Power gain exhibited by motile mechanosensory neurons in Drosophila ears

Abstract

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...

Mechanotransduction and auditory transduction in Drosophila

“…TRPV channels negatively regulate this feedback and are also required to depolarize the neuron to generate action potentials. The gating mode and stimulus that open the TRPV channels are unspecified antennae can oscillate in the absence of any stimulus [36,38]. Thus, some motor element adds mechanical energy to the system to boost sensitivity, a function similar to the outer hair cells of the mammalian cochlear amplifier.…”

Enhancement of sensitivity gain and frequency tuning by coupling of active hair bundles

“…All these properties could be understood as the consequence of nonlinear dynamic oscillators that operate in the ear (4-7). There is clear evidence for nonlinear amplification to occur in all vertebrates (3) and even some insects (8). However, the specific molecular and cellular mechanisms underlying the amplifiers in different species are still under debate.…”

Dissection of Gain Control Mechanisms inDrosophilaMechanotransduction

“…Mechanical amplification and spontaneous mechanical emissions have also been demonstrated in the hearing organ of Drosophila (Göpfert et al, 2005(Göpfert et al, , 2006. Functional mechanotransduction was required for both phenomena, indicating that as postulated in vertebrates, the transduction machinery in Drosophila is necessary for producing active amplification (Göpfert et al, 2006).…”