Thomas F. Weiss

Bidirectional transduction in vertebrate hair cells: A mechanism for coupling mechanical and electrical processes

It has been proposed that the sharp frequency selectivity exhibited by cochlear hair cells and neurons of alligator lizards results from a mechanical resonance of the stereociliary-tectorial structures of hair cells. In contrast, in the red-eared turtle this selectivity has been attributed to an electrical resonance mechanism located in the hair-cell membrane. In this report a new mechanism is proposed, one which is consistent with observations in the lizard and turtle preparations and in which hair-cell resonances result from coupling of mechanical properties of hair-cell stereociliary-tectorial structures with electrical properties of the hair-cell membrane through a receptor membrane process that has bidirectional, mechanoelectric and electromechanical, transduction properties. This same mechanism could also be the physical basis for diverse phenomena observed in mammals, including changes in mechanical properties of the ear in response to electrical stimulation in the cochlea and central nervous system, and the presence of sustained, narrow-band, acoustic emissions in the ear canals of humans.

Intracellular responses to acoustic clicks in the inner ear of the alligator lizard

Micropipets were used to record electric responses to acoustic clicks in single hair cells and supporting cells in the basilar papilla of the inner ear of the alligator lizard. Intracellular responses were less than 3‐mV peak‐to‐peak and the relation between intracellular response and sound pressure at the tympanic membrane was nonlinear. Two types of intracellular responses to acoustic clicks were identified: type A has a dominant oscillatory component whose polarity is reversed when the polarity of the click is reversed. Type B has a dominant positive component that occurs at the time of the neural (N1) component. In a few cases, the technique of intracellular dye‐marking was used to determine the cellular recording site of these waveforms. We tentatively conclude that type A responses are recorded in hair cells and type B in supporting cells. The initial polarity of the oscillatory component of the response appears to correlate with the morphological polarization of hair cells in the papilla. Fourier t...

Tuning of single fibers in the cochlear nerve of the alligator lizard: relation to receptor morphology.

(1) The general anatomy of the peripheral portion of the cochlear nerve in the alligator lizard is described. (2) Spike discharges of single units were recorded with micropipets placed in the peripheral portion of the cochlear nerve of anesthetized lizards. (3) In response to tone bursts, each unit is maximally sensitive to a charactertistic frequency (CF). There are two distinct populations of units having different CFs: a low CF population (CF in the range 0.2-0.8 kHz) recorded in the portion of the nerve that enters the apical region of the basilar papilla and a high CF population (CF in the range 0.9-4.0 kHz) recorded in the portion of the nerve that enters the basal region. The low CF units are more sharply tuned than the high CF units. (4) Comparison of cochlear nerve units of the alligator lizard with those of mammals shows that the tuning of low CF units resembles that of mammalian units of the same CF. The tuning of high CF lizard units differs significantly from mammalian units. (5) The distinct differences in tuning of low and high CF units are correlated with distinct differences in the structure of the basilar papilla in the apical and basal regions rather than with differences in the width of the basilar membrane.

A comparison of synchronization filters in different auditory receptor organs

Measurements of the frequency dependence of synchronization of cochlear nerve fibers obtained in different auditory receptor organs are compared. These synchronization filter-functions are lowpass filter-functions and differ primarily in corner frequencies which we estimate to be (in kHz): 2.5 (cat), 1.1 (guinea pig), 0.48 (alligator-lizard tectorial fibers), 0.42 (tree frog), and 0.34 (alligator-lizard free-standing fibers). Some of this variation in corner frequency can be explained by temperature-dependent lowpass-filter mechanisms with a temperature factor of 2.6-3.3 for a change in temperature of 10 degrees C. However, factors in addition to temperature must be involved in producing the differences in corner frequency between cat and guinea pig fibers and between tectorial and free-standing fibers in the alligator lizard.

A model of the peripheral auditory system.

SummaryRecent electrophysiological data obtained from auditory nerve fibers of cats have made possible the formulation of a model of the peripheral auditory system that relates the all-or-none activity of these fibers to acoustic stimulation. The components of the model are intended to represent the major functional components of the peripheral system. These components are: (i) a linear mechanical system intended to represent the outer, middle, and mechanical parts of the inner ear; (ii) a transducer intended to represent the action of the sensory cells; and (iii) a model neuron whose properties are intended to represent the nerve excitation process. A general-purpose digital computer has been used to determine the response of the model to a variety of acoustic stimuli. These results have been compared with data obtained from auditory nerve fibers.

A model for signal transmission in an ear having hair cells with free-standing stereocilia. II. Macromechanical stage

Measurements have shown that the sound-induced motion of free-standing stereocilia of hair cells in the alligator lizard cochlea exhibits tonotopically organized frequency selectivity that is correlated with the geometry of the stereociliary tuft. We propose a model in which basilar-membrane motion causes vibration of the receptor organ which drags the stereocilia back and forth through the endolymph. The stereociliary tuft is represented as a rigid rod attached to the cuticular plate by a compliant hinge. Viscous and inertial forces exerted by the endolymph on the rod are computed approximately. A transfer function, H mu(f), is derived that relates rod angular displacement to basilar-membrane velocity. H mu(f) has low- and high-frequency slopes of 10 and -20 dB/decade, respectively. The resonant frequency of H mu(f) depends on the dimensions of the rod because this frequency is inversely proportional to the square root of the product of the moment of inertia of the rod, which depends on rod dimensions, and the compliance of the hinge, which does not. In most respects, measurements of frequency selectivity and tonotopic organization of hair cells and cochlear neurons in the alligator lizard, can be accounted for by an input transfer function, HI(f) = Hm(f)H mu(f)Ha(f), where Hm(f) is the macromechanical transfer function that relates sound pressure at the tympanic membrane to basilar-membrane velocity (Rosowski et al., 1985, Hearing Res. 20, 139-155), and Ha(f) is a first-order lowpass filter. Mechanisms that could produce the additional lowpass filter process are discussed.

Static material properties of the tectorial membrane: a summary

The tectorial membrane (TM) is a polyelectrolyte gel. Hence, its chemical, electrical, mechanical, and osmotic properties are inextricably linked. We review, integrate, and interpret recent findings on these properties in isolated TM preparations. The dimensions of the TM in alligator lizard, chick, and mouse are sensitive to bath ion concentrations of constituents normally present in the cochlear fluids - an increase in calcium concentration shrinks the TM, and an increase in sodium concentration swells the TM in a manner that depends competitively on the calcium concentration. The sodium-induced swelling is specific; it does not occur with other alkali metal cations. We interpret these findings as due to competitive binding of sodium and calcium to TM macromolecules which causes a change in their conformation that leads to a change in mechanical properties. In mouse TM, decreasing the bath pH below 6 or increasing it above 7 results in swelling of the TM. Electric potential measurements are consistent with the notion that the swelling is caused by a pH-driven increase in positive fixed charge at low pH and an increase in the magnitude of the negative fixed charge at high pH which is consistent with the known protonation pattern of TM macromolecules. Increasing the osmotic pressure of the bathing solution with polyethylene glycol shrinks the TM and decreasing the ionic strength of the bathing solution swells the TM. Both results are qualitatively consistent with predictions of a polyelectrolyte gel model of the TM.

Stages of degradation of timing information in the cochlea: A comparison of hair-cell and nerve-fiber responses in the alligator lizard

Responses to clicks and tone bursts of hair cells and nerve fibers in the free-standing region of the alligator lizard cochlea were compared. The objective was to determine the extent to which the hair-cell processes that produce the receptor potential are also responsible for the attenuation of the synchronized responses of nerve fibers. The AC component of the receptor potential of these hair cells has a high-frequency attenuation of 20 dB/decade [Holton and Weiss (1983) J. Physiol. 345, 205-240], whereas the synchronized response of cochlear neurons is attenuated at a rate of least 80 dB/decade [Rose and Weiss (1988) Hear. Res. 33, 151-166]. Therefore, the processes that link the receptor potential to the nerve discharge act as a lowpass filter with a high-frequency attenuation of at least 60 dB/decade. This could be obtained from a cascade of at least three first-order lowpass filter processes.

A model for signal transmission in an ear having hair cells with free-standing stereocilia. IV. Mechanoelectric transduction stage

A model is described for mechanoelectric transduction in hair cells with free-standing stereocilia in the alligator lizard cochlea. The model relates the angular displacement of the stereocilia to the receptor potential in the absence of the hair cells membrane capacitance whose effect is considered elsewhere (Leong and Weiss, 1985, in preparation). The model consists of two parts: a population of membrane ionic channels and an electric network that relates the channel conductance to the equivalent resistance of the hair cell. The membrane ionic channels tend to open when the stereociliary tuft is displaced toward the kinocilium (or basal body) and tend to close when the tuft is oppositely displaced. The fraction of channels that is open for a given tuft displacement is governed by Boltzmann statistics and the energies of open and closed configurations of the channels are separated by a single energy barrier whose height depends on the angular displacement of the stereociliary tuft. The resulting channel conductance is a hyperbolic-tangent type function of the angular displacement of the stereociliary tuft. The channel conductance is coupled to the rest of the hair cell by an equivalent electric network containing constant resistance and a capacitance. The Thévenin equivalent resistance change across the basolateral membrane of the hair cell, called the transducer function, is also a hyperbolic-tangent type function of angular displacement. The parameters of the channel conductance and the values of resistances in the hair-cell electric model determine the scale factors and the location of the operating point of this hyperbolic-tangent type function. The hyperbolic-tangent type function is a specific example of a class of monotonically decreasing and saturating, or sigmoidal, transducer functions. The spectral properties of sigmoidal transducer functions are examined for sinusoidal angular displacements of amplitude theta. General results are obtained for arbitrary sigmoidal transducer functions; particular results are obtained for the hyperbolic-tangent type function. General conclusions concerning spectral components of the resistance change include: all spectral components are independent of the frequency of the angular displacement; the constant or DC component can be positive or negative; the fundamental component is 180 degrees out of phase with the angular displacement, i.e. the resistance decreases when the stereocilia are displaced towards the kinocilium; for small values of theta, the magnitude of the nth harmonic tends to grow as theta n for n greater than 0; the zeroth harmonic or DC component grows as theta 2.(ABSTRACT TRUNCATED AT 400 WORDS)

Element composition of inner ear lymphs in cats, lizards, and skates determined by electron probe microanalysis of liquid samples

SummarySiliconized, glass micropipets whose tips were filled with oil were used to obtain small (<100 nl) liquid samples from perilymphatic and endolymphatic regions of the inner ears of anesthetized animals: 3 cats, 19 alligator lizards (Gerrhonotus multicarinatus), and 8 skates (Raja erinacea). Samples of cerebrospinal fluid and seawater were also obtained for skates. Electron probe microanalysis was used to measure the concentrations of the following elements in each sample: K, Na, Cl, Ca, Mg, P, S. The Na and K concentrations in cat perilymph (Fig. 1 and Table 2) agree with previous estimates (Table 4) while endolymph samples show relatively low Na and high K concentrations. From a comparison of our results with previous work (Table 3), we infer that contamination of endolymph samples with perilymph is relatively low in our study, and that no large species difference in endolymph content is indicated by present data available for mammals. Our results show that Cl concentration is higher and Ca and Mg concentrations are lower in endolymph than in perilymph. The composition of perilymph in cats and alligator lizards is roughly the same (Figs. 1 and 2, Table 2). Uncontaminated endolymph samples in lizards were apparently difficult to obtain, although the compositions of a few samples suggest that endolymph K concentration is high and Na concentration is low. In skates the concentration of Na is nearly the same in the two inner ear lymphs (Fig. 3 and Table 2), in contrast to the roughly hundredfold ratio of perilymph to endolymph Na concentrations found in the higher vertebrates. The element composition of perilymph is correlated with the composition of seawater in which the skates were kept, whereas the endolymph composition shows no such correlation.