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Current distributions in the cat cochlea: a modelling and electrophysiological study.

The current distribution of bipolar electrodes implanted into the scala tympani of the cat cochlea was investigated using a two-electrode masking technique. Two electrode masking is a non-invasive technique which requires two electrically independent electrodes and relies upon the forward masking of the electrically evoked brainstem response to a probe stimulus by that of a preceding test stimulus. The technique was described in terms of a model, which enabled an approach for estimating the scala tympani length constant to be established. Model results have shown good agreement with electrophysiological results. Application of the model confirmed the scala tympani length constant within the basal turn of the cochlea to lie between 3 and 4 mm.

Animals↗

Mechanics of the basilar membrane in Caiman crocodilus.

Vibration measurements were made at a number of positions near the proximal (basal) end of the basilar membrane, and on the columella footplate, of Caiman crocodilus using a capacitive probe. The measurements established the existence of a mechanical travelling wave in this species. They showed no significant change of mechanical tuning with temperature, and were highly significantly different from previous reports of neural temperature sensitivity (Smolders, J. and Klinke, R. (1984): J. Comp. Physiol. 155, 19-30). Thus the neural sensitivity to temperature change appears not to depend upon basilar membrane mechanics. One interpretation of this is that the basilar membrane passively precedes an active temperature-sensitive filter. It was also found that the limbus supporting the basilar membrane had a measurable, but unturned, vibration and that the effect of draining scala tympani for the measurements was to increase the basilar membrane tuning frequency by a factor of about 1.5.

Animals↗

Some aspects of temporal coding for single-channel electrical stimulation of the cochlea.

Estimates of the useful frequency range for single-channel electrical stimulation of the cochlea range from 400 to 4000 Hz. Psychophysical studies in single-channel implant patients are relevant not only to the practical problem of designing stimulation strategies, but also to questions of temporal processing of pitch in the normal auditory nervous system. Patients with single-channel extracochlear devices participated in several experiments involving stimuli differing in fine temporal structure. Stochastic pulse trains, in which the probability of pulse delivery (p) for a given cycle was less than 1.0, were readily discriminated from ordinary pulse trains. Frequency discrimination using stochastic pulse trains differing only in fine temporal structure (but identical average pulse rates) was as good as with ordinary pulse trains or sinusoids for P greater than or equal to 0.5, but deteriorated rapidly for P less than 0.5. Discrimination of triangular and trapezoidal waveforms from square waves was surprisingly good: rise-times (for 0 to maximum current) as low as 0.08 ms could be discriminated. Conversely, detection of jitter in pulse trains was almost an order of magnitude worse. The results show that frequency discrimination for single-channel electrical stimulation of the cochlea is based on discrimination of inter-pulse periods, and that pulse rates which would be unnatural for acoustically-evoked VIIIth nerve activity - up to 750 Hz - are more useful for coding mid-range frequencies than low-rate stochastic stimulations of normal VIIIth nerve firing patterns. The waveform discriminations reported would be obscured by low-pass filtering even at 2000 Hz, and probably depend on changes in relative synchrony among an array of VIIIth nerve units with different thresholds. In general, these results support the use of analog coding schemes with relatively large bandwidth.

Cochlea↗

Ontogenetic changes in the position of hair cell loss after acoustic overstimulation in avian basilar papilla.

High intensity sound was used to produce localized hair cell damage within the basilar papilla of chicks at three different ages: embryonic day 20, post-hatch day 10 and post-hatch day 30. At each age separate groups of animals were exposed to broadband white noise or pure tones at 500, 1500 or 3000 Hz for 12 h at 125 dB SPL. Chicks were killed 10 days later. Their basilar papillae were then fixed, dissected free, osmicated, embedded in Epon, sectioned serially and stained. Hair cells were counted at 100 micron intervals throughout the length of the papilla. There was a systematic developmental shift in the position of damage produced by each of the acoustic stimuli. Broadband white noise produced damage only in the basal one half of the cochlea in the embryonic animals while at later ages it produced damage throughout the length of the papilla. Exposure with each of the pure tones produced a discrete area of hair cell loss. However, with each frequency the region of damage shifted apically as a function of the age of the animal at the time of sound exposure. These results suggest that the frequency representation along the basilar papilla is not fixed, but changes during the development of hearing.

Acoustic Stimulation↗

Modifications of cochlear microphonic frequency responses following transient changes of hydrostatic pressure in the perilymph.

Cochlear microphonic potential was recorded with differential electrodes implanted in the various turns of the guinea-pig cochlea. Isointensity frequency responses were plotted in normal conditions and after excessive displacements of the cochlear partition. These displacements were provoked by changes of hydrostatic pressure in the perilymph of scala tympani or scala vestibuli. Typical modifications of the frequency response were observed. The most noticeable was a division in two parts of the response zone which suggested the existence of two resonance peaks. Scanning electron microscopy revealed that changes of hydrostatic pressure provoked alterations of the stereocilia in the outer rows of external hair cells, probably in relation with a decoupling of the tectorial membrane from the organ of Corti. These results are discussed in terms of possible alterations of cochlear micromechanics.

Animals↗

Effects of section of the medial efferent tracts (crossed and uncrossed) on cochlear frequency selectivity.

The cochlear innervation of guinea pigs was sectioned midway between the midline and the external side of the cochlear nucleus, in a rostrocaudal direction at the level of the floor of the fourth ventricle, to study the effects of medial efferent pathways on cochlear frequency selectivity estimated with tuning curves of single auditory nerve fibers. Single-unit tuning curves were affected by this type of efferent sectioning. Thus, the ipsi-lateral efferent system seems to be involved, through a tonic action, in the mechanisms responsible for high frequency cochlea selectivity.

Acoustic Stimulation↗

The frequency-following response to continuous tones in humans.

Previous studies of the frequency-following response (FFR) in man suggest that it has multiple sources. Identification of these sources has been complicated by the use of tone bursts to evoke FFRs and the lack of precise methods to calculate their amplitude and latency. Tone bursts produce transient responses which confound measurements of the FFR. The use of continuous tones avoids this problem and the Fast Fourier Transform can be used to assess accurately and efficiently the presence, amplitude and phase angle of the FFR. In this study we systematically examined the frequency and intensity range over which FFRs to continuous tones could be evoked using FFRs to tone bursts for comparison. We then analyzed FFRs to continuous tones to determine the sources of this potential. FFRs to both stimuli have similar thresholds (65-90 dB SPL) and can be evoked by the same range of frequencies. Neurogenic FFRs in man occur only below 1000 Hz. The source for this potential has a latency of 8.2 +/- 0.1 ms (mean +/- SD) and is consistent with a midbrain source. At higher frequencies FFRs have a latency of less than 1 ms and are most likely cochlear microphonic. The small variation in the latency of the neurogenic FFR suggests this as a possible tool for assessing neurological disorders.

Adolescent↗

Representation of the cochlea in primary auditory cortex of the ferret (Mustela putorius).

In seven barbiturate-anesthetized ferrets, we explored the acoustically sensitive cortex with conventional microelectrode mapping techniques. A tonotopically organized field was found whose orientation was such that high tonal frequencies were represented dorsally, and low frequencies ventrally. Within this field, neurons typically had short (12-20 ms) latent periods to first spikes. In conjunction with extant anatomical evidence on the connectivity of this region, these data suggest that this field represents the ferret's primary auditory cortex.

Animals↗

A model of the effect of outer hair cell motility on cochlear vibrations.

A model of cochlear function is presented in which deformation forces within outer hair cells are assumed to occur in synchronized response to generator potentials. Assuming a 90 degree phase lag between the generator potentials and the deformation forces, it is shown that the forces act to reduce cochlear-partition damping and thus increase frequency selectivity. A number of other experimentally observed phenomena, such as the effects of efferent-fiber stimulation and electrical polarization, can also be accounted for with this model.

Basilar Membrane↗

Electrical resonance and membrane currents in turtle cochlear hair cells.

The electrical and mechanical properties of single hair cells from the turtle's cochlea were examined to investigate the basis of their electrical resonance. Receptor potentials were measured with intracellular micropipettes in the isolated basilar papilla. At the onset and termination of a step displacement of the ciliary bundle the receptor potential showed a damped oscillation reflecting the frequency selectivity of the cell. Resonance frequencies increased systematically from apex to base of the cochlea. Similar oscillations could be elicited by a current step injected through the recording electrode. Solitary hair cells enzymatically isolated from the papilla were investigated with the tight-seal whole-cell recording method. Cells retained their properties in response to current steps and had resonance frequencies between 10 and 350 Hz. In voltage clamp such cells displayed a large outward K+ current and an inward Ca2+ current both activated by depolarization from the resting potential. The relaxation time constant of the K+ current was inversely correlated with the resonance frequency of the cell, varying from 150 ms in the lowest frequency cells to less than 1 ms in the highest ones. It is argued that variation in the kinetics of this current is the major factor responsible for the range of resonance frequencies. In preparations of the isolated papilla a flexible glass fibre, attached to the tip of a ciliary bundle, was used to deliver constant force steps to the bundle and to monitor its displacement. Receptor potentials were simultaneously recorded. At the beginning and end of a force step towards the kinocilium, the bundle vibrated at a frequency which coincided with the electrical resonance frequency of the cell.(ABSTRACT TRUNCATED AT 250 WORDS)

Animals↗

Basilar membrane measurements and the travelling wave.

From the original measurements of G. von Békésy (1942) until a few years ago, the basilar membrane was considered to undergo simple passive linear vibration. Recent measurements have completely altered this notion. It is now known that the BM is highly non linear and very sharply tuned. Indeed, BM can now account for most of the properties of the eighth nerve response to sound. The non linearity can be approximated by a hyperbolic function and appears to be part of an active process in the outer hair cell. At the characteristic frequency, CAP threshold (10 dB SPL) corresponds to 0.3 nm motion and the non linearity shows half saturation at 10 nm. The sigmoid shape of the full range BM input-output curve is due to the combination of a less sensitive linear passive component with the added sensitivity of the active non linear function. A hyperbolic input-output function is also present in the cochlear microphonics, and at low frequencies the half saturation value again corresponds to 10 nm BM displacement. With induced threshold loss (e.g. noise trauma) the nonlinearity disappears from the BM, but is still present in the CM. This suggests that the pathology is in the active mechanical feedback process, rather than in the receptor system. It appears that BM mechanics at low amplitudes near the resonant frequency is controlled by a nonlinear mechano-electrical transducer followed by a vulnerable, linear, active mechanism (electro-mechanical?) feeding back in positive phase onto BM vibration.

Animals↗

Single unit clues to cochlear mechanisms.

In recent years studies on isolated hair cells have suggested that there is an inherent tuning of hair cells determined by their mechanical and electrical properties. However, tuning for mammalian cochleas appears to be much more complicated since there are typically two types of receptor cells (inner and outer hair cells) imbedded in a highly organized framework of supporting cells, membranes and fluids. The major neural output of the cochlea can be monitored by recording the activity of myelinated axons of spiral ganglion cells, not only under normal conditions, but also when the discharge patterns are altered by ototoxic drugs, acoustic trauma or olivocochlear bundle stimulation. A model system with two excitatory influences, one sharply tuned and highly sensitive, and a second, broadly tuned and relatively insensitive, can account for much of the existing data. Results from single-neuron marking studies support the notion that these two influences probably involve interactions between inner and outer hair cells. More global influences such as the endocochlear potential also can act on auditory-nerve fibers through the hair-cell systems. Thus, the inherent frequency selectivity of the receptor cell is only one of many factors that determine the tuning of mammalian auditory-nerve fibers.

Adaptation, Physiological↗

Neurobiology of cochlear inner and outer hair cells: intracellular recordings.

Recordings were made in the low-frequency region (third and fourth turns) of the guinea pig cochlea from both inner (IHC) and outer (OHC) hair cells. Certain electrical characteristics of these cells that have been described before (P. Dallos (1985) J. Neurosci. 5, 1591-1608) are reviewed. These are resting membrane potentials, response magnitude and saturation, and response phase. A comparison of sensitivity and best frequency is provided for IHCs and OHCs that are located in the same cochlear region. New data are presented for the level-dependence of response phase and for the properties of response asymmetry and the resulting dc component. The effects of intracellular polarizing current upon ac response magnitude are shown for both cell types.

Animals↗

The responses of inner and outer hair cells in the basal turn of the guinea-pig cochlea and in the mouse cochlea grown in vitro.

Until recently the responses of the mechanosensitive hair cells of the cochlea have been inferred from their morphology, morphological relationships with other structures in the cochlea, and by indirect electrophysiological measurements. With the advent of techniques for making intracellular recordings from hair cells in the cochleas of anaesthetised mammals it has been possible to measure the responses of hair cells to acoustic stimulation and to assess their roles in sensory transduction in the cochlea. Intracellular recordings of the responses of inner and outer hair cells in the basal turn of the guinea-pig cochlea show that they differ considerably from each other. The receptor potentials of inner hair cells are larger, predominantly depolarizing to low frequency tones and at their best frequencies (16-20 kHz) they generate depolarizing dc receptor potentials. Outer hair cells generate predominantly hyperpolarizing potentials to low frequency tones. They do not produce significant voltage responses at high frequencies except at high intensities when they generate slowly rising depolarizing potentials which are associated with loss of cochlear sensitivity. At low frequencies the receptor potentials of the inner hair cells phase lead those of the outer hair cell. Measurements of their frequency selectivity show that inner and outer hair cells are both sharply tuned. It is proposed that the responses of inner and outer hair cells are consistent with sensory and motor roles respectively in mechanoelectric transduction and that the outer hair cells are the site of an active mechanical process responsible for the frequency selectivity and sensitivity of the cochlea. Intracellular recordings from hair cells in the mouse cochlea maintained in vivo have provided a direct measure of the mechanosensitivity of cochlear hair cells (approximately 30 mV per degree of displacement of their stereociliary bundles) and indirect evidence that the transfer characteristics of the outer hair cells in vivo may be due to their mechanoelectrical interaction with the tectorial membrane. This is because the transfer characteristics of the inner and outer hair cells are similar in vitro in the absence of a tectorial membrane. Considerable importance is attributed to the shape of the transfer characteristics of the inner and outer hair cells. Changes in these characteristics during anoxia and following exposure to intense tones are associated with depolarization of the outer hair cells and loss of cochlear sensitivity and frequency selectivity. Current-voltage studies of hair cells in vivo show the inner and outer hair cells to be electrically nonlinear.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗

Relationship between basilar membrane tuning and hair cell condition.

Basilar membrane tuning characteristics were measured in 15 cats using laser interferometry. The experimental procedures introduced varying degrees of cochlear trauma. Variability from animal to animal was also observed in the characteristic frequency (CF) of tuning, the sensitivity at CF and lower frequencies, and the sharpness of tuning. The changes in the tuning characteristics of the basilar membrane are correlated with the extent of outer hair cell (OHC) damage. These observations lead to the conclusion that the tuning properties in the CF region are predominantly determined by the mechanical properties of the OHC and not the basilar membrane.

Animals↗

The influence of cochlear hearing loss and probe tone level on compound action potential tuning curves in humans.

The effect of cochlear hearing loss and of probe tone level on slopes and sharpness of compound action potential tuning curves was investigated. Thirty-one simultaneously masked isoreduction (50%) tuning curves were determined in 26 adults with cochlear hearing losses up to 60 dB. Probe tone frequency was 2 or 3 kHz. Probe tone level was chosen as close as possible to the action potential threshold, usually within 30 dB. In 5 cases a second tuning curve was determined at a 20-30 dB higher probe tone level in order to differentiate between effects of hearing loss and of probe tone level itself on decrease of selectivity. Tuning was analysed in terms of high- and low-frequency slopes of the tuning curves, both in the steepest parts near the tip and overall, and in terms of Q10dB. Slopes and tuning quality diminished with increasing hearing loss up to 60 dB. Part of the decrease in Q10 could be attributed to increased probe tone level, implying that frequency selectivity is also a level-dependent property. In the same group of subjects so called 'narrow-band' (or 'derived response') compound action potential latencies were determined at 90 dB pe SPL and a derived frequency similar to the probe tone in the tuning curve experiments. Narrow band latencies did not change significantly out of the normal range (2 periods) with increasing hearing loss. This implies that narrow band latencies are not related to hearing loss, but reflect only the probe-level dependent impulse response delay. Analysis shows that it is possible to derived Q10dB from narrow band latencies with probe level as a parameter.

Audiometry, Evoked Response↗

Representation of amplitude modulation in the auditory cortex of the cat. I. The anterior auditory field (AAF).

The ability of cortical neurons to follow amplitude modulation (AM) of tones was examined in the anterior auditory cortical field (AAF) of anesthetized cats using multiple-unit recording techniques. Sinusoidal and rectangular modulations (100%) of a monaural carrier tone at the characteristic frequency of each location were presented to study the degree of response synchronization and changes in firing rate as a function of the modulation frequency. All investigated locations were tuned to a 'best modulation frequency' (BMF) as determined by synchronization measures. Almost all locations (94%) were tuned to a BMF as determined by spike rate. Maximal binaural-interaction strength was observed for modulation frequencies close to the BMF of neurons. For sinusoidal AM, a correlation (r = 0.63, P less than 0.01) between BMF and CF of neurons in AAF could be demonstrated for the synchronization of the response.

Acoustic Stimulation↗