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1 Auditory Periphery external middle inner 3. movement of stapes initiates a pressure wave in cochlear fluid. 1. sound causes air pressure to increase at eardrum 5. auditory nerve conveys neural signal to cochlear nucleus 2. eardrum is pushed inward, moving the middle ear bones 4. fluid-borne mechanical signals are transduced into a neural code
2 Central pathways
3 Acoustics Periodic Sounds Sine waves are described by their frequency, amplitude, and phase. However the speed of sound is determined by the properties of the medium not by the frequency or amplitude of the sound. Sound travels through air at ~ T c ms -1 (where T c is celcius temperature) (~ 1 mile every 5s)
4 Sound Measurement Reference Values hearing threshold (1000 Hz) intensity I 0 = W/m 2 intensity is sound power per unit area, in a particular direction pressure P 0 = 2 x 10-5 N/m 2 = 20!Pa = dynes/cm 2 pressure amplitude summarizes the influence of waves from all directions P 0 is less than one billionth of atmospheric pressure!! pain threshold P 0 ~ 10,000,000,000,000 P 0 = 130 db if sound pressure increases by 10,000, what is the change in db? P A = 10 4 P A = 40 db why the factor of 10? To create deci bels. In this example the change = 4 Bels (named after Alexander Graham Bell). But since 1 decibel is ~ the JND in sound pressure, the decibel is a convenient unit. it takes about 10 times the sound pressure to sound twice as loud every 20 db increment is a factor of 10 increase in pressure
5 Hearing Sensitivity 140 Sound Pressure Level (db) human cat Frequency (Hz)
6 Hearing Sensitivity Sound Pressure Level (db) Mammals Humans Fish Birds Frequency (Hz)
7 Outer Ear pinna meatus concha eardrum
8 Cerumen (ear wax) is good for the ear Repels water Traps dust, micro-organisms, other debri Moisturizes epithelium in ear canal Odor discourages insects Antibiotic, antifungal properties so don t struggle to remove it!
9 Outer ear concha horn amplifies sound pressure Geisler 1998 At 3kHz, final amplification reaches 20 db (10 times the free field level) Møller 2000 But this filtering differs as a function of signal spectrum and source direction
10 Head-related filtering Head Related Impulse Resonse Left: 0 Elev Right: 0 Elev Azimuth (deg) Time (ms)
11 Head-Related Transfer Functions: Azimuth
12 Head-Related Transfer Functions: Elevation
13 HRTFs Left Right Measured elevation azimuth Theoretical
14 Hofman, Riswick and Van Opstal (1998)
15 Ear fine structure affects HRTFs mid-sagittal plane (azimuth 0 ) Attenuation Amplification
16 Response Elevation (deg) Response Azimuth (deg)
17 Middle Ear Eustachian Tube connects the middle ear with the nasopharynx opens during swallowing & yawning This equalizes the pressure on either side of the eardrum, improving the efficiency of sound transmission to the inner ear.
18 Impedance Matching in Middle Ear Impedance Problem: 99.9% sound is reflected due to high impedance of fluid in the cochlea (30 db loss) Solution: Middle ear ossicles overcome impedance mismatch by increasing sound pressure (34 db gain) Malleus Incus Stapes
19 Mechanisms for middle ear impedance matching Lever action of the ossicles (1.3:1) 20 log(1.3/1) = +2 db Buckling of ear drum (x2 pressure increase) 20 log(2/1) = +6dB "Area ratio of ear drum to stapes footplate (20:1) 20 log (20/1) = +26dB * Basic concept: p = f/a
20 Middle ear gain is less than predicted by an Ideal Transformer Hypothesis Tympanic membrane does not vibrate as a rigid body Force is needed to stretch ligaments and accelerate mass of ossicles Ossicular chain is not rigid (it has slippage at high frequencies).
21 Middle ear air space affects middle ear gain Static pressure opposes TM motion A small air volume can load the TM
22 Middle ear air space affects middle ear gain
23 Effects of middle ear muscle contractions Tensor Tympani pulls manubrium, TM inward increases middle ear pressure (helps open eustacian tube) Stapedius pulls incudostapedial joint sideways (perpendicular to stapes motion) reduces low-frequency middle ear gain Acoustic Reflex
24 Acoustic input to cochlea Effective input is P OW - P RW Ossicular coupling Acoustic coupling (60dB less) Bone conduction
25 The Cochlea oval window round window cochlear duct scala vestibuli scala tympani auditory nerve fibers Spiral ganglion
26 Cochlear Partition: Basilar Membrane, Tectorial Membrane, & Organ of Corti
27 cochlear duct scala vestibuli scala tympani auditory nerve fibers Spiral ganglion
28 Organ of Corti hair cells & supporting cells on the basilar membrane. 1-Inner hair cell 2-Outer hair cells 3-Tunnel of Corti 4-Basilar membrane 5-Reticular lamina 6-Tectorial membrane 7-Deiters' cells 8-Space of Nuel 9-Hensen's cells 10-Inner spiral sulcus
29 Organ of Corti hair cells & supporting cells on the basilar membrane.
30 Hair cell stereocilia shearing Cochlear processing is 1000x faster than retinal processing Retinal photoreceptors depend on a series of intricate interactions with a G protein and a 2nd messenger before their ion channels close, sending a signal to the brain. This would be much too slow processing sound. Cochlear hair cells must open and close ion channels more rapidly. Their mechanism is like a spring that opens channels when the cilia bend, without a time-consuming chemical exchange.
31 Movement of hair cell cilia bundle opens ion channels at cilia tips cilia on a hair cell in bullfrog cochlea. Pickles and Corey (1992) tip links from higher cilia pull up ion channel gates on adjoining cilia. Hudspeth
32 normal Cochlear hair cell damage loss of OHCs partial deafness loss of all HCs complete deafness ototoxic drugs aminoglycoside antibiotics antimitotic agents noise trauma presbycusis
33 Cochlear implant (prosthesis)
34 Resonance of Basilar Membrane Base is narrow & taut: most sensitive to high pitch. Apex is broad & soft: most sensitive to low pitch
35 Basilar Membrane Traveling Wave input signal basilar membrane response Human cochlea is ~35mm long; audible frequency range is ~ 20 Hz - 16 khz.
36 Coding in the Auditory System Place Code! Different frequencies are signaled by activity in neurons that are in different places in the auditory system Temporal Code! Different frequencies are signaled by the timing of nerve impulses in nerve fibers or groups of nerve fibers
37 History of Resonance/Place Theory 19th century view of resonance in the ear a few authors believed in resonance as an inner ear mechanism: e.g., John and Charles Bell (1829) expressed the following view: "There is no part of the proper organ which appears susceptible of the variety of musical notes but the scala of the cochlea. Its breadth is in regular gradation of parts from the base to- wards the apex; and whether the fibers were to be taken as the cords of a harp or the tubes like the ora of a wind instrument, every gradation of sound may be supposed to have here its corresponding organ to vibrate, and by its vibration to move a distinct part of the auditory nerve." but most doubted the existence of resonating structures in the inner ear: e.g., Francois Magendie (1822) disposed of the resonance theory in one sentence: "The osseo-membranous partition which separates the two scalae of the cochlea has given rise to a hypothesis which no one believes at the present day." Johanues Müller was strongly opposed to any kind of resonance theory. In his opinion the lamina spiralis was only to be considered as a surface upon which the nerve fibers are spread in such a manner as to provide simultaneous exposure to the condensations and rarefactions of sound waves. 30 years later Helmholtz developed the concept of a displacement resonance inside the inner ear, and reoriented thinking of physiologists and physicists. There was an increasingly solid foundation, including Fouret's theorem (1822), Ohm's acoustical law (1843), and important new micro-anatomical discoveries.
38 1886 Rutherf ord (1886)
39 Proceedings of the National Academy of Sciences, 1930, 16:
40
41 The Origins of Current Concepts The first measurements of the vibrational response to sound of the BM were carried out by Georg von Békésy, for which he was awarded the 1961 Nobel Prize for Physiology or Medicine. Working principally in the ears of human cadavers, Békésy showed that the cochlea performs a kind of spatial Fourier analysis, mapping frequencies upon longitudinal position along the BM. He de- scribed a displacement wave that travels on the BM from base to apex of the cochlea at speeds much slower than that of sound in water. As it propagates, the traveling wave grows in amplitude, reaches a maximum, and then decays. The location of the maximum is a function of stimulus frequency: high-frequency vibrations reach a peak near the base of the cochlea, whereas low-frequency waves travel all the way to the cochlear apex.
42 Georg von Békésy Mechanical model of the inner ear Békésy s mechanical model of the inner ear included a water-filled plastic tube and a 30 cm membrane. Vibration elicited traveling waves mimicking those in the normal human ear. Usable frequency range was two octaves. I decided to make a model of the inner ear with a nerve supply. An attempt to use a frog skin as a nerve supply had at an earlier time proved to be impractical, and so I simply placed my arm against the model. To my surprise, although the traveling waves ran along the whole length of the membrane with almost the same amplitude, and only a quite flat maximum at one spot, the sensations along my arm were completely different. I had the impression that only a section of the membrane, 2 to 3 cm long, was vibrating. When the frequency of vibration was increased, the section of sensed vibrations travelled toward the piston (at the right of the figure), which represents the stapes footplate of the ear; and when the frequency was lowered, the area of sensation moved in the opposite direction. The model had all the properties of a neuromechanical frequency-analyzing system, in support of our earlier view of the frequency analysis of the ear. My surprise was even greater when it turned out that two cycles of sinusoidal vibration are enough to produce a sharply localized sensation on the skin, just as sharp as for continuous stimulation. This was in complete agreement with the observations of Savart, who found that two cycles of tone provide enough cue to determine the pitch of the tone. Thus the century-old problem of how the ear performs a frequency analysis -- whether mechanically or neurally -- could be solved; from these experiments it was evident that the ear contains a neuromechanical frequency analyzer, combining a preliminary mechanical frequency analysis with a subsequent sharpening of the sensation area. Concerning the pleasures of observing, and the mechanics of the inner ear Nobel Lecture, December 11, 1961
43 The happiest period of my research was when I started to repeat all the great experiments that have been done on the ear in the past but now on the model ear with nerve supply. All the small details could be duplicated on the skin. Nothing has been more rewarding than to concentrate on the little discrepancies that I love to investigate and see slowly disappear. This always gave me the feeling of being on the right track, a new track. The simple fact that on the model the whole arm vibrates (as can be seen under stroboscopic illumination), but only a very small section is recognized as vibrating, proves that nervous inhibition must play an important role. Békésy s measurement of BM displacement as a function of frequency and place. Further investigation has shown that every local stimulus applied on the skin produces strong inhibition around the place of stimulation. This seems to be true, not only for the skin, but also for the ear and the retina. Involuntarily, this had led me to begin an investigation of the analogies between the ear and the skin and the eye. Maybe the time is not too far off when these three sense organs -- ear, skin, and eye -- so sharply separated in the textbooks of physiology, will have some chapters in common. This would lead toward a simplification of our descriptions of the sense organs. Concerning the pleasures of observing, and the mechanics of the inner ear Nobel Lecture, December 11, 1961
44 Proc. Royal Soc. Lond. B, 1948, 135:
45 Current Concepts A turning point in the understanding of cochlear mechanics came in 1971 when Rhode demonstrated that BM vibrations in live squirrel monkeys exhibit a compressive nonlinearity, growing in magnitude as a function of stimulus intensity at a rate of 1 db/db. Rhode also showed that the nonlinearity occurrs only at or near the CF, and that it disappears after death. Rhode s discoveries had to wait longer than a decade for confirmation and extension (LePage & Johnstone 1980, Robles et al 1986, Sellick et al. 1982), after several unsuccessful attempts. However, by the time the confirmatory BM experiments were published, the existence of nonlinear and active cochlear processes consistent with Rhode s pioneering findings had received unexpected but influential support from Kemp s discovery of otoacoustic emissions, sounds emitted by the cochlea which grow at compressive rates with stimulus intensity (Kemp, 1978). Kemp immediately revived Gold s prescient arguments (1948) on the need for a positive electromechanical feedback to boost BM vibrations to compensate for the viscous damping exerted by the cochlear fluids. A few years later, a possible origin for both otoacoustic emissions and the hypothetical electromechanical feedback was identified by Brownell et al. (1985), who showed that outer hair cells change their length under electrical stimulation.
46
47 Cochlea approximates bank of (nonlinear) filters The filtering allows the separation of various signal components with a good signal-to-noise ratio. Nonlinearity Each filter has dynamic range compression built into its mechanical response. This nonlinearity makes the frequency response of each filter dependent on the level of the acoustic signal.
48 OHC activity: Increases sensitivity (lowers thresholds) Increases selectivity (reduces bandwidth of auditory filter) Gives ear a logarithmic (non-linear) amplitude response Produces oto-acoustic emissions OHCs are relatively more active for quiet sounds than for loud sounds. They only amplify sounds that have the characteristic frequency of their place.
49 Nonlinear Amplifier BM is deflected by pressure gradients in surrounding fluid. Hair bundles on IHC and OHCs are deflected by shear displacement between RL and TM. Tectorial membrane outer hair cell motion & cochlear micromechanics BM motion without OHC motility: cochlear output is proportional to input. Reticular lamina IHC not shown 3 OHCs Basilar membrane OHCs contract in-phase with upward deflection of BM, absorbing BM motion, and minimizing shear. (BM displacement) Input Output (IHC displacement) OHC contraction lags BM displacement by 90. BM forces create negative damping and pump energy into the mechanical system. Energy from OHC motility improves cochlear sensitivity to low-level sounds.
50 Frequency tuning in cochlear vibrations and auditory nerve fibers RIGHT: tuning curve for an auditorynerve fiber (solid) is compared with isoresponse curves for a BM site with identical CF (9.5 khz) recorded in the same ear. At fiber CF threshold, BM peak displacement was used to plot BM isodisplacement and isovelocity tuning curves (dotted and dashed lines, respectively). LEFT: isodisplacement and isovelocity tuning curves (dotted and dashed) for TM vibrations compared with neural tuning based on averaged responses from many auditory-nerve fibers.
51 Auditory tuning curves inner hair-cell damage outer hair-cell damage 0 db SPL Normal bandwidth Abnormal Threshold Normal bandwidth Abnormal bandwidth Abnormal Threshold Normal bandwidth Normal Threshold Characteristic Frequency Normal Threshold Characteristic Frequency Log Frequency
52 Compressive nonlinearity near CF in BM Velocity-Intensity functions Chinchilla cochlea CF = 10 khz linear growth of responses to tones lower or higher than CF highly compressive growth of responses to CF tones (i.e., response magnitude grows by only 28 db with stimulus increase of 96 db). Tones # CF Tones $ CF Ruggero et al.
53 BM becomes linear without OHCs (furosemide injection)
54 Amplification greater and tuning more selective at low levels Robles, L. and Ruggero, M. A. (2001). "Mechanics of the mammalian cochlea," Physiological Review 81,
55 Compressive nonlinearity near CF also apparent in response area Chinchilla cochlea CF = 10 khz Effects are most noticeable at lower SPLs Sensitivity = (displacement stimulus pressure) Ruggero et al.
56 Two tone suppression response to one tone reduced by simultaneous presence of another guinea pig cochlea suppression of BM responses to a CF (18.8 khz) tone by a suppressor tone at various SPLs frequency specificity of two-tone suppression two-tone suppression in auditory nerve fibers probably originates in BM vibrations
57 Intermodulation distortion products originate from mechanics of the cochlea Simultaneously presented tones generate percepts of additional tones not present in the acoustic stimulus. For two-tone stimuli the pitch of these distortions corresponds to combinations of the primary frequencies (f1 and f2). Cubic difference tones in BM vibrations. Spectrum of responses to a pair of tones (each 50 db SPL) chosen so that 2f1-f2 = CF (7.5 khz). [Chinchilla data from Robles et al.] BM responses to two-tone stimuli contain several distortion products (e.g., 3f2-2f1, 2f2-f1, 2f1-f2, 3f1-2f2 and f2-f1). The number of detectable distortion products in BM responses decreases with separation of f1 and f2.
58 Frequency tuning in cochlear vibrations and auditory nerve fibers RIGHT: tuning curve for an auditorynerve fiber (solid) is compared with isoresponse curves for a BM site with identical CF (9.5 khz) recorded in the same ear. At fiber CF threshold, BM peak displacement was used to plot BM isodisplacement and isovelocity tuning curves (dotted and dashed lines, respectively). LEFT: isodisplacement and isovelocity tuning curves (dotted and dashed) for TM vibrations compared with neural tuning based on averaged responses from many auditory-nerve fibers.
59 Otoacoustic Emissions low level sounds produced by the inner ear as part of the normal hearing process.
60 Otoacoustic Emissions low level sounds produced by the inner ear as part of the normal hearing process.
61 Theory of Otoacoustic Emissions The sensitivity and resolution of the ear depends on two things: (1) the size and sharpness of cochlear travelling wave peaks. (2) the efficiency of transduction to the auditory nerve. Without active OHC function, sound energy is lost from the traveling wave before it peaks. Peaks broaden and are of reduced size. OHCs generate replacement vibration which sustains and amplifies the traveling wave, resulting in higher and sharper peaks of excitation to the IHCs. Most of the sound vibration generated by the OHCs becomes part of the forward travelling wave, but a fraction escapes. It then travels back out of the cochlea to cause secondary vibrations of the middle ear and the ear drum. The whole process can take 3 to 15 milliseconds. These cochlear driven vibrations are the source of Otoacoustic Emissions.
62 Audiological test battery Tympanometry tests the system up to the cochlea. OAE: an index of just the peripheral system up to the point of excitation of the inner hair cells but not the cells themselves. ABR: tests the auditory periphery and neural pathways as far as the brain stem. Audiogram: assesses the whole auditory system but includes unwanted central and psychological factors.
63 Audiological test battery Spontaneous otoacoustic emissions: No stimulus is required. Usually span the Hz frequency range. TEOAEs are reduced/absent in certain types of hearing loss. Transient evoked otoacoustic emissions: Clicks or tone bursts used clinically to generate responses in Hz range. Easily interpreted, often used for screening infants. Single frequency otoacoustic emissions: single tones used clinically to assess frequency range Distortion product otoacoustic emissions Produced by the normal cochlea when stimulated simultaneously by two pure tone signals (f1 and f2). Numerous distortion products (notably 2f1 f2) are generated normally at sites where the travelling waves overlap. Waves traveling along the basilar membrane in response to two tones f1 and f2. Note how f1 and f2 excite a substantial region of the cochlea, even though their frequencies are very precisely defined. Distortion products can only be generated in the region where f1 and f2 overlap.
64 Peripheral auditory processing summary Sound is filtered as it passes through the pinna and ear canal. This acoustic energy vibrates the tympanic membrane like a drum... setting the ossicles in motion, mechanically amplifying sound and changing acoustic energy to mechanical energy. The middle ear compensates for an air/fluid impedance loss The stapes displaces the oval window, hydrodynamic energy causes cochlear membranes to shear against hair cell bundles. An electrochemical signal is sent via auditory nerve to brain.
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