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First published online August 17, 2006
Journal of Experimental Biology 209, 3457-3468 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02386
`Binaural echo disparity' as a potential indicator of object orientation and cue for object recognition in echolocating nectar-feeding bats
Institut für Zoologie II, Universität Erlangen-Nürnberg, Staudtstrasse 5, 91058 Erlangen, Germany
* Author for correspondence (e-mail: mholderi{at}biologie.uni-erlangen.de)
Accepted 15 June 2006
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: echolocation, acoustic object recognition, bat-pollinated flower, impulse response
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Spatial vision, for example, is facilitated by binocular fixation of an
object. Besides the angle of convergence of the two eyeballs and the degree of
accommodation, the human central nervous system (CNS) utilizes differences
between both retinal images of an object, i.e. the binocular disparity, to
assess spatial information. Thereby, neurons of cortical area V1
systematically evaluate if structures lie before or behind the focal plane or
more specifically the binocular horopter (e.g.
DeAngelis, 2000
). Binocular
disparities are used for judging both the position (distance and direction)
and the three-dimensional structure of objects.
Echolocating bats derive a three-dimensional representation of their
immediate environment by emitting ultrasonic vocalisations and listening for
echoes generated by objects in their surroundings. Their CNS evaluates
acoustic information contained in these echoes to construct an acoustic image
of the world. This biological sonar allows bats to orient, avoid collisions in
flight and to find and acquire their food
(Griffin, 1958).
The two copies of each particular object's echo that reach the two eardrums
can differ considerably, and bats evaluate such differences by the mechanisms
of directional hearing to derive the position of objects. The CNS evaluates
interaural differences in intensity (IID) and in time of arrival (ITD) that
are indicative of the horizontal angle towards the echo-bearing object. By
adding pinnae to their ears bats and other mammals generate direction-specific
spectral filtering, which encodes the vertical bat-to-target angle
(Grinnell and Grinnell, 1965;
Fuzessery, 1996;
Wotton et al., 1995;
Firzlaff and Schuller, 2003;
Firzlaff and Schuller, 2004;
Aytekin et al., 2004).
Echolocating bats time the delay between call and echo as an indicator of
object distance (Griffin,
1958). In behavioural tests bats reached remarkable
acuity/resolution in range determination
(Simmons et al., 1995a;
Moss and Schnitzler,
1995).
A second important task of echolocation is object recognition, and bats
evaluate the echo's fine structure to extract information about the object
behind the echo. An echo arises whenever sound meets a discontinuity in the
density of the transmitting medium. For flying bats this is often a solid
object surrounded by air. Complex objects have a fine structure of several
small surfaces perpendicular to the angle of sound incidence. Each such
surface will generate a separate first-order reflection called a glint. The
time course of glints in the complex echo shows the range distribution of
reflectors in the complex object (Simmons
and Chen, 1989; Kuc,
1997). The overall strength of the reflections is an indicator of
object size [target strength (Urick,
1983; Simon et al.,
2006)], and the echo duration marks its depth
(von Helversen et al.,
2003).
There are several experiments showing that insectivorous bats can recognize
characteristics of possible prey objects by echolocation
(Griffin, 1958;
Simmons and Chen, 1989;
von der Emde and Schnitzler,
1990). However, relatively few experiments show that bats can
recognise totally motionless objects by echolocation, particularly when close
to clutter-generating background structures: Phyllostomus can
recognize and find the fruits of the Cucurbitaceae Gurania, which is
eaten by these bats, guided by their echolocation alone
(Kalko and Condon, 1998).
Carnivorous and insectivorous bat Megaderma lyra can detect its prey
even when it is motionless (Schmidt et
al., 2000). Glossophaga commissarisi finds the flowers of
the bat-pollinated vine Mucuna holtonii with the help of echo
orientation (von Helversen and von
Helversen, 1999) and recognizes even the degree of ripeness of the
bud (von Helversen and von Helversen,
2003). With artificial objects nectar-feeding bats were not only
able to discriminate between different types of artificial hollow forms, but
even generalized certain shapes independent of size, which might involve some
kind of three-dimensional shape perception by the bats
(von Helversen, 2004).
However, our understanding of how bats can achieve this is poor at the
theoretical level (but see Kuc,
1997; Kuc, 2001;
Müller and Kuc, 2000) as
well as at the neurophysiological level. Simmons and Chen discuss this problem
(Simmons and Chen, 1989).
Yet, to the best of our knowledge, there has been no systematic study of
whether the echoes heard by both ears of a bat can differ significantly, not
through direction-specific spectral filtering, but also because the object
itself sends two different echoes in the directions of the two ears. Such
differences can arise when the object's three-dimensional gestalt presents two
different range profiles towards each ear, but were often considered
negligible because the ear distance seemed too small to receive noticeable
gestalt-specific disparities (e.g. Pollak,
1988; Pollak and Casseday,
1989). Simmons et al. mention such object-specific disparities on
a temporal scale and their potential relevance for target discrimination
(Simmons et al., 1995b).
It is thus of special interest to know if such gestalt-specific binaural
disparities exist and whether they are useful for recognition of objects. Kuc
designed a (large) biomimetic robot (Kuc,
1997), which could focus objects with two mobile ears and thereby
align itself to the objects by evaluating direction-dependent binaural
differences. Additionally, this system could differentiate the front and back
of a coin based on the glint pattern generated by the coin's relief patterns.
The authors also reported that their left and right microphones picked up
different echoes, but did not evaluate such differences for object
recognition, nor did they attempt to reconstruct object features from binaural
echo disparities. Their biomimetic robot had a mouth-to-ear distance about 10
times wider than a bat.
In the following we report measurements of the disparity of the echo signals of a metal cube and a bat-pollinated flower, which are picked up by two microphones when the spatial arrangement of loudspeaker and microphones resembles the relative position of mouth or nostrils and the ears in an echolocating bat. We analyse whether gestalt-specific binaural disparities acoustically encode information about the objects' orientation, and also about its size and shape. Finally, we discuss whether such binaural disparities might actually be accessible to the bat with its limited acoustic information processing powers.
For this study we chose flowers of a bat-pollinated plant, because
nectar-feeding bats depend on these flowers' echoes to localize them, to guide
their in-flight approach and to find the right approach angle to reach the
nectar chamber. Visits at a flower last for fractions of a second and often
involve hovering (von Helversen and
Winter, 2003). Because chiropterophilous plants gain fitness when
they attract bats more efficiently, some of them have evolved flowers with
echoacoustic features that are conspicuous to their echolocating pollinators
(von Helversen and von Helversen,
1999; von Helversen and von
Helversen, 2003; von Helversen
et al., 2003). Here we discuss the binaural echoic features of a
bat-pollinated flower on structural and evolutionary grounds.
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Materials and methods |
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The microphones were placed on top of either side of the loudspeaker. The distance between the centres of loudspeaker and microphones was 18 mm and 14 mm between the centres of the microphones. Microphones and loudspeaker were pointing in the same direction and all three membranes were in the same plane (Fig. 1).
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Measurement set-up
Target objects were presented on a thin holder mounted in the centre of a
small turntable. The `artificial bat head' was placed at a distance of 20 cm
at the same height (20 cm) as the target object and pointed in its direction
(Fig. 1). The turntable allowed
the objects to be ensonified from all directions in one plane. The front view
of the objects was adjusted to 0°. This arrangement resulted in a total
angle between the centre of each microphone, the centre of the target and the
midpoint of the loudspeaker membrane of 5°9'. The corresponding
horizontal angle was 2°1'.
Echo measurements
Due to its small size, the loudspeaker could not produce a single broadband
click of sufficient sound pressure. Therefore, we employed the so-called
Maximum Length Sequence (MLS) method. A MLS
is a deterministic sequence of impulses of variable length showing a perfectly
narrow autocorrelation function. We used a custom-built sound generator (USSY,
Technische Hochschule Darmstadt, Germany) to continuously replay a MLS of
16383 samples. At a rate of 500 kHz, each repetition lasted for 32.766 ms. The
microphone signals were digitised with 12-bit resolution and recorded either
on a custom-made hard disc recorder or a custom-made A/D DSP-Card in a desktop
computer (both: Institut für Technische Elektronik, Universität
Erlangen, Germany). Replay and recording were sample-synchronous.
From MLS recordings the echo's impulse response function was derived by a
Fast Hadamard Transformation (FHT). The
target's echo impulse response was then separated in the time domain, and its
frequency response (spectrum) was calculated (FFT; window size 1024 samples;
rectangular window). To correct for the frequency characteristic of
loudspeaker and microphones, we recorded the perpendicular reflections from a
large metal plate (plate diameter: 
40 cm). The object's actual echo
spectrum, without influence of loudspeaker and microphone, is the complex
difference between the spectra of the metal plate and the object. The distance
of 20 cm between object and `artificial bat head' was chosen because then the
spectrum indicates the echo amplitude at a reference distance of 10 cm related
to the incident amplitude measured at the place of the object. This complies
with the definition of `target strength' as given (e.g. by
Møhl, 1988) and
therefore the calibrated spectra can be called `spectral target strength'.
Calculations were performed with the programs MONKEY FOREST (Audio &
Acoustics Consulting, Aachen, Germany) and MATLAB 6.5 (The MathWorks, Inc.,
Natick, MA, USA).
We turned the turntable to obtain the objects' echoes from different directions in a horizontal plane in steps of up to 1°. For each direction, signals picked up by the two microphones were recorded successively. Echoes from a range of ±60° around frontal orientation were recorded in 2° steps. For the flower, angles between ±5° were measured at 1° resolution in addition, to get a higher resolution of the small-scale acoustic echo pattern in this angular range (see below).
Objects
Echo measurements were obtained for two objects: first, a metal cube with a
side length of 10 mm and second, a bat-pollinated flower collected in a Costa
Rican lowland rainforest and measured immediately, i.e. under normal turgor.
We chose flowers of Vriesea gladioliflora, a bromeliad growing in the
canopy of tropical rainforests in Central and South America. The monaural
acoustic properties of these flowers have been described
(von Helversen et al.,
2003).
Reconstruction of object features from binaural disparities in glint delays
Complex echoes consist of several basic echoes, so-called glints,
originating from different reflective substructures in the complex object. The
temporal delay pattern of glints reflects the spatial patterns of reflective
substructures in the object (Simmons and
Chen, 1989). We analysed the binaural differences in glint delays
to calculate the position of the glint-bearing structure in a horizontal
plane. As a measure of the glint delays we used the times of ascending zero
crossings in the target's IRF. Only zero crossings above a minimum steepness
were included. In order to localize the underlying substructure the glint
needed to be present in the IRFs of both ears. From each pair of corresponding
glint delays the substructure's position was triangulated based on the
microphone distance of 14 mm and for a speed of sound of 340 m
s-1.
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Fig. 3 shows interaural intensity disparities (IIDs) at different frequencies in the IRF spectra for angles between the bat and the front of the cube from -10° to +10° in 2° steps. IIDs in frontal direction (0°) were at 0 dB, and IID was positively correlated with bat to cube front angle at all frequencies. IID increased faster with angle at high frequencies than at low frequencies. The -2° to +2° difference was approx. 1 dB at 50 kHz and increased to about 7 dB at 130 kHz. The angular region over which IID increased monotonically was larger at low frequencies (>20° at 50 kHz and 70 kHz) than at high frequencies (10° at 130 kHz). Equivalent IID vs angle functions were found for all intermediate frequencies from 40 kHz to 140 kHz.
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Binaural spectral disparities of a bat-pollinated flower's echoes
Fig. 5 presents spectra of
the same IRFs as a function of angle between bat and flower axis. Spectra span
40-145 kHz i.e. the complete spectral bandwidth of the echolocation signals of
their main pollinators [Phyllostomidae; Glossophaginae
(von Helversen and Winter,
2003)]. At the frontal angle of 0°, spectra picked up by both
ears were very similar up to 90 kHz (Fig.
5A). The differences at higher frequencies presumably result from
the fact that the flowers of V. gladioliflora are not completely
bilateral symmetric.
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Fig. 6 shows spectral IIDs for some frequencies between 40 and 90 kHz. At each frequency IID was 0 dB at about 0° with an increase to higher and a decrease to lower angles. At 40 kHz a monotonically increasing slope is present from -4° to +5° that spans about 20 dB in total. Thus, the bat to flower axis angle is encoded in the spectral IID at 40 kHz over a range of 9°. As in the cube (compare with Fig. 3), the steepness of the corresponding slope increased with frequency, and the angular range of monotonic rise shortened. At 90 kHz the IID increases monotonically only between -2° to 2° but covers 17 dB. This basic pattern was found also at all intermediate frequencies between 40 and 90 kHz, but not above 100 kHz.
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Likewise, Fig. 7Bi,ii show the same IRFs for the left and right ear, respectively, separately, but for a reduced frontal range of -5° to +5°. The delay range was reduced to better reveal temporal detail of the two corollar ridge glints. The crossing of the glint delays and their merging at the frontal direction are clearly visible. The obvious difference between both ears is that the angle of crossing lies at -1° at the right ear and at +1° at the left ear.
To test whether these binaural differences in the IRF encode spatial information characterising the flower, we segregated the IRFs into separate glints. Fig. 8 exemplifies this with the two IRFs recorded from a lateral angle of 5°. The binaural IRF difference is remarkable. Both IRFs show two separate glints, corresponding to the left and right side of the corollar ridge respectively. The circles and drop lines in Fig. 8 indicate the zero crossing delays that serve as a measure of glint delay. The additional x-axis shows the distances between bat head and the glint-producing structures corresponding to these delays.
Fig. 9 depicts the changes in IRF over bat to flower axis angles ranging from -5° to +5° in 1° steps. IRFs in Fig. 9A,C are the same as in Fig. 8, but over a somewhat longer part of the IRF and also including glints from structures inside the concave corolla. Symbols mark corresponding ascending zero crossings as a measure of corresponding glint delays. Binaural glint delay difference ranged between -2.3 µs and +2.4 µs for the first glint and was -2.9 µs at -5° and +3.0 µs at -5° for the second glint. Fig. 9B shows a schematic top view horizontal section through a V. gladioliflora corolla at the corresponding turning angles. Superimposed are the locations of the objects behind the glints marked in Fig. 9A,C. The angular pattern of glint localisations reveals that spatial information about the flower is indeed present in the binaural IRF disparity: the first glint is always correctly localised at the point of the corolla that is closest to the bat. It is particularly interesting, how the first glint gradually moves from one side to the other along the front of the corolla when the flower is turned through the frontal orientation of 0°. The second glint from the more distant side of the corolla is absent because it merges with the first glint, in all but the largest angles, i.e. -5° and +5°. At these angles the second glint source is localized, according to expectations, at the opposite side of the corollar ridge. This means that binaural glint delay differences do indeed encode first the distance between the two sides of the corolla, i.e. its diameter, and second also the angle at which the corolla is tilted.
Further glints from structures inside the corolla are much smaller in amplitude than the ridge glints. Such glints are, with very few exceptions, localized within the corolla. They might originate from the staminal column, but are very likely the product of several superimposed glints of different floral structures and/or separate reflection pathways, which might explain why some are localized outside the schematic corolla.
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Binaural disparities encoding object position
The sonar head and the experimental setup were designed to exclude any
direction-specific binaural echo disparities: the object was right in front of
the microphones such that no intra-aural differences in arrival time (ITDs)
arose. Additionally, microphones had no pinna-like structures and show a broad
directionality, such that directional spectral filtering can be assumed to be
weak. Because the microphones were identical and arranged symmetrically with
respect to the target, such weak filtering would be identical in both ears.
Thus, any echo disparity between the ears cannot be due to direction-specific
frequency filtering and is purely gestalt specific.
The actual approach flight of a bat is similar to our setup in several respects. Once the bat has initiated its approach, it will direct its head towards the flower, thereby avoiding any direction-specific ITDs. Bats do have pinnae though, and direction-specific frequency filtering will occur. Yet, the two pinnae can be regarded as identical mirror images of each other and the frequency filtering will thus ideally be identical for an object right in front of the bat. Even though the echoes picked up by the two ears will contain spectral directional information, binaural differences would therefore only be gestalt specific.
Binaural disparities encoding angle between bat and cube front
Many animals can evaluate excitation differences at the two ears to
localise a sound source [some examples: humans
(Blauert, 1997); barn owl
(Konishi, 2003), grasshopper
(Michelsen and Rohrseitz,
1995)]. Figs 2 and
5 reveal that the power spectra
of the objects' echoes show a characteristic distribution of maxima and minima
that shifts as a function of the angle between bat and object axis. This
results in a direction-specific spectral intra-aural intensity difference
(IID) pattern (Figs 3 and
6). For the cube, spectral IID
increased over a range of more than ±10° at the lowest frequency
(40-50 kHz) that is present in the nectar-feeding bat's calls
(Fig. 3). Likewise, such
information is still available at the highest frequencies of 130 kHz, but over
a restricted range of angles. Assuming that bats have a threshold of 1 dB for
spectral IIDs, they would be able to discriminate 4° at 60 kHz. Yet, above
120 kHz an angular change of 4° resulted in 5dB IID, which translates into
0.8° mean angular resolution for cube orientation. 0 dB spectral IID
reliably indicates an angle of 0° at all frequencies. Thus, binaural
spectral disparities are an accurate measure of the orientation of the metal
cube that is available over a large range of angles.
Binaural spectral disparities encoding angle between bat and flower axis
In the chiropterophilous flower, the binaural difference in overall echo
amplitude (Fig. 4) and the
spectral IID (Fig. 6) both
convey information that might be used by a bat to judge the orientation of the
floral corolla. Yet, such information is not equally available in both.
Overall IID would reliably encode flower orientation only between -1° and
+1° (Fig. 4). This is too
narrow to guide the approach flight except perhaps at close range, during the
very last phase of the approach. The angular availability of orientation
information is much wider in spectral IID: at 40 kHz IID increases
monotonically by 20 dB from -4° and +5°. At higher frequencies
(
100 kHz) the angular range decreases, but the rate at which IID changes
with flower orientation increases (Fig.
5). Assuming a spectral IID threshold of 1 dB, this would allow
the bat to judge the orientation of the flower with a resolution well below
1° from the distance of 20 cm.
Binaural temporal disparities encoding flower orientation and dimensions
A complex object's echo impulse response function (IRF) shows several
glints with delays corresponding to the distances of structures in the object
generating them. So the glint pattern is an indicator of the depth profile of
the complex object behind the echo
(Simmons and Chen, 1989), and
the relevance of binaural disparities in glint patterns for object recognition
has been discussed (Simmons et al.,
1995b). We report that IRFs picked up by the two ears can indeed
differ considerably in a bat-pollinated flower
(Fig. 8). Binaural delay
disparity of the first glint was in the range of ±2.3° between
-5° and +5°. Through triangulation this can reveal the actual
horizontal position of the closest part of the flower's corolla
(Fig. 9B, first symbol from the
left in each plot). At absolute angles above 5° the two glints from both
sides of the corolla were separated in time in the IRFs of both ears (Figs
7 and
9).
Fig. 7A shows that the two
glints are available in the IRFs from about -32° to +26° in V.
gladioliflora. The glint separation time rises from 9 µs at +5° to
58 µs at +26° and from 8 µs at -4° to 80 µs at -32° at
the left ear. Even with monaural hearing, double glint separation time would
thus be a useful source of information about floral orientation available over
a wide range of angles. However, this is only a relative measure of flower
orientation, which also depends on the opening width of the flower. In
contrast, the binaural disparity in the two glints' delays allows direct
independent triangulation of the two respective horizontal points of
reflection at the left and right part of the corolla
(Fig. 9B at -5° and
+5°). The distance between these two points can provide information about
the width of the opening of the corolla and the angle between the points can
be a reliable indicator of the flower orientation. A triangulation based on
the glint patterns in Fig. 7A
confirms that the orientation of the flower can be inferred from the relative
position of the two glints with high accuracy (measured
angle=1.08xactual angle). Thus, glint structure in the IRF potentially
is a valuable indicator of flower orientation and size that is present over a
wide range of different approach directions.
Taken together, our results suggest that the orientation of V. gladioliflora flowers is available from spectral IIDs at angles from -4° to +4° where the two glints are merged in the IRFs. Both corollar glints are separated in the IRFs at adjacent angles from -5° down to -34° and from +5° up to +26°. Over this angular range, double glint separation time is a relative measure of flower orientation, and triangulation based on binaural glint delay disparities would provide an excellent direct measure of flower orientation but also of the diameter of the corolla.
Binaural disparities during target approach
In Fig. 4 an amplitude peak
was found at horizontal angles of -1° and +1° respectively, while the
horizontal angle between each ear, the flower and the centre of sound emission
was 2°1'. Thus the highest amplitude was recorded under reflection
conditions, i.e. when the angle of inclination and the angle of reflection at
the flower where both at the same value of 1°. The same angular separation
of -1° and +1°, respectively, was found in the position of the
x-shaped crossing of two corollar glint delays in the IRF patterns of the two
ears (Fig. 7Bi,Bii). One ear
receives the same IRF pattern as the other ear that is shifted by 2°. This
shows that the observed binaural disparities can be explained by the different
locations of the ears in the complex echo field generated by the flower.
However, these angular relations are only valid for the particular distance between bat and flower during our measurement, which was 20 cm. At larger distances the angle mouth-flower-ear will decrease and all binaural disparities will become accordingly smaller. In the laboratory, nectar-feeding bats initiate their approach sequence at a distance of about 1 m (M. W. Holderied and A. Volz, manuscript in preparation). During the course of this approach the bat will start with comparably small binaural disparities and poor information about floral angle. As it gets closer the angular resolution will improve. The angular resolution achievable with spectral IIDs from a distance of 20 cm was well below 1°. It is unlikely that sub-degree angular resolution of flower orientation has any adaptive value per se, primarily because the nectar chamber is accessible from a larger range of different approach angles. The observed strong angular patterning of the spatial echo field will, however, be advantageous at greater distances when the IIDs get correspondingly smaller. On geometric grounds a resolution of 0.5° at 20 cm corresponds to 1° at 40 cm and 2.5° at 1 m. This way, a reasonable representation of floral orientation at large distances would be achieved, which will ease flight trajectory planning from a distance.
Floral shapes and echo traits
Some bat-pollinated plants have reportedly evolved acoustic floral traits
that meet the informational needs of their echolocating pollinators
(von Helversen et al., 2003;
von Helversen and von Helversen,
1999; von Helversen and von
Helversen, 2003). As a result of this plant-pollinator
co-evolution on an echoacoustic scale, it seems reasonable to hypothesise that
a spatial echo pattern of the flower has evolved to make object-specific
information available through binaural disparities that would be observable
with a bat's head as receiver.
Overall and spectral IIDs, which according to our results do carry object
orientation information, depend on how narrow the angular echo pattern is (see
Fig. 4). A narrow frontal peak
brings forth good angular resolution. All bat-pollinated bell-shaped flowers
investigated so far indeed show an angular echo pattern with such a peak in
the frontal direction (von Helversen et
al., 2003). A likely explanation for the origin of this peaked
angular pattern is that at frontal directions the full corollar ridge is
ensonified perpendicularly, thus contributing to one composite high-amplitude
glint. This frontal glint is of highest amplitude, because in any other
orientation only two lateral parts of the ridge are perpendicular to the
direction of sound incidence and thus reflect glints (see
Fig. 9). To some degree glints
from inside the concave corolla itself might further sharpen this angular
peak.
The second echo feature that carries object-specific information is the
temporal pattern of the two glints of the corollar ridge, which results in the
x-shaped glint crossing pattern in the angular IRF plot
(Fig. 7). All bell-shaped
chiropterophilous flowers show such a characteristic x-shaped glint structure
(von Helversen et al., 2003).
So both cues that bear binaural directional information - overall and spectral
IIDs as well as corollar glint delays - originate from the stiff and prominent
torus-like frontal ridge of the corolla (see inset in
Fig. 6)
(von Helversen et al., 2003;
Dobat, 1985). The noticeable
rigid ridge of all larger bell-shaped chiropterophilous flowers may function
as a mechanical grasping support for the visiting bats that sometimes land on
the corolla rather than hover in front of it. Our results indicate that this
ridge might additionally serve as indicator of object orientation. The fact
that this ridge often has a rounded cross-section cannot be explained by
mechanical constraints alone. Yet, a rounded cross-section presents a small
surface area reflecting sound perpendicularly over a wide range of different
angles of sound incidence. The presence of the prominent x-shaped double glint
delay pattern in Fig. 7 over
such a wide angle is thus a direct consequence of this rounded cross-section.
Non-rounded cross-sections would not generate glints of high amplitude over an
equivalently broad range of angles (e.g. artificial hollow hemispheres)
(von Helversen, 2004).
The representation of two separate glints originating from opposite regions of the corollar ridge is present for a wide range of relative bat to flower axis positions. But these parts of the corolla do not always have to be in a horizontal plane. On geometric grounds, those two opposite regions of the corolla will be present in the IRF with separate glints that are in the plane defined by the bat-to-flower axis and the floral axis. During lateral approach, glints will originate from the left and right parts of the corolla. In contrast, a bat approaching from below the floral axis will receive glints from the top and bottom parts of the corolla. In case bats prefer two lateral glints over two on top of each other, they might approach from a lateral position relative to the floral axis.
Extraction of object-specific information from echoes by bats
So far we have only shown that object-specific information is available
through binaural disparities in different aspects of the IRFs. However,
extracting such information holds several severe challenges for the hearing
system of a bat.
The importance of the object-specific spectral composition of echoes has
been a subject of discussion for a long time (e.g.
Simmons and Chen, 1989) and
its relevance has been shown in choice experiments
(Mogdans and Schnitzler, 1990;
Schmidt, 1988;
Schmidt, 1992). The first
problem in extracting object-specific information arises because the spectrum
of the echo reaching the eardrum will not only show peaks and notches that are
object-specific, but also others that are generated by the directional
filtering of the head and pinna. Phyllostomus discolor, a bat species
in the same family (Phyllostomidae) as most nectar-feeding bats, shows
direction-specific spectral IIDs of up to 42 dB
(Firzlaff and Schuller, 2003).
Behavioural experiments with an insectivorous bat confirmed ambiguities
introduced by direction-specific spectral notches
(Simmons et al., 2002). In
order to extract object-specific information, those spectral features that are
part of the directional filtering would need to be identified and actively
disregarded. Matsuo et al. present a model mechanism that might be involved in
the separation of object-specific and direction-specific information
(Matsuo et al., 2001). During
flower approach this task is eased in several ways: highest direction-specific
spectral IIDs only occur for lateral angles of sound incidence. During
approach the flower is in front all the time and its echoes will thus not
experience such pronounced filtering. Additionally, from experience the bat
might know the characteristics of the highly important spectral filter for
frontal directions quite well, such that all additional notches can be
identified as object-specific. Finally and most importantly, echoes from a
flower right in front will experience exactly the same directional filtering
at both ears, given both pinnae are exact mirror images. As a result any
binaural disparities will not represent directional but only object-specific
information. This makes binaural disparities particularly useful for the
extraction of object-specific information.
The second problem regards the object-specific information contained in the
delays between the first two glints in the IRFs. Bats do not have direct
access to the IRF of an echo as such, with its temporal resolution in the
µs range. In contrast, typical approach echolocation calls of
nectar-feeding bats last approximately 500 µs to 2000 µs. Clutter
interference experiments showed that the integration time for echo separation
is about 350 µs (Simmons et al.,
1998), which is more than the maximum duration of the IRF of
V. gladioliflora echoes. It has been a subject of discussion whether
and by which auditory computational processes bats can use the interference
patterns of the overlapping glint echoes of a complex target to derive the
object's range profile with a temporal acuity and resolution comparable to the
IRFs (Simmons, 1989;
Saillant et al., 1993;
Peremans and Hallam, 1998).
Behavioural experiments with double-glint phantom targets support the idea
that E. fuscus can indeed separately perceive the range of two echoes
that overlap by as little as 2-3 µs
(Simmons et al., 1998). In
V. gladioliflora monaural double-glint separation times ranged from 8
µs at -4° to 80 µs at -32° (Figs
7 and
8). With 3 µs resolution,
bats would be able to resolve the orientation of the corolla with 1.2°
resolution if they based their perception on the double glint separation time
experienced by one ear only. The experiments supporting the 2-3 µs
resolution has, however, been performed with double glints. Additional glints,
like in the flower's echoes, might complicate deduction of temporal
detail.
A connected but independent task for the bat would be to assess the
binaural difference in the onset times of the first glint with sufficient
accuracy to determine the direction to the closest part of the corolla.
Binaural first glint delay differences ranged between -3 and 3 µs at angles
between -5° and +5°. The relevant performance measure for this task is
the temporal resolution of directional hearing based on ITDs. In this respect
non-echolocating mammals such as humans achieve remarkable lateralization
resolution with broadband noise or click signals of only a few microseconds
(2-50 µs) (see Blauert,
1997). Assuming an interaural delay resolution of even 2 µs,
directional hearing by triangulation with our bat head would allow resolution
of deviations from the frontal direction of just 3.3°. In humans,
localization resolution increases with increasing bandwidth and indeed
fruit-eating and flower-visiting bats generally use echolocation calls of
remarkably broad bandwidth. The actual ability of nectar-feeding bats to
resolve ITDs by echolocation, however, still needs to be quantified.
Influence of microphone-loudspeaker arrangement on echoes
Our measurements showed that the position of the microphone (ear) relative
to the sound source (mouth) had a substantial influence on the echo's
intensity and spectral composition. For larger angular separations this had
already been shown for the echoes of the bat-pollinated vine Mucuna
holtonii (von Helversen and von
Helversen, 1999). Many recent bat-like echo measurement setups
(sonar heads) had larger mouth-to-ear distances than real bats [e.g. 6 cm
(Müller and Kuc, 2000);
5.6 cm (Siemers et al., 2001);
8 cm (Walker et al., 1998)].
The reason is that ultrasound loudspeakers are often too large in diameter to
be able to place the microphone in a natural mouth-to-ear position. One way to
overcome this size-dependent bias would be to move the oversized sonar head to
a correspondingly greater distance in the echo field, such that the angular
relations between mouth, target and ears are the same as in a bat. Yet, this
assumes that the complex echo spreads perfectly radially. At distances in the
range of the dimensions of the echo-bearing structure the prerequisite of
radial spreading might not be met. In this case close-range disparities in the
spatial echo field can only be measured correctly with a bat-sized sonar head.
If echo measurements aim to quantify the acoustic information available to the
bat at close range, the distances between loudspeaker and microphones and
between the sonar head and the target need to be adapted to natural
conditions. The fact that the two ears of a bat experience binaural
object-specific disparities has implications for behavioural experiments on
object recognition through replay of phantom targets.
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