PROCEEDINGS of the23rd International Congress on Acoustics
9 to 13 September 2019 in Aachen, Germany

Underwater Sound Localization using Internally Coupled Ears (ICE)
J. Leo van Hemmen1; Anupam P. Vedurmudi212

Physik Department der TU München, Germany

Heinz Maier-Leibnitz Zentrum der TU München & FRM II, Germany

ABSTRACTInternally coupled ears or for short ICE [1-4], where an interaural cavity acoustically couples theeardrums, are an anatomical trait present in more than half of all terrestrial vertebrates. Thesuperposition of outside and internal pressure on the two eardrums results in internal instead ofinteraural time and level differences, which are keys to sound localization. Although ICE is primarily
a low-frequency terrestrial adaptation, the African clawed frog Xenopus laevis is a fully aquaticspecies with a distinct air-filled canal between the ears. In water, the speed of sound is four times thatin air. Unlike terrestrial animals with ICE, the Xenopus interaural cavity is also medially connected tothe lungs. By modeling the inflated lungs as a Helmholtz resonator [5], we demonstrate their effect inimproving hearing in a low-frequency regime, while simultaneously enhancing sound localization in adisjoint high-frequency regime, corresponding to the frequency ranges of male advertisement calls. In
conjunction with its unique plate-like eardrums, we show how Xenopus uses its ICE-like interaural
coupling to generate considerable internal level differences between eardrum vibrations and thus
overcomes the challenges of underwater sound-localization. Taken together, the two arguments ofHelmholtz resonator and plate-like eardrums show [6] the potency of ICE and are interpreted
accordingly.
Keywords: Underwater hearing, sound localization, Xenopus, phonotaxis

1. INTRODUCTION
Being fully aquatic, the clawed frog Xenopus faces two problems: (i) how to get food and (ii) how
to find a sexual partner. The food consists of flies that drop onto the water surface during night. The
frog’s lateral-line system is well suited to localize them. Under water and for far-away sources,
however, the lateral line system is not effective as its range is of the same order as the frog‘s length.
Thus sound comes in, allowing for long-range localization. Moreover, what the animal actually hears
is not the external interaural time and level difference, ITD & ILD, but the internal time and level
difference, iTD & iLD, which result from the internal coupling; cf. Fig. 1. ICE has two distinct modesof operation. First, increase of the time difference that the animal actually perceives in a
low-frequency range by a factor of about 4. The precise value depends on the properties of theeardrum and the interaural cavity volume [3,4]. The iTD plateau ends at (typically) 500–700 Hz. Since
water has a sound velocity that is four times that in air and the interaural distance is small (cm), iTDs
are not a feasible means of sound localization. Second, just above the eardrum’s fundamental
frequency f0 there is an outspoken iLD maximum for directions ±90o. It may be as large as 15-20 dB.
Of course straight on gives iLD = 0, whereas ILD ≡ 0 for whatever direction.

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lvh@tum.deFigure 1: (Left) Middle ear cavity in Xenopus, which is the interaural canal (IAC) plus left and righttympanic cavities (TC). (Middle) Schematic diagram of air filled cavities in a submerged Xenopus.
The two tympanic cavities taper into a shared Eustachian tube or IAC, which is medially connected tothe lungs (L) through a recess (R) in the roof of the mouth. LAR denotes the larynx and is not relevant
to our present discussion. Plots adapted from Christensen-Dalsgaard and Elepfandt [7](Springer-Verlag, by permission). (Right) ICE model schematic for the air-filled cavities in Xenopus
based on the left two figures. The rigid, circular, cartilaginous tympanic plates (dark/blue) at far left
and right are suspended in a flexible annular outer membrane (red). The shallow TC have a distinct
taper in a direction away from the tympanic plates and are connected through a narrow IAC. The lungs(LUN) are represented by a single volume connected medially to the interaural canal (IAC) andfunction as a Helmholtz resonator []. Both the tympanic plates (instead of eardrums) and the lungs as
Helmholtz resonator are the keys to understanding Xenopus’ underwater hearing while exploiting ICE.

2. RESULTS
Male calls attract females and their localization is through amplitude differences. That is, throughdetermining iLD generated by ICE. It is known that the calls have two frequency centers, around 1.0
and 1.7 kHz. Figure 2 shows the effect of ICE

Figure 2:

Experimentally measured (filled triangles) and model vibration velocities (solid anddashed lines) of the Xenopus ipsilateral (left) and contralateral (right) eardrum underwater. The
eardrum vibration velocities have been measured [7] by using laser vibrometry and have beennormalized w.r.t. the input pressure. The solid (red) line corresponds to inflated lungs with a total

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volume VH = 1.5 cc and the dashed (black) line corresponds to the case VH = 0 cc, i.e., absent or fully
deflated lungs. The sound-source direction is ±90o. There is a maximum at about 1 kHz and an
outspoken difference between ipsi- and contralateral only at 1.7 kHz, which is needed for soundlocalization. As both plots show, the experimental results can be explained only with inflated lungs
that perform a Helmholtz-resonator function.

3. CONCLUSIONS
Figure 2 actually shows three things. First, without inflated lungs one cannot explain theexperimental data. Second, clawed frogs exhibit an outspoken auditory sensitivity around 1.0 kHz,
which facilitates noticing a sexual partner. Third, only around 1.7 kHz do we see a clear difference
between ipsi- and contralateral response; that is, an outspoken iLD (of about 18 dB), which allows
decently precise localization of a sound source by turning the head. After all, mating needs no narrow
time window.
Finally, why does Xenopus use a rigid plate as eardrum? A rigid plate absorbs [6] more power thana flexible eardrum near 1 kHz both in water and in air (for rare peregrinations from one pond toanother one), whereas the flexible membrane only peaks [6] below 400 Hz. This suggests that theXenopus eardrum is adapted to improve hearing around 1 kHz in both media; cf. the fictitious frog
Xenopus2 [6].

REFERENCES
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J.L. van Hemmen, J. Christensen-Dalsgaard, C.E. Carr, and P.M. Narins, Biol. Cybern. 110(4),237-246 (2016); review of ICE
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C. Vossen, J. Christensen-Dalsgaard, and J.L. van Hemmen, J. Acoust. Soc. Am. 128, 909–918(2010)
3.

A.P. Vedurmudi et al., Phys. Rev. Lett. 116, 028101 (2016)

4.

A.P. Vedurmudi, B.A. Young, and J.L. Hemmen, Biol. Cybern. 110(4–5), 359-382 (2016)

5.

A. Hirschberg and S. Rienstra, An Introduction to Acoustics (TU Eindhoven, Netherlands, 2004),

pp. 103-105
6.

A.P. Vedurmudi, J. Christensen-Dalsgaard, and J.L. van Hemmen, J. Acoust. Soc. Amer. 144(5),3010-3021 (2018)7.

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J. Christensen-Dalsgaard and A. Elepfandt, J. Comp. Physiol. A 176(3), 317-324 (1995)