Extrastriolar Regions Research Articles

Peripheral innervation patterns of vestibular nerve afferents in the bullfrog utriculus.

Vestibular nerve afferents innervating the bullfrog utriculus differ in their response dynamics and sensitivity to natural stimulation. They also supply hair cells that differ markedly in hair bundle morphology. To examine the peripheral innervation patterns of individual utricular afferents more closely, afferent fibers were labeled by the extracellular injection of horseradish peroxidase (HRP) into the vestibular nerve after sectioning the vestibular nerve medial to Scarpa's ganglion to allow the degeneration of sympathetic and efferent fibers. The peripheral arborizations of individual afferents were then correlated with the diameters of their parent axons, the regions of the macula they innervate, and the number and type of hair cells they supply. The utriculus is divided by the striola, a narrow zone of distinctive morphology, into medial and lateral parts. Utricular afferents were classified as striolar or extrastriolar according to the epithelial entrance of their parent axons and the location of their terminal fields. In general, striolar afferents had thicker parent axons, fewer subepithelial bifurcations, larger terminal fields, and more synaptic endings than afferents in extrastriolar regions. Afferents in a juxtastriolar zone, immediately adjacent to the medial striola, had innervation patterns transitional between those in the striola and more peripheral parts of the medial extrastriola. Most afferents innervated only a single macular zone. The terminal fields of striolar afferents, with the notable exception of a few afferents with thin parent axons, were generally confined to one side of the striola. Hair cells in the bullfrog utriculus have previously been classified into four types based on hair bundle morphology (Lewis and Li: Brain Res. 83:35-50, 1975). Afferents in the extrastriolar and juxtastriolar zones largely or exclusively innervated Type B hair cells, the predominant hair cell type in the utricular macula. Striolar afferents supplied a mixture of four hair cell types, but largely contacted Type B and Type C hair cells, particularly on the outer rows of the medial striola. Afferents supplying more central striolar regions innervated fewer Type B and large numbers of Type E and Type F hair cells. Striolar afferents with thin parent axons largely supplied Type E hair cells with bulbed kinocilia in the innermost striolar rows.

Comparative transduction mechanisms of hair cells in the bullfrog utriculus. I. Responses to intracellular current

1. Hair cells in whole-mount in vitro preparations of the utricular macula of the bullfrog (Rana catesbeiana) were selected according to their macular location and hair bundle morphology. The voltage responses of selected hair cells to intracellular current steps and sinusoids in the frequency range of 0.5-200 Hz were studied with conventional intracellular recordings. 2. The utricular macula is divided into medial and lateral parts by the striola, a 75- to 100-microns zone that runs for nearly the entire length of the sensory macula near its lateral border. The striola is distinguished from flanking extrastriolar regions by the elevated height of its apical surface and the wider spacing of its hair cells. A line dividing hair cells of opposing polarities, located near the lateral border of the striola, separates it into medial and lateral parts. On average, the striola consists of five to seven medial and two to three lateral rows of hair cells. 3. Utricular hair cells were classified into four types on the basis of hair bundle morphology. Type B cells, the predominant hair cell type in the utricular macula, are small cells with short sterocilia and kinocilia 2-6 times as long as their longest stereocilia. These hair cells were found throughout the extrastriola and, more rarely, in the striolar region. Three other hair cell types were restricted to the striolar region. Type C cells, found primarily in the outer striolar rows, resemble enlarged versions of Type B hair cells. Type F cells have kinocilia approximately equal in length to their longest stereocilia and are restricted to the middle striolar rows. Type E cells, found only in the innermost striolar rows, have short kinocilia with prominent kinociliary bulbs. 4. The resting potential of 99 hair cells was -58.0 +/- 7.6 (SD) mV and did not vary significantly for hair cells in differing macular locations or with differing hair bundle morphology. The RN of hair cells, measured from the voltage response to current steps, varied from 200 to > 2,000 M omega and was not well correlated with cell size. On average, Type B cells had the highest RN, followed by Type F, Type E, and Type C cells. When normalized to their surface area, the membrane resistance of hair cells ranged from < 1,000 to > 10,000 k omega.cm2. The input capacitance of hair cells ranged from < 3 to > 15 pA, corresponding on average to a membrane capacitance of 0.8 +/- 0.2 pA/cm2.(ABSTRACT TRUNCATED AT 400 WORDS)

Distribution of the 275 kD hair cell antigen and cell surface specialisations on auditory and vestibular hair bundles in the chicken inner ear.

The 275 kD hair cell antigen (HCA) is a protein that is specifically associated with the apical surface of sensory hair cells in the chick inner ear. A comparative study of the vestibular and auditory organs of the inner ear, using both wholemounts and cryosections double labelled for the HCA and F-actin, reveals that two distinct types of hair cells can be distinguished on the basis of antibody staining in each of the vestibular epithelia. One type of hair cell has the HCA restricted to the base of the stereocilia bundle and is found in the striolae of the maculae and in a large, centrally located region of each ampulla. The other type of hair cell is found in the extrastriolar regions of the maculae and the peripheral regions of the ampullae and has the HCA distributed over the entire surface of the stereocilia bundle. In the basilar papilla, the auditory epithelium of the chick inner ear, the HCA is, as in the striolar regions of the maculae, restricted to the base of the hair bundles. In all sensory epithelia the HCA is also present on the apical, nonstereociliary surface of the hair cells. Ultrastructural examination of the basilar papilla and the striolar and the extrastriolar regions of the lagenar macula after staining with ruthenium red and tannic acid shows that there are four morphologically different types of interstereociliary connectors (oblique tip connectors, horizontal tip connectors, shaft connectors and basal connectors) associated with the hair bundles. Oblique tip connectors and basal connectors are found on hair cells from all regions and have a similar distribution. Horizontal tip connectors are seen only on hair cells in the basilar papilla and the striolar region of the lagenar macula. Shaft connectors extend all the way to the tips of extrastriolar hair cell bundles, but extend only a short way up the bundles of hair cells in the basilar papilla and striolar region of the lagenar macula. Immunogold labelling confirms the results obtained with immunofluorescence microscopy and demonstrates that the distribution of the HCA on the surface of adjacent stereocilia correlates closely with that of the shaft connectors; i.e., immunostaining is observed up to the tips of the extrastriolar hair cell bundles, but is restricted to the lower regions of hair cell bundles in the striolar region and basilar papilla.(ABSTRACT TRUNCATED AT 400 WORDS)

Heterogeneity of sensory hair cells in a fish ear.

The ultrastructure of sensory hair cells in the utricle of the cichlid fish, Astronotus ocellatus, the oscar, was studied by transmission electron microscopy of serial ultrathin sections from different regions of the epithelium. Two distinctly different types of hair cell were found, one located in the striolar region of the epithelium and the other in the extrastriolar region. Striolar hair cells have a well-defined perinuclear cisterna located just below the nucleus, and large perinuclear mitochondria. Synaptic bodies of striolar cells are small and located in clusters, while those in extrastriolar cells are relatively large and individually dispersed. The extrastriolar hair cell closely resembles the amniote type II hair cell. On the basis of these data, and consistent with earlier studies, it appears that the striolar hair cells closely resemble amniote type I hair cells in many significant ways. Thus we have called them type I-like cells. The extrastriolar hair cells appear to be typical of eighth nerve mechanoreceptors commonly described for fish and closely resemble the amniote type II hair cell.

The vestibular nerve of the chinchilla. III. Peripheral innervation patterns in the utricular macula

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)