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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
Central pathways
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 ~ 331.4 + 0.6Tc ms-1 (where Tc is celcius temperature)
(~ 1 mile every 5s)
Sound Measurement Reference Values
hearing
threshold
(1000 Hz)
intensity
I0 = 10 -12 W/m 2
• intensity is sound power per unit area, in a particular direction
pressure
P0 = 2 x 10-5 N/m 2 = 20!Pa = 0.0002 dynes/cm 2
• pressure amplitude summarizes the influence of waves from all directions
P0
pain
threshold
is less than one billionth of atmospheric pressure!!
1013 P0 ~ 10,000,000,000,000 P0 = 130 dB
if sound pressure increases by 10,000, what is the change in dB?
10000 PA
= 104 PA =
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
Hearing Sensitivity
Sound Pressure Level (dB)
140
120
100
80
60
40
20
human
0
cat
-20
10
100
1000
Frequency (Hz)
10000
100000
Sound Pressure Level (dB)
Hearing Sensitivity
Mammals
Humans
100
Fish
Birds
80
60
40
20
0
10
100
1000
Frequency (Hz)
10000
100000
Outer Ear
pinna
meatus
concha
eardrum
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!
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
“Head-related” filtering
Head Related Impulse Resonse
Right: 0 Elev
Azimuth (deg)
Left: 0 Elev
Time (ms)
Head-Related Transfer Functions: Azimuth
Head-Related Transfer Functions: Elevation
HRTFs
Left
Right
elevation
Measured
azimuth
Theoretical
Hofman, Riswick and Van Opstal (1998)
Ear fine structure affects HRTFs
mid-sagittal plane (azimuth 0˚)
Attenuation
Amplification
Response Azimuth (deg)
Response Elevation (deg)
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.
Impedance Matching in Middle Ear
Impedance Problem: 99.9% sound
is reflected due to high impedance of
fluid in the cochlea
(30 dB loss)
Stapes
Solution: Middle ear ossicles
overcome impedance mismatch
by increasing sound pressure
Incus
(34 dB gain)
Malleus
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
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).
Middle ear air space affects middle ear gain
• Static pressure
opposes TM motion
• A small air volume
can “load” the TM
Middle ear air space affects middle ear gain
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
Acoustic input to cochlea
Effective input is P - P
OW
RW
• Ossicular coupling
• Acoustic coupling (60dB less)
• Bone conduction
The Cochlea
oval
window
round
window
cochlear duct
scala vestibuli
scala tympani
auditory nerve fibers
Spiral
ganglion
Cochlear Partition:
Basilar Membrane, Tectorial Membrane,
& Organ of Corti
cochlear
duct
scala vestibuli
scala tympani
auditory nerve
fibers
Spiral
ganglion
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
Organ of Corti
hair cells & supporting cells on the basilar membrane.
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.
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
normal
loss of OHCs
partial deafness
Cochlear hair cell damage
loss of all HCs
complete deafness
• ototoxic drugs
aminoglycoside antibiotics
antimitotic agents
• noise trauma
• presbycusis
Cochlear implant
(prosthesis)
Resonance of Basilar Membrane
Base is narrow & taut:
most sensitive to high pitch.
Apex is broad & soft:
most sensitive to low pitch
Basilar Membrane Traveling Wave
input signal
Human cochlea is ~35mm long; audible
frequency range is ~ 20 Hz - 16 kHz.
basilar membrane response
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
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.
1886
Rutherf ord (1886)
Proceedings of the National Academy of Sciences, 1930, 16: 344-350.
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.
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
“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
Proc. Royal Soc. Lond. B, 1948, 135: 492-498.
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.
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.
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.
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.
outer hair cell motion & cochlear micromechanics
BM motion without OHC
motility: cochlear output is
proportional to input.
Tectorial membrane
Reticular
lamina
Basilar membrane
Input
(BM displacement)
IHC not shown
3 OHCs
Output
(IHC displacement)
OHCs contract in-phase with
upward deflection of BM,
absorbing BM motion, and
minimizing shear.
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.
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.
Auditory tuning curves
inner hair-cell damage
outer hair-cell damage
Abnormal bandwidth
100
Abnormal
Threshold
log amplitude (dB SPL)
log amplitude (dB SPL)
Normal bandwidth
80
dB SPL
60
Normal
bandwidth
40
20
Normal
Threshold
Characteristic
Frequency
100
Abnormal
Threshold
80
60
Normal
bandwidth
40
20
Normal
Threshold
log frequency
Characteristic
Frequency
log frequency
Log Frequency
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.
BM becomes linear without OHCs
(furosemide injection)
Amplification greater and tuning
more selective at low levels
Robles, L. and Ruggero, M. A. (2001). "Mechanics of the mammalian cochlea,"
Physiological Review 81, 1305-1352.
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.
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
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).
• 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.
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.]
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.
Otoacoustic Emissions
low level sounds produced by the inner ear as part of the normal hearing process.
Otoacoustic Emissions
low level sounds produced by the inner ear as part of the normal hearing process.
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.
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.
Audiological test battery
TEOAEs are reduced/absent in
certain types of hearing loss.
Spontaneous otoacoustic emissions: No stimulus is required. Usually
span the 500-7000 Hz frequency range.
Transient evoked otoacoustic emissions: Clicks or tone bursts used
clinically to generate responses in 500-4000 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ﾐ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.
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.