Active control of ultrasonic hearing in frogs

Abstract

Vertebrates can modulate the sound levels entering their inner ears in the face of intense external sound or during their own vocalizations. Middle ear muscle contractions restrain the motion of the middle ear ossicles, attenuating the transmission of low-frequency sound and thereby protecting the hair cells in the inner ear. Here we show that the Chinese concave-eared torrent frog, Odorrana tormota, can tune its ears dynamically by closing its normally open Eustachian tubes. Contrary to the belief that the middle ear in frogs permanently communicates with the mouth, O. tormota can close this connection by contraction of the submaxillary and petrohyoid muscles, drastically reducing the air volume behind the eardrums. Mathematical modeling and laser Doppler vibrometry revealed that the reduction of this air volume increases the middle ear impedance, resulting in an up to 20 dB gain in eardrum vibration at high frequencies (10-32 kHz) and 26 dB attenuation at low frequencies (3-10 kHz). Eustachian tube closure was observed in the field during calling and swallowing. Besides a potential role in protecting the inner ear from intense low-frequency sound and high buccal air pressure during calling, this previously unrecognized vertebrate mechanism may unmask the high-frequency calls of this species from the low-frequency stream noise which dominates the environment. This mechanism also protects the thin tympanic membranes from injury during swallowing of live arthropod prey.