile Responses of Mammalian Type I Vestibular Hair Cells

1992 ◽  
Vol 2 (3) ◽  
pp. 181-191
Author(s):  
Hans Peter Zenner ◽  
Günter Reuter ◽  
Shi Hong ◽  
Ulrike Zimmermann ◽  
Alfred H. Gitter
Keyword(s):  
Hair Cells ◽  
Sensory Modality ◽  
Outer Hair Cells ◽  
Type I ◽  
Image Subtraction ◽  
Low Frequencies ◽  
Vestibular Hair Cells ◽  
Mechanical Responses ◽  
Contrast Enhanced ◽  
Length Changes

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.

Temporal Bone Studies of the Human Peripheral Vestibular System

2000 ◽  
Vol 109 (5_suppl) ◽  
pp. 20-25 ◽  
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.

Inward potassium rectifier current in type I vestibular hair cells isolated from guinea pig

1993 ◽  
Vol 149 (1) ◽  
pp. 51-55 ◽  
Author(s):  
Corinne Griguer ◽  
Alain Sans ◽  
Jean Valmier ◽  
Jacques Lehouelleur
Keyword(s):  
Guinea Pig ◽  
Hair Cells ◽  
Type I ◽  
Vestibular Hair Cells

Effects of KCNQ channel blockers on K+ currents in vestibular hair cells

2001 ◽  
Vol 280 (3) ◽  
pp. C473-C480 ◽  
Author(s):  
Katherine J. Rennie ◽  
Tianxiang Weng ◽  
Manning J. Correia
Keyword(s):  
Steady State ◽  
Hair Cells ◽  
Low Voltage ◽  
Dissociation Constants ◽  
Channel Blockers ◽  
Type I ◽  
Type Ii ◽  
Kcnq Channels ◽  
Vestibular Hair Cells ◽  
Inward Currents

Linopirdine and XE991, selective blockers of K+ channels belonging to the KCNQ family, were applied to hair cells isolated from gerbil vestibular system and to hair cells in slices of pigeon crista. In type II hair cells, both compounds inhibited a slowly activating, slowly inactivating component of the macroscopic current recruited at potentials above −60 mV. The dissociation constants for linopirdine and XE991 block were <5 μM. A similar component of the current was also blocked by 50 μM capsaicin in gerbil type II hair cells. All three drugs blocked a current component that showed steady-state inactivation and a biexponential inactivation with time constants of ∼300 ms and 4 s. Linopirdine (10 μM) reduced inward currents through the low-voltage-activated K+ current in type I hair cells, but concentrations up to 200 μM had little effect on steady-state outward K+ current in these cells. These results suggest that KCNQ channels may be present in amniote vestibular hair cells.

Recovery of the Vestibulocolic Reflex After Aminoglycoside Ototoxicity in Domestic Chickens

1999 ◽  
Vol 81 (3) ◽  
pp. 1025-1035 ◽  
Author(s):  
Christopher T. Goode ◽  
John P. Carey ◽  
Albert F. Fuchs ◽  
Edwin W Rubel
Keyword(s):  
Hair Cell ◽  
Hair Cells ◽  
Afferent Input ◽  
Open Loop ◽  
Cell Regeneration ◽  
Type I ◽  
Neural Pathways ◽  
Hair Cell Regeneration ◽  
Vestibular Hair Cells ◽  
Aminoglycoside Ototoxicity

Recovery of the vestibulocolic reflex after aminoglycoside ototoxicity in domestic chickens. Avian auditory and vestibular hair cells regenerate after damage by ototoxic drugs, but until recently there was little evidence that regenerated vestibular hair cells function normally. In an earlier study we showed that the vestibuloocular reflex (VOR) is eliminated with aminoglycoside antibiotic treatment and recovers as hair cells regenerate. The VOR, which stabilizes the eye in the head, is an open-loop system that is thought to depend largely on regularly firing afferents. Recovery of the VOR is highly correlated with the regeneration of type I hair cells. In contrast, the vestibulocolic reflex (VCR), which stabilizes the head in space, is a closed-loop, negative-feedback system that seems to depend more on irregularly firing afferent input and is thought to be subserved by different circuitry than the VOR. We examined whether this different reflex also of vestibular origin would show similar recovery after hair cell regeneration. Lesions of the vestibular hair cells of 10-day-old chicks were created by a 5-day course of streptomycin sulfate. One day after completion of streptomycin treatment there was no measurable VCR gain, and total hair cell density was ∼35% of that in untreated, age-matched controls. At 2 wk postlesion there was significant recovery of the VCR; at this time two subjects showed VCR gains within the range of control chicks. At 3 wk postlesion all subjects showed VCR gains and phase shifts within the normal range. These data show that the VCR recovers before the VOR. Unlike VOR gain, recovering VCR gain correlates equally well with the density of regenerating type I and type II vestibular hair cells, except at high frequencies. Several factors other than hair cell regeneration, such as length of stereocilia, reafferentation of hair cells, and compensation involving central neural pathways, may be involved in behavioral recovery. Our data suggest that one or more of these factors differentially affect the recovery of these two vestibular reflexes.

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