Effects of age and noise on tympanal displacement in the Desert Locust

Animals that sensitively detect sound evolved specialised structures that capture sound energy. Some insect sound detectors capture the particle velocity component of sound with antennae, such as fruit flies and mosquitos, whilst others detect the pressure component of sound with specialised tympani, such as crickets and locusts. Vertebrate sound receivers are exclusively tympanal but even in invertebrates, tympani are the most common form of sound receiver (Yager, 1999). The tympanum of the desert Locust has two distinct regions of different thickness and stiffness which are straddled by Müller’s organ on its interior surface. The tympanum’s thin membrane is stiffer and detects high frequencies whereas the thick membrane is less stiff and detects low frequencies. Three groups of auditory neurons attach to the different parts of the tympanum to exploit differences in mechanical tuning. As such, Müller’s organ can detect frequencies from 200 Hz to at least 40 kHz (Römer, 1976). How does the mechanical function of the tympanum change as a function of age and noise exposure?

Longitudinal measurements of the human middle ear offer a good understanding of how sound receivers change as a function of age and noise-exposure. The mechanical properties of the middle ear change with age (Ruah et al., 1991) and could explain some age-related hearing loss (Corso, 1992, Rosenhall et al., 1990). Elderly humans with abnormal tympanometry are ∼50% more likely to have age-related hearing loss (Sogebi, 2015) and middle ear admittance (compliance) tends to decrease from the age of 20 to 40 (Wada et al., 1993). A consistent finding is no further changes in middle ear properties after the age of 40. This includes tympanal static admittance, typanometric peak pressure (the pressure at which there is greatest absorption of acoustic energy in the middle-ear), or resonance frequency of the middle ear (Uchida et al., 2000, Sinha et al., 2021) and acoustic conductance (Thompson et al., 1979).

Sound receivers of insects also change as a function of age and noise. For the sound receiver of the Locust, sound-evoked tympanal displacements decrease with age (Gordon and Windmill, 2015) which is concurrent with an age-related decrease in Müller’s organ function (Blockley et al., 2022). Directly after extended (24 hour) noise-exposure the Locust’s sound-evoked tympanal displacements dramatically increase (Warren et al., 2020) but recover to normal amplitudes 48 hours later for shorter (12 hour) noise-exposure. In contrast the passive stiffness of the antennal sound receiver of the fruit fly is robust to aging in spite of deterioration of auditory organ function (Keder et al., 2020). In response to noise-exposure, changes in the antennal mechanics are determined by the active motility of the auditory neurons of Johnston’s organ (Boyd-Gibbins et al., 2021).

Electrophysiological performance and morphology of the Locust’s Müller’s organ is well characterised as a function of age (Blockley et al., 2022). The function of individual auditory neurons is well maintained but the auditory nerve response to sound decreases with age. In response to repeated noise-exposure (every three days) the function of the individual auditory neurons steadily deteriorates and auditory nerve function deteriorates. For very old Locusts, age-related auditory decline dominates such that the difference between repeatably noise-exposed aged Locusts and control aged Locusts narrows. This echoes findings in humans, where hearing loss in repeatedly noise-exposed workers is most different to non-noise-exposed workers in middle-life (Corso, 1992).

Age and noise effects on the Locusts’ Müller’s organ (Blockley et a., 2022) could be explained by changes of the tympanum. Noise-exposure in the desert Locust has focused on Group-III auditory neurons – tuned to ∼3 kHz (Jacobs et al., 1999, Warren and Matheson, 2018) - that attach, through sclerites, to the foot of the styliform body (Fig. 2A). Here, we examine the interaction of both noise-induced and age-related auditory decline by measuring tympanal displacements at the foot of the styliform body in response to 3 kHz tones.

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