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.
Highlights
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
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
The mechanical stimulation provided by the PZT actuator to the antennal shaft was designed to prevent any crosstalk with the auditory organ and the atomic force microscope (AFM) probe
Summary
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. Known as a scolopidium, is a multi-cellular cluster that essentially comprises: (i) one or several mechanosensory neurons each endowed with a central sensory cilium, (ii) a scolopale cell that envelops the neurons and contains a series of stiff scolopale rods, and (iii) attachment cells at the distal end linking the neuron and scolopale cells to the external auditory anatomy [2] This basic layout varies substantially between different species [1,2,3], the exact functions associated with the respective cellular scolopidial elements, and their structural characteristics, being not clearly understood.
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