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Emergent Phenomena in Cochlear Mechanics

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Title: Emergent Phenomena in Cochlear Mechanics


1
Emergent Phenomena in Cochlear Mechanics
Christopher A. Shera Eaton-Peabody Laboratory of
Auditory Physiology Harvard Medical School
2
What is the Biophysical Origin of the Cochlear
Amplifier?
3
The rapid conformational change associated with
channels closing together tightens tip links and
moves the hair bundle by several nanometers. It
has been suggested that this mechanism, if timed
appropriately to different stimulus frequencies
for each hair cell, could amplify the vibration
of the cochleas basilar membrane (a process
termed the cochlear amplifier). If
so, the TRPA1 protein could be at once the
hair-cell transduction channel, the gating
spring, and the cochlear amplifier.
The rapid conformational change associated with
channels closing together tightens tip links and
moves the hair bundle by several nanometers. It
has been suggested that this mechanism, if timed
appropriately to different stimulus frequencies
for each hair cell, could amplify the vibration
of the cochleas basilar membrane (a process
termed the cochlear amplifier). If
so, the TRPA1 protein could be at once the
hair-cell transduction channel, the gating
spring, and the cochlear amplifier.
4
The Debate is Misleadingly Framed
The cochlear amplifier is not EITHER somatic
motility OR hair-bundle motility.
The cochlear amplifier is not BOTH.
The cochlear amplifier is NEITHER.
5
Insights from Cochlear Modeling
Inverse method (e.g., Zweig, de Boer)
Determines functional properties of the organ of
Corti from measurements of BM motion
6
The Impedance of the Organ of Corti
ZBM(x,f )
ZPassive ZActive
Cochlear cross section at location x
What are the relative contributions of the
passive and active components?
7
BM-Admittance Frequency Responses
8
The Impedance of the Organ of Corti
ZBM(x,f )
ZPassive ZActive
Cochlear cross section at location x
9
Effects of Fluid Coupling Between the Oscillators
10
The Impedance of the Organ of Corti
ZBM(x,f )
ZPassive ZActive
Cochlear cross section at location x
11
Effects of Scalae Height (Nature of Fluid
Coupling)
12
The rapid conformational change asssociated with
channels closing together tightens tip links and
moves the hair bundle by several nanometers. It
has been suggested that this mechanism, if timed
appropriately to different stimulus frequencies
for each hair cell, could amplify the vibration
of the cochleas basilar membrane (a process
termed the cochlear amplifier). If
so, the TRPA1 protein could be at once the
hair-cell transduction channel, the gating
spring, and the cochlear amplifier.
13
Principle of Emergence
In a structured system, new properties emerge at
higher levels of integration which could not have
been predicted from a knowledge of the
lower-level components.
14
Spontaneous Otoacoustic Emissions (SOAEs)
(Allen et al. 1995)
15
Golds (1948) Local-Oscillator Model
if the feedback ever exceeded the losses, then
a resonant element in the organ of Corti would
become self-oscillatory, and oscillations would
build up to a level where linearity was not
preserved.
In spite of the self-regulating mechanism we
might expect that occasional disturbances would
bring an element into the region of
self-oscillation, when it is normally so close to
this condition. If this occurred, then we should
hear a clear note which would persist until the
adjusting mechanism has regained control, or
until the nervous sensitivity has decreased
sufficiently.
16
Spontaneous Hair-Bundle Oscillations
(Martin et al. 2001, 2003)
17
Models for Hair-Bundle Oscillators
(Hudspeth 1997)
18
SOAEs Used to Argue Against Somatic Motility as
the Active Process in Mammalian Hearing
  • The motor element of the cochlear amplifier is
    the source of SOAEs
  • Unprovoked mechanical oscillations of the motor
    element underlie the production of SOAEs
  • Although hair bundles can oscillate
    spontaneously, no spontaneous OHC contractions
    have ever been observed

19
Golds Local-Oscillator Model Gets the Chain of
Causality Exactly Backwards
The ear does not produce SOAEs because hair
cells oscillate spontaneously. Rather, hair
cells oscillate spontaneously (in vivo) because
the ear produces SOAEs.
20
Kemps (1979) Global Standing-Wave Model
SOAEs are continuously self-evoking
stimulus-frequency otoacoustic emissions (SFOAEs)
  • initiated either by sounds from the environment
    or by physiological noise

21
Spacetime Diagram Illustrating SFOAE Generation
22
Interference Patterns in Ear-Canal Pressure
23
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24
Effective Reflection Coefficients
For ingoing-waves at stapes
For outgoing-waves at stapes
25
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26
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27
Human SFOAE Amplitude and Phase
28
Spontaneous Otoacoustic Emissions
(Allen et al. 1995)
29
Human SFOAE Amplitude and Phase
30
Quantifying the Model Predictions
31
9 ears in 9 subjects
(Data from Shera Guinan 2003 and Dreisbach et
al. 1998)
32
Human SOAE Spacings
556 SOAE pairs 73 ears 47 subjects
(Data from Talmadge et al. 1993 and Burns et al.
1992)
33
Variability of SOAE Spacings
34
Summary of Results
Predictions arise naturally in the standing-wave
framework but require ad-hoc adjustment of
local-oscillator models.
35
Local-Oscillator vs Global Standing-Wave SOAEs
Local-Oscillator
Global Standing-Wave
36
The Cochlea is Acting as a Biological Laser
37
Implications for the Cellular Basis of the
Cochlear Amplifier
38
The Principle of Emergence
In a structured system, new properties emerge at
higher levels of integration which could not have
been predicted from a knowledge of the
lower-level components.
The local-oscillator model gets the causality
exactly backwards
SOAEs arise through the collective action of the
entire cochlea. Spontaneous emission of sound
from the ear does not require the autonomous
mechanical oscillation of its cellular
constituents.
39
Characteristics of Emergent Phenomena
Emergence occurs when a relatively small number
of copies of relatively simple components are
coupled together in relatively simple ways.
The parts acquire new properties by virtue of
their embedding in the whole.
Context and coupling are crucial.
40
The OHC Membrane Time-Constant Problem
41
The Crucial Role of Mathematical Modeling in the
Study of Hearing
42
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