Two classes of outer hair cells along the tonotopic axis of the cochlea

Engel, Jutta; Braig, Claudia; Rüttiger, Lukas; Kuhn, Stephanie; Zimmermann, Ulrike; Blin, Nikolaus; Sausbier, Matthias; Kalbacher, Hubert; Münkner, Stefan; Rohbock, Karin; Ruth, Peter; Winter, Harald; Knipper, Marlies

doi:10.1016/j.neuroscience.2006.08.060

Cited by 90 publications

(115 citation statements)

References 45 publications

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“…Next, the membrane time constant of OHCs restricts electromotility's ability to work on a cycle-by-cycle basis to frequencies below a few kilohertz (33,34), disabling the ratchet mechanism for higher frequencies. It is noteworthy that the ion channels of apical OHCs differ significantly from those of basal OHCs (35) and that apical OHCs are considerably longer than basal ones and can accordingly produce greater length changes (25).…”

Section: Resultsmentioning

confidence: 99%

A ratchet mechanism for amplification in low-frequency mammalian hearing

Reichenbach

Hudspeth

2010

Proc. Natl. Acad. Sci. U.S.A.

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The sensitivity and frequency selectivity of hearing result from tuned amplification by an active process in the mechanoreceptive hair cells. In most vertebrates, the active process stems from the active motility of hair bundles. The mammalian cochlea exhibits an additional form of mechanical activity termed electromotility: its outer hair cells (OHCs) change length upon electrical stimulation. The relative contributions of these two mechanisms to the active process in the mammalian inner ear is the subject of intense current debate. Here, we show that active hair-bundle motility and electromotility can together implement an efficient mechanism for amplification that functions like a ratchet: Sound-evoked forces, acting on the basilar membrane, are transmitted to the hair bundles, whereas electromotility decouples active hair-bundle forces from the basilar membrane. This unidirectional coupling can extend the hearing range well below the resonant frequency of the basilar membrane. It thereby provides a concept for lowfrequency hearing that accounts for a variety of unexplained experimental observations from the cochlear apex, including the shape and phase behavior of apical tuning curves, their lack of significant nonlinearities, and the shape changes of threshold tuning curves of auditory-nerve fibers along the cochlea. The ratchet mechanism constitutes a general design principle for implementing mechanical amplification in engineering applications.auditory system | cochlea | hair cell T he mammalian cochlea acts as a frequency analyzer in which high frequencies are detected at the organ's base and low frequencies at more apical positions. This frequency mapping is thought to be achieved by a position-dependent resonance of the elastic basilar membrane separating two fluid-filled compartments ( Fig. 1A) (1-3). When sound evokes a pressure wave that displaces the basilar membrane, the resultant traveling wave gradually increases in amplitude as it progresses to the position where the basilar membrane's resonant frequency coincides with that of the stimulus. Aided by mechanical energy provided by the active process, the wave peaks at a characteristic place slightly before the resonant position and then declines sharply (Fig. 1B). This mechanism is termed critical-layer absorption (1), for a wave cannot travel beyond its characteristic position on the basilar membrane but peaks and dissipates most of its energy there. The mechanism displays scale invariance: different stimulation frequencies induce traveling waves that display a common, strongly asymmetric form upon rescaling of the amplitude and spatial coordinate (4, 5).Two important aspects of the cochlea's mechanics remain problematical. First, the basilar membrane's resonant frequency apparently cannot span the entire range of audible frequencies. Experimental measurements of basilar-membrane stiffness suggest that high-frequency resonances are feasible but lowfrequency ones are inaccessible (6). This result accords with the analysis of threshold tuning curve...

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Section: Resultsmentioning

confidence: 99%

A ratchet mechanism for amplification in low-frequency mammalian hearing

Reichenbach

Hudspeth

2010

Proc. Natl. Acad. Sci. U.S.A.

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“…Auditory brainstem responses (ABRs) to click and pure tone auditory stimuli and the cubic 2*f1-f2 distortion product otoacoustic emission (DPOAE) for f2 ϭ 1.24*f1 and L2 ϭ L1 ϩ 10 dB were recorded in anesthetized mice aged 9 -12 weeks in a soundproof chamber as described previously (Engel et al, 2006). In short, ABR thresholds were determined with click (100 s), noise burst (1 ms), or pure tone stimuli (3 ms, including 1 ms cosine squared rise and fall envelope, 2-45 kHz).…”

Section: Methodsmentioning

confidence: 99%

Lack of Brain-Derived Neurotrophic Factor Hampers Inner Hair Cell Synapse Physiology, But Protects against Noise-Induced Hearing Loss

Zuccotti¹,

Kuhn²,

Johnson³

et al. 2012

Journal of Neuroscience

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120

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The precision of sound information transmitted to the brain depends on the transfer characteristics of the inner hair cell (IHC) ribbon synapse and its multiple contacting auditory fibers. We found that brain derived neurotrophic factor (BDNF) differentially influences IHC characteristics in the intact and injured cochlea. Using conditional knock-out mice (BDNF Pax2 KO) we found that resting membrane potentials, membrane capacitance and resting linear leak conductance of adult BDNF Pax2 KO IHCs showed a normal maturation. Likewise, in BDNF Pax2 KO membrane capacitance (⌬C m ) as a function of inward calcium current (I Ca ) follows the linear relationship typical for normal adult IHCs. In contrast the maximal ⌬C m , but not the maximal size of the calcium current, was significantly reduced by 45% in basal but not in apical cochlear turns in BDNF Pax2 KO IHCs. Maximal ⌬C m correlated with a loss of IHC ribbons in these cochlear turns and a reduced activity of the auditory nerve (auditory brainstem response wave I). Remarkably, a noise-induced loss of IHC ribbons, followed by reduced activity of the auditory nerve and reduced centrally generated wave II and III observed in control mice, was prevented in equally noise-exposed BDNF Pax2 KO mice. Data suggest that BDNF expressed in the cochlea is essential for maintenance of adult IHC transmitter release sites and that BDNF upholds opposing afferents in high-frequency turns and scales them down following noise exposure.

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“…Cholinergic inhibition of most sensory hair cells involves activation of SK channels associated with ionotropic ACh receptors containing ␣9␣10-subunits (Elgoyhen et al, 1994(Elgoyhen et al, , 2001) through which calcium enters to activate SK channels and hyperpolarize the hair cells (Housley and Ashmore, 1991;Shigemoto and Ohmori, 1991;Fuchs and Murrow, 1992;Evans, 1996). However, recent work has shown by immunofluorescence that BK channels can be found near efferent synapses on cochlear outer hair cells (OHCs; Engel et al, 2006). In vitro examination using intracellular recordings and quantitative immunofluorescence confirmed that BK channels are present only in OHCs from cochlear (highfrequency) middle and basal turns of rats aged P21, where they contribute to ACh-evoked as well as voltage-gated membrane currents (Wersinger et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Activation of BK and SK Channels by Efferent Synapses on Outer Hair Cells in High-Frequency Regions of the Rodent Cochlea

et al. 2015

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Cholinergic neurons of the brainstem olivary complex project to and inhibit outer hair cells (OHCs), refining acoustic sensitivity of the mammalian cochlea. In all vertebrate hair cells studied to date, cholinergic inhibition results from the combined action of ionotropic acetylcholine receptors and associated calcium-activated potassium channels. Although inhibition was thought to involve exclusively small conductance (SK potassium channels), recent findings have shown that BK channels also contribute to inhibition in basal, highfrequency OHCs after the onset of hearing. Here we show that the waveform of randomly timed IPSCs (evoked by high extracellular potassium) in high-frequency OHCs is altered by blockade of either SK or BK channels, with BK channels supporting faster synaptic waveforms and SK channels supporting slower synaptic waveforms. Consistent with these findings, IPSCs recorded from high-frequency OHCs that express BK channels are briefer than IPSCs recorded from low-frequency (apical) OHCs that do not express BK channels and from immature high-frequency OHCs before the developmental onset of BK channel expression. Likewise, OHCs of BK␣ Ϫ/Ϫ mice lacking the pore-forming ␣-subunit of BK channels have longer IPSCs than do the OHCs of BK␣ ϩ/ϩ littermates. Furthermore, serial reconstruction of electron micrographs showed that postsynaptic cisterns of BK␣ Ϫ/Ϫ OHCs were smaller than those of BK␣ ϩ/ϩ OHCs, and immunofluorescent quantification showed that efferent presynaptic terminals of BK␣ Ϫ/Ϫ OHCs were smaller than those of BK␣ ϩ/ϩ OHCs. Together, these findings indicate that BK channels contribute to postsynaptic function, and influence the structural maturation of efferent-OHC synapses.

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Two classes of outer hair cells along the tonotopic axis of the cochlea

Cited by 90 publications

References 45 publications

A ratchet mechanism for amplification in low-frequency mammalian hearing

A ratchet mechanism for amplification in low-frequency mammalian hearing

Lack of Brain-Derived Neurotrophic Factor Hampers Inner Hair Cell Synapse Physiology, But Protects against Noise-Induced Hearing Loss

Activation of BK and SK Channels by Efferent Synapses on Outer Hair Cells in High-Frequency Regions of the Rodent Cochlea

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