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First published online December 14, 2005
Journal of Experimental Biology 209, 152-157 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.01975
The absence of spatial echo suppression in the echolocating bats Megaderma lyra and Phyllostomus discolor
Department Biologie II, Universität München, Großhadernerstrasse 2, 82152 Planegg-Martinsried, Germany
* Author for correspondence (e-mail: lutzw{at}lmu.de)
Accepted 9 November 2005
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In a two-alternative, forced choice paradigm, a study was made of the extent to which the echolocating bats Megaderma lyra and Phyllostomus discolor spontaneously suppress the spatial information of a second reflection of their sonar emission. The delay between the first and the second reflection ranged between 0 and 12.8 ms.
In general, M. lyra (five individuals) and P. discolor (two individuals) did not suppress the spatial information of the second reflection of their sonar emission, whatever the delay. Only one M. lyra showed significant suppression for delays between 0.8 and 3.2 ms. However, this suppression could not be confirmed in an exact repetition of the experiment.
The current data indicate that although bats may be able to suppress the spatial information of a second reflection, this is not their default mode of auditory processing. The reason for this exceptional absence of spatial echo suppression may lie in the shorter time constants of cochlear processing in the ultrasonic frequency range and the strong influence of cognitive components associated with the `precedence effect'.
Key words: echolocation, precedence effect, sound localization, bat, Megaderma lyra, Phyllostomus discolor
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). Accurate sound localization is possible for most animals because the spatial information cues from the direct and shortest path from sound source to listener carries greater perceptual weight than the spatial information in the echoes. Only the directional information of the sound that reaches the ear first dominates the perceived position of a sound source. The spatial information of the echoes is suppressed.
A common behavioural paradigm used to examine the precedence effect is to simulate a direct sound source (`lead') and a single echo (`lag') with two loudspeakers in an anechoic chamber. The speakers are placed in the left and right hemi field equidistant to the listener, each presenting identical sounds offset in time such that the lagging sound is delayed relative to the leading sound. This `lead-lag paradigm' allows for the investigation of the mechanisms used by listeners to resolve spatial information for sounds in reverberant environments.
The precedence effect is characterized by three distinct but related
phenomena. (1) When the delay between leading and lagging click is zero or
close to zero (within 1 ms), the listener will hear one fused auditory event
between the two loudspeakers (`summing localization';
Litovsky et al., 1999;
Blauert, 1997). (2) For
lead-lag delays between about 1 and 5 ms, the sound and its echo remain
perceptually fused, but the perceived position of this fused sound image is
dominated by the position of the lead. This is referred to as `localization
dominance'. (3) With a further delay, both lead and lag become audible as
separate sound events. This delay is referred to as `echo threshold'.
Echo-threshold values can vary tremendously (2-50 ms). The delay range depends
on both signal duration and complexity. The lead-lag delays are much shorter
for brief stimuli such as clicks (around 6 ms) than for longer duration
stimuli such as noise and ongoing complex stimuli such as running speech.
Until now, behavioural evidence for precedence has been found in several
animals at lead-lag delays that are similar to those reported in humans (see
Discussion).
Echolocating bats are confronted with a very complex echo-acoustic situation. They always have to deal with lots of echoes, many of them being echoes of their own echolocation calls. At first sight, the ability of the bats to orient through the auditory analysis of echoes of their vocal emissions is in contrast to the precedence effect. It is just the spatial information in echoes that enables the localization of objects in the dark. Bats rely heavily on the evaluation of these echoes for orientation and hunting.
Each echo includes information about the properties of the environment, but this information can be misleading: an ensonified target object reflects an echolocation call not only directly back to the bat's ears, but also in other directions. There, the echo can be reflected by another object, e.g. a water surface or a wall. This second reflection constitutes a higher-order echo, which includes misleading spatial information of the target object. The perceptual suppression of this misleading information would facilitate the echo-acoustic localization of the target object.
However, the higher-order echoes provide information about other objects in the vicinity of the target object. Thus, it may be beneficial for a bat not to suppress the perception of the higher-order echo because the latter provides information about the distance between the target object and the other object.
The current experiments were designed to investigate whether, and to what extent, the echolocating bats Megaderma lyra and Phyllostomus discolor exhibit localization dominance behaviour consistent with the precedence effect in the processing of reflections of their echolocation calls.
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) and
based on prey-generated rustling noises
(Neuweiler, 2000). Its
echolocation calls are short, multi-harmonic frequency sweeps. An exemplary
echolocation call is shown in Fig.
1.
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Phyllostomus discolor
Phyllostomus discolor Wagner 1843, the lesser spear-nosed bat, is
a new world tropical bat. It feeds on fruit and small insects. Its
echolocation calls are also short, multi-harmonic frequency sweeps but
slightly longer than M. lyra calls and with a stronger dominance of
lower harmonics. An exemplary echolocation call is shown in
Fig. 1.
Two adult P. discolor (both female) took part in the training. The animals were housed together in a box (80 cmx40 cmx50 cm) with free access to water. In this box, they were only fed on days without training sessions, i.e. only for 2 days after a 5-day training period. They were fed with mealworms during the training breaks. During the training period, they were fed with banana pulp for reward.
Experimental design
First and second reflection of echolocation calls were simulated in a
lead-lag paradigm. In this paradigm, two ultrasonic speakers were placed at
the same distance and angle in each hemi field to the bats' starting position.
The bats were trained in a two-alternative, forced choice experiment. In an
initial training period, only one of the two speakers emitted a reflection of
the bats' ultrasonic emission to train the bats to move to the speaker
emitting the reflection to get a food reward (`lead-only trials'). The
presenting speaker alternated randomly. When the bats were able to solve this
task with a stable performance of >85% correct choices over 5-6 training
days, test trials were randomly interspersed between these lead-only trials
with a probability of 25%, such that two of eight trials were test trials. In
these test trials, both speakers emitted a reflection but the reflection from
one speaker had an additional delay of 0 ms and 0.1 ms up to 12.8 ms in
doublings (`lead-lag trials'). The lead-lag delays were presented randomly
across lead-lag trials. As in the lead-only trials, the speaker emitting the
leading reflection in the lead-lag trials varied randomly. In these trials the
bats were free to choose any speaker to receive a food reward, i.e. the
spontaneous performance of the bats was assessed. Thirty lead-lag trials were
collected for each of the nine lead-lag delays, therefore each bat completed
270 lead-lag trials interspersed between 810 lead-only trials. The performance
was calculated as decisions for the side of the leading reflection in percent
as a function of the lead-lag delay.
In the lead-lag trials, the following behaviour would be expected: the bats
were trained to move to the side of the speaker where they perceived a
reflection of their emission. If the bats experience summing localization (one
fused auditory event between the two speakers) with a lead-lag delay of 0 ms,
they could not show any side preference, thus the performance level would be
around 50%. With increasing lead-lag delay, the bats would be expected to
prefer the side of the leading speaker. If the bats perceive localization
dominance, meaning the leading reflection dominates the perceptive position of
the auditory event, they would significantly (performance >75% for 30
trials; Miller, 1996) move to
the side of the leading reflection. Reaching the echo threshold, the bats
would perceive two separate sounds in distinct positions and would again
choose one of the sides randomly.
Experimental layout
Megaderma lyra
The experiments, conducted with flying M. lyra, took place in a
weakly illuminated, echo-attenuated chamber (3.5 mx2.2 mx2.2 m).
As in former studies (Weissenbacher and
Wiegrebe, 2003; Wiegrebe and
Schmidt, 1996) the layout consisted of a starting perch on one
side of the room and two ultrasonic speakers, one in the left and one in the
right hemi field. Each speaker was associated with a feeding dish. The
distance from the loudspeakers to the bat's head was 1.2 m. The angle between
the speakers and the bat's head was 45°. The experimental layout is shown
in Fig. 2A,B.
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Phyllostomus discolor
The experiments, conducted with crawling P. discolor, took place
in a horizontal Y-shaped maze in an echo-attenuated chamber. A starting perch
was located at the bottom of the leg of the Y, and a feeder was mounted at the
end of each upper leg. The angle between the legs was 45°. An ultrasonic
speaker (Matsushita EAS 10 TH 800D) was placed in a distance of 15 cm in front
of each upper leg (see Fig.
2C). Further, a 6.35 mm microphone (B&K 4135) was located in
the middle of the maze to pick up the bats' sonar emissions. The stimulation
apparatus was identical to that used with M. lyra.
The experimenter was seated outside the chamber, controlling the experimental procedure via a computer interface and an infrared camera.
These slightly different experimental layouts were used to suit the animals' exploration behaviour under laboratory conditions: whereas P. discolor prefers to crawl to a food source, M. lyra always prefers to fly.
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Data for the two P. discolor individuals are shown in Fig. 4. Again, both individuals do not significantly prefer the first reflection over the second.
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The general absence of localization dominance in the current data is quite
different from the findings in all other species tested so far. Summing
localization similar to humans has been found in cats
(Populin and Yin, 1998).
Tested on clicks in a lead-lag paradigm, cats showed localization dominance
for delays between 0.5 and 2 ms (Cranford,
1982). Fur seals show the precedence effect in a similar time
range as humans (for clicks from around 1 ms up to 6 ms; for tonal pulses up
to 11 ms; Babushkina and Poliakov,
2001). Other studies found similar values for rats
(Kelly, 1974) and crickets
(Wyttenbach and Hoy, 1993). It
appears that these animals experience localization dominance at nearly the
same delays as human listeners do. Also birds such as budgerigars and owls
reveal localization dominance in a manner similar to humans (Dent and Dooling,
2004,
2003a,
2003b;
Keller and Takahashi, 1996a;
Keller and Takahashi,
1996b).
Why do most of the echolocating bats tested in the current experiments show no localization dominance when confronted with two reflections of their own echolocation calls?
Hartung and Trahiotis
(2001) showed that the
integration times of the peripheral auditory filters may play an important
role in echo suppression. They showed that the ringing of auditory filters in
response to the lead-lag stimulation generates changes in the central auditory
representation of interaural time differences, which can quantitatively
predict a large variety of psychophysical findings related to the precedence
effect.
In the frequency region which dominates the precedence effect in human
listeners (around 750 Hz; Tollin and
Henning, 1999), the ringing times of auditory filters are in the
range of several milliseconds. This is in good agreement with the time range
of localization dominance. For ultrasonic hearing bats, the ringing times are
very short because the auditory filters are very broad. Weissenbacher et al.
(2002) and Wiegrebe and
Schmidt (1996) showed that the
ringing time of M. lyra auditory filters does not exceed about 200
µs. Thus, if auditory-filter ringing were the main physiological basis of
localization dominance, it cannot be expected that localization dominance is
seen in bats while they are echolocating. Note that both the sonar emissions
and consequently the reflections do not provide significant acoustic energy
below about 40 kHz (cf. Fig.
1).
A possible neural correlate of spatial echo suppression has been described
in the ascending auditory pathway of cats and rabbits. In these studies,
neurons were found, the responses of which to a lag stimulus, depending on the
delay between lead and lag, were substantially reduced compared to a single
stimulus (Fitzpatrick et al.,
1999; Litovsky et al.,
1999; Tollin et al.,
2004).
A case for the possible neural correlate of a precedence effect in bats
comes from physiological studies in two microchiropteran bat species
(Burger and Pollak, 2001;
Pollak et al., 2002). They
found a persistent inhibition in the dorsal nucleus of the lateral lemniscus
(DNLL) of the Mexican free-tailed bat (Tadarida brasilensis mexicana)
and the mustached bat (Pteronotus parnellii). This inhibition is
evoked by short duration stimuli to the ipsilateral (inhibitory) ear and can
persist up to 60 ms after stimulus offset. Thus, delayed stimulation of the
contralateral (excitatory) ear is suppressed in the DNLL response.
Portfors and Wenstrup
(1999) studied delay-sensitive
inferior-colliculus neurons in P. parnellii. Apart from a relatively
large population that showed a facilitatory response to stimulus combinations
resembling a pulse-echo pair, the authors also described a small population of
neurons with an inhibited response to pulse-echo pairs. It is conceivable that
this population may be involved in the auditory processing of higher-order
echoes.
High-level, cognitive processes might also influence the precedence effect
(Blauert et al., 1989;
Clifton et al., 1994;
Mccall et al., 1998;
Freyman et al., 1991;
Damaschke et al., 2005). These
studies suggest that echo processing may depend on the listeners' prior
listening experience and the resulting expectations about the sound-source
position and the room acoustics. Also Rakerd and Hartmann
(1985) proposed that
localization of sound is a dynamic, interactive process that has inputs from
higher cognitive levels.
In our experimental paradigm, the bats were confronted with reflections of their own ultrasonic emissions. Bats orient through the auditory analysis of reflections of their own vocal emission. Conceivably, bats need all the information contained in these reflections both for an auditory assessment of space and for localizing objects in this space. For this reason they do not suppress the spatial information contained in these reflections. It cannot be excluded that bats are able suppress the spatial information of their own ultrasonic emission (as also shown in Fig. 3C); but it may be dependent on the acoustic situation the bats are confronted with. They may be able to recruit localization dominance when it is beneficial for them. Such a facultative adoption of localization dominance may underlie the different patterns of results obtained from M. lyra individual 3 (cf. Fig. 3C). While in the first acquisition, the animal chose to adopt localization dominance, in the replication of the experiment, about six months later, it chose to switch its strategy.
It is possible that this recruitment of localization dominance is also stimulus-dependent. Some bats live in reverberant caves where they congregate in large colonies. There is a lot of social interaction between the animals, accompanied by a rich repertoire of communication calls. Thus, bats not only have to cope with echoes of their own vocal emissions but also with echoes of communication calls from conspecifics. In this acoustic situation, localization dominance would facilitate the perception of the origin of communication signals from other bats and would ease social interaction. So, while the suppressing of spatial information of higher-order echoes of their own echolocation calls may cause a loss of information, a suppression of misleading spatial information in echoes of social calls might be quite beneficial for a bat. Experiments are in progress to investigate passive-acoustic localization dominance in bats similar to that observed in humans and animals.
Also hunting strategies could influence how echolocating bats deal with multiple, spatially divergent reflections. Both bat species tested here are non aerial hawkers. Instead they are very good at detecting and identifying edible prey in acoustically complex environments with many, close reflections arising from nearby objects. It is conceivable that bats hunting for flying insects in an open space may recruit a different auditory strategy to deal with multiple, spatially divergent reflections of their ultrasonic emissions.
In summary, the current data show that the two bat species studied here did not reveal spontaneous localization dominance when they were trained to lateralize reflections of their ultrasonic sonar emissions. This finding can be explained based on the different peripheral auditory processing in the far ultrasonic frequency range and a possible strong influence of cognitive processes on the precedence effect. A singular contrary data set suggests that echolocating bats may be able to recruit localization dominance facultatively in an echo-acoustic situation in which localization dominance is beneficial for them.
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