Guyton and Hall Physiology Chapter 53 - The Sense of Hearing PDF

CHAPTER 53 UNIT X The Sense of Hearing This chapter describes the me...

CHAPTER 53 UNIT X The Sense of Hearing This chapter describes the mechanisms whereby the ear malleus moves, the incus moves with it. The opposite end receives sound waves, discriminates their frequencies, of the incus articulates with the stem of the stapes, and the and transmits auditory information into the central ner- faceplate of the stapes lies against the membranous laby- vous system, where its meaning is deciphered. rinth of the cochlea in the opening of the oval window. The tip end of the handle of the malleus is attached to the center of the tympanic membrane, and this point TYMPANIC MEMBRANE AND THE of attachment is constantly pulled by the tensor tympani OSSICULAR SYSTEM muscle, which keeps the tympanic membrane tensed. This tension allows sound vibrations on any portion of CONDUCTION OF SOUND FROM THE the tympanic membrane to be transmitted to the ossicles, TYMPANIC MEMBRANE TO THE COCHLEA which would not occur if the membrane were lax. Figure 53-1 shows the tympanic membrane (commonly The ossicles of the middle ear are suspended by liga- called the eardrum) and the ossicles, which conduct sound ments in such a way that the combined malleus and incus from the tympanic membrane through the middle ear act as a single lever, having its fulcrum approximately at to the cochlea (the inner ear). Attached to the tympanic the border of the tympanic membrane. membrane is the handle of the malleus. The malleus is The articulation of the incus with the stapes causes bound to the incus by minute ligaments, so whenever the the stapes to (1) push forward on the oval window and OUTER EAR MIDDLE EAR INNER EAR Malleus Stapes Scala tympani Incus Scala vestibuli Vestibular nerve Cochlear nerve Auditory canal External acoustic meatus Cochlea Tensor tympani Stapedius muscle muscle Tympanic Oval Round membrane window window Eustachian tube Figure 53-1. The outer ear, tympanic membrane, and ossicular system of the middle ear and inner ear. 663 UNIT X The Nervous System: B. The Special Senses on the cochlear fluid on the other side of window every Another function of the tensor tympani and stapedius time the tympanic membrane moves inward; and (2) muscles is to decrease a person’s hearing sensitivity to his pull backward on the fluid every time the malleus moves or her own speech. This effect is activated by collateral outward. nerve signals transmitted to these muscles at the same time that the brain activates the voice mechanism. “Impedance Matching” by the Ossicular System. The amplitude of movement of the stapes faceplate with each sound vibration is only three-fourths as much as the ampli- TRANSMISSION OF SOUND THROUGH tude of the handle of the malleus. Therefore, the ossicular BONE lever system does not increase the movement distance of Because the inner ear, the cochlea, is embedded in a bony the stapes, as is commonly believed. Instead, the system ac- cavity in the temporal bone, called the bony labyrinth, vibra- tually reduces the distance but increases the force of move- tions of the entire skull can cause fluid vibrations in the ment about 1.3 times. In addition, the surface area of the cochlea. Therefore, under appropriate conditions, a tuning tympanic membrane is about 55 square millimeters, where- fork or an electronic vibrator placed on any bony protuber- as the surface area of the stapes averages 3.2 square millim- ance of the skull, but especially on the mastoid process near eters. This 17-fold difference times the 1.3-fold ratio of the the ear, causes the person to hear the sound. However, the lever system causes about 22 times as much total force to be energy available even in loud sound in the air is not sufficient exerted on the fluid of the cochlea as is exerted by the sound to cause hearing via bone conduction unless a special electro- waves against the tympanic membrane. Because fluid has mechanical sound-amplifying device is applied to the bone. far greater inertia than air does, increased amounts of force are necessary to cause vibration in the fluid. Therefore, the tympanic membrane and ossicular system provide imped- COCHLEA ance matching between the sound waves in air and the sound vibrations in the fluid of the cochlea. The impedance FUNCTIONAL ANATOMY OF THE matching is about 50% to 75% of perfect for sound frequen- COCHLEA cies between 300 and 3000 cycles/sec, which allows utiliza- The cochlea is a system of coiled tubes, shown in tion of most of the energy in the incoming sound waves. Figure 53-1 and in cross section in Figure 53-2. It con- In the absence of the ossicular system and tympanic sists of three tubes coiled side by side: (1) the scala ves- membrane, sound waves can still travel directly through tibuli; (2) the scala media; and (3) the scala tympani. The the air of the middle ear and enter the cochlea at the oval scala vestibuli and scala media are separated from each window. However, the sensitivity for hearing is then 15 to 20 other by Reissner’s membrane (also called the vestibular decibels less than for ossicular transmission—equivalent to membrane), shown in Figure 53-2B; the scala tympani a decrease from a medium to a barely perceptible voice level. and scala media are separated from each other by the Attenuation of Sound by Contraction of the Tensor basilar membrane. On the surface of the basilar mem- Tympani and Stapedius Muscles. When loud sounds brane lies the organ of Corti, which contains a series of are transmitted through the ossicular system and from electromechanically sensitive cells, the hair cells. They are there into the central nervous system, a reflex occurs af- the receptive end organs that generate nerve impulses in ter a latent period of only 40 to 80 milliseconds to cause response to sound vibrations. contraction of the stapedius muscle and, to a lesser extent, Figure 53-3 diagrams the functional parts of the the tensor tympani muscle. The tensor tympani muscle uncoiled cochlea for conduction of sound vibrations. pulls the handle of the malleus inward while the stape- First, note that Reissner’s membrane is missing from this dius muscle pulls the stapes outward. These two forces figure. This membrane is so thin and so easily moved that oppose each other and thereby cause the entire ossicular it does not obstruct the passage of sound vibrations from system to develop increased rigidity, thus greatly reducing the scala vestibuli into the scala media. Therefore, as far as the ossicular conduction of low-frequency sound, mainly fluid conduction of sound is concerned, the scala vestibuli frequencies below 1000 cycles/sec. and scala media are considered to be a single chamber. As This attenuation reflex can reduce the intensity of discussed later, Reissner’s membrane maintains a special lower frequency sound transmission by 30 to 40 decibels, kind of fluid in the scala media that is required for normal which is about the same difference as that between a loud function of the sound-receptive hair cells. voice and a whisper. The function of this mechanism is Sound vibrations enter the scala vestibuli from the believed to be twofold—to protect the cochlea from dam- faceplate of the stapes at the oval window. The faceplate aging vibrations caused by excessively loud sound and to covers this window and is connected with the window’s mask low-frequency sounds in loud environments. Mask- edges by a loose annular ligament so that it can move ing usually removes a major share of the background inward and outward with the sound vibrations. Inward noise and allows a person to concentrate on sounds above movement causes the fluid to move forward in the scala 1000 cycles/sec, where most of the pertinent information vestibuli and scala media, and outward movement causes in voice communication is transmitted. the fluid to move backward. 664  Chapter 53 The Sense of Hearing Helicotrema distal ends, except that the distal ends are embedded in (connection between scala the loose basilar membrane. Because the fibers are stiff vestibuli and scala tympani) Scala vestibuli and free at one end, they can vibrate like the reeds of a harmonica. Stria vascularis The lengths of the basilar fibers increase progressively, beginning at the oval window and going from the base of UNIT X Scala media the cochlea to the apex, increasing from a length of about 0.04 millimeter near the oval and round windows to 0.5 Organ of Corti millimeter at the tip of the cochlea (the “helicotrema”), a 12-fold increase in length. Scala The diameters of the fibers, however, decrease from tympani the oval window to the helicotrema, so their overall stiff- ness decreases more than 100-fold. As a result, the stiff, Modiolus short fibers near the oval window of the cochlea vibrate Spiral best at a very high frequency, whereas the long, limber ganglion Cochlear nerve fibers near the tip of the cochlea vibrate best at a low frequency. A Thus, high-frequency resonance of the basilar mem- Tectorial membrane brane occurs near the base, where the sound waves Reissner's membrane enter the cochlea through the oval window. However, low-frequency resonance occurs near the helicotrema, Stria mainly because of the less stiff fibers but also because of vascularis Scala vestibuli Spiral increased “loading” with extra masses of fluid that must Scala vibrate along the cochlear tubules. limbus media Spiral prominence TRANSMISSION OF SOUND WAVES IN THE COCHLEA—“TRAVELING WAVE” Organ Scala tympani When the foot of the stapes moves inward against the oval of Corti window, the round window must bulge outward because Basilar the cochlea is bounded on all sides by bony walls. The ini- membrane tial effect of a sound wave entering at the oval window is to Spiral ganglion B cause the basilar membrane at the base of the cochlea to Figure 53-2. The cochlea (A) and section through one of the turns bend in the direction of the round window. However, the of the cochlea (B). elastic tension that is built up in the basilar fibers as they bend toward the round window initiates a fluid wave that “travels” along the basilar membrane toward the helico- Oval Scala vestibuli trema. Figure 53-4A shows movement of a high-frequency Stapes window and scala media wave down the basilar membrane, Figure 53-4B shows a medium-frequency wave, and Figure 53-4C shows a very low-frequency wave. Movement of the wave along the basi- lar membrane is comparable to the movement of a pressure wave along the arterial walls, discussed in Chapter 15; it is Round Scala Basilar Helicotrema also comparable to a wave that travels along the surface of window tympani membrane a pond. Figure 53-3. Movement of fluid in the cochlea after forward thrust Vibration Patterns of the Basilar Membrane for of the stapes. Different Sound Frequencies. Note in Figure 53-4 the different patterns of transmission for sound waves of dif- Basilar Membrane and Resonance in the Cochlea. ferent frequencies. Each wave is relatively weak at the The basilar membrane is a fibrous membrane that sepa- outset but becomes strong when it reaches the portion rates the scala media from the scala tympani. It contains of the basilar membrane that has a natural resonant fre- 20,000 to 30,000 basilar fibers that project from the bony quency equal to the respective sound frequency. At this center of the cochlea, the modiolus, toward the outer point, the basilar membrane can vibrate back and forth wall. These fibers are stiff, elastic, reedlike structures that with such ease that the energy in the wave is dissipated. are fixed at their basal ends in the central bony structure Consequently, the wave dies at this point and fails to of the cochlea (the modiolus) but are not fixed at their travel the remaining distance along the basilar membrane. 665 UNIT X The Nervous System: B. The Special Senses b a c A High frequency d B Medium frequency A Frequency (cycles/sec) 8000 4000 2000 1000 600 400 200 C Low frequency 0 5 10 15 20 25 30 35 Figure 53-4. “Traveling waves” along the basilar membrane for high- (A), medium- (B), and low-frequency (C) sounds. B Distance from stapes (millimeters) Figure 53-5. A, Amplitude pattern of vibration of the basilar mem- brane for a medium-frequency sound (a–d). B, Amplitude patterns Thus, a high-frequency sound wave travels only a short for sounds of frequencies between 200 and 8000 cycles/sec, showing the points of maximum amplitude on the basilar membrane for the distance along the basilar membrane before it reaches different frequencies. its resonant point and dies, a medium-frequency sound wave travels about halfway and then dies, and a very low- frequency sound wave travels the entire distance along whereby the scala tympani and scala vestibuli communi- the membrane. cate (Figure 53-2). Another feature of the traveling wave is that it travels The principal method whereby sound frequencies are fast along the initial portion of the basilar membrane but discriminated from one another is based on the “place” of becomes progressively slower as it goes farther into the maximum stimulation of the nerve fibers from the organ cochlea. The cause of this difference is the high coefficient of Corti lying on the basilar membrane, as explained in of elasticity of the basilar fibers near the oval window and a the next section. progressively decreasing coefficient farther along the mem- brane. This rapid initial transmission of the wave allows the FUNCTION OF THE ORGAN OF CORTI high-frequency sounds to travel far enough into the cochlea The organ of Corti, shown in Figure 53-2 and Figure to spread out and separate from one another on the basilar 53-6, is the receptor organ that generates nerve impulses membrane. Without this rapid initial transmission, all the in response to vibration of the basilar membrane. Note high-frequency waves would be bunched together within that the organ of Corti lies on the surface of the basilar the first millimeter or so of the basilar membrane, and their fibers and basilar membrane. The actual sensory recep- frequencies could not be discriminated. tors in the organ of Corti are two specialized types of Vibration Amplitude Pattern of the Basilar nerve cells called hair cells—a single row of internal (or Membrane. The dashed curves of Figure 53-5A show “inner”) hair cells, numbering about 3500 and measuring the position of a sound wave on the basilar membrane about 12 micrometers in diameter, and three or four rows when the stapes is (a) all the way inward, (b) has moved of external (or “outer”) hair cells, numbering about 12,000 back to the neutral point, (c) is all the way outward, and and having diameters of only about 8 micrometers. The (d) has moved back again to the neutral point but is mov- bases and sides of the hair cells synapse with a network ing inward. The shaded area around these different waves of cochlear nerve endings. Between 90% and 95% of these shows the extent of vibration of the basilar membrane endings terminate on the inner hair cells, emphasizing during a complete vibratory cycle. This is the amplitude their special importance for detection of sound. pattern of vibration of the basilar membrane for this par- The nerve fibers stimulated by the hair cells lead to the ticular sound frequency. spiral ganglion of Corti, which lies in the modiolus (cen- Figure 53-5B shows the amplitude patterns of vibra- ter) of the cochlea. The spiral ganglion neuronal cells send tion for different frequencies, demonstrating that the axons—a total of about 30,000—into the cochlear nerve maximum amplitude for sound at 8000 cycles/sec occurs and then into the central nervous system at the level of near the base of the cochlea, whereas that for frequencies the upper medulla. The relation of the organ of Corti to less than 200 cycles/sec is all the way at the tip of the basi- the spiral ganglion and to the cochlear nerve is shown in lar membrane near the helicotrema, the minute opening Figure 53-2. 666  Chapter 53 The Sense of Hearing Tectorial membrane Tectorial membrane Stereocilia Reticular lamina Outer hair cells Inner hair cells Modiolus UNIT X Hair cells A Rods of Corti Basilar fiber Basilar fiber Tip link protein Spiral ganglion K+ Cochlear nerve Figure 53-6. The organ of Corti, showing especially the hair cells and K+ channel the tectorial membrane pressing against the projecting hairs. K+ Excitation of the Hair Cells. Note in Figure 53-6 that K+ minute hairs, or stereocilia, project upward from the hair cells and either touch or are embedded in the surface gel Stereocilia coating of the tectorial membrane, which lies above the K+ stereocilia in the scala media. These hair cells are similar to the hair cells found in the macula and cristae ampul- laris of the vestibular apparatus, discussed in Chapter 56. Bending of the hairs in one direction depolarizes the hair cells, and bending in the opposite direction hyperpolar- izes them. This in turn excites the auditory nerve fibers synapsing with their bases. K+ K+ K+ K+ Figure 53-7A shows the mechanism whereby vibra- Membrane tion of the basilar membrane excites the hair endings. The depolarization outer ends of the hair cells are fixed tightly in a rigid struc- ture composed of a flat plate, called the reticular lamina, supported by triangular rods of Corti, which are attached tightly to the basilar fibers. The basilar fibers, the rods of Corti, and the reticular lamina move as a rigid unit. Ca2+ Ca2+ Upward movement of the basilar fiber rocks the retic- ular lamina upward and inward toward the modiolus. Then, when the basilar membrane moves downward, the reticular lamina rocks downward and outward. The inward and outward motion causes the hairs on the hair cells to shear back and forth against the tectorial mem- Glutamate brane. Thus, the hair cells are excited whenever the basilar Afferent membrane vibrates. neuron Spiral Auditory Signals Are Transmitted Mainly by the ganglion Inner Hair Cells. Even though there are three to four times as many outer hair cells as inner hair cells, about 90% of the auditory nerve fibers are stimulated by the inner cells rather than by the outer cells. Nonetheless, if the outer B cells are damaged while the inner cells remain fully func- Figure 53-7. A, Stimulation of the hair cells by to and fro movement tional, a large amount of hearing loss occurs. Therefore, it of the hairs projecting into the gel coating of the tectorial membrane. has been proposed that the outer hair cells in some way B, Transduction of mechanical energy into neural signals by the hair control the sensitivity of the inner hair cells at different cells. When the stereocilia are bent in the direction of the longer ones, K+ channels are opened, causing depolarization, which in turn sound pitches, a phenomenon called “tuning” of the re- opens voltage-gated Ca2+ channels. The influx of Ca2+ augments the ceptor system. In support of this concept, a large number depolarization and elicits release of the excitatory transmitter gluta- of retrograde nerve fibers pass from the brain stem to the mate, which depolarizes the sensory nerve. 667 UNIT X The Nervous System: B. The Special Senses vicinity of the outer hair cells. Stimulating these nerve fib- The importance of the endocochlear potential is that the ers can actually cause shortening of the outer hair cells tops of the hair cells project through the reticular lamina and and possibly also change their degree of stiffness. These are bathed by the endolymph of the scala media, whereas per- effects suggest a retrograde nervous mechanism for con- ilymph bathes the lower bodies of the hair cells. Furthermore, the hair cells have a negative intracellular potential of −70 trol of the ear’s sensitivity to different sound pitches, acti- millivolts with respect to the perilymph but −150 millivolts vated through the outer hair cells. with respect to the endolymph at their upper surfaces, where Hair Cell Receptor Potentials and Excitation of Audi- the hairs project through the reticular lamina and into the tory Nerve Fibers. The stereocilia (i.e., the “hairs” pro- endolymph. It is believed that this high electrical potential at truding from the ends of the hair cells) are stiff structures the tips of the stereocilia sensitizes the cell an extra amount, thereby increasing its ability to respond to the slightest sound. because each has a rigid protein framework. Each hair cell has about 100 stereocilia on its apical border. These ste- DETERMINATION OF SOUND reocilia become progressively longer on the side of the hair FREQUENCY—THE “PLACE” PRINCIPLE cell away from the modiolus. The tops of the shorter ste- reocilia are attached by thin filaments to the back sides of From earlier discussions in this chapter, it is apparent that their adjacent longer stereocilia. Therefore, whenever the low-frequency sounds cause maximal activation of the basilar cilia are bent in the direction of the longer ones, the tips of membrane near the apex of the cochlea, and high-frequency the smaller stereocilia are tugged outward from the surface sounds activate the basilar membrane near the base of the of the hair cell. This causes a mechanical transduction that cochlea. Intermediate-frequency sounds activate the mem- opens 200 to 300 cation-conducting channels, allowing for brane at intermediate distances between the two extremes. the rapid movement of positively charged potassium ions Furthermore, there is spatial organization of the nerve fibers from the surrounding scala media fluid into the stereocilia, in the cochlear pathway, all the way from the cochlea to the which causes depolarization of the hair cell membrane (see cerebral cortex. Recording of signals in the auditory tracts of Figure 53-7B). The depolarization opens voltage-sensitive the brain stem and in the auditory receptive fields of the cere- calcium channels and causes influx of calcium ions, which bral cortex shows that specific brain neurons are activated augments the depolarization. Repolarization of the hair by specific sound frequencies. Therefore, the major method cell occurs mainly by exit of potassium ions through cal- used by the nervous system to detect different sound frequen- cium ion–sensitive potassium channels. cies is to determine the positions along the basilar membrane Thus, when the basilar fibers bend toward the scala that are stimulated the most, called the place principle for the vestibuli, the hair cells depolarize, and in the opposite determination of sound frequency. direction they hyperpolarize, thereby generating an alter- Referring again to Figure 53-5, one can see that the nating hair cell receptor potential that, in turn, stimulates distal end of the basilar membrane at the helicotrema is the cochlear nerve endings that synapse with the bases stimulated by all sound frequencies below 200 cycles/sec. of the hair cells. It is believed that the rapidly acting neu- Therefore, it has been difficult to understand from the place rotransmitter glutamate is released by the hair cells at principle how one can differentiate between low sound fre- these synapses during depolarization. quencies in the range of 200 down to 20 cycles/sec. These low frequencies have been postulated to be discriminated Endocochlear Potential. To explain even more fully the mainly by the so-called volley or frequency principle. That electrical potentials generated by the hair cells, we need to is, low-frequency sounds, from 20 to 1500 to 2000 cycles/ explain another electrical phenomenon called the endo- sec, can cause volleys of nerve impulses synchronized at cochlear potential. The scala media is filled with a fluid called the same frequencies, and these volleys are transmitted by endolymph, in contradistinction to the perilymph present in the cochlear nerve into the cochlear nuclei of the brain. It is the scala vestibuli and scala tympani. The scala vestibuli and scala tympani communicate directly with the subarachnoid further suggested that the cochlear nuclei can distinguish space around the brain, so the perilymph is almost identical the different frequencies of the volleys. In fact, destruction to cerebrospinal fluid. Conversely, the endolymph that fills of the entire apical half of the cochlea, which destroys the the scala media is an entirely different fluid secreted by the basilar membrane where all lower frequency sounds are stria vascularis, a highly vascular area on the outer wall of normally detected, does not totally eliminate discrimina- the scala media. Endolymph contains a high concentration tion of the lower frequency sounds. of potassium and a low concentration of sodium, which is exactly opposite to the contents of perilymph. DETERMINATION OF LOUDNESS An electrical potential of about +80 millivolts exists all the time between endolymph and perilymph, with posi- Loudness is determined by the auditory system in at least tivity inside the scala media and negativity outside. This three ways. is called the endocochlear potential, and it is generated by First, as the sound becomes louder, the amplitude continual secretion of positive potassium ions into the sca- of vibration of the basilar membrane and hair cells also la media by the stria vascularis. increases so that the hair cells excite the nerve endings at more rapid rates. 668  Chapter 53 The Sense of Hearing Second, as the amplitude of vibration increases, it Vibration Sound causes more and more of the hair cells on the fringes of 100 Pricking (0 decibel = 1 dyne/cm2) 80 (in middle ear) the resonating portion of the basilar membrane to become Pressure (decibels) stimulated, thus causing spatial summation of impulses— 60 that is, transmission through many nerve fibers rather 40 Tactual 20 threshold than through only a few. UNIT X Third, the outer hair cells do not become stimulated 0 Threshold significantly until vibration of the basilar membrane –20 of hearing –40 reaches high intensity, and stimulation of these cells pre- –60 sumably apprises the nervous system that the sound is Reference loud. – 80 - pressure = 73.8 1 2 5 10 20 100 500 2000 10,000 Detection of Changes in Loudness—The Power Law. Frequency (cycles/sec) As pointed out in Chapter 47, a person interprets changes Figure 53-8. Relation of the threshold of hearing and of somesthetic in intensity of sensory stimuli approximately in propor- perception (pricking and tactual threshold) to the sound energy level tion to an inverse power function of the actual intensity. at each sound frequency. In the case of sound, the interpreted sensation changes approximately in proportion to the cube root of the ac- sound pressure level, the sound range is 500 to 5000 cy- tual sound intensity. To express this concept in another cles/sec; only with intense sounds can the complete range way, the ear can discriminate differences in sound inten- of 20 to 20,000 cycles be achieved. In old age, this fre- sity from the softest whisper to the loudest possible noise, quency range is usually shortened to 50 to 8,000 cycles/ representing an approximately 1 trillion times increase sec or less, as discussed later in this chapter. in sound energy or 1 million times increase in amplitude of movement of the basilar membrane. Yet, the ear inter- prets this much difference in sound level as approximately CENTRAL AUDITORY MECHANISMS a 10,000-fold change. Thus, the scale of intensity is greatly “compressed” by the sound perception mechanisms of the AUDITORY NERVOUS PATHWAYS auditory system, which allows a person to interpret dif- Figure 53-9 shows the major auditory pathways. Nerve ferences in sound intensities over a far wider range than fibers from the spiral ganglion of Corti enter the dorsal would be possible were it not for compression of the in- and ventral cochlear nuclei located in the upper part of the tensity scale. medulla. At this point, all the fibers synapse, and second- Decibel Unit. Because of the extreme changes in sound order neurons pass mainly to the opposite side of the intensities that the ear can detect and discriminate, sound brain stem to terminate in the superior olivary nucleus. A intensities are usually expressed in terms of the logarithm few second-order fibers also pass to the superior olivary of their actual intensities. A 10-fold increase in sound en- nucleus on the same side. ergy is called 1 bel, and 0.1 bel is called 1 decibel. One From the superior olivary nucleus, the auditory path- decibel represents an actual increase in sound energy of way passes upward through the lateral lemniscus. Some 1.26 times. of the fibers terminate in the nucleus of the lateral lem- Another reason for using the decibel system to express niscus, but many fibers bypass this nucleus and travel on changes in loudness is that in the usual sound intensity to the inferior colliculus, where all or almost all the audi- range for communication, the ears can barely distinguish tory fibers synapse. From there, the pathway passes to the an approximately 1-decibel change in sound intensity. medial geniculate nucleus, where all the fibers do synapse. Finally, the pathway proceeds via auditory radiation to Threshold for Hearing Sound at Different the auditory cortex, located mainly in the superior gyrus Frequencies. Figure 53-8 shows the pressure thresholds of the temporal lobe. at which sounds of different frequencies can barely be Several important points should be noted. First, signals heard by the ear. This figure demonstrates that a 3,000 cy- from both ears are transmitted through the pathways of cles/sec sound can be heard even when its intensity is as both sides of the brain, with a preponderance of transmis- low as 70 decibels below 1 dyne/cm2 sound pressure level, sion in the contralateral pathway. In at least three places which is one ten-millionth microwatt per square centim- in the brain stem, crossing over occurs between the two eter. Conversely, a 100 cycles/sec sound can be detected pathways: (1) in the trapezoid body; (2) in the commissure only if its intensity is 10,000 times as great as this. between the two nuclei of the lateral lemnisci; and (3) in Frequency Range of Hearing. The frequencies of sound the commissure connecting the two inferior colliculi. that a young person can hear are between 20 and 20,000 Second, many collateral fibers from the auditory cycles/sec. However, referring again to Figure 53-8, we tracts pass directly into the reticular activating system of see that the sound range depends to a great extent on the brain stem. This system projects diffusely upward in loudness. If the loudness is 60 decibels below 1 dyne/cm2 the brain stem and downward into the spinal cord and 669 UNIT X The Nervous System: B. The Special Senses Firing Rates at Different Levels of the Auditory Pathways. Single nerve fibers entering the cochlear nuclei from the auditory nerve can fire at rates up to at least 1000/ sec, with the rate being determined mainly by the loud- ness of the sound. At sound frequencies up to 2000 to 4000 cycles/sec, the auditory nerve impulses are often synchro- nized with the sound waves, but they do not necessarily occur with every wave. In the auditory tracts of the brain stem, the firing is usually no longer synchronized with the sound frequency, Primary auditory except at sound frequencies below 200 cycles/sec. Above cortex the level of the inferior colliculi, even this synchronization Midbrain is mainly lost. These findings demonstrate that the sound Medial geniculate signals are not transmitted unchanged directly from the ear nucleus to the higher levels of the brain; instead, information from (thalamus) the sound signals begins to be dissected from the impulse traffic at levels as low as the cochlear nuclei. We will have more to say about this subject later, especially in relation to Inferior perception of direction from which sound comes. Midbrain colliculus FUNCTION OF THE CEREBRAL CORTEX IN HEARING The projection area of auditory signals to the cerebral cor- tex is shown in Figure 53-10, which demonstrates that Nucleus of the auditory cortex lies principally on the supratempo- Pons the lateral ral plane of the superior temporal gyrus but also extends lemniscus onto the lateral side of the temporal lobe, over much of the insular cortex, and even onto the lateral portion of the parietal operculum. Two separate subdivisions are shown in Figure 53- Pons 10—the primary auditory cortex and the auditory asso- ciation cortex (also called the secondary auditory cortex). Superior olivary The primary auditory cortex is directly excited by projec- Dorsal acoustic stria nucleus tions from the medial geniculate body, whereas the audi- Intermediate tory association areas are excited secondarily by impulses acoustic site from the primary auditory cortex, as well as by some pro- Medulla jections from thalamic association areas adjacent to the Cochlear nuclei medial geniculate body. Sound Frequency Perception in the Primary N. VIlI Trapezoid Auditory Cortex. At least six tonotopic maps have been body described in the primary auditory cortex and auditory association areas. In each of these maps, high-frequency sounds excite neurons at one end of the map, whereas Figure 53-9. Auditory nervous pathways. N., Nerve. low-frequency sounds excite neurons at the opposite end. In most maps, the low-frequency sounds are located ante- activates the entire nervous system in response to loud riorly, as shown in Figure 53-10, and the high-frequency sounds. Other collaterals go to the vermis of the cerebel- sounds are located posteriorly. This setup is not true for lum, which is also activated instantaneously in the event all the maps. of a sudden noise. Why does the auditory cortex have so many different Third, a high degree of spatial orientation is maintained tonotopic maps? The answer, presumably, is that each of in the fiber tracts from the cochlea all the way to the cor- the separate areas dissects out some specific feature of tex. In fact, there are three spatial patterns for termination the sounds. For example, one of the large maps in the pri- of the different sound frequencies in the cochlear nuclei, mary auditory cortex almost certainly discriminates the two patterns in the inferior colliculi, one precise pattern sound frequencies and gives the person the psychic sen- for discrete sound frequencies in the auditory cortex, and sation of sound pitches. Another map is probably used to at least five other less precise patterns in the auditory cor- detect the direction from which the sound comes. Other tex and auditory association areas. auditory cortex areas detect special qualities, such as the 670  Chapter 53 The Sense of Hearing Low frequency High frequency Indeed, the parietal portion of the auditory association cortex partly overlaps somatosensory area II, which could provide an opportunity for the association of auditory information with somatosensory information. Discrimination of Sound “Patterns” by the Auditory UNIT X Cortex. Complete bilateral removal of the auditory cortex does not prevent a cat or monkey from detecting sounds or reacting in a crude manner to sounds. However, it does greatly reduce or sometimes even abolish the animal’s ability to discriminate different sound pitches and espe- cially patterns of sound. For example, an animal that has Association Primary been trained to recognize a combination or sequence of tones, one following the other in a particular pattern, los- es this ability when the auditory cortex is destroyed; fur- thermore, the animal cannot relearn this type of response. Therefore, the auditory cortex is especially important in the discrimination of tonal and sequential sound patterns. Destruction of both primary auditory cortices in the Association human being greatly reduces one’s sensitivity for hear- Primary ing. Destruction of one side only slightly reduces hearing in the opposite ear; it does not cause deafness in the ear because of many crossover connections from side to side in the auditory neural pathway. However, it does affect one’s ability to localize the source of a sound because comparative signals in both cortices are required for sound localization. Figure 53-10. Auditory cortex. Lesions that affect the auditory association areas but not the primary auditory cortex do not decrease a per- sudden onset of sounds, or perhaps special modulations, son’s ability to hear and differentiate sound tones or even such as noise versus pure frequency sounds. to interpret at least simple patterns of sound. However, The frequency range to which each individual neuron the person is often unable to interpret the meaning of the in the auditory cortex responds is much narrower than sound heard. For example, lesions in the posterior portion that in the cochlear and brain stem relay nuclei. Referring of the superior temporal gyrus, which is called Wernicke’s to Figure 53-5B, note that the basilar membrane near the area and is part of the auditory association cortex, often base of the cochlea is stimulated by sounds of all frequen- make it impossible for a person to interpret the meanings cies and, in the cochlear nuclei, this same breadth of sound of words even though he or she hears them perfectly well representation is found. Yet, by the time the excitation and can even repeat them. These functions of the auditory has reached the cerebral cortex, most sound-responsive association areas and their relation to the overall intellec- neurons respond only to a narrow range of frequencies tual functions of the brain are discussed in Chapter 58. rather than to a broad range. Therefore, somewhere along the pathway, processing mechanisms “sharpen” the fre- DETERMINATION OF THE DIRECTION quency response. This sharpening effect is believed to be FROM WHICH SOUND COMES caused mainly by lateral inhibition, discussed in Chapter 47 in relation to mechanisms for transmitting informa- A person determines the horizontal direction from which tion in nerves. That is, stimulation of the cochlea at one sound comes by two principal means: (1) the time lag frequency inhibits sound frequencies on both sides of this between the entry of sound into one ear and its entry into primary frequency; this inhibition is caused by collateral the opposite ear; and (2) the difference between the inten- fibers angling off the primary signal pathway and exert- sities of the sounds in the two ears. ing inhibitory influences on adjacent pathways. This same The first mechanism functions best at frequencies effect is important in sharpening patterns of somesthetic below 3000 cycles/sec, and the second mechanism oper- images, visual images, and other types of sensations. ates best at higher frequencies because the head is a Many of the neurons in the auditory cortex, especially greater sound barrier at these frequencies. The time lag in the auditory association cortex, do not respond only mechanism discriminates direction much more exactly to specific sound frequencies in the ear. It is believed than the intensity mechanism because it does not depend that these neurons “associate” different sound frequen- on extraneous factors but only on the exact interval of cies with one another or associate sound information time between two acoustical signals. If a person is look- with information from other sensory areas of the cortex. ing straight toward the source of the sound, the sound 671 UNIT X The Nervous System: B. The Special Senses reaches both ears at exactly the same instant, whereas if This mechanism for detection of sound direction indi- the right ear is closer to the sound than the left ear is, the cates again how specific information in sensory signals is sound signals from the right ear enter the brain ahead of dissected out as the signals pass through different levels of those from the left ear. neuronal activity. In this case, the “quality” of sound direc- These two mechanisms cannot tell whether the sound tion is separated from the “quality” of sound tones at the is emanating from in front of or behind the person or from level of the superior olivary nuclei. above or below. This discrimination is achieved mainly by Centrifugal Signals From the Central Nervous the pinnae (the visible outer part), which act as funnels System to Lower Auditory Centers to direct the sound into the two ears. The shape of the pinna changes the quality of the sound entering the ear, Retrograde pathways have been demonstrated at each level of the auditory nervous system from the brain cortex to the depending on the direction from which the sound comes. cochlea in the ear. The final pathway is mainly from the su- It changes the quality by emphasizing specific sound fre- perior olivary nucleus to the sound-receptor hair cells in quencies from the different directions. the organ of Corti. Neural Mechanisms for Detecting Sound Direction. These retrograde fibers are inhibitory. Indeed, direct Destruction of the auditory cortex on both sides of the brain stimulation of discrete points in the olivary nucleus has been shown to inhibit specific areas of the organ of Corti, causes loss of almost all ability to detect the direction from reducing their sound sensitivities by 15 to 20 decibels. One which sound comes. Yet, the neural analyses for this detec- can readily understand how this mechanism could allow tion process begin in the superior olivary nuclei in the brain someone to direct their attention to sounds of particular stem, even though the neural pathways all the way from qualities while rejecting sounds of other qualities. This these nuclei to the cortex are required for interpretation of characteristic is readily demonstrated when one listens to the signals. The mechanism is believed to be the following. a single instrument in a symphony orchestra. The superior olivary nucleus is divided into two sec- Types of Deafness tions: (1) the medial superior olivary nucleus; and (2) the lateral superior olivary nucleus. The lateral nucleus is con- Deafness is usually divided into two types: (1) that caused by cerned with detecting the direction from which the sound impairment of the cochlea, the auditory nerve, or the central is coming, presumably by simply comparing the difference nervous system circuits from the ear, which is usually classi- fied as “nerve deafness,” and (2) that caused by impairment in intensities of the sound reaching the two ears and send- of the physical structures of the ear that conduct sound itself ing an appropriate signal to the auditory cortex to esti- to the cochlea, which is usually called “conduction deafness.” mate the direction. If either the cochlea or the auditory nerve is destroyed, The medial superior olivary nucleus, however, has a the person becomes permanently deaf. However, if the specific mechanism for detecting the time lag between cochlea and nerve are still intact but the tympanum- acoustical signals entering the two ears. This nucleus con- ossicular system has been destroyed or ankylosed (“frozen” tains large numbers of neurons that have two major den- in place by fibrosis or calcification), sound waves can still be drites, one projecting to the right and the other to the left. conducted into the cochlea by means of bone conduction The acoustical signal from the right ear impinges on the from a sound generator applied to the skull over the ear. right dendrite, and the signal from the left ear impinges Audiometer. To determine the nature of hearing dis- on the left dendrite. The intensity of excitation of each abilities, an audiometer is used. This instrument is an neuron is highly sensitive to a specific time lag between earphone connected to an electronic oscillator capable of emitting pure tones ranging from low frequencies to high the two acoustical signals from the two ears. The neurons frequencies, and it is calibrated so that zero-intensity-level near one border of the nucleus respond maximally to a sound at each frequency is the loudness that can barely be short time lag, whereas those near the opposite border heard by the normal ear. A calibrated volume control can respond to a long time lag; those in between respond to increase the loudness above the zero level. If the loudness intermediate time lags. must be increased to 30 decibels above normal before it Thus, a spatial pattern of neuronal stimulation develops can be heard, the person is said to have a hearing loss of 30 in the medial superior olivary nucleus, with sound from decibels at that particular frequency. directly in front of the head stimulating one set of olivary In performing a hearing test using an audiometer, one neurons maximally and sounds from different side angles tests about 8 to 10 frequencies covering the auditory spec- stimulating other sets of neurons on opposite sides. This trum, and the hearing loss is determined for each of these spatial orientation of signals is then transmitted to the frequencies. Then the so-called audiogram is plotted, as shown in Figure 53-11 and 53-12, depicting hearing loss auditory cortex, where sound direction is determined by at each of the frequencies in the auditory spectrum. The au- the locus of the maximally stimulated neurons. All these diometer, in addition to being equipped with an earphone signals for determining sound direction are believed to for testing air conduction by the ear, is equipped with a be transmitted through a different pathway and excite a mechanical vibrator for testing bone conduction from the different locus in the cerebral cortex from the transmis- mastoid process of the skull into the cochlea. sion pathway and termination locus for tonal patterns of Audiogram in Nerve Deafness. In nerve deafness, sound. which includes damage to the cochlea, the auditory nerve, 672  Chapter 53 The Sense of Hearing −10 is essentially normal, but conduction through the ossicular Normal system is greatly depressed at all frequencies, but more so 10 X X X at low frequencies. In some cases of conduction deafness, X X the faceplate of the stapes becomes “ankylosed” by bone 20 Loss (decibels) * * * * * X overgrowth to the edges of the oval window. Here, the per- 30 40 * X son becomes totally deaf for ossicular conduction but can UNIT X regain almost normal hearing by the surgical removal of the 50 stapes and its replacement with a minute Teflon or metal 60 prosthesis that transmits the sound from the incus to the 70 X Air conduction oval window. 80 90 * Bone conduction 100 1 250 500 1000 2000 4000 8000 Bibliography Frequency (cycles/sec) Angeloni C, Geffen MN: Contextual modulation of sound processing Figure 53-11. Audiogram of the old age type of nerve deafness. in the auditory cortex. Curr Opin Neurobiol 49:8, 2018. Avan P, Büki B, Petit C: Auditory distortions: origins and functions. Physiol Rev 93:1563, 2013. −10 Cunningham LL, Tucci DL: Hearing loss in adults. N Engl J Med Normal 377:2465, 2017. 10 * * * * * * Fettiplace R: Hair cell transduction, tuning, and synaptic transmission 20 in the mammalian cochlea. Compr Physiol 7:1197, 2017. Loss (decibels) X Fettiplace R, Kim KX: The physiology of mechanoelectrical transduc- 30 X X tion channels in hearing. Physiol Rev 94:951, 2014. 40 X X X X Gervain J, Geffen MN: Efficient neural coding in auditory and speech 50 perception. Trends Neurosci 42:56, 2019. 60 Grothe B, Pecka M, McAlpine D: Mechanisms of sound localization in 70 mammals. Physiol Rev 90:983, 2010. X Air conduction Heeringa AN, Köppl C: The aging cochlea: towards unraveling the 80 90 * Bone conduction functional contributions of strial dysfunction and synaptopathy. Hear Res 376:111, 2019. 100 Hudspeth AJ: Integrating the active process of hair cells with cochlear 125 250 500 1000 2000 4000 8000 function. Nat Rev Neurosci 15:600, 2014. Frequency (cycles/sec) Irvine DRF: Plasticity in the auditory system. Hear Res 362:61, 2018. Figure 53-12. Audiogram of air conduction deafness resulting from Jasmin K, Lima CF, Scott SK: Understanding rostral-caudal audito- middle ear sclerosis. ry cortex contributions to auditory perception. Nat Rev Neurosci 20:425, 2019. or the central nervous system circuits from the ear, the per- Joris PX, Schreiner CE, Rees A: Neural processing of amplitude- son has loss of ability to hear sound as tested by both air modulated sounds. Physiol Rev 84:541, 2004. conduction and bone conduction. An audiogram depict- King AJ, Nelken I: Unraveling the principles of auditory cortical pro- cessing: can we learn from the visual system? Nat Neurosci 12:698, ing partial nerve deafness is shown in Figure 53-11. In this 2009. figure, the deafness is mainly for high-frequency sound. Kuchibhotla K, Bathellier B: Neural encoding of sensory and behav- Such deafness could be caused by damage to the base of ioral complexity in the auditory cortex. Curr Opin Neurobiol 52:65, the cochlea. This type of deafness occurs to some extent in 2018. almost all older people. Ó Maoiléidigh D, Ricci AJ: A bundle of mechanisms: inner-ear hair-cell Other patterns of nerve deafness frequently occur as mechanotransduction. Trends Neurosci 42:221, 2019. follows: (1) deafness for low-frequency sounds caused by Moser T, Starr A: Auditory neuropathy--neural and synaptic mecha- excessive and prolonged exposure to very loud sounds (e.g., nisms. Nat Rev Neurol 12:135, 2016. a rock band or a jet airplane engine) because low-frequency Pangrsic T, Singer JH, Koschak A: Voltage-gated calcium channels: sounds are usually louder and more damaging to the organ key players in sensory coding in the retina and the inner ear. Physiol Rev 98:2063, 2018. of Corti; and (2) deafness for all frequencies caused by drug Rauschecker JP, Shannon RV: Sending sound to the brain. Science sensitivity of the organ of Corti—in particular, sensitivity to 295:1025, 2002. some antibiotics such as streptomycin, gentamicin, kana- Robles L, Ruggero MA: Mechanics of the mammalian cochlea. Physiol mycin, and chloramphenicol. Rev 81:1305, 2001. Audiogram for Middle Ear Conduction Deafness. A Takago H, Oshima-Takago T: Pre- and postsynaptic ionotropic glu- common type of deafness is caused by fibrosis in the mid- tamate receptors in the auditory system of mammals. Hear Res dle ear after repeated infection or by fibrosis that occurs in 362:1, 2018. the hereditary disease called otosclerosis. In either case, the Vélez-Ortega AC, Frolenkov GI: Building and repairing the stereocilia sound waves cannot be transmitted easily through the ossi- cytoskeleton in mammalian auditory hair cells. Hear Res 376:47, 2019. cles from the tympanic membrane to the oval window. Fig- Wang J, Puel JL: Toward cochlear therapies. Physiol Rev 98:2477, ure 53-12 shows an audiogram from a person with “middle 2018. ear air conduction deafness.” In this case, bone conduction 673