Coupling a sensory hair-cell bundle to cyber clones enhances nonlinear amplification

被引:36
作者
Barral, Jeremie [1 ]
Dierkes, Kai [2 ]
Lindner, Benjamin [2 ]
Juelicher, Frank [2 ]
Martin, Pascal [1 ]
机构
[1] Univ Paris 06, CNRS, Inst Curie, Lab Physicochim Curie, F-75005 Paris, France
[2] Max Planck Inst Phys Komplexer Syst, D-01187 Dresden, Germany
关键词
auditory amplifier; hair-bundle motility; coupled oscillators; fluctuations; SPONTANEOUS OSCILLATIONS; OTOLITHIC-MEMBRANE; MOTILITY; NOISE; RESONANCE; COCHLEA; PRESTIN; MOTION; MODEL; CA2+;
D O I
10.1073/pnas.0913657107
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
The vertebrate ear benefits from nonlinear mechanical amplification to operate over a vast range of sound intensities. The amplificatory process is thought to emerge from active force production by sensory hair cells. The mechano-sensory hair bundle that protrudes from the apical surface of each hair cell can oscillate spontaneously and function as a frequency-selective, nonlinear amplifier. Intrinsic fluctuations, however, jostle the response of a single hair bundle to weak stimuli and seriously limit amplification. Most hair bundles are mechanically coupled by overlying gelatinous structures. Here, we assayed the effects of mechanical coupling on the hair-bundle amplifier by combining dynamic force clamp of a hair bundle from the bullfrog's saccule with real-time stochastic simulations of hair-bundle mechanics. This setup couples the hair bundle to two virtual hair bundles, called cyber clones, and mimics a situation in which the hair bundle is elastically linked to two neighbors with similar characteristics. We found that coupling increased the coherence of spontaneous hair-bundle oscillations. By effectively reducing noise, the synergic interplay between the hair bundle and its cyber clones also enhanced amplification of sinusoidal stimuli. All observed effects of coupling were in quantitative agreement with simulations. We argue that the auditory amplifier relies on hair-bundle cooperation to overcome intrinsic noise limitations and achieve high sensitivity and sharp frequency selectivity.
引用
收藏
页码:8079 / 8084
页数:6
相关论文
共 39 条
[1]   Cochlear outer hair cell motility [J].
Ashmore, Jonathan .
PHYSIOLOGICAL REVIEWS, 2008, 88 (01) :173-210
[2]   HAIR-BUNDLE STIFFNESS DOMINATES THE ELASTIC REACTANCE TO OTOLITHIC-MEMBRANE SHEAR [J].
BENSER, ME ;
ISSA, NP ;
HUDSPETH, AJ .
HEARING RESEARCH, 1993, 68 (02) :243-252
[3]   Auditory sensitivity provided by self-tuned critical oscillations of hair cells [J].
Camalet, S ;
Duke, T ;
Jülicher, F ;
Prost, J .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2000, 97 (07) :3183-3188
[4]   Ca2+ current-driven nonlinear amplification by the mammalian cochlea in vitro [J].
Chan, DK ;
Hudspeth, AJ .
NATURE NEUROSCIENCE, 2005, 8 (02) :149-155
[5]   Phase noise in coupled oscillators: Theory and experiment [J].
Chang, HC ;
Cao, XD ;
Mishra, UK ;
York, RA .
IEEE TRANSACTIONS ON MICROWAVE THEORY AND TECHNIQUES, 1997, 45 (05) :604-615
[6]   A model for amplification of hair-bundle motion by cyclical binding of Ca2+ to mechanoelectrical-transduction channels [J].
Choe, Y ;
Magnasco, MO ;
Hudspeth, AJ .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 1998, 95 (26) :15321-15326
[7]   THE MECHANICAL-PROPERTIES OF CILIARY BUNDLES OF TURTLE COCHLEAR HAIR-CELLS [J].
CRAWFORD, AC ;
FETTIPLACE, R .
JOURNAL OF PHYSIOLOGY-LONDON, 1985, 364 (JUL) :359-&
[8]  
DALLOS P, 1992, J NEUROSCI, V12, P4575
[9]   Prestin-based outer hair cell motility is necessary for mammalian cochlear amplification [J].
Dallos, Peter ;
Wu, Xudong ;
Cheatham, Mary Ann ;
Gao, Jiangang ;
Zheng, Jing ;
Anderson, Charles T. ;
Jia, Shuping ;
Wang, Xiang ;
Cheng, Wendy H. Y. ;
Sengupta, Soma ;
He, David Z. Z. ;
Zuo, Jian .
NEURON, 2008, 58 (03) :333-339
[10]   Prestin and the cochlear amplifier [J].
Dallos, Peter ;
Zheng, Jing ;
Cheatham, Mary Ann .
JOURNAL OF PHYSIOLOGY-LONDON, 2006, 576 (01) :37-42