Hearing requires precise detection and coding of acoustic signals by the inner ear and equally precise communication of the information through the auditory brainstem. A membrane based motor in the outer hair cell lateral wall contributes to the transformation of sound into a precise neural code. Structural, molecular and energetic similarities between the outer hair cell and auditory brainstem neurons suggest that a similar membrane based motor may contribute to signal processing in the auditory CNS. Cooperative activation of voltage gated ion channels enhances neuronal temporal processing and increases the upper frequency limit for phase locking. We explore the possibility that membrane mechanics contribute to ion channel cooperativity as a consequence of the nearly instantaneous speed of electromechanical signaling and the fact that membrane composition and mechanics modulate ion channel function.
REFERENCES
1.
Akkin
T
, Landowne
D
, Sivaprakasam
A
(2009
) Optical coherence tomography phase measurement of transient changes in squid giant axons during activity
. J Membr Biol
231
:35
–46
2.
Aldrich
RW
, Corey
DP
, Stevens
CF
(1983
) A reinterpretation of mammalian sodium channel gating based on single channel recording
. Nature
306
:436
–441
3.
Attwell
D
, Laughlin
SB
(2001
) An energy budget for signaling in the grey matter of the brain
. J Cereb Blood Flow Metab
21
:1133
–1145
4.
Brownell
WE
, Manis
PB
, Zidanic
M
, Spirou
GA
(1983
) Acoustically evoked radial current densities in scala tympani
. J Acoust Soc Am
74
:792
–800
5.
Brownell
WE
, Farrell
B
, Raphael
RM
(2002
) Membrane electromechanics at hair-cell synapses. In: Gummer
AW
(ed) Biophysics of the Cochlea: From Molecules to Models
, New Jersey
: World Scientific
, pp. 169
–176
6.
Brownell
WE
, Qian
F
, Anvari
B
(2010
) Cell membrane tethers generate mechanical force in response to electrical stimulation
. Biophys J
99
:845
–852
7.
Brownell
WE
, Manis
PB
(2014
) Structures, Mechanisms and Energetics in Temporal Processing. In: Popper
AN
, Fay
RR
(eds) Perspectives on Auditory Research
, New York
: Springer
, pp. 9
–44
8.
Calabrese
B
, Tabarean
IV
, Juranka
P
, Morris
CE
(2002
) Mechanosensitivity of N-type calcium channel currents
. Biophys J
83
:2560
–2574
9.
Corbitt
Farinelli F
, Brownell
WE
, Farrell
B
(2012
) Tonotopic relationships reveal the charge density varies along the lateral wall of outer hair cells
. Biophys J
102
:2715
–2724
10.
de Monvel
JB
, Brownell
WE
, Ulfendahl
M
(2006
) Lateral diffusion anisotropy and membrane lipid/skeleton interaction in outer hair cells
. Biophys J
91
:364
–381
11.
Gu
CX
, Juranka
PF
, Morris
CE
(2001
) Stretch-activation and stretch-inactivation of Shaker-IR, a voltage-gated K+ channel
. Biophys J
80
:2678
–2693
12.
Ilin
V
, Malyshev
A
, Wolf
F
, Volgushev
M
(2013
) Fast computations in cortical ensembles require rapid initiation of action potentials
. J Neurosci
33
:2281
–2292
13.
Iwasa
K
, Tasaki
I
(1980
) Mechanical changes in squid giant axons associated with production of action potentials
. Biochem Biophys Res Commun
95
:1328
–1331
14.
Kitani
R
, Park
C
, Kalinec
F
(2013
) Microdomains shift and rotate in the lateral wall of cochlear outer hair cells
. Biophys J
104
:8
–18
15.
Lennie
P
(2003
) The cost of cortical computation
. Curr Biol
13
:493
–497
16.
Morris
CE
, Juranka
PF
(2007
) Nav channel mechanosensitivity: activation and inactivation accelerate reversibly with stretch
. Biophys J
93
:822
–833
17.
Naundorf
B
, Geisel
T
, Wolf
F
(2005
) Action potential onset dynamics and the response speed of neuronal populations
. J Comput Neurosci
18
:297
–309
18.
Naundorf
B
, Wolf
F
, Volgushev
M
(2006
) Unique features of action potential initiation in cortical neurons
. Nature
440
:1060
–1063
19.
Oertel
D
(1983
) Synaptic responses and electrical properties of cells in brain slices of the mouse anteroventral cochlear nucleus
. J Neurosci
3
:2043
–2053
20.
Oghalai
JS
, Zhao
HB
, Kutz
JW
, Brownell
WE
(2000
) Voltage- and tension-dependent lipid mobility in the outer hair cell plasma membrane
. Science
287
:658
–661
21.
Sala
C
, Segal
M
(2014
) Dendritic spines: the locus of structural and functional plasticity
. Physiol Rev
94
:141
–188
22.
Ursell
T
, Huang
KC
, Peterson
E
, Phillips
R
(2007
) Cooperative gating and spatial organization of membrane proteins through elastic interactions
. PLoS Comput Biol
3
:e81
23.
Wang
YX
, Wenthold
RJ
, Ottersen
OP
, Petralia
RS
(1998
) Endbulb synapses in the anteroventral cochlear nucleus express a specific subset of AMPA-type glutamate receptor subunits
. J Neurosci
18
:1148
–1160
24.
Winckler
B
, Forscher
P
, Mellman
I
(1999
) A diffusion barrier maintains distribution of membrane proteins in polarized neurons
. Nature
397
:698
–701
25.
Xu
K
, Zhong
G
, Zhuang
X
(2013
) Actin, spectrin, and associated proteins form a periodic cytoskeletal structure in axons
. Science
339
:452
–456
26.
Yamashita
T
, Hakizimana
P
, Jacob
S
, Jamshid
T
, Fang
J
, Mellado-Lagarde
M
, Leibiger
B
, Leijon
S
, Berggren
P-O
, Brownell
WA
. Fridberger
A
, Zuo
J
(2014
) Prestin and heterologously expressed membrane proteins are constrained by the trilaminate lateral wall of outer hair cells
. Assoc Res Otolaryngol Abs
, pp. 4
This content is only available via PDF.
© 2015 AIP Publishing LLC.
2015
AIP Publishing LLC
