Phonoreceptors

Hearing consists in the reception and interpretation of stimuli caused by vibrations of material particles. For this purpose the auditory sense organs have been evolved, first among lower forms that are submerged in water. Later, after emergence into the rarer medium of air, these organs become of greater importance.

In fishes the lateral-line organs, or rheoreceptors already mentioned, take the place to a considerable extent of organs of hearing, since currents produced by moving water and disturbances of slow vibrations rather than “sounds” are the most important environmental changes to dwellers in the silent aquatic world.

No doubt to many transitional thigmotactic animals, particularly to amphibians whose bodies are not yet elevated from major contact with solid earth by means of supporting legs, the vibrations which are of the greatest service and for which their sense organs are especially adapted are seismic rather than auditory in character. It is mostly, however, vibrations which pass through the air that are concerned with the true sense organs of hearing. In this rarer medium, through which sound waves pass more slowly and with less intensity than through the denser media of water and earth, it becomes the task of evolution to elaborate intensifying and collecting devices of various sorts to supplement the sensory auditory receptors.

It has thus come about that the auditory apparatus of the higher land vertebrates consists not only of a sensory receiving apparatus, the internal ear, but also' of a middle and an external ear, whose supplementary functions are primarily the collection and amplification of vibrations from the air.

Of these three pairs of “ears,” the internal ears alone are essential and present in all vertebrates that hear. In amphibians the middle pair of ears is added, although it is incorrect to speak of a “middle ear” until the external ear, which begins with reptiles and reaches its highest elaboration in mammals, is developed.

In describing the vertebrate ear it may be well to consider the simpler accessory parts first, and the more complicated and essential parts of the internal ear last, following the path taken by sound vibrations as they go to the nervous system of the listening animal.

The External Ear

The external ear of the higher vertebrates consists of a projecting flap, the pinna, which is furnished with muscles, and an auditory canal. The pinna, a mammalian acquisition, is a peculiarly molded, flat, skin-covered, elastic cartilage in man with a cuplike concha, in the center, surrounding the entrance into the auditory canal. This opening is guarded on either side by two projections, the tragus, and antitragus (Fig. 688). The lower end, or lobule of the human ear, is fleshy, pendulous, and without cartilaginous support. In a considerable percentage of human kind the lobule is absent, or at least not free from the side of the head. The upper curving edge, or helix, of the pinna often presents an appearance suggesting animal ancestors (Fig. 689). When unrolled at the upper margin and more or less pointed, it is known as the “satyr ear,” such as was possessed by Donatello in Hawthorne’s famous story of The Marble Faun. If the projecting part is folded inward it makes the so-called “Darwin’s point,” more often seen in human males than females and quite characteristic of monkeys and apes. Embryonically the pinna passes through the satyr stage before attaining it final characteristically human outline.

Pinna of a human ear

The pinna develops on either side of the spiracular cleft which becomes the locus of the auditory canal. It arises originally as six knoblike elevations, three of which are borne by the mandibular, and three by the hyoid arch (Fig. 690).

Outlines of two ears. Embryonic stages in the development of the pinna

Pinnae become degenerate in aquatic and burrowing animals, such as seals, gophers, and moles, where they would serve no good purpose and might even be a disadvantage, but they are large in animals like bats that are active at night or in twilight, as well as in fast runners of open spaces, such as deer, hares, kangaroos, and antelopes. Also in arboreal animals, like squirrels, whose eyes are protected to a certain extent by the ears from chance encounters with twigs and branches, they are generous in size.

Spallanzani (1729—1799) long ago discovered that a bat, even after it had been blinded, was still able to avoid a maze of strings stretched across a chamber. The result of this classical experiment is not so much to be wondered at when it is remembered that bats are naturally active at twilight, a time when dependence upon sight in avoiding obstacles and in encountering insect prey upon the wing is of much lessened importance. It has recently been shown that these crepuscular animals ordinarily emit 20—60 supersonic screeches per second while in flight. The supersonic waves, which are audible to bats although above the range of the human ear, are reflected by even such slender objects as strings. Large external ears enable the bats to pick up the echoes of their voices and thus to avoid obstacles. Detection of objects by a system of reflected high-frequency waves thus long antedates man’s use of radar.

In most animals pinnae aid in catching the direction whence sound waves come. A deaf person sometimes supplements this function of the pinna by cupping the ear with the hand.

Many animals have pinnae that are movably hinged to the skull and supplied with muscles, so that they may be easily directed to detect the source of sounds without the inconvenience of turning a heavy head.

The ear muscles are under the control of the will. They are of two kinds, intrinsic within the pinna itself, and extrinsic, connecting the pinna with the skull, thus effecting the movement of the external ears.

In many breeds of domestic animals, as for example, pigs, sheep, goats, dogs, and rabbits, “lop ears” develop that lack much of muscular control as contrasted with upright hinged pinnae. In the security that comes with long domestication these animals have lost something of the habitual alertness that is the salvation of wild animals. Elephants are perhaps the only wild forms with pendulous non-erectile ears, but the self-confidence that goes with dominant size no doubt makes the direction from which hostile noises come a matter of comparative indifference to them.

In mammals the external auditory canal is the passage-way that leads to the middle ear. It is about 2.5 centimeters long in man, slightly bent and larger at either end than in the middle. For the external third of its length its walls are kept rigid by cartilage, continuous with that of the pinna, while for the remainder of the way into the skull the walls become bony, forming a projecting tube from the temporal bone.

The auditory canal is lined with skin, and is supplied with wax glands and outward-projecting hairs, both of which are devices that serve not only as dust-arresters, but also for the discouragement of crawling and flying insect explorers.

The Middle Ear

A middle ear, or tympanum, in the form of an irregular air-filled chamber, is hollowed out of each temporal bone between the external auditory canal and the internal ear.

A deep attic-like dorsal recess, the epitympanum, communicates with mastoid “cells,” or spongy cavities, in the blunt mastoid process of the temporal bone. Below, the Eustachian tube opens into the nasopharynx (Figs. 691 and 692).

Diagrams of stages in the development of the ear

Across the inner end of the auditory canal and separating it from the middle ear is the “ear drum,” or external tympanic membrane, which is attached in a groove, the tympanic sulcus. In man it is about 1 mm thick and 10 mm in diameter, being slightly thicker in the center than around the margin. It is set obliquely across the passage-way, and thus a larger ear drum with a greater expanse of surface is exposed to the impact of vibrations than would be possible if it extended squarely across at right angles to the auditory canal. The ear drum is relatively nearer the surface in a child than in an adult, while a newly born infant is temporarily deaf until the collapsed tympanic cavities are filled with air by way of the Eustachian tubes, following the effort that accompanies the first protesting cries with which it greets the world. These “first cries” of the newly born have been called the most joyful sounds in all nature, for they assure the anxious listeners that the young stranger is a going concern, having marvelously made the critical transition from uterine existence to citizenship in the world.

Diagram of the ear region of an adult mammal

On the face of the tympanic wall opposite the ear drum and next to the inner ear, are two windows, the fenestra ovalis and the fenestra rotunda, similarly curtained by drumhead-like membranes, so that the middle ear bears some resemblance to a hollow drum with very small membranous heads at the two ends (Fig. 692).

The tympanic cavity, or middle ear, in land forms is derived from the inner part of the ancestral spiracular cleft of the elasmobranch fishes that lies between the mandibular and hyoid arches of the primitive splanchnocraniums. In forming the middle ear the pharyngeal pouch never breaks through to the outside. The intervening “skin” remaining at the outer end of the spiracular pharyngeal pouch becomes the external tympanic membrane, while the opposite end extends to the pharynx as the Eustachian tube. Thus the external tympanic membrane is made up of an ectodermal layer on the outside and an endodermal layer on the inside.

The Eustachian tube is a ventilator of the tympanic cavity. Broader at the pharyngeal than at the tympanic end, it remains closed except during the act of swallowing when it may open sufficiently to permit an adjustment of air within the tympanic cavity. When the pressure of air is so adjusted that it is the same on the inside of the tympanic membrane as on the outside, the membrane is thus made free to vibrate slightly back and forth in response to the impact of sound waves. When one enters a tunnel in which the pressure of the air is above that of the atmosphere outside, the ear drum is pressed slightly inward and, like a bellying sail in a stiff breeze, does not vibrate. To relieve the sense of pressure in the ears, when it occurs, it is only necessary to swallow, thus admitting more air through the Eustachian tube into the middle ear chamber.

Ear bones within the tympanic cavity

Sound waves which impinge upon the tympanic membrane are handed across the tympanic cavity to the inner ear, intensified and with their amplitude reduced during the passage, by means of a chain of three tiny ear bones, the “hammer,” malleus; the “anvil,” incus; and the “stirrup,” stapes (Fig. 693).

The malleus is attached to the inner face of the ear drum by its “handle,” while the stapes, which is articulated to it by means of the intervening incus, fits into the membrane stretched across the fenestra ovalis and, somewhat like the plunger of a piston, transfers by a thrust to the inner ear the sound vibrations which strike the drum.

Ear bones of urodeles

In amphibians, instead of a chain of three bones, there is a single rod-like columella, extending from the ear drum directly to the fenestra vestibuli (Fig. 694a) . This device forwards vibrations from the drum to the inner ear with equal power and amplitude, instead of with an increased thrust and lessened amplitude as is the case with the chain of ear bones in mammals.

There may be two parts to the columella in reptiles and birds, either jointed or fused with each other (Fig. 694b). The inner element, which is homologous with the stapes of mammals, is the plectrum, while the outer part close to the drum is called the extra-columella.

In monotremes and marsupials the stapes remains cylindrical and solid at the enlarged inner end, like a pestle, but in other mammals it is pierced by a hole through which a blood vessel passes, so that it takes on a fancied resemblance to a stirrup, hence its name.

Two tiny muscles lie within the tympanic cavity. The tensor tympani, attached to the malleus and supplied from the VIIth cranial nerve, regulates the tension of the tympanic membrane. The stapedius, which is fastened to the stapes and supplied from the Vth cranial nerve, adjusts the fitting of the stapes in the fenestra ovalis.

The ear bones have a dramatic origin, being made over from skeletal elements of the splanchnocranium that formerly were put to quite different uses. The amphibian columella corresponds to the hyomandibular element of fishes, that is, to the most dorsal part of the hyoid arch. The inner end of the columella is homologous with the stapes of the mammalian ear, while the malleus and incus, which are peculiar to mammals, are derived from the articular bone of the primitive lower jaw, and the quadrate bone of the original upper jaw respectively (Table VII). Thus mammals may be said to hear through the jaw bones of their phylogenetic ancestors.

The Internal Ear

The baffling internal ear, buried in the dense temporal bone, is made up of extremely delicate cells surrounded in life by fluids. It is a very difficult structure to dissect, and consequently histological sections, owing to different technics employed in their preparation with the inevitable distortion that results, have not always presented a dependable picture of the truth. Nevertheless essential agreement about many details has been gained.

The internal ear, which contains the essential phonoreceptors, is a closed ectodermal sac, the membranous labyrinth, peculiarly molded and called a “labyrinth” on account of its complicated structure (Fig. 686). It is filled with a fluid known as endolymph and is surrounded by a bony labyrinth in the form of a case hollowed out of the petrosal part of the temporal bone, conforming intimately to the contours of the membranous labyrinth. For the most part the membranous labyrinth does not adhere closely to the bony labyrinth but is separated from it by a space filled with perilymph.

Development of the Membranous Labyrinth

The inner ear, being primarily a static organ, is placed at the anterior end of the system of lateral-line organs and is probably derived from it. Like the pits of the lateral-line organs the membranous labyrinth of the ear is first of all an ectodermal invagination, appearing as an isolated vesicle on either side of the head about opposite the anterior end of the myelencephalon. As it sinks below the surface it leaves an invagination canal, which at first remains open to the outside but later is closed off, thus making the vesicle of the future inner ear a completely closed sac surrounded by mesodermal tissues (Fig. 695).

Four stages in the development of the human membranous labyrinth, as seen in lateral views of the left ear

By constriction this sac is next marked off into a dorsal utriculus and a ventral sacculus. At three points in the utricular region the walls become pinched together into flattened, semicircular folds placed approximately at right angles to one another. By this pinching process the two walls of each of these flattened folds come into contact with each other except along its curved outer edge. Thus along the outer margin of each fold there is formed a semicircular canal, opening at either end into the main part of the utriculus. Absorption of the central parts of the folds leaves behind the three loops of the semicircular canals without destroying the continuity of the general cavity within the sac or allowing the sac to break through to the outside.

Meanwhile the sacculus sends out a cochlear sac which eventually elongates and coils to form the cochlear duct with an auditory rather than a static function.

Structure in Mammals

For the most part the membranous labyrinth lies suspended in the perilymph, being held in place by strands of connective tissue which extend from it to the periosteal lining of the bony labyrinth. In the cochlear region, however, parts of the duct are in direct contact with its bony envelope.

In each membranous labyrinth there are six sensory areas: a crista ampullaris in the ampulla of each semicircular canal, as already described; the macula utriculi in the wall of the utriculus; the macula sacculi, in that part of the sacculus that is not drawn out to form the cochlear duct; and the organ of Corti in the cochlear duct (Fig. 696). The cristae and maculae are innervated by the vestibular branch of the acoustic (VIIIth) nerve while the organ of Corti is supplied by the cochlear branch of the same nerve.

Diagram of the right membranous labyrinth as seen from medial side

In the adult human ear, only a slender tube, the utriculosaccular duct connects the utriculus with the sacculus. From this duct a slender endolymphatic duct extends to the inner surface of the petrous bone where it enlarges into the endolymphatic sac lying just beneath the dura. The sacculus is also connected with the cochlear duct by a slender canal, the ductus reuniens.

The bony cochlear canal, in which lies the cochlear duct, spirals about a conical axis, the modiolus (Fig. 697). From the modiolus a shelf of bone, the spiral lamina, projects into the canal, somewhat like the thread of a screw. Extending along the opposite wall of the canal is the spiral ligament, a thickened portion of the periosteum.

Axial section through a decalcified

In cross sections of the cochlea the cochlear duct appears triangular (Figs. 697 and 698). One side of the triangle lies against the outer wall of the canal in contact with the spiral ligament. Another side, the basilar membrane, extends from the ligament across the canal and onto the upper surface of the spiral lamina. The third side is the thin vestibular membrane, or Reissner’s membrane, which extends from the spiral lamina obliquely across to the upper part of the spiral ligament. Thus in cross section (Fig. 698), the bony cochlear canal encloses three cavities. Above the cochlear duct is a perilymphatic space, the seala vestibuli, bounded by the vestibular membrane and the upper wall of the bony canal. Below the cochlear duct is another perilymphatic space, the scala tympani, bounded by the wall of the bony canal, the bony spiral lamina, part of the spiral ligament, and the basilar membrane. The third cavity is the scala media, or cavity of the cochlear duct itself, which is filled with endolymph.

Axial section through one of the whorls of the cochlea

Near the apex of the cochlea the cochlear duct ends a short distance from the end of the bony canal. Consequently the vestibular and tympanic scalae become continuous at this point in a narrow space known as the helicotrema (Fig. 697).

The basal end of the cochlear duct lies against the wall separating the air-filled middle ear cavity from the fluid filled cavity of the bony labyrinth (Fig. 699). At the basal end of the scala vestibuli is the fenestra ovalis, also known as the fenestra vestibuli. This window is closed by a membrane to which the enlarged “lower” end of the stapes is attached. At the basal end of the scala tympani is the fenestra rotunda also known as the fenestra tympani or, more commonly and less appropriately, the fenestra cochleae.

Diagrammatic section through the internal ear of man, showing by arrows the course of vibrations in the perilymph

Inside the cochlear duct and supported on the basilar membrane are orderly rows of differentiated cells running lengthwise, like a striped ribbon, to the tip of the cochlea (Fig. 700). These rows of cells form the organ of Corti, or the receptor apparatus for hearing, named in honor of Alphonso Corti (1822—1876), who in 1851 first discovered many microscopic details of the inner ear.

Cross section through the organ of Corti, within the membranous labyrinth

The most important cells of the organ of Corti in man are the several rows of hair cells, which are the phonoreceptors proper. They are connected with neurons of the auditory nerve that transmit to the auditory centers in the temporal lobes of the cerebral cortex the vibratory stimuli received. The hair cells in the human ear are variously estimated to be from 13,000 to 54,000 in number, each one with perhaps 40 cilia, or “hairs” at the receptive end, projecting into the endolymph. They are arranged along the basilar membrane in two bands separated from each other by two rows of supporting pillar cells that lean against each other so as to form an archway.

The inner band of hair cells consists of a single row while the number of rows in the outer band varies, there being three in the basal coil of the cochlea, four in the middle coil and five in the apical part. The rounded base of each hair cell rests upon a supporting cell, known as a phalangeal cell, which in turn rests upon the basilar membrane. Additional supporting cells make up both the inner and outer edges of the organ of Corti, those of the inner edge being known as border cells, those of the outer edge as the cells of Hensen. The latter grade over into the cells of Claudius which lie along the outer part of the basilar membrane and extend onto the spiral ligament.

From the upper surface of the bony spiral lamina there extends into the endolymph a somewhat flat ribbon-like structure, the membrana tectoria, the outer free edge of which extends as far as the cells of Hensen. Its exact relationships are difficult to determine because its outer free edge tends to curl up when treated with fixing reagents. It is probable that in the living condition its lower surface lightly impinges upon the free ends of the hairlike processes of the hair cells.

Along the inner wall of the cochlear canal, following the line of attachment of the lamina spiralis to the modiolus, is a group of nerve cell bodies making up the spiral ganglion. From this ganglion dendrites run through the lamina into the organ of Corti where their terminal branches are associated with hair cells. The neurites of these neurons run out through the base of the modiolus as the cochlear branch of the acoustic nerve.

Physiology of Hearing

Sound waves, originating at some sonorous outside point in the form of material particles of air hitting upon one another, reach the ear drum and set it into vibration, if the pressure on the two sides is equalized. The vibrations of the drum are handed on to the chain of ear bones that span the tympanic chamber of the middle ear. The last bone in this chain, the stapes, fitting into the fenestra vestibuli, acts as a rocking plunger that agitates the perilymph in the scala vestibuli (Fig. 701).

Schematic representation of the displacement of the stapes, due to the contraction of the stapedius muscle

Pressure changes in the perilymph are transmitted through the thin vestibular membrane to the endolymph within the cochlear duct. These changes cause movements of the basilar membrane which not only lead to stimulation of the cochlear nerve, as described below, but also affect the pressure in the scala tympani. Any tendency to generate excessive pressure in the practically incompressible fluids of the internal ear is offset by the secondary tympanic membrane which bulges outward, into the middle ear cavity, with each inward movement of the stapes. The passage of fluid through the helicotrema, as an aid in equalizing pressure differences in the two perilymphatic scalae, is now considered to be of negligible significance because of the small diameter of this region, located at the point farthest from the stapes which brings about the initial pressure changes in the fluid.

According to the most generally accepted theory of hearing, a modification of the resonance theory proposed by Helmholtz many years ago, any given frequency causes most vigorous movements of only a localized area of the ribbon-like basilar membrane. There is thus a place on the membrane for each pitch (or frequency); hence, this is known as the place theory of hearing. Striking of the hair-cell “hairs” of the affected region against the tectorial membrane stimulates their associated nerve endings. Impulses carried by certain fibers of the cochlear nerve are then interpreted by the cerebral cortex as particular tones. In support of this theory is the work which has shown that the higher audible frequencies stimulate fibers associated with the basal part of the cochlear duct, where the basilar membrane is narrowest, while low frequencies affect the apical region where the membrane is widest (Fig. 702).

Scheme of basilar membrane of the cochlea, represented as rolled out flat, to show distribution of pitch reception along the membrane

The amplitude of the vibrations determines the loudness of the tones produced, while the pitch, whether it be high or low, is correlated with the frequency, or relative number of vibrations per unit of time. The quality, or timbre, of a tone, by which the difference between a human voice and a violin, for example, is detected when producing the same musical note, is dependent upon the character, or shape, of the sound waves when visually recorded, as also upon the overtones, or accompanying sympathetic vibrations of different harmonious nodal lengths which may be added to the fundamental tone. Vibrations without uniformity in wave length or shape fall upon the ear as “noises,” while vibrations repeated with regularity of form and shape give rise to “tones.”

Comparative Anatomy

There is no ear in amphioxus. Among cyclostomes the membranous labyrinth in Myxine is a simple undifferentiated sac with one single semicircular canal. In Petromyzon two canals are present, with a constriction in the sac that indicates the beginning of a separation into utriculus and sacculus. A macula communis in the saccular end, along with a crista in each ampulla, represents the nerve terminals.

In fishes generally the ear hardly rises above the static function of equilibration. Three well-developed semicircular canals and a primitive sacculus, provided with otoconia or an otolith, offer anatomical evidence that the ear of fishes is static rather than auditory in function. On the posterior side of the sacculus is a small outpocketing, the lagena, in which is a sensory area, the macula lagenae, of doubtful function (Fig. 703). There are also cristae ampullares, in the semicircular canals, a macula utriculi and a macula sacculi. In addition these animals have another utricular sensory area, the macula neglecta, which is double in some cases. It is extremely doubtful whether fishes can “hear,” although they respond readily to certain types of jarring or vibration, by means of their lateral-line organs. Whatever vibrations from the surrounding water reach the labyrinth of the ear, do so through the skull or through the spiracular opening, for no middle ear or outer passage-way is yet elaborated. Another reason why fishes are probably oblivious to sounds borne on the air is that, although sound waves transferred under water or through solid objects, as a telegraph wire for example, travel more readily than in air, it is very difficult for vibrations to pass unhindered from thin air into the denser medium of water.

Lateral-view diagrams of the left labyrinth of the ear

In frogs and toads but not in urodcles, the spiracular cleft enlarges into the tympanic cavity, which is not properly a “middle ear” since no externa] ear is present. A large external ear drum, connccted by a columella with the internal ear, is placed at the level of the skin, and is consequently much exposed to injury. The first true auditory nerve terminals appear in amphibians in the form of the macula neglecta and the papilla basilaris, the latter structure being of importance since it is the forerunner of the organ of Corti which becomes incorporated within the lagena that later coils to form, the cochlea duct.

The macula neglecta continues to be represented in reptiles and birds but disappears in mammals. The ear drum becomes sunken in reptiles and birds, forming a pit which is the beginning of the external auditory canal. Some lizards and crocodiles have an earfold at the margin of the pit which foreshadows the pinna of the mammalian ear. By means of this fold an alligator is enabled to close the short auditory canal while submerged in water. “Homed owls” and certain other birds have the earfold supplemented by upstanding feathers. The tympanic cavity of snakes and legless lizards is much reduced or absent, since direct contact with the ground is the means employed for the reception of seismic vibrations on the part of these highly thigmotactic animals. In birds and crocodiles the two Eustachian canals form a median duct that enters the mid-dorsal region of the pharynx by a single opening. The lagena elongates and becomes slightly curved in crocodiles and birds.

In mammals the lagena curves still more to form the compact spiral space-saving cochlea. The number of turns in the cochlea of various mammals is as follows: Echidna, 1/2; whale, 1/2; horse, 2; rabbit, 2 1/2; man, 2 3/4; cat, 3; cow, 3 1/2; pig, 4; South American “paca,” Coelogenys, 5. The cochlear duct becomes attached along two sides of the bony canal thus dividing the perilymphatic space into the scalae vestibuli and tympani. The establishment of the fenestra tympani as a safety valve against excessive vibrations is a further mammalian refinement. The malleus and incus of the middle ear are also added in mammals, while the auditory canal of the outer ear becomes elongated and bent, thus affording greater protection to the ear drum.