Active tympanic tuning facilitates sound localization in animals with internally coupled ears.

Earlier studies have reported that numerous vertebrate taxa have skeletal muscle(s) attaching directly, or indirectly, onto the tympanic membrane. The present study links these prior studies by quantitatively modeling the influence of skeletal muscle contraction on tympanic tension, tympanic dampening, and, ultimately, the fundamental frequency. In this way, the efficacy of these tympanic muscles to dynamically alter the sensory response of the vertebrate ear is quantified. Changing the tension modifies the eardrum's fundamental frequency, a key notion in understanding hearing through internally coupled ears (ICE) as used by the majority of terrestrial vertebrates. Tympanic tension can also be modulated by altering the pressure acting on the deep (medial) surface of the tympanum. Herein we use the monitor lizard Varanus as an example to demonstrate how active modulation of the pharyngeal volume permits tuning of an ICE auditory system. The present contribution offers a behaviorally and biologically realistic perspective on the ICE system, by demonstrating how an organism can dynamically alter its morphology to tune the auditory response. Through quantification of the relationships between tympanic surface tension, damping, membrane fundamental frequency, and auditory cavity volume, it can be shown that an ICE system affords a biologically relevant range of tuning.

Modeling underwater hearing and sound localization in the frog Xenopus laevis.

Animals that are small compared to sound wavelengths face the challenge of localizing a sound source since the main cues to sound direction-interaural time differences (ITD) and interaural level differences (ILD)-both depend on size. Remarkably, the majority of terrestrial vertebrates possess internally coupled ears (ICE) with an air-filled cavity connecting the two eardrums and producing an inherently directional middle-ear system. Underwater, longer wavelengths and faster sound-speed reduce both ITD and ILD cues. Nonetheless, many animals communicate through and localize underwater sound. Here, a typical representative equipped with ICE is studied: the fully aquatic clawed frog Xenopus laevis. It is shown that two factors improve underwater sound-localization quality. First, inflated lungs function as Helmholtz resonator and generate directional amplitude differences between eardrum vibrations in the high-frequency (1.7-2.2 kHz) and low-frequency (0.8-1.2 kHz) range of the male advertisement calls. Though the externally arriving ILDs practically vanish, the perceived internal level differences are appreciable, more than 10 dB. As opposed to, e.g., lizards with thin and flexible eardrums, plate-like eardrums are shown to be Xenopus' second key to successfully handling aquatic surroundings. Based on ICE, both plate-like eardrums and inflated lungs functioning as Helmholtz resonators explain the phonotaxis performance of Xenopus.

Internally coupled ears: mathematical structures and mechanisms underlying ICE.

In internally coupled ears (ICE), the displacement of one eardrum creates pressure waves that propagate through air-filled passages in the skull, causing a displacement of the opposing eardrum and vice versa. In this review, a thorough mathematical analysis of the membranes, passages, and propagating pressure waves reveals how internally coupled ears generate unique amplitude and temporal cues for sound localization. The magnitudes of both of these cues are directionally dependent. On the basis of the geometry of the interaural cavity and the elastic properties of the two eardrums confining it at both ends, the present paper reviews the mathematical theory underlying hearing through ICE and derives analytical expressions for eardrum vibrations as well as the pressures inside the internal passages, which ultimately lead to the emergence of highly directional hearing cues. The derived expressions enable one to explicitly see the influence of different parts of the system, e.g., the interaural cavity and the eardrum, on the internal coupling, and the frequency dependence of the coupling. The tympanic fundamental frequency segregates a low-frequency regime with constant time-difference magnification (time dilation factor) from a high-frequency domain with considerable amplitude magnification. By exploiting the physical properties of the coupling, we describe a concrete method to numerically estimate the eardrum's fundamental frequency and damping solely through measurements taken from a live animal.