Reconstruction of sound driven, actively amplified and spontaneous motions within the tree cricket auditory organ

Abstract

Hearing consists of a delicate chain of events. Sound is first captured by an eardrum or similar organ which is set into vibrations, these vibrations must then be transmitted to sensory cells in a manner that opens mechanosensory channels generating an electrical signal. Studying this process is challenging. Auditory vibrations are in the nano- to picometer-scale and occur at fast temporal scales of milli to microseconds. Finally, most of this process occurs within the body of the animal where it is inaccessible to conventional measurement techniques. For instance, even in crickets, a century-old auditory model system, it is unclear how sound evoked vibrations are transmitted to sensory neurons. Here, we use optical coherence tomography (OCT) to measure how vibrations travel within the auditory organ of the western tree cricket (Oecanthus californicus). We also measure the reversal of this process as mechanosensory cells generate spontaneous oscillations and amplify sound-evoked vibrations. Most importantly, we found that while the mechanosensory neurons were not attached to the peripheral sound collecting structures, they were mechanically well-coupled through acoustic trachea. Thus, the acoustic trachea are not merely conduits for sound but also perform a mechanical function. Our results generate several insights into the similarities between insect and vertebrate hearing, and into the evolutionary history of auditory amplification.

Coupled membranes: a mechanism of frequency filtering and transmission in the field cricket ear evidenced by micro-computed tomography, laser Doppler vibrometry and finite element analysis

“…However, in 2021, the bushcricket (Tettigoniidae) ‘tracheal septum’, a structure that is analogous to the field cricket dividing membrane, was shown by optical coherence tomography (OCT) to move in-phase with the PTM, thus indicating its role in mechanically coupling transmission from the PTM to the sensory neurons [47]. In the same year, an OCT study on the tree cricket (Oecanthinae) acoustic trachea revealed similar results [24]. While the morphology of the field cricket tracheal branches differs from that of these ensiferans, our findings align with these recent studies and reinforce the importance of continuing to investigate how tracheal structures mechanically transmit and filter signals from the tympana to the auditory neurons.…”

“…The tracheal branches of the ensiferan ear have previously been thought to function mainly to channel sound in the air column to the tympana [ 24 ]. However, in 2021, the bushcricket (Tettigoniidae) ‘tracheal septum’, a structure that is analogous to the field cricket dividing membrane, was shown by optical coherence tomography (OCT) to move in-phase with the PTM, thus indicating its role in mechanically coupling transmission from the PTM to the sensory neurons [ 47 ].…”

“…The field cricket anterior tracheal branch (ATB) is distinct compared to other more arboreal ensiferans: Eneopeterinae [ 21 ], Oecanthinae [ 24 ], Tettigoniidae [ 25 ] and Hagloidea [ 26 ]. Unlike these taxa, the Gryllinae ATB is not in direct contact with the ATM and is considerably smaller than the PTB (see figure 2 c ).…”

Auditory mechanics in the grig ( Cyphoderris monstrosa ): tympanal travelling waves and frequency discrimination as a precursor to inner ear tonotopy

“…These two modalities may therefore simply aid in the tonotopy of the CA, which then begins to further filter vibrations by their frequency composition. Non-invasive mechanical measurements of the CA of C. monstrosa by novel methods such as optical coherence tomography [ 18 , 46 ] would be useful in clarifying the relative contribution of the tympana to overall frequency discrimination.…”

“…Recently, it was shown in Tettigoniidae that the DW of the anterior tracheal branch is tonotopic and contributes heavily to the mechanotransduction process [ 18 ]. Given that the anterior tympanum and mechanosensory units of C. monstrosa are mechanically coupled by the anterior tracheal branch like in most Ensiferans [ 46 ], we postulate that the tonotopic vibrations of the DW have originated from a tonotopic tympanum, with the vibrations shifting dorsally along the anterior tracheal branch over evolutionary time to reduce internal attenuation of the peripheral mechanical displacement. Observations of the displacement of the tympana of tettigoniid species show that while the CA and DW are tonotopic, the tympana are not [ 10 , 11 , 35 ], and thus the tonotopic arrangement may have simply shifted to the DW, with the process of hearing involving an additional mechanical step [ 8 , 18 , 35 ].…”