Active auditory mechanics in mosquitoes

Göpfert, MC; Robert, Daniel

doi:10.1098/rspb.2000.1376

Cited by 169 publications

(161 citation statements)

References 41 publications

(42 reference statements)

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“…1 A). These spontaneous twitches built up into large-amplitude, self-sustained oscillations when the physiological condition of the animal deteriorated [e.g., after thoracic injection of DMSO (17,22)] and disappeared with the animal's death ( Fig. 1 A).…”

Section: Resultsmentioning

confidence: 99%

Power gain exhibited by motile mechanosensory neurons in Drosophila ears

Göpfert

Humphris²,

Albert³

et al. 2004

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

117

137

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In insects and vertebrates alike, hearing is assisted by the motility of mechanosensory cells. Much like pushing a swing augments its swing, this cellular motility is thought to actively augment vibrations inside the ear, thus amplifying the ear's mechanical input. Power gain is the hallmark of such active amplification, yet whether and how much energy motile mechanosensory cells contribute within intact auditory systems has remained uncertain. Here, we assess the mechanical energy provided by motile mechanosensory neurons in the antennal hearing organs of Drosophila melanogaster by analyzing the fluctuations of the sound receiver to which these neurons connect. By using dead WT flies and live mutants (tilB 2 , btv 5P1 , and nompA 2 ) with defective neurons as a background, we show that the intact, motile neurons do exhibit power gain. In WT flies, the neurons lift the receiver's mean total energy by 19 zJ, which corresponds to 4.6 times the energy of the receiver's Brownian motion. Larger energy contributions (200 zJ) associate with self-sustained oscillations, suggesting that the neurons adjust their energy expenditure to optimize the receiver's sensitivity to sound. We conclude that motile mechanosensory cells provide active amplification; in Drosophila, mechanical energy contributed by these cells boosts the vibrations that enter the ear.cochlear amplifier ͉ hearing ͉ auditory mechanics ͉ cell mobility ͉ hair cell T he cochlear amplifier is the dominant unifying concept in cochlear mechanics (1). The concept assumes that the cochlea is endowed with a biological energy source that amplifies the ear's input by pumping mechanical energy into the vibrations inside the ear (1-6). The validity of the concept is supported by the mechanics of the cochlea and its mechanosensory cells. Hair cells, the cochlear mechanosensory cells, provide a source of mechanical energy. In addition to transducing mechanical vibrations into electrical responses, some hair cells are equipped with molecular motors that convert metabolic or electrical energy into mechanical energy, resulting in active movements of the cells (1, 3-7). These cellular movements, in turn, exert positive feedback on the cochlear mechanics. By nonlinearly undamping the cochlear resonances as the stimulus intensity declines, this feedback selectively improves the ear's sensitivity to small vibrations induced by faint sound (1, 3-6). Notably, this hair cell-based feedback occasionally becomes unstable, leading to self-sustained feedback oscillations within the cochlear duct. Such self-sustained feedback oscillations may account for the ear's ability to generate spontaneous otoacoustic emissions, i.e., to spontaneously emit sound (8, 9).Collectively, the hair cells' motility, the cochlea's nonlinearity, and the ear's spontaneous otoacoustic emissions document the presence of hair cell-based mechanical feedback inside the cochlear duct. Yet, whether this feedback brings about power gain by expending biological energy, as assumed by the concept of the cochlear ampli...

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Section: Resultsmentioning

confidence: 99%

Power gain exhibited by motile mechanosensory neurons in Drosophila ears

Göpfert

Humphris²,

Albert³

et al. 2004

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

117

137

View full text Add to dashboard Cite

show abstract

“…In a quiet environment, in turn, excess feedback can lead to spontaneous oscillations, explaining the fascinating ability of the cochlea to spontaneously emit sound (9,10). Nonlinearity and spontaneous oscillations have recently been documented for the auditory system of mosquitoes (11), putting forward the question of whether the auditory mechanosensory neurons that mediate hearing in insects mechanically assist audition in a hair cell-like way (12)(13)(14)(15). Here, we dissect the auditory mechanics in Drosophila melanogaster and show that its mechanosensory neurons are motile.…”

mentioning

confidence: 99%

Motion generation by Drosophila mechanosensory neurons

Göpfert

Robert

2003

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

163

128

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In Drosophila melanogaster, hearing is supported by mechanosensory neurons transducing sound-induced vibrations of the antenna. It is shown here that these neurons additionally generate motions that mechanically drive the antenna and tune it to relevant sounds. Motion generation in the Drosophila auditory system is betrayed by the auditory mechanics; the antenna of the fly nonlinearly alters its tuning as stimulus intensity declines and oscillates spontaneously in the absence of sound. The susceptibility of auditory motion generation to mechanosensory mutations shows that motion is generated by mechanosensory neurons. Motion generation depends on molecular components of the mechanosensory transduction machinery (NompA, NompC, Btv, and TilB), apparently involving mechanical activity of ciliated dendrites and microtubule-dependent motors. Hence, in analogy to vertebrate hair cells, the mechanosensory neurons of the fly serve dual, transducing, and actuating roles, documenting a striking functional parallel between the vertebrate cochlea and the ears of Drosophila.

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“…In O. nigricornis SOs show the same characteristics as SOs in other well characterised insect auditory systems such as Drosophila and mosquitoes (Göpfert and Robert 2001;Göpfert and Robert 2003); they are around the best frequency of the receiver, they increase in amplitude following ethanol injection and they are never seen post mortem. Although their amplitude is in the picometer range, they are observed above the noise floor of the measurement system.…”

Section: Active Auditory Systemmentioning

confidence: 66%

“…To induce SOs, repetitive acoustic stimulation and injection of ethanol or DMSO have previously been used (Göpfert and Robert 2001). Here, some animals were exposed to white noise with a bandwidth of 10 kHz for 30 minutes at 60 dB SPL.…”

Section: Self-sustained Oscillationsmentioning

confidence: 99%

“…To achieve this many animals have evolved a nonlinear auditory response, whereby the receiver shows increased sensitivity to quiet sounds and sensory cells selectively and actively tune into frequencies of interest. Auditory nonlinearities are known across all vertebrate groups (Manley 2000;Manley et al 2008) and in insects have been found in mosquitoes (Göpfert and Robert 2001), Drosophila (Göpfert and Robert 2003) and the tree cricket, O. henryi (Mhatre and Robert 2013). The female O. henryi auditory system becomes selectively tuned into male call frequencies at low amplitudes, but at high stimulus amplitudes this tuning is lost.…”

Section: Introductionmentioning

confidence: 99%

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