Stereovillar Bundles Research Articles

Current concepts of hair cell differentiation and planar cell polarity in inner ear sensory organs.

Phylogenetically and ontogenetically, vertebrate development led to the generation of several inner ear sensory organs. During embryogenesis, cell fate specification determines whether each progenitor cell differentiates into a sensory hair cell or a supporting cell within the common sensory primordium. Finally, all sensory epithelia of the inner ear consist of a hair cell/supporting cell mosaic, albeit with anatomical differences depending on the sensory organ type. Hair cells develop a polarized bundle of stereovilli that is of functional importance for mechanotransduction. After initiating stereovillar development, hair cells align their bundles in a coordinated fashion, generating a characteristic hair cell orientation pattern, a process referred to as planar cell polarity (PCP). The pathway that controls PCP in the inner ear needs both to establish the development of a polarized morphology of the stereovillar bundle of the hair cell and to organize a systematic hair cell alignment. Because the hair cell orientation patterns of the various inner ear organs and vertebrate species differ fundamentally, it becomes apparent that in vertebrates, different aspects of PCP need to be independently controlled. In spite of important progress recently gained in the field of PCP research, we still need to identify the mechanisms (1) that initiate molecular asymmetries in cells, (2) that guide the transmission of polarity information from cell to cell, and (3) that consistently translate such polarity information into morphological asymmetries of hair cells.

Inner-Ear Morphology of the New Zealand Kiwi (Apteryx mantelli) Suggests High-Frequency Specialization

The sensory systems of the New Zealand kiwi appear to be uniquely adapted to occupy a nocturnal ground-dwelling niche. In addition to well-developed tactile and olfactory systems, the auditory system shows specializations of the ear, which are maintained along the central nervous system. Here, we provide a detailed description of the auditory nerve, hair cells, and stereovillar bundle orientation of the hair cells in the North Island brown kiwi. The auditory nerve of the kiwi contained about 8,000 fibers. Using the number of hair cells and innervating nerve fibers to calculate a ratio of average innervation density showed that the afferent innervation ratio in kiwi was denser than in most other birds examined. The average diameters of cochlear afferent axons in kiwi showed the typical gradient across the tonotopic axis. The kiwi basilar papilla showed a clear differentiation of tall and short hair cells. The proportion of short hair cells was higher than in the emu and likely reflects a bias towards higher frequencies represented on the kiwi basilar papilla. The orientation of the stereovillar bundles in the kiwi basilar papilla showed a pattern similar to that in most other birds but was most similar to that of the emu. Overall, many features of the auditory nerve, hair cells, and stereovilli bundle orientation in the kiwi are typical of most birds examined. Some features of the kiwi auditory system do, however, support a high-frequency specialization, specifically the innervation density and generally small size of hair-cell somata, whereas others showed the presumed ancestral condition similar to that found in the emu.

Lizard ears and simple solutions to auditory coding.

The variety of lizard auditory organs provides an optimal substrate for examining structure‐function relationships. What does an auditory organ need to perform the basic tasks in the coding of acoustic stimuli? The single‐ossicle tympanic middle ears of lizards are connected through the head, providing for sensitive directional hearing with little neural processing. Lizards evolved hair cells whose frequency responses were determined by the morphological details of their stereovillar bundles and tectorial material, enabling a tonotopic arrangement of frequency sensitivity. Modern lizards achieve this with few hair‐cell rows, showing that tonotopicity does not demand an extensive epithelium. Finally, different lizard families achieved dissimilar frequency selectivity through manipulations of anatomical features, especially of the tectorial membrane. There is a pay‐off between the size of the auditory papilla and its ability to code different frequencies. Long papillae allow very local coupling of hair‐cell bundles with very selective frequency tuning. Short papillae generally abandon tectorial coupling to allow for useful tuning but this results in poorer sensitivity and poorer tuning selectivity. Lizards demonstrate that sensitive and selective hearing organs need only a few hundred hair‐cells organized along a straight axis. [work supported by the German Research Foundation DFG (MA 871‐10.)]

What have lizard ears taught us about auditory physiology?

The structure of the basilar papilla of the inner ear of lizards is the most diverse among all vertebrates. Research on a variety of lizard ears, animals that are remarkably robust under laboratory conditions, has provided the field of auditory research with valuable information, particularly on the minimum structural requirements for sensitive, selective hearing and on the importance of the tectorial membrane and active processes in this regard. Despite the absence of a tuned basilar membrane, lizard ears produce highly frequency selective hearing through micromechanical tuning of small, resonant hair-cell-tectorial units or of free-standing hair bundles. These units are driven by an active process that also underlies spontaneous and other otoacoustic emissions. Lizard ears provided the first in vivo evidence that the active process is calcium-sensitive and lies within the stereovillar bundles of the hair cells.

Spontaneous otoacoustic emissions from free-standing stereovillar bundles of ten species of lizard with small papillae

Spontaneous otoacoustic emissions (SOAE) were measured in 10 lizard species from the families Iguanidae, Agamidae and Anguidae. The typical feature of these papillae is that the hair cells in the higher-frequency papillar regions that produce SOAE are not covered by a tectorial structure. The number of hair cells in the species used here was between 58 and 292 per ear. SOAE could be measured from all species, but some of their characteristics varied with papillar anatomy. Thus very small papillae produced fewer and smaller SOAE than larger papillae.

In vivo evidence for a cochlear amplifier in the hair-cell bundle of lizards.

Vertebrate sensory hair cells achieve high sensitivity and frequency selectivity by adding self-generated mechanical energy to low-level signals. This allows them to detect signals that are smaller than thermal molecular motion and to achieve significant resonance amplitudes and frequency selectivity despite the viscosity of the surrounding fluid. In nonmammals, a great deal of in vitro evidence indicates that the active process responsible for this amplification is intimately associated with the hair cells' transduction channels in the stereovillar bundle. Here, we provide in vivo evidence of hair-cell bundle involvement in active processes. Electrical stimulation of the inner ear of a lizard at frequencies typical for this hearing organ induced low-level otoacoustic emissions that could be modulated by low-frequency sound. The unique modulation pattern permitted the tracing of the active process involved to the stereovillar bundles of the sensory hair cells. This supports the notion that, in nonmammals, the cochlear amplifier in the hair cells is driven by a bundle motor system.

Otoacoustic emissions, hair cells, and myosin motors.

The stereovillar bundles of hair cells show active movements that may be generated by the putative myosin-actin interactions underlying hair-cell adaptation. Such movement is a possible candidate for the generation of spontaneous otoacoustic emissions (SOAE) in the ear canal of nonmammals. In the basilar papilla of certain lizard families, most hair cells are not coupled by a tectorial membrane, making it easier to assign the energy in emission peaks to defined groups of hair cells. We have studied 62 SOAE in the Bahamian Anole Anolis sagrei, which has about 140 hair cells with "free-standing" bundles in the high-frequency area of its papilla. Individual SOAE peaks were traced to between 3 and 38 hair cells, and the mean power output per hair cell was calculated to be 141 aW. The number of bundle myosins putatively involved in the generation of each SOAE was estimated and the force generated by each myosin at 1 kHz calculated to be approximately 0.1 pN. The data support the idea that hair cells generate emissions and suggest that myosin produces sufficient power to be the emission motor.

Quantitative anatomical basis for a model of micromechanical frequency tuning in the Tokay gecko, Gekko gecko

The basilar papilla of the Tokay gecko was studied with standard light- and scanning electron microscopy methods. Several parameters thought to be of particular importance for the mechanical response properties of the system were quantitatively measured, separately for the three different hair-cell areas that are typical for this lizard family. In the basal third, papillar structure was very uniform. The apical two-thirds are subdivided into two hair-cell areas running parallel to each other along the papilla and covered by very different types of tectorial material. Both of those areas showed prominent gradients in hair-cell bundle morphology, i.e., in the height of the stereovillar bundles and the number of stereovilli per bundle, as well as in hair cell density and the size of their respective tectorial covering. Based on the direction of the observed anatomical gradients, a ‘reverse’ tonotopic organization is suggested, with the highest frequencies represented at the apical end.

Mechanical and electromechanical properties of the stereovillar bundles of isolated and cultured hair cells of the chicken

Isolated single chicken hair cells and pieces of epithelium without the tectorial membrane, either freshly isolated or in tissue culture, were studied using water-jet stimulation of their stereovillar bundles and current injection. Responses were measured under enhanced video-microscopic observation or while using a differential photodiode technique sensitive down into the nanometer range. When stimulated with a water jet at low displacement amplitudes up to about 200 nm, the stereovillar bundle displacement was asymmetrical, indicating a lower stiffness in the excitatory direction, but the reverse was true at higher displacement amplitudes. Undamaged bundles showed no mechanical resonances below 1 kHz. In damaged bundles, however, such resonances were prominent and accompanied by splaying of the stereovilli. Hair cells in the epithelium showed small bundle movements (0.6 nm/mV) whose polarity depended on the polarity of the injected current. These movements probably resulted from activation of the bundle's adaptation motors.

The cuticular plate of the hair cell in relation to morphological gradients of the chicken basilar papilla

The aim of the present study was to provide details on the diversity and morphological gradients in the anatomy of the cuticular plate of.hair cells in the chicken basilar papilla. The structure of the cuticular plate, which is mainly made up of a network of actin filaments, may be related to differences in the mechanical demands on the anchorage of the stereovillar bundle. We describe the morphological gradients in the cuticular plates as seen in transverse section for four positions along the basilar papilla. Three different shapes of cuticular plate could be distinguished. In general, cuticular plates in neurally-lying hair cells have their main mass on the neural side of the cells; for abneural cells, the converse is true. The shape of the plates changes gradually across the papilla; symmetrical forms exist. The hair-cell bundle orientation (and thus the preferred direction of stimulation of the bundle), as measured using scanning EM preparations, does not correlate with the shape of the plate in transverse section. The present data confirm the notion developed from other studies that (1) there are no distinct populations of hair cells, (2) there are no linear or monotonie morphological gradients, and (3) the gradients on the papilla are species- and position-specific.

Morphology of the basilar papilla of the bobtail lizard Tiliqua rugosa

The morphology of the basilar papilla of the bobtail lizard was investigated with standard light- and scanning-electron-microscopical methods. The papilla can be subdivided into two parts: a small apical segment which is rather uniform in structure and a long basal segment which displays various systematic changes along its length, for example in the density of the hair cells, the height and shape of the hair-cell stereovillar bundles, the number of stereovilli per bundle and the size of the tectorial structure. In addition, the tectorial structures overlying the two segments are very different in size and morphology. Both tectorial structures are probably sensitive to changes in their ionic environment. The possible functional implications of the papular morphology described here are discussed with respect to a model of frequency tuning in the bobtail lizard.

The basilar papilla of the barn owl Tyto alba: A quantitative morphological SEM analysis

The barn owl has the longest basilar papilla (about 12 mm) of all bird species studied. In the apical half several morphological parameters change regularly: stereovillar number per hair cell, length of the stereovillar bundle and cell surface area decrease from basal to apical. Cell number across the papilla, width of stereovillar bundle, diameter of a single stereovillus and height of stereovilli increase in the same direction. The orientation of the stereovillar bundles' long axis is parallel (0°) to the edges of the papilla at the neural and the abneural sides, whereas along the midline there is a zone with an orientation of 50 ° towards the apex; apically, this change in orientation may increase up to 90°. In the basal half of the owl papilla the situation is different: most parameters are fairly constant, e.g. stereovillar height, mean orientation of stereovillar bundles (0 °), bundle shape and stereovillar number per hair cell. As the basilar papilla of birds is known to be tonotopically organized, with the high frequency range being represented basally, the different organization of the basal half of the owl papilla may be a specialization related to the excellent high frequency hearing.