Vestibular Type I and Type II Hair Cells. 1: Morphometric Identification in the Pigeon and Gerbil

1997 ◽  
Vol 7 (5) ◽  
pp. 393-406
Author(s):  
Anthony J. Ricci ◽  
Katherine J. Rennie ◽  
Stephen L. Cochran ◽  
Golda A. Kevetter ◽  
Manning J. Correia
Keyword(s):  
Hair Cell ◽  
Hair Cells ◽  
Cell Types ◽  
Type I ◽  
Type Ii ◽  
Body Width ◽  
Fixed Tissue ◽  
Neck Width ◽  
I Cells ◽  
Plate Width

Classically, type I and type II vestibular hair cells have been defined by their afferent innervation patterns. Little quantitative information exists on the intrinsic morphometric differences between hair cell types. Data presented here define a quantitative method for distinguishing hair cell types based on the morphometric properties of the hair cell’s neck region. The method is based initially on fixed histological sections, where hair cell types were identified by innervation pattern, type I cells having an afferent calyx. Cells were viewed using light microscopy, images were digitized, and measurements were made of the cell body width, the cuticular plate width, and the neck width. A plot of the ratio of the neck width to cuticular plate width (NPR) versus the ratio of the neck width to the body width (NBR) established four quadrants based on the best separation of type I and type II hair cells. The combination of the two variables made the accuracy of predicting either type I or type II hair cells greater than 90%. Statistical cluster analysis confirmed the quadrant separation. Similar analysis was performed on dissociated hair cells from semicircular canal, utricle, and lagena, giving results statistically similar to those of the fixed tissue. Additional comparisons were made between fixed tissue and isolated hair cells as well as across species (pigeon and gerbil) and between end organs (semicircular canal, utricle, and lagena). In each case, the same morphometric boundaries could be used to establish four quadrants, where quadrant 1 was predominantly type I cells and quadrant 3 was almost exclusively type II hair cells. The quadrant separations were confirmed statistically by cluster analysis. These data demonstrate that there are intrinsic morphometric differences between type I and type II hair cells and that these differences can be maintained when the hair cells are dissociated from their respective epithelia.

Differences Between Stereocilia Numbers on Type I and Type II Vestibular Hair Cells

2004 ◽  
Vol 92 (5) ◽  
pp. 3153-3160 ◽  
Author(s):  
W. J. Moravec ◽  
E. H. Peterson
Keyword(s):  
Hair Cell ◽  
Hair Cells ◽  
Direct Evidence ◽  
Cell Types ◽  
Type I ◽  
Type Ii ◽  
Functional Roles ◽  
Vestibular Hair Cells ◽  
Mechanoelectric Transduction ◽  
Bundle Structure

A major outstanding goal of vestibular neuroscience is to understand the distinctive functional roles of type I and type II hair cells. One important question is whether these two hair cell types differ in bundle structure. To address this, we have developed methods to characterize stereocilia numbers on identified type I and type II hair cells in the utricle of a turtle, Trachemys scripta. Our data indicate that type I hair cells, which occur only in the striola, average 95.9 ±16.73 (SD) stereocilia per bundle. In contrast, striolar type II hair cells have 59.9 ± 8.98 stereocilia, and type II hair cells in the adjacent extrastriola average 44.8 ± 10.82 stereocilia. Thus type I hair cells have the highest stereocilia counts in the utricle. These results provide the first direct evidence that type I hair cells have significantly more stereocilia than type II hair cells, and they suggest that the two hair cell types may differ in bundle mechanics and peak mechanoelectric transduction currents.

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.

Temporal Bone Studies of the Human Peripheral Vestibular System

2000 ◽  
Vol 109 (5_suppl) ◽  
pp. 3-13 ◽  
Author(s):  
Saumil N. Merchant ◽  
Kojiro Tsuji ◽  
Conrad Wall ◽  
Luis Velázquez-Villaseñor ◽  
Robert J. Glynn ◽  
...  
Keyword(s):  
Hair Cell ◽  
Hair Cells ◽  
Type I ◽  
Type Ii ◽  
Sense Organs ◽  
Age Related ◽  
The Mean ◽  
Cell Densities ◽  
Temporal Bones ◽  
Total Type

Quantitative studies of the vestibular system with serially sectioned human temporal bones have been limited because of difficulty in distinguishing hair cells from supporting cells and type I from type II hair cells. In addition, there is only a limited amount of normative data available regarding vestibular hair cell counts in humans. In this study, archival temporal bone sections were examined by Nomarski (differential interference contrast) microscopy, which permitted visualization of the cuticular plate and stereociliary bundle so as to allow unambiguous identification of hair cells. The density of type I, type II, and total numbers of vestibular hair cells in each of the 5 sense organs was determined in a set of 67 normal temporal bones that ranged from birth through 100 years of age. The mean total densities at birth were 76 to 79 cells per 0.01 mm2 in the cristae, 68 cells per 0.01 mm2 in the utricle, and 61 cells per 0.01 mm2 in the saccule. The ratio of type I to type II hair cells at birth was 2.4:1 in the cristae and 1.3:1 in the maculae. There was a highly significant age-related decline in all sense organs for total, type I, and type II hair cell densities that was best fit by a linear regression model. The cristae lost type I cells with advancing age at a significantly greater rate than the maculae, whereas age-related losses for type II cells occurred at the same rate for all 5 sense organs. Hair cell densities in the cristae were significantly higher at the periphery than at the center. There were no significant sex or interaural differences for any of the counts. Mathematical models were developed to calculate the mean and 95% prediction intervals for the total, type I, and type II hair cell densities in each sense organ on the basis of age. There was overall good agreement between the hair cell densities determined in this study and those reported by others using surface preparation techniques. Our data and related models will serve as a normative database that will be useful for comparison to counts made from subjects with known vestibular disorders.

Electrical filtering in gerbil isolated type I semicircular canal hair cells

1996 ◽  
Vol 75 (5) ◽  
pp. 2117-2123 ◽  
Author(s):  
K. J. Rennie ◽  
A. J. Ricci ◽  
M. J. Correia
Keyword(s):  
Membrane Potential ◽  
Hair Cells ◽  
Semicircular Canal ◽  
Input Resistance ◽  
Constant Current ◽  
Type I ◽  
Type Ii ◽  
Peak Voltage ◽  
Type I Cells ◽  
I Cells

1. Membrane potential responses of dissociated gerbil type I semicircular canal hair cells to current injections in whole cell current-clamp have been measured. The input resistance of type I cells was 21.4 +/- 14.3 (SD) M omega, (n = 25). Around the zero-current potential (Vz = -66.6 +/- 9.3 mV, n = 25), pulsed current injections (from approximately -200 to 750 pA) produced only small-amplitude, pulse-like changes in membrane potential. 2. Injecting constant current to hyperpolarize the membrane to around -100 mV resulted in a approximately 10-fold increase in membrane resistance. Current pulses superimposed on this constant hyperpolarization produced larger and more complex membrane potential changes. Depolarizing currents > or = 200 pA caused a rapid transient peak voltage before a plateau. 3. Membrane voltage was able to faithfully follow sine-wave current injections around Vz over the range 1-1,000 Hz with < 25% attenuation at 1 kHz. A previously described K conductance, IKI, which is active at Vz, produces the low input resistance and frequency response. This was confirmed by pharmacologically blocking IKI. This conductance, present in type I cells but not type II hair cells, would appear to confer on type I cells a lower gain, but a much broader bandwidth at Vz, than seen in type II cells.

scholarly journals Unmyelinated type II afferent neurons report cochlear damage

2015 ◽  
Vol 112 (47) ◽  
pp. 14723-14727 ◽  
Author(s):  
Chang Liu ◽  
Elisabeth Glowatzki ◽  
Paul Albert Fuchs
Keyword(s):  
Hair Cell ◽  
Hair Cells ◽  
Outer Hair Cell ◽  
Cell Damage ◽  
Large Diameter ◽  
Outer Hair Cells ◽  
Type I ◽  
Type Ii ◽  
Inner Hair Cell ◽  
Hair Cell Damage

In the mammalian cochlea, acoustic information is carried to the brain by the predominant (95%) large-diameter, myelinated type I afferents, each of which is postsynaptic to a single inner hair cell. The remaining thin, unmyelinated type II afferents extend hundreds of microns along the cochlear duct to contact many outer hair cells. Despite this extensive arbor, type II afferents are weakly activated by outer hair cell transmitter release and are insensitive to sound. Intriguingly, type II afferents remain intact in damaged regions of the cochlea. Here, we show that type II afferents are activated when outer hair cells are damaged. This response depends on both ionotropic (P2X) and metabotropic (P2Y) purinergic receptors, binding ATP released from nearby supporting cells in response to hair cell damage. Selective activation of P2Y receptors increased type II afferent excitability by the closure of KCNQ-type potassium channels, a potential mechanism for the painful hypersensitivity (that we term “noxacusis” to distinguish from hyperacusis without pain) that can accompany hearing loss. Exposure to the KCNQ channel activator retigabine suppressed the type II fiber’s response to hair cell damage. Type II afferents may be the cochlea’s nociceptors, prompting avoidance of further damage to the irreparable inner ear.

Morphological Changes in Rat Vestibular System Following Weightlessness

1993 ◽  
Vol 3 (3) ◽  
pp. 241-251
Author(s):  
Muriel D. Ross
Keyword(s):  
Hair Cells ◽  
Space Shuttle ◽  
Morphological Changes ◽  
Distributed Processing ◽  
Type I ◽  
Type Ii Cells ◽  
Type Ii ◽  
Ribbon Synapses ◽  
Gravity Receptors ◽  
I Cells

Mammalian gravity receptors (maculas) are morphologically organized for weighted, parallel distributed processing of information. There are two basic circuits: 1) highly channeled, type I cell to calyx; and 2) distributed modifying, type II cells to calyces and processes. The latter circuit should be the more adaptable since it modifies final output. To test this hypothesis, rats were flown in microgravity for 9 days aboard a space shuttle and euthanized shortly after landing. Hair cells and ribbon synapses from maculas of 3 flight and 3 ground control rats were studied ultrastructurally in blocks of 50 serial sections. Synapses increased by approximately 41% in type I cells and by approximately 55% in type II cells in flight animals. There was a shift toward the spherular form of ribbon synapse in both types of hair cells in flight animals (P ⩽ 0.0001), a near doubling of pairs in the flight rats (P ⩽ 0.0001), and an increase, by a factor of 12, in groups of synapses in type II cells (P ⩽ 0.0001). Current findings tend to support the stated hypothesis and indicate that mature utricular hair cells retain synaptic plasticity, permitting adaptation to an altered gravitational environment.

Architecture of the Mouse Utricle: Macular Organization and Hair Bundle Heights

2008 ◽  
Vol 99 (2) ◽  
pp. 718-733 ◽  
Author(s):  
A. Li ◽  
J. Xue ◽  
E. H. Peterson
Keyword(s):  
Hair Cell ◽  
Hair Cells ◽  
Quantitative Data ◽  
Posterior Margin ◽  
Adult Mouse ◽  
Type I ◽  
Type Ii ◽  
Cell Type ◽  
Vestibular Hair Cells ◽  
Utricular Macula

Hair bundles are critical to mechanotransduction by vestibular hair cells, but quantitative data are lacking on vestibular bundles in mice or other mammals. Here we quantify bundle heights and their variation with macular locus and hair cell type in adult mouse utricular macula. We also determined that macular organization differs from previous reports. The utricle has ∼3,600 hair cells, half on each side of the line of polarity reversal (LPR). A band of low hair cell density corresponds to a band of calretinin-positive calyces, i.e., the striola. The relation between the LPR and the striola differs from previous reports in two ways. First, the LPR lies lateral to the striola instead of bisecting it. Second, the LPR follows the striolar trajectory anteriorly, but posteriorly it veers from the edge of the striola to reach the posterior margin of the macula. Consequently, more utricular bundles are oriented mediolaterally than previously supposed. Three hair cell classes are distinguished in calretinin-stained material: type II hair cells, type ID hair cells contacting calretinin-negative (dimorphic) afferents, and type IC hair cells contacting calretinin-positive (calyceal) afferents. They differ significantly on most bundle measures. Type II bundles have short stereocilia. Type IC bundles have kinocilia and stereocilia of similar heights, i.e., KS ratios (ratio of kinocilium to stereocilia heights) ∼1, unlike other receptor classes. In contrast to these class-specific differences, bundles show little regional variation except that KS ratios are lowest in the striola. These low KS ratios suggest that bundle stiffness is greater in the striola than in the extrastriola.

Evidence for an Na+-K+-Cl−cotransporter in mammalian type I vestibular hair cells

1997 ◽  
Vol 273 (6) ◽  
pp. C1972-C1980 ◽  
Author(s):  
K. J. Rennie ◽  
J. F. Ashmore ◽  
M. J. Correia
Keyword(s):  
Hair Cell ◽  
Hair Cells ◽  
Cell Swelling ◽  
Type I ◽  
Vestibular Hair Cells ◽  
Type I Cells ◽  
High K ◽  
I Cells ◽  
Shape Changes ◽  
External K

In amniotes, there are two types of hair cells, designated I and II, that differ in their morphology, innervation pattern, and ionic membrane properties. Type I cells are unique among hair cells in that their basolateral surfaces are almost completely enclosed by an afferent calyceal nerve terminal. Recently, several lines of evidence have ascribed a motile function to type I hair cells. To investigate this, elevated external K+, which had been used previously to induce hair cell shortening, was used to induce shape changes in dissociated mammalian type I vestibular hair cells. Morphologically identified type I cells shortened and widened when the external K+ concentration was raised isotonically from 2 to 125 mM. The shortening did not require external Ca2+ but was abolished when external Cl− was replaced with gluconate or sulfate and when external Na+ was replaced with N-methyl-d-glucamine. Bumetanide (10–100 μM), a specific blocker of the Na+-K+-Cl− cotransporter, significantly reduced K+-induced shortening. Hyposmotic solution resulted in type I cell shape changes similar to those seen with high K+, i.e., shortening and widening. Type I cells became more spherical in hyposmotic solution, presumably as a result of a volume increase due to water influx. In hypertonic solution, cells became narrower and increased in length. These results suggest that shape changes in type I hair cells induced by high K+ are due, at least in part, to ion and solute entry via an Na+-K+-Cl− cotransporter, which results in cell swelling. A scheme is proposed whereby the type I hair cell depolarizes and K+ leaves the cell via voltage-dependent K+channels and accumulates in the synaptic space between the type I hair cell and calyx. Excess K+ could then be removed from the intercellular space by uptake via the cotransporter.

Autocorrelation Analysis of Hair Bundle Structure in the Utricle

2006 ◽  
Vol 96 (5) ◽  
pp. 2653-2669 ◽  
Author(s):  
M. H. Rowe ◽  
E. H. Peterson
Keyword(s):  
Hair Cell ◽  
Hair Cells ◽  
Cell Types ◽  
Head Movements ◽  
Type I ◽  
Autocorrelation Analysis ◽  
Response Dynamics ◽  
Hair Bundles ◽  
Vestibular Organs ◽  
Bundle Structure

The ability of hair bundles to signal head movements and sounds depends significantly on their structure, but a quantitative picture of bundle structure has proved elusive. The problem is acute for vestibular organs because their hair bundles exhibit complex morphologies that vary with endorgan, hair cell type, and epithelial locus. Here we use autocorrelation analysis to quantify stereociliary arrays (the number, spacing, and distribution of stereocilia) on hair cells of the turtle utricle. Our first goal was to characterize zonal variation across the macula, from medial extrastriola, through striola, to lateral extrastriola. This is important because it may help explain zonal variation in response dynamics of utricular hair cells and afferents. We also use known differences in type I and II bundles to estimate array characteristics of these two hair cell types. Our second goal was to quantify variation in array orientation at single macular loci and use this to estimate directional tuning in utricular afferents. Our major findings are that, of the features measured, array width is the most distinctive feature of striolar bundles, and within the striola there are significant, negatively correlated gradients in stereocilia number and spacing that parallel gradients in bundle heights. Together with previous results on stereocilia number and bundle heights, our results support the hypothesis that striolar hair cells are specialized to signal high-frequency/acceleration head movements. Finally, there is substantial variation in bundle orientation at single macular loci that may help explain why utricular afferents respond to stimuli orthogonal to their preferred directions.

Voltage-Gated Calcium Channel Currents in Type I and Type II Hair Cells Isolated From the Rat Crista

2003 ◽  
Vol 90 (1) ◽  
pp. 155-164 ◽  
Author(s):  
Hong Bao ◽  
Weng Hoe Wong ◽  
Jay M. Goldberg ◽  
Ruth Anne Eatock
Keyword(s):  
Hair Cells ◽  
Type I ◽  
Type Ii Cells ◽  
Type Ii ◽  
Α Subunit ◽  
Voltage Gated ◽  
Type I Cells ◽  
Channel Currents ◽  
I Cells

When studied in vitro, type I hair cells in amniote vestibular organs have a large, negatively activating K+ conductance. In type II hair cells, as in nonvestibular hair cells, outwardly rectifying K+ conductances are smaller and more positively activating. As a result, type I cells have more negative resting potentials and smaller input resistances than do type II cells; large inward currents fail to depolarize type I cells above –60 mV. In nonvestibular hair cells, afferent transmission is mediated by voltage-gated Ca2+ channels that activate positive to –60 mV. We investigated whether Ca2+ channels in type I cells activate more negatively so that quantal transmission can occur near the reported resting potentials. We used the perforated patch method to record Ca2+ channel currents from type I and type II hair cells isolated from the rat anterior crista (postnatal days 4–20). The activation range of the Ca2+ currents of type I hair cells differed only slightly from that of type II cells or nonvestibular hair cells. In 5 mM external Ca2+, currents in type I and type II cells were half-maximal at –41.1 ± 0.5 (SE) mV ( n = 10) and –37.2 ± 0.2 mV ( n = 10), respectively. In physiological external Ca2+ (1.3 mM), currents in type I cells were half-maximal at –46 ± 1 mV ( n = 8) and just 1% of maximal at –72 mV. These results lend credence to suggestions that type I cells have more positive resting potentials in vivo, possibly through K+ accumulation in the synaptic cleft or inhibition of the large K+ conductance. Ca2+ channel kinetics were also unremarkable; in both type I and type II cells, the currents activated and deactivated rapidly and inactivated only slowly and modestly even at large depolarizations. The Ca2+ current included an L-type component with relatively low sensitivity to dihydropyridine antagonists, consistent with the α subunit being CaV1.3 (α1D). Rat vestibular epithelia and ganglia were probed for L-type α-subunit expression with the reverse transcription-polymerase chain reaction. The epithelia expressed CaV1.3 and the ganglia expressed CaV1.2 (α1C).

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