Detection of Airborne Sound by a Cockroach ‘Vibration Detector’: A Possible Missing Link in Insect Auditory Evolution

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Abstract
Extracellular recordings from nerve 5 in metathoracic legs of Periplaneta americana disclose a sense organ that is extremely responsive to vibration but also detects sound (best response near 1.8 kHz) with a sensitivity similar to some insect auditory organs. The energy required from an auditory signal for a criterion response is similar or even smaller than for an optimal vibratory input. Responses originate in the subgenual organs (SGO) in the proximal tibiae, and cross-modal adaptation indicates that the same cells respond to both vibration and sound. Sound is picked up directly on some internal structure, not via sound-induced substratum vibration. Adaptation at different frequencies discloses no frequency-selectivity in the SGO. The nerve response is a burst of synchronized impulses at a frequency, fR, of approximately 300 Hz, that is practically invariant both with sound intensity and within the burst, suggesting that fR might represent some underlying resonance phenomenon, either of the SGO or of air in the tracheal system. The latter possibility is ruled out by observations made while the tracheae are perfused with He–O2. Similar responses can be recorded from the pro-and mesothoracic legs. Although Periplaneta is thought to be deaf and appears to ignore loud tones presented to the home colony, a more sensitive assay detects small leg movements in response to sound, confirming the presence of a functional auditory sense. The SGO is suspended from an expansion of the leg trachea, which may function to enhance sensitivity to vibration. This linkage preadapts the SGO to detect airborne sound transmitted in the tracheal system, and contact vibration may also stimulate the system in part by deforming the tracheae. It is proposed that auditory organs of crickets evolved from an ancestral SGO that already possessed dual responsiveness by subsequently developing effective vibration-isolating filters.