Our sense of hearing boasts exquisite sensitivity to periodic signals. Experiments and modeling imply, however, that the auditory system achieves this performance for only a narrow range of parameter values. As a result, small changes in these values could compromise the ability of the mechanosensory hair cells to detect stimuli. We propose that, rather than exerting tight control over parameters, the auditory system employs a homeostatic mechanism that ensures the robustness of its operation to variation in parameter values. Through analytical techniques and computer simulations we investigate whether a homeostatic mechanism renders the hair bundle’s signal-detection ability more robust to alterations in experimentally accessible parameters. When homeostasis is enforced, the range of values for which the bundle’s sensitivity exceeds a threshold can increase by more than an order of magnitude. The robustness of cochlear function based on somatic motility or hair bundle motility may be achieved by employing the approach we describe here.

1.
Sivian
LJ
and
White
SD
(
1933
)
On minimum audible sound fields
.
J. Acoust Soc Am
4
(
4
):
288
321
2.
de Vries
HL
(
1948
)
Brownian movement and hearing
.
Physica
14
(
1
):
48
60
3.
Harris
GG
(
1968
)
Brownian motion in the cochlear partition
.
J. Acoust Soc Am
44
(
1
):
176
186
4.
Dalhoff
E
,
Turcanu
D
,
Zenner
HP
, and
Gummer
AW
(
2007
)
Distortion product otoacoustic emissions measured as vibration on the eardrum of human subjects
.
Proc Natl Acad Sci U S A
104
(
5
):
1546
1551
5.
Hudspeth
AJ
(
2014
)
Integrating the active process of hair cells with cochlear function
.
Nat Rev Neurosci
15
(
9
):
600
614
6.
Hudspeth
AJ
(
2008
)
Making an effort to listen: mechanical amplification in the ear
.
Neuron
59
(
4
):
530
545
7.
Martin
P
and
Hudspeth
AJ
(
2001
)
Compressive nonlinearity in the hair bundles active response to mechanical stimulation
.
Proc Natl Acad Sci U S A
98
(
25
):
14386
14391
8.
Blackwell
DL
,
Lucas
JW
, and
Clarke
TC
(
2014
)
Summary health statistics for U.S. adults: National Heath Interview Survey, 2012
.
National Center for Health Statics. Vital Health Stat.
10
(
260
):
1
161
9.
Daniel
E
(
2007
)
Noise and hearing loss: a review
.
J. Sch Health
77
(
5
):
225
231
10.
Nadrowski
B
,
Martin
P
, and
Jülicher
F
(
2004
)
Active hair-bundle motility harnesses noise to operate near an optimum of mechanosensitivity
.
Proc Natl Acad Sci U S A
101
(
33
):
12195
12200
11.
Salvi
JD
Ó Maoiléidigh
D
,
Fabella
BA
,
Tobin
M
, and
Hudspeth
AJ
(
2015
)
Control of a hair bundle’s mechanosensory function by its mechanical load
.
Proc Natl Acad Sci U S A
112
(
9
):
E1000
E1009
12.
Salvi
JD
Ó Maoiléidigh
D
, and
Hudspeth
AJ
(
2016
)
Identification of bifurcations from observations of noisy biological oscillators
.
Biophys J.
111
(
4
):
798
812
13.
Ó Maoiléidigh
D
,
Nicola
EM
, and
Hudspeth
AJ
(
2012
)
The diverse effects of mechanical loading on active hair bundles
.
Proc Natl Acad Sci U S A
109
(
6
):
1943
1948
14.
Tinevez
J-Y B
,
Jülicher
F
, and
Martin
P
(
2004
)
Unifying the various incarnations of active hair-bundle motility by the vertebrate hair cell
.
Biophys J.
93
(
11
):
4053
4067
15.
Hirono
M
,
Denis
CS
,
Richardson
GP
, and
Gillespie
PG
(
2004
)
Hair cells require phosphatidylinositol 4,5-bisphosphate for mechanical transduction and adaptation
.
Neuron
44
(
2
):
309
320
16.
Lumpkin
EA
and
Hudspeth
AJ
(
1998
)
Regulation of free Ca2+ concentration in hair-cell stereocilia
.
J. Neurosci
18
(
16
):
6300
6318
17.
Ricci
AJ
,
Wu
YC
, and
Fettiplace
R
(
1998
)
The endogenous calcium buffer and the time course of transducer adaptation in auditory hair cells
.
J. Neurosci
18
(
20
):
8261
8277
18.
Yamoah
EN
,
Lumpkin
EA
,
Dumont
RA
,
Smith
PJ
,
Hudspeth
AJ
, and
Gillespie
PG
(
1998
)
Plasma membrane Ca2+-ATPase extrudes Ca2+ from hair cell stereocilia
.
J. Neurosci
18
(
2
):
610
624
19.
Howard
J
and
Hudspeth
AJ
(
1987
)
Mechanical relaxation of the hair bundle mediates adaptation in mechanoelectrical transduction by the bullfrog’s saccular hair cell
.
Proc Natl Acad Sci U S A
84
(
9
):
3064
3068
20.
Vollrath
MA
and
Eatock
RA
(
2003
)
Time course and extent of mechanotransducer adaptation in mouse utricular hair cells: comparison with frog saccular hair cells
.
J. Neurophysiol
90
(
4
):
2676
2689
21.
Ó Maoiléidigh
D
and
Jülicher
F
(
2010
)
The interplay between active hair bundle motility and electromotility in the cochlea
.
J. Acoust Soc of Am
128
(
3
):
1175
1190
22.
Pickles
JO
.
An introduction to the physiology of hearing
, fourth edition
Bingley
:
Emerald Group Publishing. Print
.
23.
Goutman
JD
,
Elgoyhen
AB
, and
Gómez-Casati
ME
(
2015
)
Cochlear hair cells: the sound-sensing machines
.
FEBS Lett
589
(
22
):
3345
3361
24.
Guinan
JJ
(
2006
)
Olivocochlear efferents: anatomy, physiology, function, and the measurement of efferent effects in humans
.
Ear Hear
27
(
1
):
589
607
25.
Ruggero
MA
,
Rich
NC
,
Recio
A
,
Narayan
SS
, and
Robles
L
(
1997
)
Basilar-membrane responses to tones at the base of the chinchilla cochlea
.
J. Acoust Soc Am
101
(
4
):
2151
2163
This content is only available via PDF.