The mechanical basis of Drosophila audition
Institute of Zoology, University of Zurich, Winterthurerstraße
190, CH-8057 Zurich, Switzerland
1 Present address: School of Biological Sciences, University of Bristol,
Woodland Road, Bristol BS8 1UG, UK
* e-mail: m.gopfert{at}bristol.ac.uk
Accepted 8 February 2002
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Summary |
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Key words: acoustic communication, auditory tuning, biomechanics, bioacoustics, chordotonal organ, courtship, dynamic range compression, ear, insect, antenna, hearing, song, Johnston's organ, mechanosensation, non-linearity, Drosophila melanogaster
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Introduction |
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Since the discovery of acoustic signalling in fruit flies
(Shorey, 1962), the generation
of these signals has been extensively studied at the behavioural,
physiological, genetic and molecular levels (for reviews, see
Bennet-Clark, 1971
;
Ewing, 1983
;
Greenspan, 1997
;
Greenspan and Ferveur, 2000
;
Hall, 1994
,
1998
;
Yamamoto et al., 1997
).
Surprisingly little, however, is known about the sensory aspects of this
acoustic communication system. A series of early studies, mostly dating from
the 1960s and 1970s, established that the antennae of Drosophila to
serve as `love song' detectors (Ewing,
1983
); as in most flies, the antennae of Drosophila are
characteristically composed of three segments including (from proximal to
distal) the scape, the pedicel and the funiculus. The latter carries an
elongated and branched lateral process, the antennal arista
(Fig. 1). Ablation of either
the funiculus or only the arista results in a severely reduced receptivity,
indicating that the antennal arista and possibly the funiculus are involved in
sound perception, presumably by constituting the sound receiver proper
(Manning, 1967
;
von Schilcher, 1976
). This
idea was supported by the reduced sexual receptivity of antennal mutants (e.g.
aristaless) (Burnet et al.,
1971
) and by the stroboscopic observation of antennal vibrations
induced by intense sound (Manning,
1967
; Bennet-Clark,
1971
). Electrophysiological recordings, in turn, finally
demonstrated that Johnston's organ, a mechanosensory chordotonal organ in the
pedicel of the antenna, serves as the auditory sensory organ
(Ewing, 1978
). Taken together,
these early studies documented the auditory function of Drosophila
antennae. More detailed information about the underlying anatomical,
biomechanical and neurophysiological mechanisms, however, remained elusive,
presumably reflecting the technical limitations arising from the small size of
the flies' antennal hearing organs.
|
Recently, audition in Drosophila melanogaster has attracted
renewed interest. Because of its amenability to genetic and molecular
research, the species is currently used as a model organism to examine the
fundamental processes underlying mechano- and auditory transduction
(Kernan et al., 1994;
Kernan and Zuker, 1995
; Eberl
et al., 1997
,
2000
). Research in this
context has made considerable progress and led to the identification of
several auditory-relevant genes (Kernan et
al., 1994
; Eberl et al.,
1997
,
2000
;
Eddison et al., 2000
;
Walker et al., 2000
;
Chung et al., 2001
). Now,
complementary information about the biomechanical events underlying
Drosophila audition is needed to evaluate comprehensively the
consequences of mutant defects on the auditory performance of the fly
(Eberl et al., 2000
;
Göpfert and Robert,
2001a
).
The present account focuses on the first steps in audition in Drosophila melanogaster, i.e. on the conversion of acoustic energy to mechanical vibrations and on the transmission of vibration to the sensory organ. Using computer-controlled laser Doppler vibrometry in conjunction with anatomical investigations and acoustic near-field measurement techniques, the structural and mechanical bases of Drosophila audition are examined. The main aim of this study is to establish the fundamental mechanical characteristics of the antennal hearing organs of wild-type flies and, thus, to provide a framework for comparative analyses in auditory mutants. To investigate the antenna's suitability as a detector of courtship song, the mechanical measurements are supplemented by acoustic analysis of these songs.
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Materials and methods |
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Mechanical measurements
Antennal vibrations were analyzed in response to acoustic excitation with
pseudo-random noise signals (frequency range 100-1500 Hz). The acoustic
signals were generated by a Stanford Research System Network analyzer
(Stanford Research Systems, model SR 780), passed through a step attenuator
(custom-built), amplified (dB-Technologies, model PL 500) and fed to a
loudspeaker (Uher, model UL-1302, 13 cm in diameter, fitted with a baffle 25
cm in diameter).
Sound-induced mechanical vibrations were examined by means of input/output
analyses based on simultaneous measurements of the vibration velocity
vib of the antennal structures and the particle velocity
air in the surrounding air
(Fig. 2A).
vib
was assessed using a microscanning laser Doppler vibrometer (Polytec, model
PSV 200) with an OFV-055 scanning head. To facilitate vibration measurements
coaxial to the direction of sound propagation, a linear arrangement of the
laser, the animal and the loudspeaker was chosen, with the laser pointing to
the centre of the loudspeaker and the experimental animal being positioned
between the loudspeaker and the laser vibrometer
(Fig. 2A). The distances
between the loudspeaker and the animal and between the animal and the laser
vibrometer were 5 and 21 cm, respectively, the latter corresponding to the
focal length of the laser optics. The laser beam (approximately 5 µm spot
diameter) was positioned with a spatial accuracy of approximately 1 µm
using an OFV-3001-S vibrometer beam controller, and the spot position was
monitored online via the coaxial video system of the scanning head.
It is noteworthy that both the sensitivity of the vibrometry apparatus and the
high accuracy of beam positioning obviated the use of reflecting beads on any
of the measured structures.
To monitor air, a miniature Emkay NR 3158 pressure gradient
microphone (distributed by Knowles Electronics Inc., Itasca, Illinois, USA)
was used in combination with an integrating amplifier (modified after
Bennet-Clark, 1984
). The
dimensions of the NR 3158 microphone are 5.6 mmx4.0 mmx2.2 mm, the
latter corresponding to the spacing between the microphone's ports. The
microphone shows a symmetrical figure-of-eight pattern of directivity.
Sensitivity is maximal when the microphone's diaphragm faces the incident
sound and drops by 42 dB (at a frequency of 500 Hz) when turned through
90°. Turning the microphone through 180° so that its back surface
faced the incident sound does not affect sensitivity (change in sensitivity
less than ±0.5 dB at 500 Hz) and results in the expected 180° phase
shift in the microphone's response.
The voltage output of this microphone was calibrated against the output of
a precision pressure microphone (Bruel & Kjaer, type 4138) under far-field
conditions and, thus, could be directly converted to the corresponding
particle velocity. Far-field calibration against the pressure microphone also
confirmed the output of the pressure gradient microphone to be flat within
±0.6 dB at frequencies between 100 and 1500 Hz. During the vibration
measurements, the pressure gradient microphone was positioned next to the
antenna (distance 0.5 cm) with its diaphragm oriented perpendicular to the
direction of sound propagation (Fig.
2A) so that its response was maximal. Control measurements of
sound-induced antennal vibrations in the presence and absence of the
microphone confirmed that the microphone did not affect the sound field at the
position of the antenna. The sound field has been described by Göpfert et
al. (1999).
To analyse the data, the laser and microphone signals were digitized at
12.5 kHz using an Analogic 16 Fast A/D board. To produce frequency spectra,
groups of 3-5 windows, each 120 ms in length, were collected, subjected to the
Fast Fourier transform using a rectangular window, and subsequently averaged.
Frequency spectra were estimated with a resolution of 6.25 Hz. To measure
mechanical responses, the laser signal was normalized to the microphone signal
by computing a transfer function, calculated as the cross-power spectrum
between the laser and microphone signals divided by the autopower spectrum of
the latter. Magnitude information was subsequently converted to the
corresponding vib/
air value. Data reliability
was assessed by computing coherence functions. Resonance parameters (i.e. the
resonance frequency f0, the quality factor Q and the dimensionless
mechanical sensitivity
vib/
air at f0)
were determined by means of a least-squares fit according to a simple harmonic
oscillator model using a software package in Microsoft Excel 7.0
(Frank et al., 1999
). By
fitting the function to the complex data, both the magnitude and the phase
information were taken into account. Consistently, the model produced a
near-perfect fit to the data (Fig.
2C).
Courtship song recordings
Courtship songs were recorded using conventional methods
(Bennet-Clark, 1984). In brief,
couples of previously isolated males and females were introduced into a small
Perspex tube (10 mm diameter) containing the pressure gradient microphone at
its centre. As soon as the male started to sing, its song was recorded. The
signals were stored on DAT and subsequently resampled at a rate of 10 kHz for
offline analysis. The frequency composition of the songs was evaluated on the
basis of 40 ms time traces centred on the onset of single song pulses. Per
animal, 20-30 such time-traces were averaged and subsequently converted to the
frequency domain using the software Canary (rectangular time window, 0 %
overlap, 4.4 Hz frequency resolution).
Anatomy
The histological methods used to examine the auditory anatomy of flies have
been described (Robert and Willi,
2000). The animals were cooled to 4°C prior to decapitation.
The heads were subsequently fixed in 3 % glutaraldehyde and embedded in
Spurr's medium. Serial sections, 5 µm in thickness, were conventionally
stained with Methylene Blue and examined under a light microscope (Axiophot;
Zeiss). For documentation, the sections were digitized using an on-chip
integration digital camera (ProgRes; Karton Electronics).
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Results |
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The pedicel of the antenna is almost filled by scolopidia, the
multi-cellular mechanoreceptor units of Johnston's organ. These scolopidia are
amphinematic, comprising a distal tube that extends into a distal thread (for
classification and terminology, see
Moulins, 1976; McIver, 1985).
As seen in cross sections (Fig.
3B,C), the funicular nerve separates Johnston's organ into two
distinct groups of scolopidia, a medial and a posterior group. Both groups
project to the pedicel/funiculus joint. The tubes of the scolopidia are
embedded in the hypodermis which, in the joint region, is detached from the
cuticle (Fig. 3A-C). Only the
distal threads pass through the hypodermis. Reflecting the different
orientations of the two groups of scolopidia, the threads of the posterior
series are nearly straight, whereas those of the medial series are strongly
bent. As a result, all the receptors attach with their threads to the lateral
sides of the joint and, hence, perpendicular to the hook
(Fig. 3C). `V'-shaped rims of
specialized cuticle, identified by their strong staining with Methylene Blue,
serve as attachment sites. These rims, which are part of the funiculus and are
located on either side of the funicular hook, are flexibly suspended by thin
membranes formed by the adjacent cuticle of the pedicel
(Fig. 3C).
The arista connects to the funiculus via a ring of specialized
cuticle that stains strongly with Methylene Blue
(Fig. 3D). Two more rings occur
further distally, dividing the arista in two basal parts and an elongated,
distal part. All these connections lack membranous regions of cuticle as found
at the pedicel/funiculus joint and, in addition, lack mechanoreceptors (see
also Foelix et al., 1989).
Arista tip response
The mechanical response characteristics of the antennal structures to a
quantified and reproducible pseudo-random noise stimulus were examined
(Fig. 4A). The intensity
characteristics of this stimulus, measured as air, were
frequency-dependent. At frequencies between 100 and 1000 Hz,
air decreased by approximately 3 dB octave-1. In
absolute terms, the amplitude of
air was ±0.1 mm
s-1 at 100 Hz and ±0.03 mm s-1 at 1000 Hz
[corresponding to 63 dB and 53 dB root mean square (rms), re.
5x10-8 m s-1, respectively]. These intensities
were sufficient to obtain highly coherent vibration measurements
(Fig. 4B).
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Arista tip responses measured at the most distal part of the arista were
remarkably uniform among animals. Examination of four male and four female
aristae revealed a low inter-individual variability and no apparent sex
differences. Consistently, a single resonance occurred in the range of
frequencies examined. This resonance manifest itself as a peak in the
magnitude response (Fig. 4C)
accompanied by a shift in the phase response
(Fig. 4D). As expected for the
velocity response of a second-order system, the phase between the
vib and
air characteristically shifted from +90
to -90° at a frequency around resonance. Only at f0
were
vib and
air in phase. Individual values of
f0 varied between 405 and 445 Hz (426±16 Hz; mean
±1 S.D.). The quality factor Q ranged between 1.1 and 1.3
(1.2±0.1). At f0, mechanical sensitivity
vib/
air reached its maximum, ranging between 1.1
and 1.5 (1.3±0.2) for the eight aristae examined. According to these
response characteristics, the arista tips of male and female antennae are
moderately tuned to frequencies around 425 Hz, with the maximum vibration
velocity slightly exceeding the particle velocity in the surrounding air.
Vibrational patterns
To be relevant for audition, sound-induced vibrations of the arista tip
need to be transmitted to the funiculus and then to the receptors in the
pedicel. Vibration measurements at different positions on the arista
(Fig. 5A, left panel) revealed
that the resonance observed at the tip extends along the entire length of the
arista. Apart from a continuous approximately 10-fold drop in the response
magnitude from the tip to the base, the shapes of the magnitude responses
(Fig. 5B, left panel) and the
phase responses (Fig. 5C, left
panel) were almost identical for all measurement points. Hence, the three
elements that make up the arista (Fig.
3D) do not vibrate relative to each other; they are stiffly
coupled. The entire arista can be considered to move as a stiff rod when
stimulated acoustically.
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Comparative vibration measurements taken at the base of the arista and on the lateral edge of the funiculus demonstrate that these two antennal parts are also stiffly connected. The resonance observed on the arista could be detected at the site of the arista/funiculus connection (Fig. 5B, left panel, lowest curve) and on the lateral edge of the funiculus (Fig. 5, middle panel, red circles and curves). At both measurement sites, the responses exhibited almost identical magnitude and phase characteristics, demonstrating that the arista does not vibrate relative to its insertion on the funiculus. Consequently, the arista and the funiculus constitute a single mechanical entity.
The resonance observed on the lateral edge of the funiculus did not extend
to its central region. Here, vibrations were hardly detectable and coherent
measurements could not be obtained (data not shown). When the laser beam was
positioned on the opposite, medial edge of the funiculus, however, the
resonance built up again (Fig.
5, middle panels, blue circles and curves). Response magnitudes
along opposite funicular edges were similar, with a maximum sensitivity
vib/
air of around 0.15
(Fig. 5B, middle panel). The
response phases, however, were shifted by 180° within the entire range of
frequencies examined (Fig. 5C, middle panel). This means that the two opposite edges of the funiculus move in
opposite directions. The 180° phase shift, together with the equal
response magnitudes obtained along the two funicular edges and the absence of
vibrations in the central funicular region, is an unambiguous indication that
the funiculus rotates about its longitudinal axis in the presence of
sound.
The rotation of the funiculus does not extend to the pedicel. Consistently, vibration magnitudes obtained from different locations on the pedicel were much lower than those observed on the funicular edges, and these minute vibrations were not coherent with the stimulus (Fig. 5, right panels, green circles and curves). Comparably low-amplitude vibrations were also detected on the compound eyes (Fig. 5, right panels, orange circle and curves), confirming that the pedicel of the antenna does not undergo vibration relative to the head. Consequently, only the funiculus and the arista vibrate in response to sound.
Intensity characteristics
The analysis applied describes the antenna's mechanical response
completely, provided that the system is linear. The responses of both
funiculus and arista, however, exhibit a considerable degree of non-linearity
that results in an intensity-dependent tuning. To evaluate this non-linear
effect, the response of individual arista tips was measured at different
stimulus intensities. The intensity of the random-noise stimulus depicted in
Fig. 4A was varied in 3 dB
steps over a range of 36 dB (Fig.
6A). The corresponding absolute amplitudes of air
ranged between ±0.03 and ±1.8 mm s-1 at 100 Hz (53-88
dB re. 5x10-8 m s-1) and between ±0.007 and
±0.5 mm s-1 at 1000 Hz (41-77 dB re. 5x10-8
m s-1).
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With increasing stimulus intensity, the peak in the magnitude response and
the associated zero crossing in the phase response shifted continuously
towards higher frequencies (Fig.
6B,C). As shown by measurements on two male and two female
aristae, this effect occurred reliably in animals of both sexes
(Fig. 7A). Within the range of
intensities examined, f0 shifted from approximately 360 to
620 Hz with an average increase of 7.3 Hz dB-1 (linear regressions:
slopes 7.1-7.6 Hz dB-1, r2-values 0.98-1;
P<0.001; Spearman's rank correlation, one-tailed significance)
(Fig. 7A). This shift was
accompanied by a slight decrease in sensitivity
vib/
air at f0 (linear
regressions: slopes -0.004 to -0.007 dB-1,
r2-values 0.3-0.7; P<0.01; two-tailed
significance). Tuning sharpness Q, however, remained unaffected
(r2-values <0.2, P>0.5) (data not
shown).
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Corresponding non-linear effects were observed when the arista tip
vibrations were measured in response to continuous pure tones of different
intensities (Fig. 7B).
Intensity/response functions obtained in this way exhibited a considerable
degree of non-linearity that became apparent when
vib/
air at the stimulus frequency was plotted
against the corresponding
air
(Fig. 7B). Here, the data
points were not parallel to the intensity axis, as would be the case for a
linear system but, instead, exhibited a sensitivity maximum at specific
intensities. In accordance with the intensity-dependent resonance observed in
the responses to random noise (Fig.
6), the sensitivity varied with the frequency of the pure tone.
The higher the tone frequency, the higher the intensity at which the maximum
occurred (Fig. 7B), reflecting
the increase in f0
(Fig. 7A).
Courtship songs
Courtship songs of Drosophila melanogaster consist of two
components, sine songs and pulsed songs
(Ewing, 1983). Pulsed songs
are produced more regularly, are higher in intensity and constitute the song
component that has been demonstrated to increase female receptivity
(Ewing, 1983
;
Crossley et al., 1995
).
Accordingly, the analysis was focused on this song component. In the present
recordings, the songs always consisted of trains of evenly spaced sound pulses
(Fig. 8A), each pulse
consisting of one dominant, highamplitude oscillation cycle
(Fig. 8B). The duration of this
cycle, measured on the basis of at least 20 averaged pulses per individual
(N=5), varied between 4.8 and 6 ms. In agreement, the frequency
spectra of these pulses revealed maxima at the corresponding frequencies, i.e.
between 160 and 210 Hz (Fig.
8C). The high-frequency roll-off in the spectra was steep, with
amplitude decreasing by approximately 15 dB octave-1.
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Discussion |
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Coupling mechanisms
Our measurements demonstrate that the distal parts of the
Drosophila antenna serve as the sound receiver. The funiculus and the
arista are stiffly coupled and constitute a single mechanical entity. Only
this entity undergoes significant and coherent vibration when stimulated
acoustically; it must be directly driven by sound, converting acoustic energy
into mechanical vibrations.
The mechanical entity formed by the funiculus and the arista exhibits an
unconventional rotatory pattern of vibration. This rotation is a consequence
of the asymmetric antennal structure: because sound acts on both sides of the
rotational axis, only a structural asymmetry can prevent equilibrium between
clockwise and counterclockwise torque. In Drosophila, the arista
breaks antennal symmetry. Inserted radial to the rotational axis of the
funiculus, the arista constitutes a moment arm, enlarges the effective surface
area and, thus, determines the torque exerted by sound. Given this vibrational
pattern, it is not surprising that arista ablation reduces acoustically evoked
behavioural responses by approximately the same amount as removal of the
entire arista/funiculus complex (Manning,
1967).
Being surrounded by the pedicel, the proximal region of the funiculus is
not accessible to direct mechanical examination. Our anatomical investigation,
however, clearly illustrates that this proximal region focuses mechanical
vibrations onto the auditory receptors and counterbalances the asymmetry
introduced by the arista. The funicular stalk is oriented coaxial to the
rotational axis. Hence, it will join the rotation of the free, distal region
of the funiculus, thereby mediating the downstream transmission of rotation.
The funicular hook, however, is oriented radial to the rotational axis; it
thus balances the asymmetry introduced by the arista. Like the arista, the
hook will undergo predominantly translatory movements during funicular
rotation. The direction of these movements will be tangential to the
rotational axis of the funiculus a pattern of movement that is
facilitated by articulating membranes at the pedicel/funiculus joint. The
hook's vibration will then maximally stretch and compress the auditory
receptors, which all attach perpendicular to the sides of the hook. Finally,
the two groups of receptors attaching to opposite sides of the hook will be
stimulated in an alternate manner, a scenario that is supported by the
harmonic structure of the compound electrical response of Johnston's organ
(Eberl et al., 2000). Taken
together, the anatomy of the funiculus and the pedicel/funiculus joint
guarantees receptor activation that compares with that of other insect
chordotonal organs (Keil,
1997
), despite the unusual rotational pattern of funicular
vibration.
Response characteristics
According to its mechanical response characteristics, the arista/funiculus
complex can be described as a moderately damped simple harmonic oscillator.
Remarkably, this oscillator exhibits a considerable degree of non-linearity
that does not simply reflect overloading during intense stimulation, but
occurs within a wide range of intensities. As shown here,
f0 increases continuously with intensity, whereas tuning
sharpness and sensitivity at f0 are not affected or only
weakly affected. Taken together, such intensity characteristics demonstrate
the presence of a non-linear stiffness, a type of non-linearity that differs
from the non-linear damping known from the response of vertebrate auditory
systems (Dallos, 1996) and
mosquito antennal hearing organs
(Göpfert and Robert,
2001b
). The non-linear damping observed in vertebrates and
mosquitoes involves negative damping introduced by an additional power source,
i.e. the active motility of the auditory receptors
(Dallos, 1996
). This negative
damping opposes the ear's passive damping in an intensity-dependent way.
Non-linear stiffness as observed in Drosophila may also be introduced
actively. Alternatively, it may result from a passive stiffening of the
auditory receptors or the cuticular components that make up the
pedicel/funiculus joint. Further investigations, especially in auditory
mutants (Eberl et al., 2000
),
promise to trace the elements in the chain of hearing, from biomechanical
substrates to cellular components, that bring about auditory non-linearity in
the fly and possibly active auditory mechanics.
Antennal mechanics and courtship song detection
The intensity-dependent change in f0 is a rather
surprising characteristic for an auditory filter. It results in an
intensity-dependent mismatch between antennal tuning and songs. The acoustic
analysis of male `love songs' revealed a dominant frequency at approximately
200 Hz. The antenna will be tuned to this frequency only as long as intensity
is low [air=17-29 dB (re. 5x10-8
ms-1) according to a linear extrapolation,
Fig. 7A]. During courtship,
however, the female's antennae and the male's vibrating wing are usually only
5-2.5 mm apart, resulting in a particle velocity of around 80-95 dB
(Bennet-Clark, 1971
) and,
according to the data presented here, in antennal resonance between 550 and
800 Hz. Acoustic communication in Drosophila thus operates with a
frequency mismatch of up to two octaves. Several mechanisms, however, ensure
signal detectability. First, acoustic communication in the fly relies on the
temporal pattern of the song rather than on frequency cues
(Ewing, 1983
). Hence, there is
no a priori requirement for frequency-selective hearing. Instead, the
rather broad antennal tuning comes with the benefit of high temporal
resolution. Second, the broad tuning, together with the short communication
distance, apparently ensures that the songs induce antennal vibrations that
are sufficiently large to be detected even at frequencies below antennal
resonance. Third, intensity-dependent tuning may well be useful, especially in
the context of close-range acoustic communication. In effect, in the acoustic
near-field, the particle velocity of the sound radiated by the
Drosophila wing drops steeply by 18 dB per doubling distance
(Bennet-Clark, 1971
). Hence,
the flies have to cope not only with considerable sound intensities but also
with considerable distance-dependent intensity fluctuations. By improving the
antenna's sensitivity at low song intensities and reducing it at high
intensities, the non-linear stiffness provides dynamic range compression. This
mechanical compression may account for the saturation of and the decline in
the neural and behavioural responses at high stimulus intensities
(von Schilcher, 1976
;
Crossley et al., 1995
;
Kernan et al., 1994
;
Eberl et al., 2000
).
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Acknowledgments |
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