First published online December 1, 2006
Journal of Experimental Biology 209, 4984-4993 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02594
Voices of the dead: complex nonlinear vocal signals from the larynx of an ultrasonic frog
Roderick A. Suthers1,*,
Peter M. Narins2,
Wen-Yu Lin3,
Hans-Ulrich Schnitzler4,
Annette Denzinger4,
Chun-He Xu5 and
Albert S. Feng3
1 School of Medicine, Department of Biology, and Program for Neuroscience,
Jordan Hall, 1001 E. Third Street, Indiana University, Bloomington, IN 47405,
USA
2 Departments of Physiological Science and Ecology and Evolutionary Biology,
University of California, Los Angeles, CA 90095, USA
3 Department of Molecular and Integrative Physiology, University of
Illinois, Urbana, IL 61801, USA
4 Lehrstuhl Tierphysiologie, Zoologisches Institut, Universität
Tübingen, D-72076 Tübingen, Germany
5 Shanghai Institutes of Biological Sciences, The Chinese Academy of
Science, Shanghai, P. R. China
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Fig. 1. Sequence of sounds produced by air flowing through the larynx of a
euthanized frog, showing bifurcations from a limit cycle to subharmonics and
chaos as sublaryngeal pressure driving airflow increases (A), and reverse
sequence from chaos through subharmonic regimes as pressure decreases (B).
Note the abrupt drop in the sound level during the harmonic window in the
chaos. Subharmonics that are fractional integers of fundamental frequency
(f0) are only faintly visible because of roll-off of the
ultrasonic microphone. An 8 s segment of chaos between the end of (A) and
beginning of (B) is omitted. 1 cmH2O=98 Pa.
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Fig. 2. Power spectra of selected subharmonic and chaotic regimes of sound in
Fig. 1. (A) Subharmonics at
integer multiples of 0.5 fundamental frequency (f0). The
0.5 f0 component is low intensity and coincides with a
faint tonal artifact. (B) Chaos. (C) Subharmonics at 0.1
f0. Subharmonics that are fractional integers of
f0 are at a low level because of roll-off of the
ultrasonic microphone and some are masked in noise. Each power spectrum
represents a 5 ms segment of sound at the time indicated by vertical arrows a,
d and e in Fig. 1. Shaded peaks
below approximately 12 kHz did not arise from the frog, but are low-amplitude
tonal artifacts present in the recording even when sublaryngeal pressure was
at ambient level and no air was flowing through the frog's vocal system.
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Fig. 3. Sublaryngeal pressure during 40-ms interval beginning 20 ms before
bifurcation. Left column (A,C,E) is pressure at first appearance of
nonlinearity as pressure gradually increases. Right column (B,D,F) is pressure
at end of last occurrence of nonlinearity as pressure decreases. (A,B), limit
cycle; (C,D), subharmonics; (E,F), apparent deterministic chaos. Beginning and
end of the same pressure cycle is represented by matching color for given type
of sound. Black line, linear regression of mean. Mean slopes are not
significant, r2 0.003. 1 cmH2O=98 Pa.
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Fig. 4. Nonlinear phenomena at sonic frequencies. (A) Fundamental frequency of
audible sound is correlated with the amplitude of the driving air pressure.
(B) A small pressure increase at approximately 3.2 s coincides with an eight-
to seven mode-locking transition and an increase in the sound level. It is not
clear whether the change in pressure is the cause or result of the sudden
transition in the oscillatory state and amplitude. (C) Period doubling,
frequency jumps and chaos with a low audible fundamental frequency
(f0). Click-like spikes in sound indicated by diagonal
arrows are artifacts caused by flexing of a plastic membrane that sealed the
open end of a centrifuge tube around the frog's neck. All data are from frog
#4. 1 cmH2O=98 Pa.
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Fig. 5. Example of apparent biphonation that may involve separate portions of the
vocal cords that are specialized for sonic and ultrasonic frequencies. (A)
Ultrasonic recording extending to 100 kHz recorded with a custom-built
ultrasonic condenser microphone. (B) Same sound showing only the `audible'
frequencies recorded on a separate channel with an Audio Technica model AT835b
microphone. A well-defined harmonic audible sound with a fundamental frequency
(f0) of between 3 and 5 kHz is superimposed on
deterministic chaos in both the sonic and ultrasonic ranges. The tonal and
chaotic components are presumably generated by different oscillators. Data are
from frog #2. 1 cmH2O=98 Pa.
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Fig. 6. Horizontal sections through the larynx of Amolops tormotus. (A)
Male larynx, through dorsal-third of vocal cords. (B) Male larynx through
mid-portion of vocal cords showing shape of vocal cords along most of their
length. Vocal cords consist of lateral and medial vocal ligaments. Elastic
fibers are dark purple. Elastin pads and adjacent epithelium extending into
laryngeal lumen from aditus are distortion artifacts of tissue processing and
normally line the adjacent wall of the laryngeal lumen. Note the highly
vascularized network of serous cells surrounding air channels in the posterior
laryngeal pouch. (C) The female larynx of A. tormotus is
approximately twice the size of the male larynx. In other frogs the male
larynx is larger than that of the female. arc, arytenoid cartilage; ce,
ciliated epithelium of pharynx; ctc, cricotracheal cartilage; dmi, laryngeal
dilator muscle, inferior branch; dms, laryngeal dilator muscle, superior
branch; ll, lateral vocal ligament; pmh, posterior medial process of hyoid;
mlca, medial vocal ligament, caudal portion; mlcr,
medial vocal ligament, cranial portion; spm, sphincter muscle; vn,
vascularized network filling caudal laryngeal pouch. Arrow represents
direction of expiratory airflow. Sections are 10 µm. (A,B) Gomori's
aldehyde-fuchsin stain for elastic fibers counterstained with Haematoxylin and
Eosin. (C) Masson's trichrome stain. Elastic fibers are unstained and appear
gray. Bar, 500 µm; applies to all sections.
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© The Company of Biologists Ltd 2006
