The vestibular nerve of the chinchilla. I. Peripheral innervation patterns in the horizontal and superior semicircular canals

1988 ◽  
Vol 60 (1) ◽  
pp. 167-181 ◽  
Author(s):  
C. Fernandez ◽  
R. A. Baird ◽  
J. M. Goldberg

1. Afferent fibers supplying the horizontal and superior semicircular canals of the chinchilla were labeled by extracellular injections of horseradish peroxidase (HRP) into the vestibular nerve. The arborizations of labeled fibers within the sensory epithelium were reconstructed from serial sections of the crista. 2. The sensory epithelium of the crista can be divided into central, intermediate, and peripheral zones of approximately equal areas. The three zones can be distinguished in normal material by the density of hair cells and by the morphology of calyx endings. 3. Labeled fibers supply either the canalicular or the utricular side of the crista. Axons seldom bifurcate below the basement membrane and they begin dividing into their terminal arborizations almost immediately upon entering the sensory epithelium. The arborizations are compact, seldom extending more than 50 micron from the parent axon. 4. Both calyx and bouton endings were labeled. Calyces can be simple or complex. Simple calyces innervate individual hair cells, whereas complex calyces supply two to three adjacent hair cells. Complex calyces are commonly found only in the central zone. Simple calyces and boutons are located in all regions of the epithelium. Calyces emerge from the parent axon or one of its thick branches. Boutons, whether en passant or terminal, are always located on thin processes. 5. Fibers were classified as calyx, bouton, or dimorphic. The first type only has calyx endings, the second only has bouton endings, and the third has both kinds of endings. Dimorphic units make up some 70% of the labeled fibers, bouton units some 20%, and calyx units some 10%. The three fiber types differ in the diameters of their parent axons and in the regions of the crista they supply. Axon diameters are largest for calyx units and smallest for bouton units. Calyx units are concentrated in the central zone of the crista, whereas bouton units are largely confined to the peripheral zone. Dimorphic units are seen throughout the sensory epithelium. 6. Calyx units are almost always unbranched and end as simple calyces or, less often, as complex calyces. The terminal arbors of bouton units consist of fine processes containing 15-80 endings. Dimorphic units vary in complexity from fibers with a single calyx and a few boutons to those with one to four calyces and more than 50 boutons. 7. The results emphasize the importance of dimorphic units, which were the most numerous type of afferent fiber labeled in this study and were the only units found to innervate all regions of the sensory epithelium.(ABSTRACT TRUNCATED AT 400 WORDS)

1990 ◽  
Vol 63 (4) ◽  
pp. 767-780 ◽  
Author(s):  
C. Fernandez ◽  
J. M. Goldberg ◽  
R. A. Baird

1. Nerve fibers supplying the utricular macula of the chinchilla were labeled by extracellular injection of horseradish peroxidase into the vestibular nerve. The peripheral terminations of individual fibers were reconstructed and related to the regions of the end organ they innervated and to the sizes of their parent axons. 2. The macula is divided into medial and lateral parts by the striola, a narrow zone that runs for almost the entire length of the sensory epithelium. The striola can be distinguished from the extrastriolar regions to either side of it by the wider spacing of its hair cells. Calyx endings in the striola have especially thick walls, and, unlike similar endings in the extrastriola, many of them innervate more than one hair cell. The striola occupies 10% of the sensory epithelium; the lateral extrastriola, 50%; and the medial extrastriola, 40%. 3. The utricular nerve penetrates the bony labyrinth anterior to the end organ. Axons reaching the anterior part of the sensory epithelium run directly through the connective tissue stroma. Those supplying more posterior regions first enter a fiber layer located at the bottom of the stroma. Approximately one-third of the axons bifurcate below the epithelium, usually within 5-20 microns of the basement membrane. Bifurcations are more common in fibers destined for the extrastriola than for the striola. 4. Both calyx and bouton endings were labeled. Calyces can be simple or complex. Simple calyces innervate individual hair cells, whereas complex calyces supply 2-4 adjacent hair cells. Complex endings are more heavily concentrated in the striola than in the extrastriola. Simple calyces and boutons are found in all parts of the epithelium. Calyces emerge from the parent axon or one of its thick branches. Boutons, whether en passant or terminal, are located on thin collaterals. 5. Fibers can be classified into calyx, bouton, or dimorphic categories. The first type only has calyx endings; the second, only bouton endings; and the third, both kinds of endings. Calyx units make up 6% of the labeled fibers, bouton units less than 2%, and dimorphic units greater than 92%. The three fiber types differ in the macular zones they supply and in the diameters of their parent axons. Calyx units were restricted to the striola. The few bouton units were found in the extrastriola.(ABSTRACT TRUNCATED AT 400 WORDS)


1997 ◽  
Vol 78 (6) ◽  
pp. 3234-3248 ◽  
Author(s):  
I. M. Purcell ◽  
A. A. Perachio

Purcell, I. M. and A. A. Perachio. Three-dimensional analysis of vestibular efferent neurons innervating semicircular canals of the gerbil. J. Neurophysiol. 78: 3234–3248, 1997. Anterograde labeling techniques were used to examine peripheral innervation patterns of vestibular efferent neurons in the crista ampullares of the gerbil. Vestibular efferent neurons were labeled by extracellular injections of biocytin or biotinylated dextran amine into the contralateral or ipsilateral dorsal subgroup of efferent cell bodies (group e) located dorsolateral to the facial nerve genu. Anterogradely labeled efferent terminal field varicosities consist mainly of boutons en passant with fewer of the terminal type. The bouton swellings are located predominately in apposition to the basolateral borders of the afferent calyces and type II hair cells, but several boutons were identified close to the hair cell apical border on both types. Three-dimensional reconstruction and morphological analysis of the terminal fields from these cells located in the sensory neuroepithelium of the anterior, horizontal, and posterior cristae were performed. We show that efferent neurons densely innervate each end organ in widespread terminal fields. Subepithelial bifurcations of parent axons were minimal, with extensive collateralization occurring after the axons penetrated the basement membrane of the neuroepithelium. Axonal branching ranged between the 6th and 27th orders and terminal field collecting area far exceeds that of the peripheral terminals of primary afferent neurons. The terminal fields of the efferent neurons display three morphologically heterogeneous types: central, peripheral, and planum. All cell types possess terminal fields displaying a high degree of anisotropy with orientations typically parallel to or within ±45° of the longitudinal axis if the crista. Terminal fields of the central and planum zones predominately project medially toward the transverse axis from the more laterally located penetration of the basement membrane by the parent axon. Peripheral zone terminal fields extend predominately toward the planum semilunatum. The innervation areas of efferent terminal fields display a trend from smallest to largest for the central, peripheral, and planum types, respectively. Neurons that innervate the central zone of the crista do not extend into the peripheral or planum regions. Conversely, those neurons with terminal fields in the peripheral or planum regions do not innervate the central zone of the sensory neuroepithelium. The central zone of the crista is innervated preferentially by efferent neurons with cell bodies located in the ipsilateral group e. The peripheral and planum zones of the crista are innervated preferentially by efferent neurons with cell bodies located in the contralateral group e. A model incorporating our anatomic observations is presented describing an ipsilateral closed-loop feedback between ipsilateral efferent neurons and the periphery and an open-loop feed-forward innervation from contralateral efferent neurons. A possible role for the vestibular efferent neurons in the modulation of semicircular canal afferent response dynamics is proposed.


2000 ◽  
Vol 83 (5) ◽  
pp. 2740-2756 ◽  
Author(s):  
S. Masetto ◽  
P. Perin ◽  
A. Malusà ◽  
G. Zucca ◽  
P. Valli

The electrophysiological properties of developing vestibular hair cells have been investigated in a chick crista slice preparation, from embryonic day 10 ( E10) to E21 (when hatching would occur). Patch-clamp whole-cell experiments showed that different types of ion channels are sequentially expressed during development. An inward Ca2+ current and a slow outward rectifying K+current ( I K(V)) are acquired first, at or before E10, followed by a rapid transient K+current ( I K(A)) at E12, and by a small Ca-dependent K+ current ( I KCa) at E14. Hair cell maturation then proceeds with the expression of hyperpolarization-activated currents: a slow I h appears first, around E16, followed by the fast inward rectifier I K1around E19. From the time of its first appearance, I K(A) is preferentially expressed in peripheral ( zone 1) hair cells, whereas inward rectifying currents are preferentially expressed in intermediate ( zone 2) and central ( zone 3) hair cells. Each conductance conferred distinctive properties on hair cell voltage response. Starting from E15, some hair cells, preferentially located at the intermediate region, showed the amphora shape typical of type I hair cells. From E17 (a time when the afferent calyx is completed) these cells expressed I K, L, the signature current of mature type I hair cells. Close to hatching, hair cell complements and regional organization of ion currents appeared similar to those reported for the mature avian crista. By the progressive acquisition of different types of inward and outward rectifying currents, hair cell repolarization after both positive- and negative-current injections is greatly strengthened and speeded up.


2000 ◽  
Vol 83 (3) ◽  
pp. 1202-1223 ◽  
Author(s):  
Alan M. Brichta ◽  
Jay M. Goldberg

The turtle posterior crista consists of two hemicristae. Each hemicrista extends from the planum semilunatum to the nonsensory torus and includes a central zone (CZ) surrounded by a peripheral zone (PZ). Type I and type II hair cells are found in the CZ and are innervated by calyx, dimorphic and bouton afferents. Only type II hair cells and bouton fibers are found in the PZ. Units were intraaxonally labeled in a half-head preparation. Bouton (B) units could be near the planum (BP), near the torus (BT), or in midportions of a hemicrista, including the PZ and CZ. Discharge properties of B units vary with longitudinal position in a hemicrista but not with morphological features of their peripheral terminations. BP units are regularly discharging and have small gains and small phase leads re angular head velocity. BT units are irregular and have large gains and large phase leads. BM units have intermediate properties. Calyx (C) and dimorphic (D) units have similar discharge properties and were placed into a single calyx-bearing (CD) category. While having an irregular discharge resembling BT units, CD units have gains and phases similar to those of BM units. Rather than any single discharge property, it is the relation between discharge regularity and either gain or phase that makes CD units distinctive. Multivariate statistical formulas were developed to infer a unit's morphological class (B or CD) and longitudinal position solely from its discharge properties. To verify the use of the formulas, discharge properties were compared for units recorded intraaxonally or extracellularly in the half-head or extracellularly in intact animals. Most B units have background rates of 10–30 spikes/s. The CD category was separated into CD-high and CD-low units with background rates above or below 5 spikes/s, respectively. CD-low units have lower gains and phases and are located nearer the planum than CD-high units. In their response dynamics over a frequency range from 0.01–3 Hz, BP units conform to an overdamped torsion-pendulum model. Other units show departures from the model, including high-frequency gain increases and phase leads. The longitudinal gradient in the physiology of turtle B units resembles a similar gradient in the anamniote crista. In many respects, turtle CD units have discharge properties resembling those of calyx-bearing units in the mammalian central zone.


2005 ◽  
Vol 93 (1) ◽  
pp. 267-280 ◽  
Author(s):  
Sapan S. Desai ◽  
Hussain Ali ◽  
Anna Lysakowski

We made flattened neuroepithelial preparations of horizontal and vertical (anterior and posterior) cristae from mouse, rat, gerbil, guinea pig, chinchilla, and tree squirrel. Calretinin immunohistochemistry was used to label the calyx class of afferents. Because these afferents are restricted to the central zone of the crista, their distribution allowed us to delineate this zone. In addition to calyx afferents, calretinin also labels ∼5% of type I hair cells and 20% of type II hair cells throughout the mouse and rat crista epithelium. Measurements of the dimensions of the cristae and counts of hair cells and calyx afferents were determined on all species. Numbers of calyx afferents, hair cells, area, length, and width of the sensory epithelium increase from mouse to tree squirrel. As in the companion paper, we obtained additional data on vestibular end organ dimensions from the literature to construct a power law function describing the relationship between crista surface area and body weight. The vertical cristae of the mouse, rat, and gerbil have an eminentia cruciatum, a region located transversely along the midpoint of the sensory organ and consisting of nonsensory cells. Apart from this eminentia cruciatum, there are no statistical differences between horizontal and vertical cristae with regard to area, width, length, the number and type of hair cells, and number of calretinin-labeled calyx afferents.


1995 ◽  
Vol 73 (3) ◽  
pp. 1253-1269 ◽  
Author(s):  
C. Fernandez ◽  
A. Lysakowski ◽  
J. M. Goldberg

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)


2021 ◽  
Author(s):  
Jing-cui Qi ◽  
Qing-qing Jiang ◽  
Long Ma ◽  
Shuo-long Yuan ◽  
Wei Sun ◽  
...  

Abstract Background:. Pathological changes of the cochlea and hearing loss have been well addressed in Waardenburg syndrome (WS). However, the vestibular organ malformation in WS is still largely unknown. In this study, the differentiation and development of vestibular sensory epithelium and vestibular function caused by SOX10 mutation, a critical gene induces WS, has been studied in minature pig model. Results: Degeneration of vestibular hair cells was found in this Sox10 mutation porcine model. Inner ear phenotype of the SOX10+/R109W miniature pigs showed cochlear abnormalities as well as saccular hypofunction. In the mutant pigs, no prominent dissimilarity was shown in the bone structure of the semicircular canals. However, the saccular membrane was collapsed and the infusion of stereocilia of the hair cells were observed. There was no dark cells in the uticules in th mutant pigs. The density of the utricular hair cells was also significantly lower in the mutant pigs compared to the wild type. Conclusions: Our study demonstrated that the SOX10 gene and melanocytes play important roles in the vestibular organ development. Sox10 mutation disrupts the KIT-DCT signaling pathway, affects the development of melanocytes and leads to vestibule morphogenesis.


2002 ◽  
Vol 88 (6) ◽  
pp. 3259-3278 ◽  
Author(s):  
Alan M. Brichta ◽  
Anne Aubert ◽  
Ruth Anne Eatock ◽  
Jay M. Goldberg

The turtle posterior crista is made up of two hemicristae, each consisting of a central zone containing type I and type II hair cells and a surrounding peripheral zone containing only type II hair cells and extending from the planum semilunatum to the nonsensory torus. Afferents from various regions of a hemicrista differ in their discharge properties. To see if afferent diversity is related to the basolateral currents of the hair cells innervated, we selectively harvested type I and II hair cells from the central zone and type II hair cells from two parts of the peripheral zone, one near the planum and the other near the torus. Voltage-dependent currents were studied with the whole cell, ruptured-patch method and characterized in voltage-clamp mode. We found regional differences in both outwardly and inwardly rectifying voltage-sensitive currents. As in birds and mammals, type I hair cells have a distinctive outwardly rectifying current ( IK,L), which begins activating at more hyperpolarized voltages than do the outward currents of type II hair cells. Activation of IK,Lis slow and sigmoidal. Maximal outward conductances are large. Outward currents in type II cells vary in their activation kinetics. Cells with fast kinetics are associated with small conductances and with partial inactivation during 200-ms depolarizing voltage steps. Almost all type II cells in the peripheral zone and many in the central zone have fast kinetics. Some type II cells in the central zone have large outward currents with slow kinetics and little inactivation. Although these currents resemble IK,L, they can be distinguished from the latter both electrophysiologically and pharmacologically. There are two varieties of inwardly rectifying currents in type II hair cells: activation of IK1is rapid and monoexponential, whereas that of Ihis slow and sigmoidal. Many type II cells either have both inward currents or only have IK1; very few cells only have Ih. Inward currents are less conspicuous in type I cells. Type II cells near the torus have smaller outwardly rectifying currents and larger inwardly rectifying currents than those near the planum, but the differences are too small to account for variations in discharge properties of bouton afferents innervating the two regions of the peripheral zone. The large outward conductances seen in central cells, by lowering impedances, may contribute to the low rotational gains of some central-zone afferents.


1988 ◽  
Vol 60 (1) ◽  
pp. 182-203 ◽  
Author(s):  
R. A. Baird ◽  
G. Desmadryl ◽  
C. Fernandez ◽  
J. M. Goldberg

1. The relation between the response properties of semicircular canal afferents and their peripheral innervation patterns was studied by the use of intra-axonal labeling techniques. Fifty physiologically characterized units were injected with horseradish peroxidase (HRP) or Lucifer yellow CH (LY) and their processes were traced to the crista. The resting discharge, discharge regularity, and responses to both externally applied galvanic currents and sinusoidal head rotations were determined for most neurons. Terminal fields were reconstructed and, as in the preceding paper, the fibers were classified as calyx, bouton, or dimorphic units. 2. To determine if the intra-axonal sample was representative, the physiological properties of the labeled units were compared with those of a sample of extracellularly recorded units. A comparison was also made between the morphology of the intra-axonal units and those labeled by extracellular injection of HRP into the vestibular nerve Most of the discrepancies between the intra-axonal and the two extracellular samples can be explained by assuming that small-diameter fibers are underrepresented in the former sample. 3. A normalized coefficient of variation (CV*), independent of discharge rate, was used to classify units as regular, intermediate, or irregular. The CV* ranged from 0.020 to 0.60. Regular units (CV* less than or equal to 0.10) outnumbered irregular units (CV* greater than or equal to 0.20) by an approximately 3:1 ratio and had higher resting discharges. 4. Calyx units were invariably irregular. The one recovered bouton unit was regular. The discharge regularity of dimorphic units was related to their epithelial location, with those found in the periphery of the crista having a more regular discharge than those located more centrally. Dimorphic units, even those with quite similar morphology, can differ in their discharge regularity. Calyx and dimorphic units, which differ in their morphology, can both be irregular. These observations imply that discharge regularity is not determined by the branching pattern of a fiber or the number and types of hair cells it contacts. 5. The galvanic sensitivity (beta*) of an afferent, irrespective of its peripheral innervation pattern, was strongly correlated with CV*. This is consistent with the notion that discharge regularity and galvanic sensitivity are causally related, both being determined by postspike recovery mechanisms of the afferent nerve terminal.(ABSTRACT TRUNCATED AT 400 WORDS)


1998 ◽  
Vol 107 (3) ◽  
pp. 207-212
Author(s):  
Darin L. Wright ◽  
Richard R. Gacek ◽  
Joanne E. Schoonmaker

The vestibular nerve is composed of fibers with a wide spectrum of diameters. The fibers of largest diameter are known to innervate the type I hair cells of the cristae, while the small-diameter fibers innervate the type II hair cells. Midsized fibers (dimorphic fibers) represent neurons that innervate both type I and type II hair cells. Reports by others have commented on the tendency for clustering of fibers with like diameters. Rigorous statistical proof for or against clustering has not yet been presented. The explanation for this is, in part, the mathematic complexity of analyzing clustering in a system composed of three elements. We report a new method for analysis of fiber clustering and apply this method to large-, medium-, and small-diameter fibers in the feline vestibular nerve. The fiber grouping in the caudal and rostral ends of the vestibular nerves of six normal animals is compared to that in similar areas of the nerves of five animals 12 to 17 months after unilateral labyrinthectomy. No statistically significant clustering of fiber types was found in the rostral portion of either the control or the labyrinthectomized animals. In the caudal portion of the control nerves, clustering of the large fibers was demonstrated (p <.005, χ2 test). This clustering was not demonstrated after labyrinthectomy. An explanation of these findings is discussed. The method used in this study to analyze fiber clustering may be applicable to other nerve systems of greater complexity.


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