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PubMed2004

Do forward- and backward-traveling waves occur within the cochlea? Countering the critique of Nobili et al.

The question of whether or not forward- and backward-traveling waves occur within the cochlea constitutes a long-standing controversy in cochlear mechanics recently brought to the fore by the problem of understanding otoacoustic emissions. Nobili and colleagues articulate the opposition to the traveling-wave viewpoint by arguing that wave-equation formulations of cochlear mechanics fundamentally misrepresent the hydrodynamics of the cochlea [e.g., Nobili et al. (2003) J. Assoc. Res. Otolaryngol. 4:478-494]. To correct the perceived deficiencies of the wave-equation formulation, Nobili et al. advocate an apparently altogether different approach to cochlear modeling--the so-called "hydrodynamic" or "Green's function" approach--in which cochlear responses are represented not as forward- and backward-traveling waves but as weighted sums of the motions of individual basilar membrane oscillators, each interacting with the others via forces communicated instantaneously through the cochlear fluids. In this article, we examine Nobili and colleagues' arguments and conclusions while attempting to clarify the broader issues at stake. We demonstrate that the one-dimensional wave-equation formulation of cochlear hydrodynamics does not misrepresent long-range fluid coupling in the cochlea, as claimed. Indeed, we show that the long-range component of Nobili et al.'s three-dimensional force propagator is identical to the hydrodynamic Green's function representing a one-dimensional tapered transmission line. Furthermore, simulations that Nobili et al. use to discredit wave-equation formulations of cochlear mechanics (i.e., cochlear responses to excitation at a point along the basilar membrane) are readily reproduced and interpreted using a simple superposition of forward- and backward-traveling waves. Nobili and coworkers' critique of wave-equation formulations of cochlear mechanics thus appears to be without compelling foundation. Although the traveling-wave and hydrodynamic formulations impose strikingly disparate conceptual and computational frameworks, the two approaches ultimately describe the same underlying physics.

Animals↗

PubMed2005

Survival of partially differentiated mouse embryonic stem cells in the scala media of the guinea pig cochlea.

The low regenerative capacity of the hair cells of the mammalian inner ear is a major obstacle for functional recovery following sensorineural hearing loss. A potential treatment is to replace damaged tissue by transplantation of stem cells. To test this approach, undifferentiated and partially differentiated mouse embryonic stem (ES) cells were delivered into the scala media of the deafened guinea pig cochlea. Transplanted cells survived in the scala media for a postoperative period of at least nine weeks, evidenced by histochemical and direct fluorescent detection of enhanced green fluorescent protein (EGFP). Transplanted cells were discovered near the spiral ligament and stria vascularis in the endolymph fluid of the scala media. In some cases, cells were observed close to the damaged organ of Corti structure. There was no evidence of significant immunological rejection of the implanted ES cells despite the absence of immunosuppression. Our surgical approach allowed efficient delivery of ES cells to the scala media while preserving the delicate structures of the cochlea. This is the first report of the survival of partially differentiated ES cells in the scala media of the mammalian cochlea, and it provides support for the potential of cell-based therapies for sensorineural hearing impairment.

Animals↗

PubMed1984

Met-enkephalin characterization in the cochlea: high-performance liquid chromatography and immunoelectron microscopy.

The present paper extends and refines previous observations of enkephalin-like immunoreactivity in the guinea-pig cochlea. Firstly, Met-enkephalin was identified and a quantitative evaluation was made by combining high-performance liquid chromatography (HPLC) and a specific radioimmunoassay. Both the antibody specificity and the HPLC purification allowed us to demonstrate the co-existence, in the cochlea, of at least 3 opioid peptides: Met-enkephalin, Leu-enkephalin and Met-enkephalin-Arg6-Phe7. Secondly, a pre-embedding immunoperoxidase technique was used on whole or dissected cochleas. Immunoreactivity was localized in efferent fibers (coming from the brainstem) in the inner spiral bundle, tunnel spiral bundle and intraganglionic spiral bundle. In the inner spiral bundle vesiculated Met-enkephalin-immunoreactive fibers could be seen synapsing with afferent auditory dendrites. It is hypothesized that these Met-enkephalin immunoreactive fibers (belonging to the lateral efferent system) could be responsible for an inhibitory effect upon the gross cochlear action potential.

Animals↗

PubMed1990

Electrical stimulation of the inferior colliculus at low rates protects the cochlea from auditory desensitization.

The effects of inferior collicular (IC) stimulation on cochlear responses were tested with pulsed electrical trains and with 1 min long continuous bursts. Pulsed trains did not cause any effects at the contralateral cochlea. However, a 1 min burst, containing pulses at low rates, was able to significantly reduce temporary threshold shifts (TTS) in cochlear sensitivity caused by a loud sound exposure. Intracochlear perfusion of hexamethonium blocked this effect. The time course of the hexamethonium blocking action paralleled its blocking action on the cochlear effects of electrical stimulation at the brainstem of an auditory efferent pathway, the crossed olivocochlear bundle (COCB). The protective IC effects were persistent and TTS reductions could be obtained even with a 5 min delay between IC stimulus and the loud sound. However, these persistent protective effects did not appear to occur at the cochlea. Finally, electrical stimulation at the IC ipsilateral to a cochlea exposed to loud sound also reduced TTS, but only by smaller amounts and at higher stimulation rates. Thus the IC appears to provide a strong descending influence that modulates the excitability levels of the olivocochlear nuclei in the brainstem. Both crossed and uncrossed OCB appear to be involved and able to reduce TTS. It is proposed that the protective effects may be due solely to the medial olivocochlear system and possibly only those fibres originating from one of the nuclei of the medial system.

Acoustic Stimulation↗

PubMed1991

Selective degeneration of a putative cholinergic pathway in the chinchilla cochlea following infusion with ethylcholine aziridinium ion.

Ethylcholine aziridinium ion (AF64A) diluted in artificial perilymph, or artificial perilymph alone was infused into the cochlea of chinchillas. After a survival time of 7 days, the cochleas were fixed with aldehydes, post-fixed in osmium and embedded in epoxy resin for light and electron microscopy. The ultrastructure of the cochleas infused with artificial perilymph was normal. Infusion of 1 microM AF64A resulted in massive degeneration of the axons of the lateral efferent system, a putative cholinergic pathway that originates in the brainstem and terminates on dendrites of the spiral ganglion innervating cochlear inner hair cells. The axons and terminals of a second putative cholinergic pathway, the medial efferent system which terminates on the outer hair cells, were normal. Infusion of AF64A in a concentration of 10 microM resulted in significant pathology of cochlear and supporting cells as well as the loss of efferent terminals at both inner and outer hair cell regions. The results suggest that AF64A is a selective neurotoxin when used under low-dosage conditions, and that certain pathways may be more susceptible to the effects of AF64A than others. One interpretation of these findings is that lateral efferent axons may have a higher rate of high-affinity choline uptake than terminals of the medial efferent axons.

Acetylcholine↗

PubMed1992

Early efferent innervation of the developing rat cochlea studied with a carbocyanine dye.

The olivocochlear pathway in the developing rat was visualized in fixed material. The fluorescent carbocyanine dye 1,1'-Dioctadecyl-3,3,3',3'-tetramethylindocarbocyanine perchlorate (DiI) was applied to the cut central axons of the olivocochlear neurones at the floor of the fourth ventricle, and the termination pattern within the cochlea was examined after dye diffusion. From the day of birth (P0) to postnatal day 2 (P2), efferent innervation of the cochlea was exclusively in the region of the inner hair cells. Between P2 and P11, progressive outgrowth of neuronal processes to the outer hair cell region occurred; possible connections with the outer hair cells were occasionally seen at P4 and approached the mature pattern by P6. The efferent innervation of the organ of Corti appeared to mature progressively from the cochlear base to the apex, with outgrowth to the outer hair cells occurring earlier in the basal turn of the cochlea than in the second and third cochlear turns. Numerous blind axonal endings were observed in the spiral lamina especially at early postnatal ages. These findings may be consistent with a sequential pattern of arrival of efferent axons at the organ of Corti and ongoing death of efferent neurones in the brainstem during this period of development.

Animals↗

PubMed1989

HPLC detection of dopamine and noradrenaline in the cochlea of adult and developing rats.

The presence and postnatal development of dopamine (DA) and noradrenaline (NA) in the rat cochlea were detected by high-performance liquid chromatography coupled with electrochemical detection. Cochlear DA content rose gradually after birth. Conversely, NA concentrations rose rapidly between postnatal day 1 and 8; then, up to day 30, it increased more slowly. On day 30, both DA and NA levels were around 5 times higher than on day 1. In the adult rat cochlea, NA mean content was 234 +/- 22.2 pg/mg protein, while DA mean content was 23.6 +/- 1.1 pg/mg protein. Adrenaline was always undetectable. The present study is the first report describing directly the presence of DA in the rat cochlea. DA might serve as one of the lateral efferent neurotransmitters, whereas NA probably acts as a neurotransmitter of the sympathetic cochlear innervation. Nevertheless, their influences on the cochlear physiology, either in adulthood or during development are still a matter of discussion.

Aging↗

PubMed1992

Mechanical preprocessing in the mammalian cochlea.

The mammalian cochlea responds with exquisite sensitivity to the small fluctuations in air pressure that make up the stimulus of sound. Moreover, it responds to pressure fluctuations that occur extremely rapidly and that vary over a wide range of intensities--in both cases, to an extent outside the capabilities of unaided nerve fibres. Research performed during the past decade has shown that these properties are dependent on a physiological source of mechanical energy that operates probably within the outer hair cells of the organ of Corti. These cells, which are anatomically and functionally similar to the primary receptor cells, the inner hair cells, are believed to function as a source of mechanical power to assist the mechanical sensitivity of the cochlea, by mechanisms that currently are not understood. Several possible mechanisms have been proposed, but each has limitations that may make it an unsuitable candidate. Recent work has also demonstrated the likely role of mechanoelectrical transduction in outer hair cells in controlling the power source and thereby influencing the sensitivity and amplitude range of the cochlea.

Animals↗

PubMed1988

Melatonin and other serotonin derivatives in the guinea pig membranous cochlea.

In mammals, the indolealkylamine melatonin is synthesized mainly in the pineal gland and to a lesser degree in a number of extrapineal sites. To obtain more information on its distribution, melatonin was measured in the membranous cochlea of the guinea pig. Moreover, melatonin and other serotonin derivatives were determined in organ cultures after incubation with 14C-labelled serotonin. The results show that melatonin is detectable in the organ of Corti and the basilar membrane, and to a lesser degree also in the cochlear nerve and stria vascularis, including the spiral ligament. In vitro studies reveal the occurrence of a number of radiolabelled serotonin derivatives indicating that two of the melatonin-forming enzymes, serotonin N-acetyltransferase (NAT) and hydroxyindole-O-methyltransferase (HIOMT) are present in membranous cochlea. It is concluded that melatonin is synthesized in the guinea pig cochlea. Its role as modulator of hair cell function is dissolved.

Acetylserotonin O-Methyltransferase↗

PubMed1983

Localization of enkephalin-like immunoreactivity in acetylcholinesterase-positive cells in the guinea-pig lateral superior olivary complex that project to the cochlea.

Olivocochlear fibers have been demonstrated to have acetylcholinesterase-positive staining both in brainstem and cochlea. Olivocochlear fibres in the cochlea have also been determined to contain enkephalin-like immunoreactivity. In this study, we first determined the source of olivocochlear fibers in the guinea-pig using horseradish peroxidase and wheat germ agglutinin in retrograde transport studies. These cells were then examined for enkephalin-like immunoreactivity followed by acetylcholinesterase staining on the same sections to determine which cells and fibers showed staining for both. It was found that cells in the guinea-pig lateral superior olive that project to the cochlea have both enkephalin-like immunoreactivity staining and acetylcholinesterase-positive staining. Cells in other areas giving rise to olivocochlear fibers showed only acetylcholinesterase staining. These results suggest that there is co-localization of enkephalin and acetylcholine in a population of olivocochlear cells and fibers.

Acetylcholinesterase↗

PubMed1986

Identification of polyamines in the cochlea of the rat and their potential role in hearing.

The occurrence of reversible hearing loss in patients treated with the polyamine biosynthesis inhibitor, alpha-difluoromethylornithine (DFMO), led to the hypothesis that this functional hearing deficit might be due to polyamine depletion in the cochlea. To test this hypothesis the polyamine content (putrescine, spermidine and spermine) of the cochleas of normal rats was measured and compared to that of DFMO-treated rats. For the first time, it was demonstrated that in the cochleas of normal rats there were substantial amounts of spermidine and spermine but no detectable putrescine. There was also no measurable ornithine decarboxylase. The DFMO treatments employed in this study were not effective, however, in depleting the cochlear polyamines to levels generally considered critical for disrupting polyamine-dependent processes in other systems. Thus, it is not surprising that auditory thresholds, which were evaluated using brainstem evoked potentials, remained unaltered in the DFMO-treated rats. Demonstration of a role for polyamines in hearing awaits further investigation with the use of more potent inhibitors or other model systems for hearing.

Animals↗

PubMed1983

Muscarinic acetylcholine receptor binding in the guinea pig cochlea.

Because of the possibility that olivocochlear bundles may use acetylcholine as an inhibitory transmitter, we examined the cochlea of the guinea pig for cholinergic receptor binding sites. Binding of the potent muscarinic antagonist [3H]quinuclidinyl benzilate (3H-QNB) showed that the cochlea has sites with the pharmacological specificity of muscarinic cholinergic receptors. Specific 3H-QNB binding was saturated at 0.8 nM and was half-saturated at 0.03 nM concentrations. Total 3H-QNB binding was reduced 70% in the presence of saturating doses of acetylcholine, oxotremorine and atropine, and half-maximal competition occurred at doses comparable to those at other muscarinic sites in the central and peripheral nervous systems. The nicotinic specific antagonist d-tubocurarine did not block 3H-QNB binding at concentrations known to be effective in electrophysiological experiments, indicating the sites measured here were not the mixed muscarinic-nicotinic receptor type postulated for some systems. Localization of binding sites, as done by hand microdissection methods, showed that basal cochlear turns had five times the number of sites as apical turns. Most of the sites were evenly divided between the bony modiolus and the auditory nerve, although some sites were measured in sensory tissue. These results support the idea that cholinergic communication occurs in the cochlea, but they are also consistent with the hypothesis that other receptor mechanisms may be involved in olivocochlear inhibition.

Acetylcholine↗

PubMed1984

Transganglionic transport of D-aspartate from cochlear nucleus to cochlea--a quantitative autoradiographic study.

This study concerns the connections of the inner and outer hair cells and the different types of ganglion cells of the mammalian cochlea with the central nervous system by making use of their putative neurotransmitters. D-[3H]Aspartate (D-ASP), a putative marker for glutamatergic neurons, was injected into the cochlear nucleus of cats and guinea pigs and the cochleas prepared for light microscopic autoradiography after varying survival times. A quantitative, statistical autoradiographic method is described. Grain counts per unit area were made for each of 14 tissue compartments in the cochlea and normalized to permit comparisons between cases. An operationally defined background labeling level was computed for each case and a statistical test for significance applied to the neuron-containing tissue compartments. With increasing survival times, significant labeling appeared successively in the cochlear nerve root, in each type of spiral ganglion cell, and in the neuron-containing tissue compartments of the organ of Corti. The findings are consistent with uptake of D-ASP and retrograde transport by cochlear nerve axons from the cochlear nucleus to the perikarya and peripheral processes of the spiral ganglion. We conclude that axons of all spiral ganglion cells project to the cochlear nucleus and that this nucleus is directly connected with both the inner and outer hair cells. Transganglionic transport of D-ASP from the cochlear nucleus is consistent with the hypothesis that the cochlear nerve axons use glutamate or aspartate as a neurotransmitter.

Animals↗

PubMed1985

Physiological and morphological characterization of efferent neurones in the guinea pig cochlea.

Efferent neurones within the intraganglionic spiral bundle of the guinea pig cochlea were characterized in terms of their response properties, and their pattern of termination within the receptor organ revealed by intracellular labelling with horseradish peroxidase. All neurones subsequently identified as efferent neurones had clear features of their response properties which distinguished them from primary auditory afferents. They had long latency, low maximum discharge rate and low levels of spontaneous activity under Nembutal/Innovar anaesthesia. The pattern of discharge was extremely regular, revealed by symmetrical interspike interval histograms. 49.4% responded best to ipsilateral, 43.3% to contralateral sound and a third group of 7.3% responded equally well to either ipsilateral or contralateral sound. In cochleae in good physiological condition, these efferents were as sensitive and as sharply tuned as primary afferents with the same characteristic frequencies (CFs). All efferents fully traced in histological processing terminated on the outer hair cells. Several efferents showed extensive branching beneath the inner hair cells which might represent en passant synapses with other neuronal elements. There was clear evidence of tonotopic organization of the efferent projection. The site of termination on the outer hair cells in most instances was very close to the region of the cochlea predicted from the fibres' CF and the known place-frequency map for primary afferent neurones in the guinea pig.

Anesthesia, General↗

PubMed1987

Segregation of efferent projections to different turns of the guinea pig cochlea.

Localized intracochlear injections of the fluorescent retrograde label diamidino yellow were used to investigate the organization of efferent projections from the brainstem to different turns of the cochlea, in the guinea pig. It was found that the location of small neurones within the lateral superior olive ipsilateral to the injection varied in a systematic manner when injections proceeded from base to apex of the cochlea. In addition, a cruder form of cochleotopic organization was present in that most of the large medial system efferent neurones were labelled only after injection into the 3 most basal turns of the cochlea. The decline of medial system efferent innervation proceeding from base to apex was most striking for the contralateral efferent neurones. The details of base to apex innervation density were different for the different nuclei of origin of the medial system, implying the existence of complex subsystems within the medial neurone population.

Animals↗

PubMed1987

The morphology and physiology of hair cells in organotypic cultures of the mouse cochlea.

Organotypic explant cultures were prepared from the cochleas of 1 to 3 day post-natal mice and maintained in vitro for up to 5 days. The hair cells retain morphological integrity for the duration of the culture period although they exhibit embryological features such as a kinocilium and additional microvilli on their apical surfaces. The resting membrane potentials of mouse inner hair cells (IHCs) in vitro are similar to those of guinea-pig IHCs in vivo but the membrane potentials of outer hair cells (OHCs) in the mouse cochlea in vitro are less polarized than the resting membrane potentials of OHCs in the basal turn of the guinea-pig cochlea in vivo. The voltage responses of IHCs and OHCs to sinusoidal displacements of their stereocilia are similar to each other in waveform and dynamic range, although the responses of IHCs are larger than those of OHCs. The relationship between transducer conductance and stereocilia displacement in IHCs and OHCs is non-linear and largely accounts for the depolarizing asymmetry of the voltage response. The receptor potentials of IHCs and OHCs reverse close to 0 mV indicating that the transducer conductance is non-selective for cations. The voltage responses of IHCs and OHCs to intracellular current injection rectify when the membrane potentials are more depolarized than about -30 mV. This rectification is most pronounced in OHCs. OHCs also exhibit a time-dependent, voltage-sensitive conductance although they do not behave as electrical resonators.

Animals↗

PubMed1988

An ipsilateral cochlear efferent loop protects the cochlea during intense sound exposure.

One suggested physiological function of the efferent nerve fibers innervating the cochlea is that they protect the cochlea against the effects of intense sound exposure. In order to test this hypothesis, we studied the effects of intense sound in the presence and in the absence of strychnine which blocks the efferent nerve fibers. The results show that in presence of strychnine an ipsilateral intense sound has a greater effect on the cochlea than in the absence of strychnine. We conclude that the ipsilateral cochlear efferents may act as protectors against intense sound exposure.

Action Potentials↗

PubMed1990

Reconstructions of efferent fibers in the postnatal hamster cochlea.

It is well known that adult-like physiological functioning of the mammalian postnatal cochlea occurs coincidentally with the presence of efferent synapses on outer hair cells (OHCs). This study described the cochlear innervation patterns of thick efferent fibers traveling in the vestibular nerve in postnatal hamsters ranging in age from day zero to day 10. At least three kinds of efferent fibers were labeled via an in vitro horseradish peroxidase (HRP) technique: varicose, thin efferents; nonvaricose, thin efferents; and nonvaricose, thick efferents. Nonvaricose thick efferents were reconstructed from the basal third of the cochlea. Reconstructed efferent fibers traversed in the intraganglionic spiral bundle (IGSB) on the peripheral edge of the spiral ganglion and branched profusely in the osseous spiral lamina (OSL). From day zero to day five, large (greater than 1.0 microns) diameter nonvaricose efferent fibers gave rise to branches that either terminated underneath inner hair cells or appeared to end blindly in the OSL. Efferent fibers also had branches that traveled in the inner spiral bundle (ISB) and tunnel spiral bundle (TSB). In cochleae from hamsters six to eight days old, some thin and thick diameter efferent fibers contacted both inner and outer hair cells. By the tenth day, large diameter fibers traveled radially across the tunnel of Corti to terminate on one to five OHCs. As early as day seven, large diameter fibers also appear to terminate preferentially on OHCs in row one. These observations are consistent with the notion that the end of the first postnatal week represents a critical period in the formation of adult-like synapses on the OHCs. The data also suggest a developmental transition period when efferent fibers contact both hair cell types before contacting OHCs separately.

Animals↗