Afferent Innervation of the Utricular Macula in Pigeons

2003 ◽  
Vol 89 (3) ◽  
pp. 1660-1677 ◽  
Author(s):  
Xiaohong Si ◽  
Mridha Md. Zakir ◽  
J. David Dickman
Keyword(s):  
Hair Cells ◽  
Wide Band ◽  
Type I ◽  
Type Ii ◽  
Cellular Organization ◽  
Biotinylated Dextran Amine ◽  
Utricular Macula ◽  
Innervation Patterns ◽  
Biotinylated Dextran ◽  
Afferent Innervation

Biotinylated dextran amine (BDA) was used to retrogradely label afferents innervating the utricular macula in adult pigeons. The pigeon utriclar macula consists of a large rectangular-shaped neuroepithelium with a dorsally curved anterior edge and an extended medioposterior tail. The macula could be demarcated into several regions based on cytoarchitectural differences. The striola occupied 30% of the macula and contained a large density of type I hair cells with fewer type II hair cells. Medial and lateral extrastriola zones were located outside the striola and contained only type II hair cells. A six- to eight-cell-wide band of type II hair cells existed near the center of the striola. The reversal line marked by the morphological polarization of hair cells coursed throughout the epithelium, near the peripheral margin, and through the center of the type II band. Calyx afferents innervated type I hair cells with calyceal terminals that contained between 2 and 15 receptor cells. Calyx afferents were located only in the striola region, exclusive of the type II band, had small total fiber innervation areas and low innervation densities. Dimorph afferents innervated both type I and type II hair cells with calyceal and bouton terminals and were primarily located in the striola region. Dimorph afferents had smaller calyceal terminals with few type I hair cells, extended fiber branches with bouton terminals and larger innervation areas. Bouton afferents innervated only type II hair cells in the extrastriola and type II band regions. Bouton afferents innervating the type II band had smaller terminal fields with fewer bouton terminals and smaller innervation areas than fibers located in the extrastriolar zones. Bouton afferents had the most bouton terminals on the longest fibers, the largest innervation areas with the highest innervation densities of all afferents. Among all afferents, smaller terminal innervation fields were observed in the striola and large fields were located in the extrastriola. The cellular organization and innervation patterns of the utricular maculae in birds appear to represent an organ in adaptive evolution, different from that observed for amphibians or mammals.

Afferent Innervation Patterns of the Saccule in Pigeons

2003 ◽  
Vol 89 (1) ◽  
pp. 534-550 ◽  
Author(s):  
M. Zakir ◽  
D. Huss ◽  
J. D. Dickman
Keyword(s):  
Hair Cells ◽  
Three Dimensional ◽  
Otolith Organs ◽  
Type I ◽  
Innervation Patterns ◽  
Receptor Organ ◽  
Oriented Parallel ◽  
Biotinylated Dextran ◽  
Afferent Innervation ◽  
Anterior Posterior

The innervation patterns of vestibular saccular afferents were quantitatively investigated in pigeons using biotinylated dextran amine as a neural tracer and three-dimensional computer reconstruction. Type I hair cells were found throughout a large portion of the macula, with the highest density observed in the striola. Type II hair cells were located throughout the macula, with the highest density in the extrastriola. Three classes of afferent innervation patterns were observed, including calyx, dimorph, and bouton units, with 137 afferents being anatomically reconstructed and used for quantitative comparisons. Calyx afferents were located primarily in the striola, innervated a number of type I hair cells, and had small innervation areas. Most calyx afferent terminal fields were oriented parallel to the anterior-posterior axis and the morphological polarization reversal line. Dimorph afferents were located throughout the macula, contained fewer type I hair cells in a calyceal terminal than calyx afferents and had medium sized innervation areas. Bouton afferents were restricted to the extrastriola, with multi-branching fibers and large innervation areas. Most of the dimorph and bouton afferents had innervation fields that were oriented dorso-ventrally but were parallel to the neighboring reversal line. The organizational morphology of the saccule was found to be distinctly different from that of the avian utricle or lagena otolith organs and appears to represent a receptor organ undergoing evolutionary adaptation toward sensing linear motion in terrestrial and aerial species.

Synaptic ribbon plasticity, ribbon size and potential regulatory mechanisms in utricular and saccular maculae

2005 ◽  
Vol 15 (1) ◽  
pp. 17-30 ◽  
Author(s):  
Muriel D. Ross ◽  
Joseph Varelas
Keyword(s):  
Hair Cells ◽  
Smooth Endoplasmic Reticulum ◽  
Type I ◽  
Synaptic Ribbons ◽  
Type Ii ◽  
Synaptic Ribbon ◽  
Utricular Macula ◽  
Ribbon Synapses ◽  
New Finding ◽  
The Mean

The mean number of synaptic ribbons in type II hair cells of the rat utricular macula increased significantly in weightlessness. In contrast, ribbon synapses of saccular type I hair cells displayed a significant decline early inflight and postflight, and a late numerical overshoot. Further study indicated that the saccular macula had less ultrastructural complexly than the utricular. Additionally, synaptic ribbons were statistically larger in type II hair cells of both maculae, apparently a locus-related scaling effect. A major new finding is that mitochondria in calyces and collateral terminals were linked to vesicles, tubules of smooth endoplasmic reticulum and cell membranes by filaments, forming mitochondrial complexes (MCs). MCs predominated basally in the calyx where calyceal/type I hair cell borders were bound by filaments; at calyceal invaginations of type I hair cells; in calyces and collaterals near synaptic ribbon sites; and in collaterals near reciprocal synapses. MCs may participate in feedback mechanisms at these locations to help regulate synaptic ribbon activity and plasticity in altered gravitational environments.

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.

Second Place — Resident Basic Science Award 1994: Subcellular Innervation Patterns of the Calcitonin Gene-Related Peptidergic Efferent Terminals in the Chinchilla Vestibular Periphery

1994 ◽  
Vol 111 (4) ◽  
pp. 385-395 ◽  
Author(s):  
Akira Ishiyama ◽  
Ivan Lopez ◽  
Phillip A. Wackym
Keyword(s):  
Vestibular System ◽  
Hair Cells ◽  
Calcitonin Gene Related Peptide ◽  
Type I ◽  
Type Ii ◽  
Primary Afferent ◽  
Related Peptide ◽  
Calcitonin Gene ◽  
Innervation Patterns ◽  
Immunoreactive Axons

We examined the ultrastructural distribution of calcitonin gene-related peptide immunoreactivity in the peripheral vestibular system of the chinchilla to study the Innervation patterns of this efferent neuropeptide. Immunoelectron microscopic localization of calcitonin gene-related peptide immunoreactive terminals in the maculae and cristae revealed an extensive innervation pattern on the afferent vestibular pathway. Calcitonin gene-related peptide immunoreactive terminals made synaptic contacts with the unmyelinated portions of the primary afferent vestibular dendrites innervating both type I and type II hair cells. Abundant synaptic contact between calcitonin gene-related peptide immunoreactive terminals and the chalices surrounding type I hair cells was observed. Direct contact between calcitonin gene-related peptide immunoreactive terminals and type II hair cells was observed. In addition, vesiculated efferent terminals without calcitonin gene-related peptide Immunoreactivity were seen synapsing on the chalices of type II hair cells and on the surrounding type I hair cells. The primary afferent somata in the vestibular ganglion of Scarpa did not contain calcitonin gene-related peptide Immunoreactivity. Unmyelinated calcitonin gene-related peptide immunoreactive axons passed among the primary afferent fibers in Scarpa's ganglion, and these fibers continued through the subepithelial regions of the vestibular end-organs. The calcitonin gene-related peptide immunoreactive axons ramified to produce numerous calcitonin gene-related peptide immunoreactive terminals throughout the neurosensory epithelium of the maculae and cristae. These data suggest that calcitonin gene-related peptide—mediated modulation of the afferent vestibular system is functionally important.

Hair-cell counts and afferent innervation patterns in the cristae ampullares of the squirrel monkey with a comparison to the chinchilla

1995 ◽  
Vol 73 (3) ◽  
pp. 1253-1269 ◽  
Author(s):  
C. Fernandez ◽  
A. Lysakowski ◽  
J. M. Goldberg
Keyword(s):  
Squirrel Monkey ◽  
Hair Cells ◽  
Central Zone ◽  
Peripheral Zone ◽  
Nerve Fibers ◽  
Type I ◽  
Type Ii ◽  
Cell Counts ◽  
Afferent Fibers ◽  
Innervation Patterns

1. The numbers of type I and type II hair cells were estimated by dissector techniques applied to semithin, stained sections of the horizontal, superior, and posterior cristae in the squirrel monkey and the chinchilla. 2. The crista in each species was divided into concentrically arranged central, intermediate, and peripheral zones of equal areas. The three zones can be distinguished by the sizes of individual hair cells and calyx endings, by the density of hair cells, and by the relative frequency of calyx endings innervating single or multiple type I hair cells. 3. In the monkey crista, type I hair cells outnumber type II hair cells by a ratio of almost 3:1. The ratio decreases from 4-5:1 in the central and intermediate zones to under 2:1 in the peripheral zone. For the chinchilla, the ratio is near 1:1 for the entire crista and decreases only slightly between the central and peripheral zones. 4. Nerve fibers supplying the cristae in the squirrel monkey were labeled by extracellular injections of horseradish peroxidase (HRP) into the vestibular nerve. Peripheral terminations of individual fibers were reconstructed and related to the zones of the cristae they innervated and to the sizes of their parent axons. Results were similar for the horizontal, superior, and posterior cristae. 5. Axons seldom bifurcate below the neuroepithelium. Most fibers begin branching shortly after crossing the basement membrane. Their terminal arbors are compact, usually extending no more than 50-100 microns from the parent exon. A small number of long intraepithelial fibers enter the intermediate and peripheral zones of the cristae near its base, then run unbranched for long distances through the neuroepithelium to reach the central zone. 6. There are three classes of afferent fibers innervating the monkey crista. Calyx fibers terminate exclusively on type I hair cells, and bouton fibers end only on type II hair cells. Dimorphic fibers provide a mixed innervation, including calyx endings to type I hair cells and bouton endings to type II hair cells. Long intraepithelial fibers are calyx and dimorphic units, whose terminal fields are similar to those of other fibers. The central zone is innervated by calyx and dimorphic fibers; the peripheral zone, by bouton and dimorphic fibers; and the intermediate zone, by all three kinds of fibers. Internal (axon) diameters are largest for calyx fibers and smallest for bouton fibers. Of the entire sample of 286 labeled fibers, 52% were dimorphic units, 40% were calyx units, and 8% were bouton units.(ABSTRACT TRUNCATED AT 400 WORDS)

A delayed rectifier conductance in type I hair cells of the mouse utricle

1996 ◽  
Vol 76 (2) ◽  
pp. 995-1004 ◽  
Author(s):  
A. Rusch ◽  
R. A. Eatock
Keyword(s):  
Hair Cells ◽  
Time Course ◽  
Dissociation Constants ◽  
Resting Potential ◽  
Delayed Rectifier ◽  
Type I ◽  
Type Ii ◽  
Voltage Range ◽  
Average Maximum

1. Membrane currents of hair cells in acutely excised or cultured mouse utricles were recorded with the whole cell voltage-clamp method at temperatures between 23 and 36 degrees C. 2. Type I and II hair cells both had delayed rectifier conductances that activated positive to -55 mV. 3. Type I, but not type II, hair cells had an additional delayed rectifier conductance (gK,L) with an activation range that was unusually negative and variable. At 23-25 degrees C, V(1/2) values ranged from -88 to -62 mV in 57 cells. 4. gK,L was very large. At 23-25 degrees C, the average maximum chord conductance was 75 +/- 65 nS (mean +/- SD, n = 57; measured at -54 mV), or approximately 21 nS/pF of cell capacitance. 5. gK,L was highly selective for K+ over Na+ (permeability ratio PNa+/PK+:0.006), but unlike other delayed rectifiers, gK,L was significantly permeable to Cs+ (PCs+/PK+:0.31). gK,L was independent of extracellular Ca2+. 6. At -64 mV, Ba2+ and 4-aminopyridine blocked gK,L with apparent dissociation constants of 2.0 mM and 43 microM, respectively. Extracellular Cs+ (5 mM) blocked gK,L by 50% at -124 mV. Apamin (100 nM) and dendrotoxin (10 nM) has no effect. 7. The kinetic data of gK,L are consistent with a sequential gating model with at least two closed states and one open state. The slow activation kinetics (principal time constants at 23-25 degrees C:600-200 ms) had a thermal Q10 of 2.1. Inactivation (Q10:2.7) was partial at all temperatures. Deactivation followed a double-exponential time course and had a Q10 of 2.0. 8. At 23-25 degrees C, gK,L was appreciably activated at the mean resting potential of type I hair cells (-77 +/- 3.1 mV, n = 62), so that input conductances were often more than an order of magnitude larger than those of type II cells. If these conditions hold in vivo, type I cells would produce unusually small receptor potentials. Warming the cells to 36 degrees C produced parallel shifts in gK,L's activation range (0.8 +/- 0.3 mV/degrees C, n = 8), and in the resting potential (0.6 +/- 0.3 mV/degrees C, n = 4). Thus the high input conductances were not an artifact of unphysiological temperatures but remained high near body temperature. It remains possible that in vivo gK,L's activation range is less negative and input conductances are lower; the large variance in the voltage range of activation suggests that it may be subject to modulation.

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.

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

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.

scholarly journals Quantal and Nonquantal Transmission in Calyx-Bearing Fibers of the Turtle Posterior Crista

2007 ◽  
Vol 98 (3) ◽  
pp. 1083-1101 ◽  
Author(s):  
Joseph C. Holt ◽  
Shilpa Chatlani ◽  
Anna Lysakowski ◽  
Jay M. Goldberg
Keyword(s):  
Ampa Receptor ◽  
Hair Cells ◽  
Ultrastructural Study ◽  
Nerve Fibers ◽  
Type I ◽  
Outer Face ◽  
Type Ii ◽  
Intracellular Recordings ◽  
External Concentration ◽  
Voltage Gated

Intracellular recordings were made from nerve fibers in the posterior ampullary nerve near the neuroepithelium. Calyx-bearing afferents were identified by their distinctive efferent-mediated responses. Such fibers receive inputs from both type I and type II hair cells. Type II inputs are made by synapses on the outer face of the calyx ending and on the boutons of dimorphic fibers. Quantal activity, consisting of brief mEPSPs, is reduced by lowering the external concentration of Ca2+ and blocked by the AMPA-receptor antagonist CNQX. Poisson statistics govern the timing of mEPSPs, which occur at high rates (250–2,500/s) in the absence of mechanical stimulation. Excitation produced by canal-duct indentation can increase mEPSP rates to nearly 5,000/s. As the rate increases, mEPSPs can change from a monophasic depolarization to a biphasic depolarizing–hyperpolarizing sequence, both of whose components are blocked by CNQX. Blockers of voltage-gated currents affect mEPSP size, which is decreased by TTX and is increased by linopirdine. mEPSP size decreases severalfold after impalement. The size decrease, although it may be triggered by the depolarization occurring during impalement, persists even at hyperpolarized membrane potentials. Nonquantal transmission is indicated by shot-noise calculations and by the presence of voltage modulations after quantal activity is abolished pharmacologically. An ultrastructural study shows that inner-face inputs from type I hair cells outnumber outer-face inputs from type II hair cells by an almost 6:1 ratio.

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