Joumal of
Comparative
Physiology , - .
J Comp Physiol A (1989) 165:383-393
Sensory,
.and
~.~,,
Behavioral
,~,o,~,
9 Springer-Verlag 1989
Accuracy of target ranging in echolocating bats:
acoustic information processing
Cynthia F. Moss * and Hans-Ulrich Schnitzler
Universit~it Ttibingen, Tierphysiologie, D-7400 Tiibingen, Federal Republic of Germany
Accepted March 4, 1989
Summary. 1. Echolocating bats use the time delay
between emitted sounds and returning echoes to
determine the distance to an object. This study examined the accuracy of target ranging by bats and
the effect of echo bandwidth on the bat's performance in a ranging task.
2. Six big brown bats (Eptesicus fuscus) were
trained in a yes-no procedure to discriminate between two phantom targets, one simulating a stationary target that reflected echoes at a fixed delay
and another simulating a jittering target that reflected echoes undergoing small step-changes in delay.
3. Eptesicusfuscus emits a frequency modulated
sonar sound whose first harmonic sweeps from approximately 55 to 25 kHz in about 2 ms. Sound
energy is also present in the second and third harmonics, contributing to a broadband signal in
which each frequency in the sound can provide
a time marker for its arrival at the bat's ears. We
estimated range jitter discrimination in bats under
conditions in which the echo information available
to the bat was manipulated. Baseline performance
with unfiltered echoes was compared to that with
filtered echoes (low-pass filtered at 55 kHz and at
40 kHz; high-pass filtered at 40 kHz).
4. The results indicate that the low-frequency
portion of the first harmonic (25-40 kHz) is sufficient for the bat to discriminate echo delay changes
of 0.4 microseconds. This echo delay discrimination corresponds to a distance discrimination of
less than 0.07 mm.
Abbreviation: A B B A (design), see Methods
* Present address : Harvard University, Department of Psychology, Cambridge, Massachusetts 02138, USA
Introduction
An echolocating bat emits ultrasonic sounds and
perceives its surroundings by listening to the returning echoes of these sounds (Griffin 1958). The
features of the echoes carry various kinds of information about a target, such as range, size, and
shape (Simmons and Vernon 1971 ; Simmons 1973 ;
Schnitzler and Henson 1980). Target range is a
particularly important parameter for tracking insect prey, and this information is conveyed by the
time delay between a sonar emission and echo reception (Simmons 1973). It has been postulated
that bats use the frequency modulated (FM) components of their echolocation sounds for target
ranging (Griffin 1958; Strother 1961; McCue
1966; Schnitzler 1968, 1970, 1973; Simmons 1973).
Several receiver models have been proposed to
describe the process of echo ranging in bats (see
for example, Altes 1976, 1980, 1984; Hackbarth
1984; Menne 1988; Simmons and Stein 1980).
Here, we will briefly consider three such models,
a semi-coherent ideal receiver, a coherent ideal receiver, and a matched filter bank receiver.
Both a coherent and a semi-coherent ideal receiver cross-correlate the transmitted signal with
the returning echo by passing the echo through
a receiver matched to the emitted signal. The crosscorrelation function is a time-compressed representation of the sound and is used to estimate echo
arrival time. A semi-coherent receiver cannot make
use of the fine structure of the cross-correlation
function (i.e. the instantaneous frequency and a
constant, time-invariant phase shift of echoes) but
instead uses the envelope of the function for echo
arrival-time estimation (Woodward 1964). A co-
384
herent ideal receiver operates like a semi-coherent
receiver with the added capability of using the fine
structure of the cross-correlation function to estimate echo arrival time (Woodward 1964). Echo
ranging performance of both semi-coherent and
coherent receivers depends on the bandwidth of
the signal (centralized rms bandwidth for the semicoherent receiver and rms bandwidth for the coherent receiver) and the signal-to-noise ratio (see
Burdic 1968; Simmons 1968; Schnitzler and Henson 1980; Schnitzler et al. 1985; Menne and Hackbarth 1986). Performance of a filter-bank receiver
(Hackbarth 1984; Menne 1988) also depends on
the signal bandwidth and the signal-to-noise ratio,
but differs from the classical ideal receivers in that
it does not make optimal use of all information
in the sonar sound for estimating target range. This
receiver operates by passing the signal through a
series of overlapping band-pass filters, followed by
envelope detectors; the filter bandwidth is set to
minimize timing error for a given frequency sweep
rate, and the receiver averages the output across
channels to estimate echo arrival time.
Simmons (1973) presents behavioral data
which suggest that target range discrimination by
a bat is related to the bandwidth of its echolocation
signal. He trained bats in a two-alternative forcedchoice procedure to select the closer of two targets,
and found that a species using comparatively narrowband sounds showed poorer range discrimination than a species using broadband sounds. For
example, the C F - F M bat Rhinolophus ferrurnequinum successfully discriminated a range difference between two targets as small as 25 mm. This
bat emits an 83 kHz CF sound followed by a shallow F M sweep from approximately 83 to 70 kHz.
By contrast, the F M bat Eptesicus fuscus emits a
three harmonic sound whose fundamental sweeps
from approximately 55 to 25 kHz. This species successfully discriminated a 13 mm range difference
between two targets.
Simmons (1973) also reports a close correspondence between the range discrimination performance of each species tested and the envelope of
the autocorrelation function of that species' echolocation sound. (For a stationary target that reflects well at all frequencies, the autocorrelation
function is a good approximation to the cross-correlation function of the emitted sound and returning echo.) He uses this finding to suggest a hypothesis that the bat operates as a semi-coherent ideal
receiver which uses some neurophysiological
equivalent of cross-correlation processing. Simmons argues that the width of the envelope of the
autocorrelation function is broader for a narrow-
C.F. Moss and H.-U. Schnitzler: Target ranging accuracy in bats
band sound than it is for a broadband sound, and
the width of the function determines the extent
to which a bat experiences ambiguity in a ranging
task: Indeed, Eptesicus was able to discriminate
a smaller range difference between two targets than
Rhinolophus. The difference in range discrimination performance between the two species cannot,
however, be used to confirm that bats use optimal
filtering to estimate echo arrival time. The performance of an ideal receiver depends on the echo
signal-to-noise ratio (Burdic 1968), and in Simmons's experiment, it can be inferred from the
structure of the echolocation sounds that performance for Rhinolophus and Eptesicus was measured at different signal-to-noise ratios (see
Schnitzler and Henson 1980).
In an experiment on ranging accuracy by echolocating bats, Simmons (1979) trained Eptesicus to
discriminate between two phantom targets, one
simulating a stationary target that reflected echoes
at a fixed delay and another simulating a jittering
target that reflected echoes undergoing small step
changes in delay. The bats successfully discriminated jitter of echo delay as small as 0.5 gs, suggesting that Eptesicus may be able to discriminate the
distance to an object within a fraction of a millimeter. He also reports a parallel between the bat's
performance in an echo jitter discrimination task
and the fine structure (half-wave rectified) of the
autocorrelation function of the bat's sonar sound.
The fine structure of the autocorrelation function
of Eptesicus' echolocation sound shows a narrow
central peak, flanked by side peaks separated by
30 gs intervals (the average period of the F M
sweep). If the delay of the returning echo is jittered
by 30 gs on alternating emissions, a bat that perceives the equivalent of the fine structure of the
autocorrelation function would encounter ambiguity, confusing the central peak and the side peak.
Indeed, Simmons reports an increase in the bat's
errors for discriminating 30 ~ts jitter compared to
smaller and larger values. He offers this finding
as evidence that the bat perceives the fine structure
of the cross-correlation function and that this function describes the bat's perceptual image of a target
(Simmons 1987). These data do not, however, confirm that the bat operates as an ideal receiver, since
the signal-to-noise ratio under which performance
was measured is unknown. Furthermore, Simmons
simulated the phantom targets in the jitter experiment with an analog delay line. The analog delay
line may have introduced an acoustic artifact
which could have aided the bats in the discrimination task and perhaps also contributed to the rise
in errors at 30 gs jitter.
C.F. Moss and H.-U. Schnitzler: Target ranging accuracy in bats
T h e b e h a v i o r a l e x p e r i m e n t s d e s c r i b e d a b o v e ind i c a t e t h a t the a c c u r a c y o f t a r g e t r a n g i n g is
r e m a r k a b l y h i g h ( S i m m o n s 1979) a n d s u g g e s t t h a t
e c h o l o c a t i o n s i g n a l b a n d w i d t h m a y p l a y a role i n
e s t i m a t i n g e c h o a r r i v a l t i m e ( S i m m o n s 1973). T h e
d a t a h a v e i m p o r t a n t i m p l i c a t i o n s f o r a s s e s s i n g diff e r e n t r e c e i v e r m o d e l s o f e c h o l o c a t i o n a n d elucid a t i n g the process of acoustic i m a g i n g by bats.
B o t h o f these f i n d i n g s , h o w e v e r , r e q u i r e f u r t h e r
i n v e s t i g a t i o n : T h e a n a l o g d e l a y line u s e d to m e a sure r a n g i n g a c c u r a c y m a y h a v e i n t r o d u c e d d e l a y related spectral changes, a n d the c o m p a r i s o n of
t w o d i f f e r e n t species a t d i f f e r e n t s i g n a l - t o - n o i s e ratios leaves o p e n t h e q u e s t i o n o f w h a t effect e c h o
b a n d w i d t h h a s o n t a r g e t r a n g i n g b y a single species
a t the s a m e s i g n a l - t o - n o i s e r a t i o .
T h e p u r p o s e o f this s t u d y w a s to a d d r e s s the
issues r a i s e d a b o v e . W e m e a s u r e d r a n g e a c c u r a c y
p e r f o r m a n c e i n Eptesicusfuscus w i t h a p a r a d i g m
s i m i l a r to t h a t u s e d b y S i m m o n s (1979), b u t instead used a digital delay system which permitted
target simulation without introducing delay-dep e n d e n t f r e q u e n c y artifacts. T o c a r e f u l l y m o n i t o r
response bias under different stimulus conditions,
we a l s o i m p l e m e n t e d a d i f f e r e n t p s y c h o p h y s i c a l
m e t h o d t h a n that used by S i m m o n s . A n d finally,
we c o m p a r e d the b a t ' s r a n g i n g p e r f o r m a n c e w i t h
n a t u r a l e c h o l o c a t i o n s o u n d s a n d w i t h filtered
s o u n d s to e v a l u a t e the effect o f s i g n a l b a n d w i d t h
o n e c h o a r r i v a l t i m e e s t i m a t i o n i n a single species.
Methods
Six big brown bats were trained in a yes-no procedure to discriminate between two phantom targets, one that simulated
a stationary target that reflected echoes at a fixed delay and
another that simulated a jittering target that reflected echoes
undergoing small step changes in delay (see Simmons 1979).
Bats were trained to stand at the base of a Y-shaped observing
platform and to emit sonar sounds into a 1/4" microphone
(windscreen covering the diaphragm; Brfiel & Kjaer, 4135) located at the end of the left arm of the platform, 15 cm from
the bat. Sounds picked up by the microphone were amplified
with a custom-built amplifier, digitized (12 bit ADC at a sampling rate of 250 kHz) and filtered (Medav GmbH FIRFIL
82/VO1, 27 coefficients). The digitized sounds could be delayed
by variable amounts in steps of 0.4 ps, and the delays were
set under computer control using software developed specifically for this system. Analog waveforms of the digitized sonar
sounds were played back to the bats through a custom-built
ultrasonic loudspeaker (designed by Lee Miller, Odense, Denmark; for calibration curve, see Fig. 1 C) located at a distance
of 1 m from the bat. The loudspeaker had a frequency response
similar to those used in Simmons's jitter experiment (Simmons,
personal communication; see Simmons etal. 1979). These
sounds simulated echoes returned by a phantom target positioned about mid-way between the bat and the loudspeaker
(see Fig. 1A).
The distance to the phantom target depended upon the
computer controlled delay of the playback sounds. On 50%
385
of all trials, the sounds emitted by the bat were played back
at a fixed delay of 3.67 ms, simulating a stationary target located 63.14cm from the bat on its observing platform. On
the remaining 50% of all trials, the sounds were played back
at 3.67 ms on alternating emissions; for every other sound the
bat emitted, a time value (ranging from 0.4 to 100 ps) was
subtracted from the base echo delay of 3.67 ms. In these trials,
the change in echo delay from one emission to the next simulated a target that jittered in space (see Fig. I B), and the second
echo (more distant reflecting element) from the jittering target
occurred at the same delay as that from the non-jitteringtarget.
The spatial relation between the jittering and non-jittering targets differed in this experiment from the arrangement used by
Simmons (1979). In his experiment, the jittering target was centered about the range (echo delay) of the non-jittering target.
The order of presentation of jitter and catch (no jitter)
trials followed a pseudorandom schedule (Gellerman 1933). The
subtracted time value was always the same on a given trial,
i.e. the size of the jitter was fixed. While performing in the
task, bats typically emitted sounds of about 1.8 ms in duration;
echoes produced by sounds reflecting off the loudspeaker returned after 5.814 ms, more than 2.1 ms following the sound
played back to the bat. The microphone at 15 cm produced
an echo 2.8 ms earlier than the phantom target echo. Thus,
there was rarely overlap between the simulated echoes played
through the loudspeaker and the echoes reflecting off the microphone or loudspeaker; there was also no overlap between successive sound emissions and simulated target echoes.
When presented with sounds that returned at an alternating
delay, bats learned to indicate a 'yes' (jitter present) response
by approaching the left arm of the platform, and when presented with sounds that returned at a fixed delay, they learned
to indicate a ' n o ' (jitter absent) response by approaching the
right arm of the platform. The magnitude of the jitter was
reduced from 100 ps to 0.4 gs in small steps (0.4-20 gs, the
step size increasing with the jitter value) to estimate the smallest
jitter that bats can reliably detect. Percentage hits ('yes' response, jitter present) and false alarms ('yes' response, jitter
absent) were calculated for individual animals at each jitter
magnitude tested.
Animals were tested with only one jitter value on any given
test day, following a modified descending method of limits.
Each bat was first tested with 100 gs jitter, and if the bat performed with a minimum of 85% hits and a maximum of 20%
false alarms on 3 consecutive test days, it was then tested on
2-3 consecutive days with 80 ps jitter. Bats were then tested
with smaller and smaller jitter values, over a minimum of 2
consecutive test days at each value. If the bat's performance
dropped below 75% hits on any test day, a larger jitter value
was presented on the subsequent test day to ensure that the
bat's behavior reflected a change in stimulus discriminability
and not in the bat's motivation to participate in the task. Data
collection at the smaller jitter value was then repeated on the
following day. It was necessary to implement this rule for handling poor performance for only two bats. Moreover, the occasional poor performance of these two bats occurred only for
jitter values greater than 40 gs, probably because the animals
became more skilled at the task over time, and the testing of
large jitter values preceded the testing of small values. In every
case, performance improved on the subsequent test day, and
the modified descending method of limits was continued. A
minimum of 35 trials were run for each bat for each jitter
value tested; however, most often between 50 and 100 trials
were run. Following each correct response, animals were rewarded with a small piece of mealwonn. Following each incorrect response, the animals received correction trials, which were
excluded from the data analysis.
386
C.F. Moss and H.-U. Schnitzler: Target ranging accuracy in bats
A
B
JITTER
~ " ~
speaker
( ~ phantom
JITTER CATCH
YES hit
target
EMISSION
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EMISSION
ECHO
false
alarm
NO miss correct
reject
=31,
L
sy
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TIME
Fig. 1 A. Schematic of apparatus. Bat sat on a Y-shaped
platform and emitted sounds into a 1/4" microphone. The
sounds were amplified, filtered and electronically delayed
before they were presented to the bat through a loudspeaker
located I m from the bat. The electronically-delayed sounds
simulated echoes from a target located at a mean distance of
about 63 cm from the bat. The bat listened to the simulated
echoes and determined if the distance to the phantom target
jittered (see B). The bat was trained to move onto the left
platform to indicate a 'yes' (jitter present) response and to
move onto the right platform to indicate a ' n o ' (jitter absent)
response. Bats received a food reward for each correct
response. B Schematic illustration of simulated jittered
(changing distance) and non-jittered (constant distance)
targets. For the jittered targets, the echo was delayed by two
different values on alternating vocal emissions. For the nonjittered targets, the echo was delayed by the same value for
each emission. For the purpose of graphic illustration, echo
jitter shown here is much greater than that actually used in
the experiment. C Calibration curve of the custom-made
loudspeaker
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In order to assess the role of echo bandwidth in the bat's
performance in an echo ranging task, both unfiltered and filtered echolocation sounds were presented to the animals.
Eptesicus fuscus emits a three-harmonic F M sound whose
fundamental sweeps from approximately 55 to 25 kHz. To
test the relative importance of selected components of the
bat's sound for range jitter discrimination, performance
was measured under the following stimulus conditions : Echoes
low-pass filtered at 55 kHz (leaving the first harmonic), at
40 kHz (leaving only a portion of the first harmonic from
25-40 kHz), and echoes high-pass filtered at 40 kHz (leaving
a portion of the first harmonic and the entire second and third
harmonics). Digital filtering (Medav GmbH) permitted sharp
attenuation of unwanted frequencies (exceeding 250 dB/octave)
and avoided phase-shifts typical of analog filtering. Spectrograms of unfiltered and filtered echolocation sounds are shown
in Fig. 2.
On a given test day, bats were tested in blocks of trials
containing 12 trials each. Half of the blocks of trials contained
filtered playback sounds and half contained unfiltered sounds;
half of the trials in a given block contained echo jitter and
half contained no jitter (catch trials). To ensure that a change
in performance reflected a stimulus manipulation and not a
change in motivation, blocks of filtered and unfiltered sound
trials were counterbalanced following an ABBA design. Performance of individual bats for filtered and unfiltered sounds was
compared at each jitter amplitude studied, and thus, each bat
served as its own control.
Echolocation sounds of the bats performing in the task
were picked up with the 1/4" Brfiel & Kjaer microphone and
taped using a Racal high-speed recorder (60 ips). The sounds
were later played back at 1 3/4 ips and analyzed using a Medav
Color Display Spectrum Analyzer (effective bandwidth
128 kHz). Recordings were also made of the filtered and unfiltered sounds played back to the bat (simulated echoes), picked
up at the output of the delay apparatus to the speaker. The
recordings of the bat's emissions and the playback sound were
digitized for cross-correlation and further spectral analysis (Interactive Laboratory System Modules; Signal Technology,
Inc.).
C.F. Moss and H.-U. Schnitzler: Target ranging accuracy in bats
EMISSION
387
ECHO
f(kRz)
10o
oi
55kHz
low-pass
filtered
5
100
40kHz
low-pass
filtered
f(NHz)
high-pass
'~176
50-
filtered
0
1
0
,
1.0
2.0
,
3.0
9
0
,
1.0
2.0
3.0
t(ms)
-80
]
- 40
0
t(rns)
Fig. 2. Spectrograms of natural and filtered echolocation
sounds. The natural echolocation sound (left) contains 3 harmonics, the first sweeping from approximately 55 to 25 kHz
in about 2 ms. For the 55 kHz low-pass filtered sound, the
second and third harmonics have been removed; for the 40 kHz
low-pass filtered sound, all but the low-frequency portion of
the first harmonic have been removed; and for the 40 kHz
high-pass filtered sound, all but the low-frequency portion of
the first harmonic have been retained
Fig. 3. Sequence of echolocation sounds emitted by Eptesicus
fuscus shortly before making its decision in the jitter discrimina-
Results
time-jittered and stable echoes for jitter values
down to 0.4 gs, for which the percentage hits is
at or above 80% and false alarms at or below
20%. Unfortunately, the apparatus could not produce jitter values smaller than 0.4 gs; and therefore, it was not possible to assign an arbitrary
threshold (e.g. 75 % hits), where performance would
fall between 100% (clear discrimination) and 50%
(chance). There is for bat 17, however, a 15% decrease in percentage hits between 3.2 and 0.4 gs
jitter. This observation, along with data from Simmons (1979) showing jitter discrimination thresholds for Eptesicus of about 0.5 gs, suggests that
an arbitrary threshold estimate of 75% hits might
fall just below 0.4 gs for at least one animal tested.
The zero value on the abscissa in Fig. 4 represents a condition in which the bat was never presented with jittered echoes and was rewarded according to a random schedule. Since no echoes
were temporally jittered, no hits could be scored.
Every time the bat moved to the left arm of the
platform, indicating a 'yes' (jitter present) re-
The echolocation behavior of the bats performing
in this task showed no reliable change across conditions. A typical sequence of echolocation sounds
emitted by a bat shortly before making its decision
are shown in Fig. 3. Bats typically emitted between
10 and 40 sounds/s, increasing the sound repetition
rate before indicating a 'yes' or ' n o ' response.
Range-jitter discrimination of unfiltered echoes
Figure 4 A shows the performance of two individual bats for jitter values between 0.4 and 4.8 gs.
In this and subsequent Figs., percentage hits are
plotted with filled symbols (left ordinate), and percentage false alarms are plotted with open symbols
(right ordinate). Discrimination performance for
jitter values larger than 4.8 ~ts are not shown; however, hits remain consistently above 85% and false
alarms at or below 20% for the larger jitter values.
Figure 4 shows that the bats discriminated between
tion task. During this sequence, the bat was presented with
0.8 gs jitter and a 40 kHz low-pass filtered echo (dotted outline). Frequency (kHz) is plotted on the ordinate and time (ms)
on the abscissa
388
C.F. Moss and H.-U. Schnitzler: Target ranging accuracy in bats
AI
UNFILTERED ECHOES
B.
55
kHZ
FILTERED ECHOES
LOW-PASS
BAT 12
1001
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Fig. 4A. Baseline echo jitter delay discrimination for two individual bats presented with the complete echolocation sound.
Percentage hits are plotted with filled symbols (left ordinate),
percentage false alarms are plotted with open symbols (right
ordinate). Performance for jitter values out to 4.8 gs is shown.
B Echo jitter delay discrimination for two individual bats presented with only the first harmonic of the echolocation sound
(55 kHz low-pass filtered)9 Axes and symbols as in A
sponse, a false alarm was scored. This condition
was run to control for any hidden artifact in our
apparatus, and indeed, the data show how infrequently the bats indicated 'yes' when no jitter was
introduced across an entire block of trials. Care
was taken to limit the number of trials in this condition on any day to less than 20 to avoid confusing the bat.
Range-jitter discrimination of filtered echoes
In these conditions, the bats discriminated between
jittered and stable phantom targets which were simulated with filtered electronically-delayed echo-
0".
o'8
l:s
2'A
~2
4',0
4,8
0
JITTER
location sounds. Individual performance curves for
two bats presented with the first harmonic alone
(55 kHz low-pass filtered sounds) are shown in
Fig. 4B. For bat 12 performance under filtered
sound conditions remains virtually unchanged
from unfiltered conditions. This bat discriminates
jitter of only 0.4 gs in approximately 90% of all
trials. Bat 17 shows a different pattern in performance: For jitter values at or greater than 0.8 gs,
performance under filtered and unfiltered conditions is essentially the same; however, at the smallest jitter value tested (0.4 gs), performance under
the filtered condition drops below that under the
unfiltered condition to 69.6%. For this animal
under the 55 kHz low-pass filtered condition, an
arbitrary threshold (75% hits) can be assigned at
0.56 gs. It should be noted that bat 17 was the
only animal tested whose performance dropped below 75% under either filtered or unfiltered conditions.
Overall, the jitter discrimination performance
under the 55 kHz low-pass filtered-echo condition
does not differ from that under the unfiltered-echo
condition. This is illustrated by the group average
C.F. Moss and H.-U. Schnitzler: Target ranging accuracy in bats
GROUP PERFORMANCE
100-
-100
80
70 '11
80-
7060-
55 kHZ
LOW-PASS
UNFILTERED FILTERED
A
.
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w
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P.-. 50"1-
40-
hits
30-
false alarms
A--~/,
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m
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20-
20
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0
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;
1'0
1'5
2'0
2'5
30
JITTER
(usec)
Fig. 5. Group performance, Jitter discrimination under baseline
(triangles) and 55 kHz low-pass filtered (circles) conditions.
Percentage hits are plotted with filled symbols (left ordinate),
and percentage false alarms are plotted with open symbols
(right ordinate). Performance for jitter values out to 30 gs is
shown. Average of 6 bats
389
low-frequency portion of the first harmonic of its
echolocation sound. Figure 6 shows the performance curve for bat 5 under these conditions for
jitter values between 0.4 and 4.8 gs (circles). Also
plotted are jitter discrimination data under unfiltered conditions (triangles). This figure illustrates
that jitter discrimination remains undisturbed by
40 kHz low-pass filtering, even for a jitter value
of 0.4 gs.
The performance of three bats was also studied
under conditions of 40 kHz high-pass filtering.
These bats were required to discriminate temporal
jitter without the low-frequency portion of the first
harmonic. Under these conditions, bats failed to
perform: After 3-4 trials, the animals refused to
make a choice, either remaining at the base of the
observing platform or flying away. This behavior
occurred immediately following performance of
approximately 90% hits with unfiltered or lowpass filtered echoes. Each bat was tested, however,
only once in the high-pass filtering condition.
BAT 5
-lO0
100-
9 90
(/I
80-
. 8 0 0z
70-
~'
970 "n
6050-
3:
UNFILTERED
40-
hits
30 ~
lO~ ~
=
~--~'
false alarms
20-
~
....... ~ ................
40 kHZ
- 6 0 F~
Ill
LOW-PASS-so
>
F I L T E R E D - 4 0 r-30
0-----0
-20
& .............
OJ
0
r
, lO
---
0:8
1:6
214
JITTER
(usec)
3~2
410
0
4.8
Fig. 6. Echo jitter delay discrimination for an individual bat
under baseline (triangles) and 40 kHz low-pass filtered (circles)
conditions. Percentage hits are plotted with filled symbols (left
ordinate), and percentage false alarms are plotted with open
symbols (right ordinate). Performance for jitter values out to
4.8 gs is shown
data from six bats shown in Fig. 5. Data collected
under unfiltered conditions are plotted with triangles and those collected under 55 kHz low-pass filtered conditions with circles: Discrimination
curves for the two conditions are shown for jitter
values out to 30 gs, and the two curves essentially
overlap. Even for 0.4 gs jitter, the average performance is at 80% under both filtered and unfiltered
conditions. At all jitter values tested, the average
false alarm rate is at or below 20%, indicating
that the bat's response bias remained stable.
One bat was also tested with 40 kHz low-pass
filtered echoes. This animal discriminated between
jittered and stable phantom targets with only the
Discussion
The results of this study show that Eptesicus is
indeed sensitive to small changes in echo delay.
They further suggest that the low-frequency portion of the first harmonic of Eptesicus' echolocation sound is sufficient for the bat to discriminate
jitter of echo delay down to 0.4 gs, corresponding
to a target distance discrimination of less than
0.07 mm. Such fine accuracy of distance measurement is consistent with data reported by Simmons
(1979), who also measured echo delay discrimination in bats presented with unfiltered echoes of
their sonar sounds.
In this study, the emitted sounds and electronically-delayed phantom target echoes never overlapped. There was rarely overlap between the
phantom target echoes and clutter echoes from objects such as the loudspeaker and microphone. The
bat's sonar emissions, the phantom target echoes,
and clutter echoes were, however, correlated, with
a delay separation of about 3.67 ms between each
emission and phantom echo, a separation of about
2.1 ms between the phantom echo and the speaker
reflection, and a separation of about 2.8 ms between the microphone reflection and the phantom
echo. The time separations between the bat's sonar
emission, the phantom target echo and the clutter
echoes may have provided acoustic cues which
could give rise to the psychological phenomenon
of pitch (typically referred to as time-separationpitch or repetition pitch; see for example, Thurlow
and Small 1955; Bilsen and Ritsma 1969/1970; de
390
Boer 1976), and these acoustic cues may have conceivably aided in the bat's discrimination of the
echo jitter. We consider this possibility unlikely,
however, since the pitch changes that might be associated with echo jitter in the microsecond range
would be extremely small if time-separation pitch
operates in bats as it does in humans.
The bat evidently can discriminate range differences of less than 0.07 m m using only the low frequency portion (25-40 kHz) of its echolocation
sound. Substantially reducing the overall bandwidth of the echoes returning to Eptesicus thus
does not interfere with this level of fine distance
discrimination. Although each frequency in the
broadband FM sound provides a potential marker
for the time of occurrence of a returning echo,
the low-frequencies provide sufficient information
for fine range discrimination of 0.07 mm. Perhaps
filtering out the higher frequencies would have disrupted range discrimination closer to threshold
(i.e. distance changes smaller than 0.07 m m or echo
delay changes of less than 0.4 gs). A suggestion
of this possibility comes from data from the single
animal (bat 17) whose discrimination performance
under the 55 kHz low-pass filter condition began
to break down for the jitter value of 0.4 gs. Clearly,
however, a large reduction in echo bandwidth (retaining only the low-frequency portion of the first
harmonic) does not disturb range discrimination
for echo delay changes greater than 0.4 gs.
For Eptesicus, a large portion of the sound energy that returns in echoes from distant targets
is contained between 25 and 40 kHz. Therefore,
it is perhaps not surprising that bats can make
fine distance discriminations while listening to
echoes containing only these frequencies. Simmons
and Grinnell (1988) propose that frequencies between about 25 and 40 kHz may be particularly
useful for marking the echo time of arrival, since
the periods of these sound frequencies are longer
than those of the higher frequencies. Although
phase-locking of primary auditory nerve fibers to
pure tones has never been reported at ultrasonic
frequencies, the relatively longer periods of the
lower frequencies of the first harmonic may make
these frequencies especially significant in carrying
a temporal code for broadband transients.
Simmons (1973) asserts that it is unlikely that
the bat extracts target distance information directly from time-domain cross-correlation processing
but rather reduces sound emissions and echoes
into neural displays of spectrograms before deriving the equivalent of the cross-correlation function.
Altes (1980, 1981, 1984) has elaborated on this notion to show mathematically that the correlation
C.F. Moss and H.-U. Schnitzler: Target ranging accuracyin bats
function of a sonar emission and echo may be reconstructed from spectrogram representations if
each frequency in the FM sweep is registered with
sharply-tuned impulses in parallel, overlapping frequency-tuned channels. Spectrogram formation
destroys phase information; however, Altes (1980)
demonstrates that the fine structure of the crosscorrelation function can be reconstructed from
emission and echo spectrograms (revealing the
side-peaks) if a phase measurement at the output
of any single filter can be made. Thus, a bat may
perceive the equivalent of the fine structure of the
correlation function without necessarily operating
with a classical matched filter. If indeed the bat
does use a spectrogram-correlation process for target ranging, the phase information needed to reconstruct the fine structure of the correlation function may be carried by the low-frequency portion
of the first harmonic; the periods of these frequencies are longer than those of the higher frequencies,
and a phase measurement seems to require that
the timing of nerve impulses representing any one
frequency have a distribution narrower than the
period of that frequency (Simmons and Grinnell
1988).
The hypothesis that the bat perceives the equivalent of fine structure information in sonar emissions and echoes is based on a comparison of the
bat's performance curve in the echo jitter discrimination task and the shape of the half-wave rectified
autocorrelation function. Specifically, Simmons
(1979, 1987) observed an increase in the bat's errors for discriminating 30 gs jitter, a stimulus condition that would produce perceptual ambiguity
for an ideal coherent receiver. In the present study,
we found no rise in errors for 30 gs echo jitter
compared to larger and smaller values. Moreover,
the filtering manipulation changes the cross-correlation function such that one would predict a pronounced increase in errors for 30 ~ts jitter if indeed
this function represents the bat's perceptual image:
The low-pass filtering does not change the location
of the side-peaks of the cross-correlation function;
it does, however, raise the height of the side-peaks
with respect to the central peak. The discrepancy
in echo jitter discrimination performance at 30 ~s
between our findings and those reported by Simmons is difficult to explain, but it may be due to
differences in the spatial arrangement of the jittering target with respect to the non-jittering target.
In Simmons's experiment, the jittering target was
centered in range about the non-jittering target;
whereas, in our experiment, the more distant reflecting element of the jittering target was presented at the same range as the non-jittering target.
C.F. Moss and H.-U. Schnitzler : Target ranging accuracy in bats
A comparison of the absolute performance of the
bats in the two experiments shows that errors are
greater in the target range configuration used in
the present experiment than in that used by Simmons. The data reported by Simmons (1979) show
the bat's discrimination performance at 10-20,
40-50, and again at 70-80 gs to be about 94-100%
correct. By contrast, our group data show discrimination performance to be about 86-90% correct
(combining hits and correct rejections) for these
same jitter values, the lowest value differing by
only 2% from that reported by Simmons (1979)
at 30 gs (84% correct). Although it seems possible
that the differences in results between the two
experiments could be attributed to differences in
the equipment and psychophysical procedures,
Simmons et al. (in preparation) have found that
placement of the non-jittering target at the same
range as either the first or second reflecting
element of the jittering target indeed reduces the
bat's overall discrimination performance below
that measured with the non-jittering target centered within the jitter interval. Such a reduction
in discrimination performance may have therefore
obscured the presence of the side peaks at 30 gs
in our data.
In contrast to a coherent cross-correlation receiver model of echolocation, a matched filter bank
model does not propose the use of fine structure
information (Hackbarth 1984; Menne 1988).
Rather, a filter bank model incorporates a series
of overlapping bandpass filters whose frequency
range encompasses the entire echolocation signal.
An F M sweep successively activates each filter
when the frequency components of the sweep correspond to the bandpass frequency. An envelope
detector follows each filter, and activation of
each separate channel serves as a marker of echo
arrival time. This model assumes that the bandwidth of the filters is matched to the frequency
sweep rate of the echolocation signal to minimize
timing error at the output of each channel, and
that an echo delay estimate is based on an average
across channels. Timing error by a matched filter
bank receiver depends on the bandwidth of the
echolocation signal, yet it is conceivable that performance would remain relatively undisturbed by
low-pass filtering at favorable signal-to-noise ratios.
For a given signal-to-noise ratio, the predicted
accuracy of target ranging differs for the crosscorrelation and filter bank receiver models described above. Assuming a signal-to-noise ratio of
about 30 dB, the predicted accuracy of echo arrival
time estimation by Eptesicus fuscus is 0.45 gs for
391
a semi-coherent receiver, 0.006 gs for a coherent
receiver (Menne and Hackbarth 1986) and 1.2 gs
for a matched filter bank receiver (Menne 1988).
These predictions provide some basis for evaluating which receiver model may describe echo ranging in bats. Our data show that bats can discriminate jitter of echo delay down to 0.4 gs, a value
somewhat better than that predicted for both a
semi-coherent ideal receiver and a matched filter
bank receiver. Although 0.4 ~ts is well above the
predicted accuracy for a coherent ideal receiver,
our apparatus did not permit us to measure performance with smaller jitter values. Therefore, we are
unfortunately unable to conclusively accept or reject any one of these receiver models based on the
accuracy of time delay estimation.
The mechanisms of target ranging have been
studied electrophysiologically in several different
species of bats, and the response properties of single neurons cannot yet account for the behavioral
accuracy measured in Eptesicusfuscus. At the level
of the inferior colliculus, there are neurons whose
latency of response is considerably stable from one
stimulus presentation to the next. These cells, identified in the F M bat, Tadarida brasiliensis rnexicana, have been termed constant latency responders, and show a variability of response latency on the order of 100-200 gs (Pollak et al.
1977; Bodenhamer et al. 1979). This variability, although low, is still several orders of magnitude
greater than the ranging accuracy of Eptesicusfuscus (present study; Simmons 1979). In the midbrain of Eptesicus fuscus, some neurons respond
only to pulse-echo pairs, not to a single sound.
Moreover, such cells are selectively responsive to
a particular time interval between the pulse and
echo, suggesting that they code target range (Feng
et al. 1978). Range-tuned cells have also been identified in the auditory cortex of the F M bat Myotis
lucifigus (Sullivan 1982a, b; Wong and Shannon
1988) and the CF-FM bat Pteronotus parnellii
(Suga and O'Neill 1979; O'Neill and Suga 1979).
For all three species, the width of the delay tuning
curves is in the ms range; whereas the behavioral
estimates of echo delay discrimination (measured
only for Eptesicus) are in the fractional-gs range.
Although there is a discrepancy between the single
cell data and the bat's performance, it is possible
to account for high behavioral accuracy with
broadly tuned receptive fields by invoking mechanisms of ensemble coding (see for example McI1wain 1976; Heiligenberg 1987). That is, central
sharpening of acoustic images may arise from the
activation of many broadly tuned range-sensitive
neurons, operating in parallel.
392
When bats catch insects, they estimate the location of their prey with an accuracy of approximately 1-3cm (Webster and Griffin 1962; Trappe
1982). They use the tail membrane or wing to
scoop up insects in flight, and this relatively large
surface area facilitates the capture of prey without
requiring range accuracy of less than a millimeter.
Furthermore, our finding that bats can discriminate jitter of echo delay down to 0.4 gs with only
the low frequency portion of the first harmonic
strongly suggests that the full bandwidth of Eptesicus" echolocation sound is not necessary for the
capture of prey under natural conditions. If a bat
can discriminate echo delay changes of 0.4 gs without the frequency components of its echolocation
sound above 40 kHz, what is the importance of
the broadband echolocation signal ? The higher frequency portion of the sonar sound may play an
important function in the localization and discrimination of natural insect prey in the approach stage
of insect pursuit, when the bandwidth of the echolocation sound is the broadest. Natural stimuli
have depth structure, containing many reflecting
surfaces, and the high frequency components of
the bat's sounds may convey important spectral
information about target shape. For example, the
echolocation sound of Eptesicus is 1.5-2 ms in duration. If the spatial separation of the multiple reflecting surfaces of a target is less than a couple
of centimeters, the multiple echo reflections will
be largely overlapping, resulting in cancellation
and reinforcement at particular frequencies of a
composite echo spectrum. This information may
be used by the bat to discriminate target shape
(e.g. Simmons et al. 1974; Schnitzler et al. 1985),
and the higher frequencies of the bat's echolocation sound would add richness to this information.
The results of this study demonstrate not only
that the big brown bat is capable of making very
fine distance discriminations but also that it can
do so with echoes containing only the low-frequency portion of its first harmonic. That this capability is so robust suggests its potential importance to the sophisticated acoustic imaging system
of the echolocating bat.
Acknowledgements. This research was supported by N A T O and
A A U W postdoctoral fellowships awarded to C.F. Moss and
by the Deutsche Forschungsgemeinschaft (SFB 307). We express our appreciation to D. Menne, L. Miller, B. Mohl, J.
Ostwald, A. Simmons, J. Simmons, A. Surlykke, and three
anonymous reviewers who provided helpful comments on this
work and to D. Menne who designed the echo delay apparatus
and L. Miller who designed the loudspeakers. We also thank
I. Kaipf, J. Mogdens and P. Pilz for technical assistance.
C.F. Moss and H.-U. Schnitzler: Target ranging accuracy in bats
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