Joseph E. Hawkins

Sensory and Neural Degeneration with Aging, as Seen in Microdissections of the Human Inner Ear:

Presbycusis, the gradual loss of hearing that occurs with advancing age, is as subtle and complex as the aging process itself. Schuknecht’has suggested that there are four main types of presbycusis: 1) sensory, with primary loss of the hair cells of Corti’s organ; 2 ) neural, with primary degeneration of neurons of the cochlear nerve and central auditory pathways; 3 ) metabolic, with primary atrophy of the stria vascularis; and 4 ) mechanical, with primary changes in the physical properties of the basilar membrane. To these four might be added vascular presbycusis, characterized by loss of minute vessels supplying the spiral ligament, stria vascularis, and tympanic lip, of which metabolic presbycusis may prove to be a special case. Central presbycusis, with loss of neurons from the cochlear nucleus and other auditory centers of the brain, might also be classified as a distinct type, the term neural presbycusis being reserved for degeneration of first-order neurons of the cochlear nerve. Above all, it should be emphasized that the various types of presbycusis seldom, if ever, occur singly. Any attempt, therefore, to set up an exhaustive classification or a complete list of causative factors in presbycusis at this time is necessarily premature.

Vascular Changes in the Human Inner Ear Associated with Aging

This study is conccrned with the condition of the minute vessels of the inner car as seen in a collection of temporal bones obtained at autopsy from patients of widely varying ages. Its purpose is to examine the microvascular pathology that occurs with aging and to consider its possible relation to presbycusis. Because of the difficulty of setting up any standards of normal vascularization, the approach is qualitative and descriptive rather than quantitative and statistical.

EFFECT OF KANAMYCIN ON COCHLEAR CYTOARCHITECTURE.

Surface preparations of the organ of Corti have been studied by phase contrast microscopy in guines pigs treated with minimal doses of kanamycin. One of the earliest changes observed is a disturbance of the orderly W-pattern of the stereocilia of the outer hair cells in the basal coil. Occasional cells also show enlarged nuclei. Gaps appear in the ranks of the outer hair cells, especially in the first row, where cells have degenerated and disappeared, leaving only the empty reticular framework. At a later stage the inner hair cells also begin to drop out. Cell counts are presented showing the distribution of the losses. The method permits a quick, direct, quantitative assessment of damage to the organ of Corti, without the delays and uncertainties of the celloidin technique.

Functional and Morphological Changes in Experimental Endolymphatic Hydrops

Electrocochleograms (ECochG) in response to tone bursts and electronystagmograms (ENG) during sinusoidal rotational stimulation were monitored in guinea pigs equipped with chronically implanted round-window and periocular electrodes before and for as long as 90 days after uni- or bilateral surgical obliteration of the endolymphatic duct. The presence of cochlear and saccular endolymphatic hydrops was verified during microdissection of the inner ear, and cochlear hair cell counts were performed in some of the animals. The results indicate that in surgically-induced endolymphatic hydrops, cochlear and vestibular changes occur similar to those observed clinically in Menières disease: fluctuant threshold shifts, threshold elevation at low frequencies, sensorineural loss at all frequencies with recruitment, increase in the ratio of summating potential to compound action potential (SP/CAP), asymmetry and recruitment in the ENG, and increased vestibular excitability, with occasional post-rotational and spontaneous nystagmus. Functional changes could not be clearly correlated with those seen by light microscopy, since hair cell loss was confined mainly to the apical coil. The observations indicate that the guinea pig with surgically-induced endolymphatic hydrops can be a useful model of Menières disease, not only on morphological grounds, but also on the basis of functional changes, which over the relatively short term of observation represent a dysfunction rather than a loss of sensorineural structures.

Melanocytes of the Vestibular Labyrinth and Their Relationship to the Microvasculature

The melanocytes of the vestibular labyrinth as seen in colored guinea pigs show a characteristic pattern of distribution in the wall of the utricle and in the ampullae, but they are not present in the wall of the saccule. They are found mainly in well-vascularized regions of apparent secretory or metabolic importance, including the “dark cell” areas. Their dendrite-like processes are often in intimate contact with the capillaries, although no pinocytotic vesicles or other indications of transfer of substances between the melanocytes and the capillary endothelium are seen under the electron microscope. In the human ear, the apparent density of the melanocytes varies with skin color. They are numerous in the cochlea, especially in the bony wall of the modiolus and on the osseous spiral lamina, and they occur also in Reissners membrane and in the stria vascularis. In the vestibular system they are found in the wall of the saccule as well as in the utricle, the crus commune, and the ampullae, but not in the semicircular canals. They tend to be diffusely scattered, rather than to form the well-defined, intensely pigmented areas that are characteristic of the guinea pig. Close contacts with capillaries are seen mainly in the tympanic portion of the spiral ligament. The significance of melanin and the melanocytes in the labyrinth is unknown, but both the anatomical relation of certain melanocytes to capillaries, and the biochemical relation of melanin to the catecholamines support the hypothesis that they may have a vasomotor function. Other evidence, including the not infrequent association of sensorineural deafness with hereditary disorders of pigmentation also suggests that the melanocytes may play a role of some biological consequence in the inner ear.

Cochlear microvasculature in normal and damaged ears.

The minute vessels of the cochlea were examined post mortem in normal guinea pigs and in others exposed to intense noise or treated with the ototoxic drugs gentamicin and quinine. The benzidine stain was used to display the capillary networks, and osmic acid for surface preparations, “thick” sections, and ultrathin sections for electron microscopic examination.

Degeneration patterns in human ears exposed to noise.

Various forms of sensorineural degeneration patterns related to noise exposure are illustrated in six pairs of temporal bones selected from a group of 33 male patients with histories of noise exposure. For the entire group the commonest form of lesion, associated with a 4-kHz dip in the audiogram, was a relatively diffuse degeneration in the second quadrant of the basal turn, in the 9–13 mm area. An advanced form of this lesion had a wide gap of more or less complete sensorineural degeneration affecting the entire second quadrant and displaying various degrees of extension toward the apex and base. The pattern associated with an “abrupt high-tone loss,” with more or less complete hair cell and nerve degeneration in both the second and first quadrants and extending to the basal end of the cochlea, was rare. In one case this pattern appeared to have evolved from the first type of lesion as the remaining nerve fibers in the first quadrant had degenerated. The protective effect of the acoustic shadow of the head for the right ear, in shooting from the right shoulder, is demonstrated for the higher frequencies. Two almost identical cases of sharply-circumscribed single areas of degeneration in the first quadrant and one case with two such areas represent the third type of lesion. In one of these cases there was a history of firearm usage. It is postulated that this type of lesion is caused by impulse noise. In most of the material the degeneration pattern differed markedly from the diffuse degeneration seen with presbycusis. Degeneration patterns with knife-sharp transitions between completely degenerated and apparently undamaged areas appear to be characteristic of noise-induced injuries.

Hearing Loss and Cochlear Pathology in Monkeys After Noise Exposure

Old World monkeys were exposed to octaveband noise from 0.5 to 8 kHz at 120 dB SPL, 8 hours daily for 20 days. Restricted permanent threshold shifts and localized loss of outer hair cells were produced, which were reasonably well correlated with the exposure frequencies. There was also a loss of both inner and outer hair cells at the extreme basal end of Cortis organ, regardless of the exposure frequency. Implications for human inner ear pathology are discussed.

Cytoarchitecture of the Organ of Corti

The author has used special preparation techniques and phase contrast microscopy for the study of the normal and the pathologically changed cochlea of guinea pigs and squirrel monkeys. A short description of this technique of making surface preparations of the organ of Corti will be given, as well as a presentation of figures showing the outstanding way in which it permits in one specimen the analysis of damage in every single one of more than a thousand consecutive sensory cells. The surface preparation has replaced the preparation techniques earlier used by the author for several purposes and is characterized by its simplicity and reliability.

Otolithic Membranes of the Saccule and Utricle in Man

The otolithic membranes of the human saccule and utricle can be prepared as whole mounts or surface specimens for microscopic examination. They are not simple, homogeneous, gelatinous structures as heretofore described. Instead, each shows a definite and characteristic fibrillar design, which appears to be correlated with the known cytoarchitectural pattern of the underlying neuroepithelium.