Frequency doubling by activein vivomotility of mechanosensory neurons in the mosquito ear

Abstract

Across vertebrate and invertebrate species, nonlinear active mechanisms are employed to increase the sensitivity and acuity of hearing. In mosquitoes, the antennal hearing organs are known to use active force feedback to enhance auditory acuity to female generated sounds. This sophisticated form of signal processing involves active nonlinear events that are proposed to rely on the motile properties of mechanoreceptor neurons. The fundamental physical mechanism for active auditory mechanics is theorized to rely on a synchronization of motile neurons, with a characteristic frequency doubling of the force generated by an ensemble of motile mechanoreceptors. There is however no direct biomechanical evidence at the mechanoreceptor level, hindering further understanding of the fundamental mechanisms of sensitive hearing. Here, using in situ and in vivo atomic force microscopy, we measure and characterize the mechanical response of mechanosensory neuron units during forced oscillations of the hearing organ. Mechanoreceptor responses exhibit the hallmark of nonlinear feedback for force generation, with movements at twice the stimulus frequency, associated with auditory amplification. Simultaneous electrophysiological recordings exhibit similar response features, notably a frequency doubling of the firing rate. This evidence points to the nature of the mechanism, whereby active hearing in mosquitoes emerges from the double-frequency response of the auditory neurons. These results open up the opportunity to directly investigate active cellular mechanics in auditory systems, and they also reveal a pathway to study the nanoscale biomechanics and its dynamics of cells beyond the sense of hearing.

Material stiffness variation in mosquito antennae

“…[41], in that the prongs act more or less as rigid-body extensions of the flagellum. Possible variations inside the pedicel would likely be due to the scolopidia, which have recently been shown, by direct measurement using atomic force microscopy, to be motile [42], having long been suspected as the source of stiffness gating. Further studies have shown the importance of the scolopidia for both power gain of the antenna, and the intra- and interspecifc variations seen in antennal mechanics [32].…”

“…This is in agreement with Avitabile et al [41], in that the prongs act more or less as rigid-body extensions of the flagellum. Possible variations inside the pedicel would likely be due to the scolopidia, which have recently been shown, by direct measurement using atomic force microscopy, to be motile [42], having long been suspected as the source of stiffness royalsocietypublishing.org/journal/rsif J. R. Soc. Interface 16: 20190049 gating.…”

Atomic force microscopy-based mechanobiology

“…Interestingly, neurons from peripheral nervous systems show higher resistance to mechanical damage than neurons from the brain 99 , providing insight into how neurons may cope with mechanical trauma. Other recent advances include the use of optical microscopy to guide the atomic force microscope probe to mechanically stimulate cellular systems involved in the hearing of mice or insects and to characterize their functional response [100][101][102] , leading to the observation that the response of mechanosensory neurons of the hearing organ to mechanical stimulation is nonlinear 102 .…”

Olfactory systems across mosquito species

“…1, H1-H3). Apart from having an olfactory function, antennae also mediate sound detection in mosquitoes (e.g., Warren et al 2010;Lapshin 2012;Windmill et al 2018;Su et al 2018) and the evolution of overall antennal morphology has most likely been driven by demands of both olfaction and hearing.…”