Unifying the various incarnations of active hair-bundle motility by the vertebrate hair cell.
The dazzling sensitivity and frequency selectivity of the vertebrate ear rely on mechanical amplification of the hair cells' responsiveness to small stimuli. As revealed by spontaneous oscillations and forms of mechanical excitability in response to force steps, the hair bundle that adorns each hair cell is both a mechanosensory antenna and a force generator that might participate in the amplificatory process. To study the various incarnations of active hair-bundle motility, we combined Ca(2+) iontophoresis with mechanical stimulation of single hair bundles from the bullfrog's sacculus. We identified three classes of active hair-bundle movements: a hair bundle could be quiescent but display nonmonotonic twitches in response to either excitatory or inhibitory force steps, or oscillate spontaneously. Extracellular Ca(2+) changes could affect the kinetics of motion and, when large enough, evoke transitions between the three classes of motility. We found that the Ca(2+)-dependent location of a bundle's operating point within its force-displacement relation controlled the type of movement observed. In response to an iontophoretic pulse of Ca(2+) or of a Ca(2+) chelator, a hair bundle displayed a movement whose polarity could be reversed by applying a static bias to the bundle's position at rest. Moreover, such polarity reversal was accompanied by a 10-fold change in the kinetics of the Ca(2+)-evoked hair-bundle movement. A unified theoretical description, in which mechanical activity stems solely from myosin-based adaptation, could account for the fast and slow manifestations of active hair-bundle motility observed in frog, as well as in auditory organs of the turtle and the rat.
Tinevez
Jean-Yves
JY
Laboratoire Physico-Chimie Curie, CNRS, Institut Curie, Paris, France.
Jülicher
Frank
F
Martin
Pascal
P
D000818:Animals; D001683:Biological Clocks / Q000502:physiology*; D002465:Cell Movement / Q000502:physiology; D002478:Cells, Cultured; D003198:Computer Simulation; D054777:Hair Cells, Ampulla / Q000502:physiology*; D040542:Mechanotransduction, Cellular / Q000502:physiology*; D008954:Models, Biological; D010812:Physical Stimulation / Q000379:methods*; D011892:Rana catesbeiana; D013314:Stress, Mechanical
Proc Natl Acad Sci U S A. 2005 Nov 22;102(47):16996-7001
16287969
J Neurosci. 2005 Aug 24;25(34):7831-9
16120785
Nat Neurosci. 2007 Jan;10(1):87-92
17173047
J Neurophysiol. 1999 Nov;82(5):2171-81
10561397
Proc Natl Acad Sci U S A. 1999 Dec 7;96(25):14306-11
10588701
Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3183-8
10737791
Phys Rev Lett. 2000 May 29;84(22):5232-5
10990910
J Neurosci. 2000 Oct 1;20(19):7131-42
11007868
Proc Natl Acad Sci U S A. 2000 Oct 24;97(22):12026-31
11027302
J Neurophysiol. 2001 Aug;86(2):541-9
11495929
Proc Natl Acad Sci U S A. 2001 Dec 4;98(25):14386-91
11724944
J Neurosci. 2002 Jan 1;22(1):44-52
11756487
J Acoust Soc Am. 2002 May;111(5 Pt 1):2208-12
12051440
Biophys J. 2002 Dec;83(6):3188-201
12496088
J Biol Chem. 2003 Feb 14;278(7):5478-87
12466270
J Neurosci. 2003 Jun 1;23(11):4533-48
12805294
Nat Neurosci. 2003 Aug;6(8):832-6
12872124
Curr Opin Neurobiol. 2003 Aug;13(4):459-68
12965294
EMBO J. 2004 Apr 7;23(7):1433-40
15014434
Proc Natl Acad Sci U S A. 2004 Aug 17;101(33):12195-200
15302928
J Neurosci. 1983 May;3(5):942-61
6601693
Science. 1985 Jan 11;227(4683):194-6
3966153
J Physiol. 1985 Jul;364:359-79
4032304
Proc Natl Acad Sci U S A. 1987 May;84(9):3064-8
3495007
Proc Natl Acad Sci U S A. 1989 Apr;86(8):2918-22
2468161
Proc Natl Acad Sci U S A. 1989 Jul;86(14):5371-5
2787510
J Neurosci. 1989 Nov;9(11):3988-97
2555460
Neuron. 1988 May;1(3):189-99
2483095
Hear Res. 1990 Oct;48(3):247-63
2272934
J Physiol. 1991 Mar;434:369-98
1708822
Anal Biochem. 1991 Feb 15;193(1):16-9
1645933
Neuroreport. 1991 Feb;2(2):69-72
1883987
Cold Spring Harb Symp Quant Biol. 1990;55:547-61
1983446
J Neurosci. 1992 Sep;12(9):3291-309
1527581
J Neurophysiol. 1992 Sep;68(3):927-32
1432057
Neuron. 1993 Oct;11(4):581-94
8398149
Hear Res. 1993 Sep;69(1-2):163-75
8226337
J Neurosci. 1994 Oct;14(10):6217-29
7931574
Neuroscience. 1994 Oct;62(3):963-74
7870316
J Biol Chem. 1999 Oct 29;274(44):31373-81
10531338
Annu Rev Biophys Biomol Struct. 1995;24:59-83
7663129
Proc Natl Acad Sci U S A. 1996 Apr 30;93(9):4462-4
8633090
J Neurosci. 1996 Sep 15;16(18):5629-43
8795619
Curr Opin Neurobiol. 1997 Aug;7(4):480-6
9287199
Proc Natl Acad Sci U S A. 1997 Oct 28;94(22):11923-8
9342338
J Neurosci. 1998 Aug 15;18(16):6300-18
9698322
Proc Natl Acad Sci U S A. 1998 Dec 22;95(26):15321-6
9860967
J Neurosci. 1999 Oct 1;19(19):8377-88
10493739
Nat Neurosci. 2005 Feb;8(2):149-55
15643426
Nature. 2005 Feb 24;433(7028):880-3
15696193
Neuron. 2005 Aug 18;47(4):541-53
16102537
Biophys J. 2006 Jan 1;90(1):124-39
16214875