automatic gain control in the bat`s sonar receiver and the

automatic gain control in the bat`s sonar receiver and the
The Journal of Neuroscience
Vol. 4, No. 11, pp. 2725-2737
November 1984
0270.6474/84/0411-2725$02.00/O
Copyright 0 Society for Neuroscience
Printed in U.S.A.
AUTOMATIC
GAIN CONTROL
IN THE BAT’S
THE NEUROETHOLOGY
OF ECHOLOCATION’
SHELLEY
A. KICK
AND
JAMES
Institute
SONAR
RECEIVER
AND
A. SIMMONS2
of Neuroscience,
University
of Oregon, Eugene,
Oregon 97403
Received December 27, 1983; Revised May 25, 1984; Accepted May 30, 1984
Abstract
The sensitivity of the echolocating
bat, Eptesicus fuscus, to sonar echoes at different time delays after sonar
emissions was measured in a two-choice echo detection experiment.
Since echo delay is perceptually
equivalent
to target range, the experiment
effectively
measured sensitivity
to targets at different
ranges. The bat’s
threshold for detecting sonar echoes at a short delay of only 1.0 msec after emissions (corresponding
to a range
of 17 cm) was 36 dB SPL (peak to peak), but the threshold
decreased to 8 dB SPL at a longer delay of 6.4
msec (a range of 1.1 m). Prior research has shown that, at even longer delays (corresponding
to ranges of 3 to
5 m), the bat’s threshold is in the region of 0 dB SPL. Contractions
of the bat’s middle ear muscles synchronized
with the production
of echolocation
sounds cause a transient
loss in hearing sensitivity
which appears to
account for the observed echo detection threshold shifts.
The bat’s echo detection thresholds increase by approximately
11 dB for each reduction in target range by a
factor of 2 over the span from 17 cm to 1.1 m. As range shortens, the amplitude
of echoes from small targets
also increases, by 12 dB for each 2-fold reduction in range. Thus, when approaching
a target, the bat compensates
for changes in echo strength as target range shortens by changing its hearing threshold. Since this compensation
appears to occur in the middle ear, the bat regulates echoes reaching the cochlea to a stable amplitude
during
its approach to a target such as a flying insect. In addition to this automatic gain control linked to target range,
the bat aims its head to track a target’s position during approach, thus stabilizing
echo amplitude
even if the
target’s direction changes. We hypothesize that the bat’s directional
emissions, directional
hearing, middle ear
muscle contractions,
and head aim response collectively create a three-dimensional
spatial tracking filter which
the bat locks onto targets to stabilize echo amplitudes
during interception
of prey. We further hypothesize that
this regulation,
which cancels echo amplitude changes caused by the target’s changing spatial position, leaves
the bat free to observe echo amplitude
changes caused by the target’s own actions, such as insect wing beats.
Elimination
of spatially
dependent
echo amplitude
changes removes the cause of potentially
troublesome
changes in neural response latency and keeps stimulation
from echoes in the “tip” region of auditory nerve
fiber tuning curves. The spatial tracking filter thus may stabilize the bat’s acoustic images of a target’s location
and contribute
to enhancement
of the quality of these images.
Echolocating
bats emit ultrasonic
sounds to perceive objects
in the environment.
Echoes of these sounds return to the bat’s
ears, and the bat uses acoustic images derived from these echoes
for spatial perception
(Griffin,
1958; Novick, 1977; Simmons
and Stein, 1980). Many species of echolocating
bats are insectivorous and use their sonar to detect, locate, identify, and
capture flying prey (Griffin,
1958; Simmons et al., 1979b; Simmons and Kick, 1983). To detect such small targets as flying
insects at useful distances of several meters (Kick, 1982), bats
often transmit very intense sonar signals. Peak-to-peak
sound
1Written for T. T. Sandel, who showed us how to integrate ethological, psychophysical, and physiological thinking. This work was
supported by National Science Foundation Grant BNS So-13170 and
by grants from the Whitehall Foundation and the Medical Research
Foundation of Oregon. We thank D. R. Griffin, A. D. Grinnell, W. M.
Masters,
for their
A. L. Megela, A. J. M. Moffat,
critical
comments.
* To whom correspondence
H. -U. Schnitzler,
should be addressed.
and N. Suga
pressures of 100 to 110 dB SPL or more are frequently observed
at short distances in front of the bat’s mouth or nasal broadcasting organ (Griffin,
1958; Novick, 1977). These emissions
are, in fact, so intense as to be near the limits for linear sound
propagation
in the atmosphere.
Sounds of significantly
greater
strength would undergo harmonic
distortion
while traveling
toward the target (Gallego-Ju6rez
and Gaete-Garretbn,
1983).
Bats possess mechanisms which protect their hearing from
the full strength of their sonar transmissions.
The sonar sounds
themselves
are projected
primarily
forward
toward targets
rather than back toward the ears (Pye, 1980; Schnitzler
and
Henson, 1980). Also, the bat’s middle ear muscles contract at
the time of vocalization
to attenuate direct self-stimulation
of
the inner ear (Wever and Vernon,
1961; Henson, 1965; Suga
and Jen, 1975). Still, the outgoing sonar signal is a fairly strong
stimulus and might well affect the bat’s ability to hear much
weaker echoes returning
from targets very shortly after the
emission (Griffin,
1958). Targets at biologically
relevant distances, which for the most part extend out to about 5 m, return
2725
2726
Kick and Simmons
echoes at delays of 30 msec or less. When echolocation
was
discovered, there was considerable
concern about whether bats
could hear the necessarily weak echoes returning
from insectsized targets so soon after emissions, and several early theories
of echolocation
were proposed
in part to account for this
apparent difficulty
(Nordmark,
1960; Pye, 1960; Kay, 1962).
However, experiments
in which bats used echolocation
to detect
obstacles to flight or flying insects clearly showed that bats
have no great practical
problem
in hearing echoes (Griffin,
1958). The early neurophysiological
experiments
of Grinnell
(1963) and of Suga (1964) demonstrated,
too, that the bat’s
auditory system was indeed sensitive to weak sounds occurring
immediately
after stronger sounds, removing the need to worry
about bats being deaf to echoes.
Contractions
of the bat’s middle ear muscles at the time of
vocalization
persist for 5 to 8 msec after the emission (Henson,
1965; Suga and Jen, 1975), and their gradual relaxation
could
reduce the bat’s sensitivity to echoes during this interval (Henson, 1967). Furthermore,
neural events observed to be associated with vocalization
suggest that bats have some central
mechanism for inhibition
of neural responses specifically at the
time of generation
of sonar signals which the bat itself emits
(Suga and Schlegel, 1972). However, no attempt has been made
to measure directly the bat’s sensitivity
to sonar echoes occurring shortly after vocalization,
even though these physiological
observations
suggest that it would be worthwhile
to do so.
Accordingly,
we report here measurements
of thresholds
for
echo detection by the big brown bat, Eptesicus fuxus, at different echo delays. The results contribute
significantly
to organizing our understanding
of relationships
between the bat’s
echolocation
behavior and characteristics
of its sonar receiver.
Materials
Vol. 4, No. 11, Nou. 1984
The target simulator
and the bat’s behavior
in echo detection
trials
are shown
in Figure
1. Two Bruel
& Kjaer
model
4135 condenser
microphones
were placed 10 cm in front of the bat’s head in positions
separated
by an angle of 40” when viewed
from the bat’s observing
position
at the center
of the Y-shaped
platform.
The sonar
signals
emitted
by the bat were recorded
by the microphones,
amplified
and
filtered
with Rockland
model 442 bandpass
filters,
and then delivered
to electrostatic
loudspeakers,
each driven
by a high-voltage
transistor
(Simmons
et al., 1979a), for return
to the bat as artificial
echoes. The
loudspeakers
were placed 40” apart at varying
distances
from the bat
(see below).
Only one of the signal-returning
channels
was activated
on each trial so that a single target would be simulated
either on the
left or the right (Fig. 1). Trials
were begun by placing
the bat on the
center
of the Y-shaped
platform.
The bat would emit sonar sounds
toward
the left and right sides by scanning
back and forth a few times
with its head and then would respond
by crawling
onto the platform
arm corresponding
to the active simulator
channel.
Correct
responses
were rewarded
with food, and the bat was left alone (“time-out”)
for
about 30 set when it made an incorrect
choice.
When
the bat had
consumed
its reward,
it was picked
up and re-placed
at the observing
position
for the next trial.
(Bats readily
adapt to this procedure
by
crawling
or hopping
onto the experimenter’s
hand for return
to the
center
of the platform.)
The distance
from the bat to each of the loudspeakers
(Fig. 1) was
adjusted
to produce
the desired
delay in echo time-of-arrival
after the
bat’s sonar emissions.
The delay of echo stimuli
consists
of the time
required
for the sonar
signals
to travel
10 cm from the bat to the
microphone
(0.29 msec for a velocity
of sound at 344 m/set)
and then
the time required
for the sound to return
from the loudspeaker
to the
bat. The electronic
delay between
the microphone
and the loudspeaker
is neglected
here because
it is infinitesimally
short.
The loudspeakers
were placed
at distances
of 25, 54, 75, 100, or 200 cm in different
repetitions
of the echo detection
procedure.
The corresponding
times
and Methods
Echolocating
bats of the species Eptesicus
fuscu.s (big brown
bats;
Chiroptera,
Vespertilionidae)
were used as subjects
in these experiments.
The bats were collected
in the Willamette
Valley
of western
Oregon
and were maintained
in the laboratory
in a moist room at 22
to 25°C on a diet of mealworms
(Tenebrio
larvae).
The echo detection
experiments,
with echoes returned
at controlled
delays after the bat’s emissions,
were carried
out using a two-choice
simultaneous
discrimination
procedure
adapted
for studying
echolocation (Simmons
and Vernon,
1971). Electronically
simulated
echoes
(replicas
of the bat’s own sonar signals)
were delivered
to the bat as
stimuli
using a target simulator
system described
elsewhere
(Simmons,
1973, 1979). Testing
took place in a closed room (3.8 m long, 2.5 m
wide, and 2.9 m high) that was soundproofed
and made anechoic
at
ultrasonic
frequencies
by covering
the walls, ceiling,
and floor with
convoluted
polyurethane
foam sheets.
Ambient
noise at ultrasonic
frequencies
was too low to measure
with our equipment.
Overall
noise
sound pressure
must have been less than 10 dB SPL. Attenuation
of
reverberation
exceeded
40 dB at frequencies
above 20 kHz. The apparatus consisted
of an elevated
Y-shaped
platform
on which
the bat
rested while emitting
sonar sounds
to scan for the simulated
target.
The bat’s response
was to crawl
from its observing
position
on the
central
part of the Y-shaped
platform
toward
the simulated
target and
onto one of the two side arms of the platform,
whichever
was in the
direction
of the simulated
target. The bat was rewarded
with a piece of
a mealworm
offered
in forceps
for responding
correctly.
At first, to prepare
the bats for the experiments,
each bat was trained
in an earlier
procedure
(Kick,
1982) to detect a real target,
a plastic
cylinder
3.2 cm in diameter
and 5.0 cm high, suspended
vertically
on a
0.15-mm-diameter
nylon
filament
at a distance
of about 20 cm. The
target was presented
to the bat either on the left or on the right of the
bat’s observing
position,
and the bat was pretrained
to approach
this
target by crawling
toward
it and thus onto the left or the right platform.
When the bat would reliably
detect the cylindrical
target at better than
80 to 90% correct
responses
for several days in succession,
with at least
20 detection
trials per day, the target was moved away from the bat by
a few centimeters
and more trials were conducted.
When the bat could
reliably
detect the cylindrical
target as far away as 50 cm, it was judged
ready to receive
electronic
echoes simulating
the presence
of a target,
and the cylinder
was removed.
I
I
I
I
I
If
I
I
I
,I’ b
I
r.
:
I
I
I
Figure
1. A diagram
of the two-choice
procedure
and apparatus
used
for presenting
the bat with electronic
echoes in echo detection
experiments. The bat’s sonar signals are recorded
with two microphones
(m)
and conducted
electronically
to two loudspeakers
(s). Switches
(d, and
db) permit
operation
of only one channel
at a time. The bat is trained
to respond
by moving
toward
the side which presents
the electronically
simulated
target (a) and not to respond
to the silent channel
(b).
The Journal
of Neuroscience
Echo Gain Control
and Neuroethology
required
for electronically
delivered
signals
to travel
from one of the
loudspeakers
back to the bat are 0.73, 1.6, 2.2, 2.9, or 5.8 msec. When
the additional
time required
for the bat’s sonar sounds to travel initially
to the microphones
is taken
into account,
the total time delay of
electronic
echoes presented
to the bat was 1.0, 1.9, 2.5, 3.2, or 6.4 msec.
These delays correspond
to simulated
target distances
of 17,33,43,55,
and 110 cm. The distances
were chosen to span the range of echo delays
that previous
studies
indicated
would
involve
residual
amounts
of
contraction
of the bat’s middle
ear muscles
(Henson,
1965; Suga and
Jen, 1975).
Once they were trained
to detect the cylindrical
target as far away
as 50 cm or so, the bats were transferred
to electronic
echoes as stimuli,
with a delay of 2.5 msec simulating
a target at a distance
of 43 cm. The
initial
amplitude
of the artificial
echoes was set at 80 to 85 dB SPL
(peak to peak), which was approximately
the same as the amplitude
of
echoes produced
by the pretraining
target (the cylinder)
at this distance.
Using this electronically
returned
echo as the stimulus,
the bats were
then trained
to choose reliably
the side of the Y-shaped
platform
which
corresponded
to the simulated
target
(the side corresponding
to the
acitve loudspeaker
in Fig. 1). The presentation
of the artificial
echoes
on the bat’s right or left was varied
from trial to trial according
to a
pseudorandom
schedule
used in previous
two-choice
experiments
(Simmons and Vernon,
1971). Switches
placed below the elevated
platform
controlled
the location
of the simulated
target on the appropriate
side
of the apparatus
by turning
on one or the other of the two feedback
channels.
When
each bat learned
to detect
the electronic
echoes delayed
by
2.5 msec at better than 85 to 90% correct
responses
for several consecutive days, the actual
experiment
commenced.
The strength
of the
electronic
echoes was reduced
in 5-dB steps (using attenuators
placed
just prior to the power amplifiers
and just after the power amplifiers
to maximize
electronic
signal-to-noise
ratios
at the loudspeakers)
to
determine
the bat’s threshold
for detecting
the sounds.
Beginning
at a
peak-to-peak
sound pressure
of 80 dB SPL, 20 to 50 experimental
trials
were conducted
at each level in a progressively
declining
series of echo
amplitudes
until the bat’s performance
fell below the threshold
criterion of 75% correct
responses
(halfway
between
chance
performance
at
50% and perfect
performance
at 100%). Fifty trials were conducted
at
each amplitude
level near the bat’s
threshold,
and echo intensity
decrements
of 2 dB were sometimes
used near threshold.
After
the
threshold
was determined
at a simulated
range of 43 cm, the other
distances
were tested. These distances
were presented
to the bats in a
mixed order to obtain
a set of five threshold
estimates
for each bat.
The raw data for each bat at each echo delay or simulated
target range
thus consisted
of a percentage
of correct
responses
on a block of 20 to
50 trials at each stimulus
amplitude
from 80 dB SPL (peak to peak)
down, in 2- or 5-dB decrements,
to an amplitude
that was below the
bat’s echo detection
threshold.
These data were then reduced
to the
threshold
estimates
themselves
for graphic
display.
The sonar
signals
emitted
by the bats during
experimental
trials
were observed
on a Non-Linear
Systems
model MS-15
portable
oscilloscope mounted
in easy view near the elevated
platform
used for the
experiments.
Echolocation
signals used by each bat to detect stimuli
at
levels near threshold
were recorded
on a Racal Store-4
instrumentation
tape recorder
for later analysis
with a real-time
sound spectrograph
specially
constructed
for analyzing
the echolocation
sound of bats. The
two-channel
acoustic
recording
and reproducing
system
that constituted the target simulator
(Fig. 1) was calibrated
using a Bruel & Kjaer
microphone
placed
at the bat’s observing
position
on the Y-shaped
platform.
The frequency
response
of the simulator
system
from the
point of reception
of the bat’s sonar emissions
(the position
of the
microphones
in Fig. 1) to the location
of the bat’s ears was flat to
within
+3 dB from 20 to 60 kHz. This frequency
range contains
the
first-harmonic
components
of the sonar sounds of E. fuscus, which the
bat uses for target detection
(Simmons
et al., 1978; Kick,
1982). The
frequency
response
peaked from 30 to 50 kHz to ensure that statements
about the gain of the simulation
system
and the strength
of echoes
reaching
the bat’s ears came as close as possible
to specifying
conditions
related
to detection
of echoes in natural
conditions
by the bat. From
20 to 100 kHz the system’s
frequency
response
was flat to within
t8
dB. Stimuli
delivered
to the bat’s ears were characterized
as having
a
particular
peak-to-peak
sound pressure
at 30 to 40 kHz, which corresponds both to the frequency
region emitted
most strongly
by the bat
and to the region
of strongest
response
of the simulator
system.
It
should be remembered
that the final stimulus
magnitudes
can only be
known
from the levels of the sonar signals
emitted
by the bats during
2727
of Echolocation
the experiments.
selected trials
This was the reason for making
near the bat’s threshold.
tape recordings
during
Results
Four
individual
bats
completed
the
echo
detection
threshold
measurements
at simulated target ranges from 17 to 110 cm,
except that one bat became sick and never completed
the
threshold measurement
at a range of 55 cm. Figure 2 shows the
performance
of one bat on a descending
series of stimulus
amplitudes
at each of the five different echo delay times which
were simulated electronically.
This bat’s data are representative
of the data from the other bats in the experiments.
The curves
in Figure 2 illustrate how the bat’s sensitivity to echoes depends
upon
echo
delay.
For
example,
at a delay
of 6.4
msec
the
bat’s
threshold
for echo detection
at a criterion
of 75% correct
responses is approximately
6 dB SPL peak to peak. At a delay
of 1.9 msec the threshold
is 31 dB SPL, indicating
a loss in
sensitivity.
Curves such as those shown in Figure 2 are used to
estimate thresholds
at each delay value for each bat, and it is
these thresholds
at different
delays which constitute
the primary results of the experiments.
As Figure 2 reveals, there is
in fact considerable
change in the bat’s threshold
for hearing
echoes depending upon echo delay.
The threshold
estimates depend upon the strength of the
sonar signals produced by the bats. The sonar signals emitted
by the bats during near-threshold
detection trials were similar
to the echolocation
sounds previously
observed to be used by
E. fuscus in target detection experiments
(Simmons et al., 1978;
Kick, 1982). The signals were frequency modulated
(FM) and
contained two equal-strength
harmonic
components:
a fundamental or first harmonic sweeping from 60 to 65 kHz down to
30 kHz
and
to 60 kHz.
a second
harmonic
sweeping
from
120
kHz
down
The peak-to-peak
sound pressures ranged from 105
to 110 dB SPL, with 109 dB SPL being the most typical
amplitude. Accordingly,
an amplitude of 109 dB SPL at 40 kHz
was used as the basis for acoustic calibration
of the amplitude
of stimuli actually delivered to the bats in these experiments.
1
c
70
i-7.
I
I
I
0
IO
20
30
40
50
60
ti
70
dB SPL (peak-to-peak)
Figure
2. A graph showing
the results of the echo detection
experiment for an individual
bat at five echo delay values
from 1.0 to 6.4
msec. The bat’s echo detection
thresholds
are determined
from the
points
where
these curves
cross the level of 75% correct
responses
(horizontal
dashed line). The curves reveal a general improvement
in
the bat’s sensitivity
to echoes
as the delay of echoes
(or simulated
target range) increases.
2728
Kick
and Simmons
Variations
in the amplitude
of sonar emissions of any of the
bats during detection trials amounted to about 5 dB, which is
similar to the range of variation
seen in threshold
estimates
among all four bats at any particular
echo delay.
Figure 3 shows the echo detection threshold
estimates for
each bat (solid data points) at different echo delays or simulated
target ranges (horizontal
axes). (The graph in Fig. 3 contains a
number of additional
pieces of information
to be discussed
below. For the present, ignore the line marked point target, for
example.) The solid circles, triangles, diamonds, and squares in
Figure 3 indicate for different bats the echo detection thresholds obtained in the experiments
conducted here. These thresholds (vertical axis) are expressed in terms of peak-to-peak
echo
sound pressure in decibels sound pressure level at 40 kHz, for
a 109-dB SPL sonar emission. The variability
inherent in each
threshold estimate is determined
partly by the number of trials
going into the threshold
estimate, and this consists of the 50
trials at the stimulus attenuation
setting yielding a performance
just above 75% correct responses plus the 50 trials at the
attenuation
setting yielding
a performance
just below 75%
correct responses. Stimulus attenuation
was adjusted in 2- or
5-dB steps, which produces a larger inherent
variability
in
threshold estimates than does the 50-trial size of the data blocks
(Grant, 1946). Thus, each threshold
estimate probably
is accurate to within about 5 dB.
The echo detection thresholds obtained at shorter delays are
substantially
higher than thresholds obtained at longer delays.
The mean echo detection threshold
at a simulated range of 17
cm (referring
to the lower horizontal axis of Fig. 3) is about 36
dB SPL (peak to peak), whereas the bat’s threshold
falls to
about 8 dB SPL when the range increases to 110 cm. The
delay (msec)
1
40
2
I
I
a
E\
1 \
\
30
\
3
I
4
I
56
I,,,,,
8
10
20
30
I
40 50
I I
l
20 -
dB
SPL
P.toP,O
decrease in echo detection
thresholds
over the span of echo
delays tested in these experiments-l.0
to 6.4 msec (referring
to the upper horizontal
axis of Fig. 3)-amounts
to 28 clE$.
Intermediate
echo delays produce intermediate
decreases in
echo detection thresholds.
The graph in Figure 3 hints at an
approximately
linear relationship
between the bat’s echo detection threshold
expressed in decibels (that is, on a logarithmic
scale) and the logarithm
of target range. The regression line
(dashed line in Fig. 3) calculated
for the data points in the
graph is
ym = -37
o48mm
O-
-101
01
019 1 mm
0.2
0 3
0.5
07
range
1
2
3
4
56
810
(m)
Figure 3. A graph showing the results of the echo detection experiments. The lower horizontal
axis shows simulated target range in
meters, the upper horizontal axis shows echo delay in milliseconds
(assuming a velocity of sound in air of 344 m/set), and the vertical axis
shows peak-to-peak echo sound pressure in decibels sound pressure
level at the bat’s threshold.
The solid data points show echo detection
thresholds
from experiments
conducted
using the procedure
illustrated
in Figure 1. The open data points
show echo detection
thresholds
estimated
from target
detection
experiments
with 4.6 and 19.1-mm
spheres
(Kick,
1982). The sloping &shed
line is the regression
line for
the echo threshold
data (solid data points).
The sloping, slightly
curued,
solid line marked
point
target shows the amplitude
of echoes
from a
small target
at different
distances
from the bat (Lawrence
and Simmons, 1982a). Only its slope is significant
here; similar
curves can be
placed at different
vertical
positions
to represent
echoes from differentsized targets.
log(delay)
+ 36
This regression line has a slope of -11 dB for each increase in
echo delay by a factor of 2, between delays of 1.0 and 6.4 msec.
The correlation
coefficient for this relationship
is -0.96, which
is strongly significant.
The threshold
for echo detection in E.
fuscus
is inversely dependent
upon the delay of echoes after
emissions, or upon target range.
Discussion
The results of the echo detection
experiments
shown in
Figure 3 indicate
that the sensitivity
of E. fuscus
to sonar
echoes is not constant but does in fact improve as echoes occur
at times increasingly
remote from the sonar emission. Over a
span of delays from 1.0 to 6.4 msec the bat’s sensitivity
improves by almost 30 dB. These delays correspond
to target
ranges from 17 to 110 cm, which is significant,
as will be seen
below, since these distances encompass the most critical stage
of the pursuit of flying insect prey by E. fuscus.
It is helpful to compare the bat’s echo detection thresholds
in the experiments
reported
here with threshold
estimates
obtained in previous target detection experiments
(Kick, 1982).
The echoes which E. fuscus
receives from spherical targets at
the maximum range of detection are about 5 dB SPL (peak to
peak) from 4.8.mm spheres at a range of 2.9 m, and -2 dB SPL
from 19.1-mm spheres at a range of 5.1 m. These estimated
threshold
values are shown in Figure 3 as open data points
(circles) located in the lower right corner of the graph. Taken
together, the echo detection thresholds
measured here (Fig. 3,
solid data points)
and the echo magnitudes
estimated
from
target detection experiments
(Fig. 3, open data points) reveal a
pattern of change in the bat’s sensitivity to sonar echoes which
depends upon the temporal proximity
of echoes to the sonar
emissions
_
Vol. 4, No. 11, Nov. 1984
which
produced
them.
The
bat’s
threshold
remains
low if echoes return at delays greater than roughly 6 to 10 msec,
or if the targets which return these echoes are at distances
greater than about 1 to 1.7 m. The bat’s threshold for detecting
echoes at these relatively
long delays is in the region of 0 dB
SPL (peak to peak). If echo delay is shorter than 6 to 10 msec,
or if target range is shorter than 1 to 1.7 m, the bat’s threshold
for detecting echoes rises by about 11 dB for each reduction in
delay (or range) by half. At a delay of 1.0 msec, or a range of
17 cm, the bat’s threshold
may be as much as 36 dB higher
than it is when targets are at relatively long ranges. Some event
associated with the production
of a sonar sound appears temporarily to reduce the sensitivity
of hearing in E. fuscus,
and
the effect of this loss in sensitivity persists for a span of time
that is biologically
relevant to the bat. We examine below the
consequences
of this transient
loss in hearing sensitivity
for
the process of echolocation.
Not only did the bat receive the electronically
produced
echoes in this experiment,
but it also received echoes from
various objects present in the experimental
room. In particular,
the faces of the loudspeakers
which broadcast echoes back to
the bat also reflected the bat’s sonar emissions to return real
echoes (see Fig. 1). Since these real echoes from the loudspeakers returned to the bat shortly after the artificial echoes which
served as stimuli, they conceivably could have affected the bat’s
The Journal
of Neuroscience
Echo Gain Control
and Neuroethology
sensitivity
to the electronic echoes. A control experiment
was
conducted to determine
the size of the zone of target range
within which echoes from one target can interfere with echoes
from another target. This experiment
developed a life of its
own and is described elsewhere (J. A. Simmons, S. A. Kick, A.
J. M. Moffat, and W. M. Masters, manuscript
in preparation).
The zone of clutter interference
along the dimension
of range
is about 15 cm wide and is such that the real echoes from the
loudspeaker
may have affected the bat’s sensitivity to artificial
echoes in the condition
of shortest delay (1.0 msec) or shortest
simulated range (17 cm), but not at other delays or ranges. The
magnitude
of the interference
effect is small since the real
echoes from the loudspeakers
have an amplitude of 43 dB SPL
(peak to peak) when at a distance of 25 cm. This is only about
13 dB above the bat’s threshold at a range of 25 cm and only a
few decibels more than the echoes which the bat detects at its
36-dB SPL threshold at a range of 17 cm. Furthermore,
when
a bat has approached
to within a distance of 17 cm from a
target under natural conditions,
it has reached the terminal
stage of the interception
process. During this stage, the bat’s
sonar emissions decline in amplitude
by about 6 dB (Griffin,
1958; Webster, 1967), thus raising the bat’s threshold
for detecting sonar targets because the strength of the emission itself
helps to determine the strength of echoes. (The repetition
rate
of emissions during the terminal
stage also increases to more
than 100 sounds/set,
altering the dynamic properties
of the
mechanism
that appears to cause the loss in sensitivity
to
echoes shown in Fig. 3; see below.) The bats in our experiments,
however, did not decrease the amplitude
of their emissions
when detecting
echoes at short delays in the experiments
reported here. Thus, the echo detection
threshold
shown in
Figure 3 at a distance of 17 cm is about 6 dB too low compared
to natural conditions
because the bat would have used weaker
sounds under natural conditions
when this close to a target. It
may be a few decibels too high because weak interfering
effects
could have occurred due to the echoes from the faces of the
loudspeakers.
At other, longer ranges, neither of these complications occur.
Automatic
gain control for target range. The strength of
echoes returning
to an echolocating
bat from a target depends
upon the target’s range. The nearer the target, the stronger the
echoes. As range increases, the strength of echoes declines by
an amount determined
by the nature of the acoustic wavefront
of the bat’s sonar emission, by the nature of the wavefront
scattered by the target, and by atmospheric
absorption
of sound
(Griffin, 19581971;
Pye, 1980; Lawrence and Simmons, 1982a).
Spreading losses for the emission and the echo from a small
target reduce the strength of echoes by a total of 12 C-B for
every doubling of target range. The effects of atmospheric
attenuation here are small since the distances which concern us are
less than a meter or two and the frequencies are only 30 to 40
kHz.
The bat’s threshold for detecting sonar echoes declines by an
estimated 11 dB for every doubling of target range, while the
strength of the echoes themselves declines by 12 dB for every
doubling of range. For target ranges from 17 cm out to 1 to 1.7
m, the sensitivity
of the bat’s hearing for sonar echoes changes
by an amount that approximately
compensates for associated
changes in the amplitude
of the echoes themselves. Over this
span of ranges, the bat holds its threshold at a constant level
with respect to echoes returning
from a small target. Echoes
thus are heard at a constant sensation level. The solid line
markedpoint
target in Figure 3 traces the decline in echo sound
pressure for echoes from a small target at progressively
greater
distances. This line has a slope of -12 dB for every doubling
of target range, plus a slight downward
curvature
due to the
cumulative
effect of atmospheric
attenuation
at frequencies of
30 to 40 kHz. Only the slope of the point target line concerns
of Echolocation
2729
us here; lines with this same slope can be drawn at any vertical
position on the graph depending
upon the actual size of the
object acting as a point target. Larger spherical targets reflect
stronger echoes at any particular
distance, but the decline in
echo strength for a given target at different distances follows
the slope of the curve for point targets in Figure 3. The
particular
curve in Figure 3 shows how the echoes from a
spherical target, which are just barely detectable by the bat at
a distance of 17 cm, would remain just barely detectable by the
bat at greater and greater distances out to 1 to 1.7 m, where
the bat’s hearing thresholds
level off at about 0 dB SPL.
As a sonar target appears at shorter distances, or as the bat
flies closer to the target, it receives increasingly
intense echoes,
but these echoes would remain at a fixed level with respect to
the bat’s hearing threshold even though the distance becomes
smaller. The bat evidently possesses some mechanism within
its auditory
system which uses the time delay of echoes to
compensate for echo intensity changes by changing the sensitivity of hearing. Such a mechanism functions as an automatic
gain control for the bat’s sonar receiver. Range-related
control
of sensitivity
to echoes previously
has been suggested to exist
in echolocation
(Johnson and Titlebaum,
1976), and its discovery in the data shown in Figure 3 reveals what must be an
extremely
important
aspect of echo information
processing.
The shaping of the time course of sensitivity
of hearing after
the emission
of a sonar signal to conform to the relative
strength of echoes from a target at different distances indicates
how thoroughly
the bat’s auditory system must be adapted for
use as a sonar receiver.
The middle ear muscles and range-related
gain control. Two
experimental
studies document the time course of the effects
of middle ear muscle contractions
upon the bat’s sensitivity
to
sounds occurring shortly after vocalization
(Henson, 1965; Suga
and Jen, 1975). These muscles are at the most peripheral
site
in the bat’s auditory system to consider as an obvious possibility
for controlling
sensitivity
to echoes (Henson, 1967; Johnson
and Titlebaum,
1976) because they contract at the time of
emission of echolocation
sounds and relax subsequently.
In the
two species of bats studied, Tadarida
brasiliensis
and Myotis
lucifugus, the middle ear muscles begin to contract before any
sound is produced and reach a maximum state of contractionand, therefore, of middle ear attenuation
of sound-just
at the
time the sound is emitted. Measurements
in M. lucifugus, for
example, show that ultrasonic
sounds reaching the cochlea of
the inner ear through the middle ear are attenuated
by 25 to
27 dB immediately
after the emission. An interval of 5 to 8
msec is required for this attenuation
to decay to zero as the
muscles relax (Suga and Jen, 1975).
The maximum amount of attenuation
produced by the middle
ear muscles of bats corresponds
very closely to the threshold
elevation of 28 dB (from 8 dB SPL at 110 cm to 36 dB SPL at
17 cm) observed in echo detection experiments
(Fig. 3). Furthermore, the 5- to 8-msec time course of the decay of middle
ear muscle contractions
matches the time course of the threshold shift occurring
after emissions. It would therefore appear
that most, if not all, of the rise in the bat’s threshold
for
detecting echoes can be accounted for in terms of middle ear
muscle contractions
occurring
in synchrony with emission of
sonar sounds, assuming that the middle ear muscle observations
in T. brasiliensis
and M. lucifugus would also be true in E.
fuscus.
The contraction
of middle ear muscles in bats has been
assigned a role in protecting
the bat’s hearing from the intense
sonar vocalizations
(Hartridge,
1945; Griffin, 1958; Wever and
Vernon,
1961; Henson, 1965,1967; Suga and Jen, 1975). In
addition,
it has been suggested that their function
extends
beyond mere protection
to include regulation
of signal amplitudes to particular
levels for optimal auditory processing (Suga
2730
Kick and Simmons
and Jen, 1975). The correspondence
between echo attenuation
brought about by contractions
of the middle ear muscles and
the echo detection threshold
shift shown in Figure 3 demonstrates that the middle ear muscles do in fact exercise a regu
latory effect, matching
sensitivity
for echoes to the physical
acoustics of the scattering
of ultrasonic
echoes from point
targets at different
distances from the bat. The concept of
“regulation”
implies a criterion to which something is adjusted.
The role of the bat’s middle ear muscles in compensating
for
the decrease in echo amplitude associated with increasing target
range may thus be the first quantitatively
complete example of
such a regulatory
function for the middle ear system. The fact
that the regulatory
action is exerted at the middle ear and,
therefore, affects signals reaching the cochlea to stimulate the
auditory nerve suggests that this regulation
may occur for the
benefit of the auditory nerve’s responses to echoes.
A three-dimensional
spatial tracking filter in echolocation.
The discovery that E. fuscus apparently
regulates the amplitude
of echoes from targets at different distances to a stable amplitude at the inner ear sensitizes us to think about whether there
are other mechanisms
of this type in the bat’s sonar receiver.
The bat’s middle ear muscle contractions
appear to remove
from echoes reaching the cochlea those variations in amplitude
which are produced by changes in target range. Are there other
regulatory
actions which similarly
eliminate
echo intensity
variations
originating
in changes in a target’s horizontal
and
vertical position? The data in Figure 3 show that, when the bat
is flying toward a target, echoes from the target probably fall
under the influence of the middle ear automatic gain control at
a distance of 1 to 1.7 m. This distance corresponds
roughly to
the distance of 1 to 2 m at which an echolocating
bat first
shows overt reactions to the presence of a target such as a
flying insect (Griffin, 1958; Griffin et al., 1960). These reactions
have been considered
as the end of the search stage of the
process of intercepting
prey and the start of the approach stage.
As the bat is closing in to capture a target, it increases the rate
of emission of its sonar sounds during the approach stage, and
it also commences to track the target in horizontal
and vertical
directions by aiming its head at the target. As Figure 3 reveals,
these two reactions may very well be accompanied by activation
of the middle ear automatic gain control.
The bat emits sonar sounds that are moderately
directional
(Griffin,
1958; Pye, 1980), so that the strength of the sound
which is incident upon the target depends upon whether the
target is directly in front of the bat’s mouth (or nasal emitter)
or off to one side. The bat’s action of pointing
its head at the
target keeps the target in the center of the beam of sound. The
accuracy of the bat’s head aim during interception
has been
judged roughly from stroboscopic photographs
to be about a5”
(Webster and Brazier, 1965). Results obtained in recent experiments using new techniques with E. fuscus indicate that the
accuracy of head aim tracking is more like +l” (W. M. Masters,
A. J. M. Moffat, and J. A. Simmons, manuscript
in preparation). E. fuscus emits sonar sounds that have a directional
beam
width of about f22” at 30 kHz (Simmons, 1969). If the bat can
track the target with an accuracy of even a few degrees, the
sound that is incident
upon the target will probably vary by
only 1 dB or so due to directional
effects. The amount of
variation in the vertical plane is likely to be similar (Shimozawa
et al., 1974).
The bat’s hearing, too, is directional
(Henson, 1970; Grinnell
and Schnitzler,
1977; Schnitzler
and Henson, 1980). Sounds
coming from straight ahead or slightly to one side are received
through the external ear, which acts as a receiving antenna,
with greater sensitivity
than sounds coming from directions
more extremely
to the side, above, or below (Grinnell
and
Grinnell,
1965). The directionality
of sound reception is only
moderately
sharp in E. fuscus, whether measured physiologically (N. Suga, personal communication)
or acoustically
(J. A.
Vol. 4, No. 11, Nov. 1984
Simmons, manuscript
in preparation).
Again, if the bat keeps
its head pointed
at the target with an accuracy of several
degrees, variations
in the strength
of sounds from straight
ahead reaching the eardrum through the external ear will be
about 1 dB. When both sound emission and reception are taken
into account, echoes reaching the bat’s ears from a target that
is within a few degrees of straight ahead will only vary by 1 or
2 dB due to directional
effects (J. A. Simmons, manuscript
in
preparation).
In contrast, if the target were 10” to one side,
echoes would be 4 dB weaker at the eardrum, and, if the target
were 30” to one side, echoes would be 10 to 15 dB weaker.
It should be noted that this discussion of directonality
concerns changes that would occur in echo strength at the eardrum
if the target were to wander off of the main axis of the
echolocation
system. Directionality
as such is only peripherally
related to the bat’s actual perception
of the target’s direction,
which for E. fuscus appears to be based primarily
upon the
timing of echoes at the two ears for horizontal
directions
(Simmons et al., 1983) and the fine structure of echo waveforms
reverberating
through the complex directional
transfer function
of the external ears for vertical directions
(Lawrence and Simmons, 198213). (Whether
these echo timing cues are mediated
within the auditory system by time or frequency domain representations
is irrelevant
to this point.) The overall intensity
of echoes may not be used by E. fuscus for fine localization
but
instead is kept relatively
stable at the two ears by the bat’s
tracking of the target with head aim, a response that we suggest
may be driven from perception
of target position based on echo
timing cues.
Clearly, one effect of the bat’s reaction of keeping its head
pointed at the target would be to stabilize echo amplitude
at
the eardrum and, therefore, at the inner ear, after the target is
detected. Variations
in echo amplitude that would occur as the
target moves in different directions relative to the body axis or
flight velocity vector of the bat are reduced because the bat
tracks the target with its head and ears. In conjunction
with
the middle ear muscle contractions,
the bat’s head movements
can be seen as part of a system which prevents echoes reaching
the bat’s cochlea from varying greatly in amplitude
due to the
changing momentary
position of the target relative to the bat.
We propose that echolocating
bats such as E. fuscus possess a
spatial tracking filter which locks onto the target’s range, horizontal direction, and vertical direction,
tracking the target as
it moves relatively nearer and from one horizontal
or vertical
position to another during pursuit. The immediate effect of this
three-dimensional
spatial tracking filter is to nullify echo amplitude variations
related to the target’s spatial position with
respect to the bat.
Interception
of flying insects by echolocation. Bats use their
sonar to detect, locate, and identify the flying insects which
they feed upon. The pursuit of prey is a relatively
stereotyped
sequence of behaviors in many species of bats (Griffin,
1958;
Ajrapetjantz
and Konstantinov,
1974; Novick, 1977; Simmons
et al., 197913; Schnitzler
and Henson, 1980) and we can best
discern the significance
of the data shown in Figure 3 if we
place it in the context of interception
of prey. There are three
distinct
stages to the acoustic behavior
of bats during the
interception
process-the
search, approach,
and terminal
stages-which
are identified
entirely by the pattern of emission
of sonar sounds. When a bat has approached to a distance of 1
to 1.5 m from a flying insect or an airborne target, it begins to
increase the repetition
rate of its sonar signals from approximately 10 to 20 sounds/set to approximately
30 to 50 sounds/
set (Griffin,
1958; Griffin
et al., 1960; Webster and Brazier,
1965). This event marks the transition
from the search stage
to the approach stage. When the bat has approached
to about
20 to 50 cm from the target, it abruptly increases the repetition
rate of its emissions to as much as 100 to 200 sounds/set. The
second, especially dramatic increase marks the transition
from
The Journal
of Neuroscience
Echo Gain Control
and Neuroethology
the approach to the terminal
stage. Shortly thereafter,
the bat
seizes the target in its wing or tail membrane
(Webster and
Griffin, 1962). The terminal
stage is often called the “feeding
buzz” because the rapid sequence of sonar emissions makes a
buzzing sound when listened to with a “bat detector” (Griffin,
1958; Sales and Pye, 1974; Simmons et al., 1979a). The search
stage, beginning
at a distance of 1 to 1.5 m, really refers to a
period prior to the bat’s first reliable acoustic reaction to the
target’s presence, rather than to a period prior to detection
itself (Griffin,
1958). Eptesicus can detect individual
insectsized spheres at greater distances of 3 to 5 m (Kick, 1982), and
there are also some observations
of bats in flight reacting to
such targets at distances of several meters (Griffin, 1958; Webster and Brazier, 1965; Ajrapetjantz
and Konstantinov,
1974).
The sequence of perceptual
events taking place simultaneously with the acoustical stages shown by the bat’s emissions
are variously described as target detection, localization,
trajectory evaluation,
target discrimination,
and capture (Webster,
1967), or detection, fixation, tracking, and capture (Schnitzler
and Henson, 1980). Eptesicus can detect insect-sized targets at
distances of 3 to 5 m (Kick, 1982), although
it is not known
whether flying bats might integrate information
across several
echoes to decide that a target is present. If so, the detection of
a flying insect might occur a little nearer than detection of a
of Echolocation
2731
sphere. In addition, at about the time of the noticeable increase
in repetition
rate marking the beginning of the approach stage,
the bat begins to track the direction of the target with the aim
of its head (Webster and Brazier, 1965; Webster, 1967). Localization or fixation must therefore have occurred by this time.
Furthermore,
experiments
in which bats choose between a
mealworm
and a plastic or metal target thrown into the air
reveal that the bat makes its decision identifying
the target as
edible or inedible from echoes received prior to the terminal
stage. Thus, bats use echolocation
to discriminate
targets by
size and shape, probably when they are between about 1.5 and
0.5 m away, or during the approach stage (Griffin et al., 1965).
We see from Figure 3 that, when the bat is increasing
the
repetition
rate of its sonar signals, tracking the target with the
aim of its head, and attempting
to identify the target, it also
appears to experience range-related
changes in hearing sensitivity caused by the middle ear gain control system. Because
the acoustic rather than the perceptual
stages of interception
are most frequently
used in describing the bat’s behavior, it is
desirable to modify the three-stage description
to include a new
stage which explicitly
recognizes the bat’s tracking activities.
The four stages of interception
of prey. Figure 4 shows a
composite diagram of the capture of an insect by an aerialfeeding bat (Fenton,
1982) which emits predominantly
FM
Figure 4. A diagram
of successive
positions
of an insectivorous
bat and a flying insect during
the bat’s interception
of the insect
(based on
stroboscopic
photographs
by Webster
(1967)).
The images of the bat (1 to 11) and of the insect (1 to 10) are separated
by 100 msec. The distance
from the bat to the insect for each pair of images appears
as a dotted line. The bat’s sonar emissions
appear as short bars perpendicular
to the
bat’s flight path. The bat detects
the target (between
images 1 and 2) at a distance
of 3 m, thus ending the search stage of pursuit.
The bat flies
nearer to the target during the approach
stage, while receiving
echoes that progressively
increase
in strength
(images 2 to 6). At a distance of 1.3
m (image 6) the bat enters the region in which its echo gain control
functions,
and it increases
the rate of emission
of its sonar sounds
while
also tracking
the target’s
position
with the aim of its head and ears. The bat in the tracking
stage (images 6 to 9) is observing
target features
to
decide whether
it is an insect and worth
capturing.
The terminal
stage (images 9 to 11) involves
the bat in coordinating
its flight to seize the
insect in its wing or tail membrane
and is characterized
by a very high rate of emission
of sonar sounds.
2732
Kick and Simmons
sonar sounds, such as M. lucifugus or E. fuseus. It is based upon
stroboscopic photographs
of an actual interception
made by M.
lucifugus
(Webster,
1967) combined
with drawings
of hypothetical
actions immediately
preceding
the photographs.
In
Figure 4, the bat (image 1, on the left) initially
detects the
target, which is a small flying insect (image 1, on the right), at
a distance of 3 m. The drawing shows 11 successive images of
the bat and the target separated in time by 100 msec, the rate
at which the stroboscopic flash operated in obtaining the actual
photographs
of images 7 to 11. The images from 1 to 6 are
drawn from and are entirely
in keeping with the previous
photographic
studies of interception
(Griffin,
1958; Webster
and Brazier, 1965; Webster, 1967). In addition to the images of
the bat and the insect, the diagram shows schematically
the
time of occurrence of echolocation
sounds (as short bars placed
perpendicular
to the solid line tracing the bat’s flight path) and
the four stages in the pursuit process, indicated
as search,
approach, track, and terminal.
At a distance of about 3 m, E. fuscus is just able to detect a
spherical target with a diameter of 5 mm (Kick, 1982). Prior to
detection (Fig. 4, image 1) the bat would have been flying in
the search stage of pursuit, emitting sonar sounds at a rate of
about 10 to 20/set, and presumably
would have been vigilantly
seeking a target. After detection, the bat gives little sign that
it has detected the target (Fig. 4, images 2 to 5) until it has
approached
to within approximately
1.5 m (Fig. 4, image 6).
Even so, during this interval the bat is receiving echoes from
the target and must be perceiving
the target to some extent.
This is the approach stage as we shall consider it here. At a
distance of about 1.3 m in this example (Fig. 4, image 6), the
bat begins to react overtly to the target by gradually increasing
the repetition
rate of its sonar emissions to about 40 sounds/
set and aiming its head to track the target (Griffin,
1958;
Webster and Brazier, 1965). The sonar sounds also become
shorter, and approximately
at this distance the bat’s middle
ear gain control starts to regulate the amplitude
of echoes from
the insect to a fixed level above the bat’s threshold (see Fig. 3).
This is the beginning
of the tracking stage of pursuit, during
which the bat locks onto the target in range, horizontal
direction, and vertical direction using the three-dimensional
spatial
tracking filter. During the trucking stage of interception
(images
6 to 9 in Fig. 4), echoes reaching the bat’s cochlea will vary
significantly
in amplitude
only if the target’s acoustic reflectivity changes from one moment to the next or if the bat changes
the intensity
of its emissions. The tracking filter cancels out
the larger part of echo amplitude
variability
which originates
in the target’s changing position with respect to the bat. Bats
trained to discriminate
between edible and inedible airborne
targets make the decision concerning
whether to capture the
target during the tracking stage (Griffin et al., 1965). When the
bat has flown to within 20 to 50 cm of the insect (Fig. 4, image
9), it enters the terminal stage of pursuit and completes the
capture of the target by seizing it in the wing or tail membrane
(Webster and Griffin,
1962). If the bat decides not to capture
the target because it judges the target to be an inedible object,
it breaks off the pursuit by failing to enter the terminal stage.
Stimulation
of the bat’s ears during interception.
The sonar
signals transmitted
by insectivorous
bats which forage in the
air for flying insects are exceedingly
intense. Signals recorded
in the laboratory
at distances of about 10 cm from the bat
commonly have peak-to-peak
amplitudes
of 100 to 110 dB SPL
(dB re 20 PPa), and similar magnitudes
are estimated
from
recordings made under field conditions
(Griffin,
1958; Novick,
1977; Pye, 1980). From comparisons
of laboratory
and field
recordings
of the echolocation
signals of E. fuscus (Griffin,
1958; Simmons, 1979; Kick, 1982), we estimate the sonar signals
likely to be emitted as the bat flies through
the search, approach, and tracking stages of Figure 4 at about 109 to 110 dB
Vol. 4, No. 11, Nov. 1984
SPL peak to peak. During the terminal
stage of pursuit, the
bat progressively
decreases the strength of its emissions by a
total of about 6 dB (Griffin, 1958; Webster, 1967). The level of
signals observed during interception
also varies in an irregular
fashion by several decibels, but we assume this to be a consequence of the bat’s motion relative to the microphone
since
signals recorded
in the laboratory
when the bat’s head is
stationary
do not vary much at all (Simmons
and Vernon,
1971). When the sonar emissions of E. fuscus have peak-topeak amplitudes
of 109 to 110 dB SPL, the sound pressure at
30 kHz is about 104 dB SPL (Kick, 1982). We thus know
approximately
the strength of the signals which the bat transmits at the target. Furthermore,
we know that these sonar
signals have an effective strength at the cochlea that is 40 to
50 dB weaker: 20 to 25 dB of this is due to the directional
beaming properties of the emissions and the directional
receiving properties of the ears, and the rest is due to the synchronized
contractions
of the middle ear muscles (Henson, 1967, 1970;
Suga and Jen, 1975; Jen, 1982; J. A. Simmons, manuscript
in
preparation;
N. Suga, personal communication).
Figure 5 shows the estimated sound pressures of the sonar
signals emitted by the bat and the echoes received from the
target during the interception
illustrated
in Figure 4. (See the
legend to Fig. 5 for an explanation
of its relationship
to Fig. 4).
Figure 5A shows the estimated amplitude of the sonar emissions
which were depicted in Figure 4 as short bars placed along the
bat’s flight path. The values given are for peak-to-peak
sound
pressure at approximately
10 cm from the bat’s mouth and at
a frequency of 30 kHz in the FM sweep emitted by the bat.
These emissions have ampitudes
40 to 50 dB lower at the
cochlea. Thus, the bat hears its own sonar signals at about 54
to 64 dB SPL during the search, approach, and tracking stages
of pursuit, with amplitudes
falling to about 48 to 58 dB during
the terminal
stage. The middle ear muscles of bats do not
continue to contract synchronously
with vocalizations
at the
highest repetition
rates of the terminal
stage. Instead, they
reach a condition
of tetanic contraction,
resulting in attenuation of emissions and echoes alike (Henson, 1965; Suga and
Jen, 1975). Since echoes return at very short delays during the
terminal stage, the effects of the gain control system probably
are preserved into the terminal
stage through the combination
of reduced amplitudes
of emissions and sustained contractions
of middle ear muscles.
Figure 5B shows the peak-to-peak
amplitude
of echoes reflected back to the bat if the target in Figure 4 is a sphere with
a diameter of 5 mm. Echoes from the sphere are 35 dB weaker
at 30 kHz just due to the acoustic characteristics
of the target
(Griffin,
1958; Kick, 1982). The solid line (solid data points) in
Fig. 5B shows the progressive
increase in echo strength from
the spherical target as the bat flies nearer during the interception maneuver. The dashed line (open data points) in Figure 5B
shows the amplitude
of echoes from a target with the same 35dB average echo reduction
as the 5-mm sphere, but with a f5
dB amplitude modulation
at a rate of 30 Hz to simulate changes
in echo strength due to the target’s tumbling motions in the air
or to such actions as insect wing beats. This is a reasonable
rate and amount of modulation;
airborne mealworms and other
experimental
targets reflect echoes that vary over this range
from one aspect angle to another within the time available for
the bat to gather echoes (Griffin,
1967), and echo amplitude
modulations
from flying moths match or even exceed this range
depending
upon the aspect angle and the size of the moth
(Schnitzler,
1983).
The curves in Figure 5B show the manner in which stimuli
reaching the bat’s external ears change throughout
the pursuit
of prey. The bat would detect the 5-mm target at a distance of
3 m when the amplitude
of echoes first rises above the longrange detection
threshold
in the region of 0 dB SPL, thus
The Journal
of
Neuroscience
Echo Gain Control
1056
5
2
m95-
- A
al
-
vv
5
and Neuroethology
of Echolocation
2733
105
5
emitted
signals
3
at 30
kHz
-95
2
I
I
I
GO- B
60
echoes
50-
from
target
;;$ ---- ;-- --; ____g _____=
-I 0
5
l ---directional
sensitivity
:C
-
(-35
E--s
dB)
-
\\ ,*..---•=
at 30
-
kHz
: - ---
I
00
middle -ear
muscles
-k
4
-20
-30
v
I
2
,
-4
30-
D
echo
stimuli
I
at Inner
IO0
search-l-
640
I
1
ear
msec
approach
-M
track
-I-
terminal
--I+
capture
Figure
5. Graphs
for determining
the level of stimulation
reaching
the bat’s inner
ear during
the
interception
shown
in Figure
4. The horizontal axis gives the distance
from the bat to the target,
and
successive
image numbers
from Figure 4 are shown
in diamonds along the horizontal axis. Vertical bars
along the horizontal axis show the time (or position)
of the bat’s sonar signals. The stages of pursuit
are
indicated
at the bottom
(E). A gives the peak-to-peak
sound pressure
of the bat’s sonar emissions
at 30
kHz. B shows the strength
of the echoes returning
from the target.
The solid curue shows echoes from a
5-mm sphere,
and the dashed curve shows echoes from a model insect with 30-Hz wing beats and f5 dB
echo amplitude
modulation.
C shows the effects
of the bat’s spatial
tracking
filter,
consisting
of the
middle
ear response
(solid curue) and the head aim response
(dashed curue). D shows the estimated
strength
of echoes at the bat’s cochlea
from the &mm sphere (solid curve) and from the “insect”
(dashed
curue). Note that the vertical axis for D is in terms of echo sensation
level, or sound pressure
with respect
to the bat’s threshold.
ending the search stage. As the bat flies nearer, the echoes
increase gradually
in amplitude
to a level about 20 to 25 dB
above threshold, at a distance of 1 m. The amplitude of echoes
then rises more steeply as the bat approaches nearer yet, with
sound pressures of about 60 dB SPL toward the end of the
terminal stage. At the bat’s eardrum, the strength of stimulation
directly caused by the emissions (approximately
20 to 25 dB
weaker than the emissions, or 73 to 78 dB SPL) is not much
greater than the level of stimulation
produced by echoes from
an insect-sized target in the final moments of pursuit. Larger
targets actually yield echoes at close range that are stronger
than stimulation
provided by the emissions themselves (Henson, 1967, 1970). Amplitude
modulations
imposed upon echoes
by the beating of the “insect’s”
wings are very noticeable
as
variations
in the course of the dashed line around the smooth
curve followed by the solid line in Figure 5B.
Figure 5C shows the combination
of the effects of the gradual
relaxation
of the bat’s middle ear muscles following their contraction
synchronous
with vocalization,
and the tracking
of
target direction with the aim of the bat’s head. Echoes reaching
the bat’s middle ear are stripped of amplitude variations related
to target direction
by the head aim tracking response, which
commences
in Figure 4 approximately
at image 6. Echoes
reaching the bat’s inner ear additionally
are stripped of amplitude variations
related to target range by the state of relaxation
of middle ear muscles. The dashed curue in Figure 5C in
2734
Kick
and Simmons
particular
shows the amount of attenuation
of echoes stimulating the bat’s cochlea as a consequence of the misalignment
of
the bat’s head aim with the target’s direction
between images
3 and 6 in Figure 4. (The bat’s head is assumed to point straight
ahead, along the direction
of flight, until the bat begins its
tracking
response at image 6). The solid curve in figure 5C
shows the amount of echo attenuation
accumulated
by the
middle ear muscle contractions
as the bat moves closer than 1
m to the target and the delay of echoes falls below 6 msec. The
regression line from Figure 3 is plotted as the middle ear muscle
curve in Figure 5, with middle ear attenuation
starting to
weaken echoes at a range of 1.1 m. This is conservative,
since
the low thresholds
for echo detection estimated from experiments with 4.8 and 19.1-mm spheres suggest that, at a distance
of 1.1 m, about 8 dB of middle ear muscle attenuation
may
already be present.
Figure 50 shows the amplitude
of echoes from the target
actually reaching the bat’s inner ear to stimulate the cochlea.
The solid curve (solid data points) in Figure 5D gives echo
amplitudes
above the bat’s threshold
(sensation
levels) for
echoes from the 5mm sphere, and the dashed curve (open data
points) gives echo amplitudes
from the “insect.” These curves
demonstrate
dramatically
the consequence of the action of the
bat’s spatial tracking
filter in stabilizing
the amplitude
of
echoes for the bat’s auditory nervous system to process. Echoes
from insect-sized
spherical targets are regulated to a steady,
rather low sensation level during the tracking
and terminal
stages of pursuit. Because amplitude
variations
related to the
target’s location
are effectively
eliminated,
those variations
related to the target’s fluttering
movements become very conspicuous. It seems likely that one important
function of the
tracking filter system is to render target-related
variations
in
echo strength more readily available
to the bat’s perception
than they would be if combined with the much larger variations
originating
in the target’s changing range and direction.
The
overall size of the target is still available for the bat to perceive
from the average sensation level of echoes during the tracking
stage of pursuit,
since larger targets will yield echoes that
stimulate the cochlea more strongly. The size of a target is an
important
cue for the bat to use in distinguishing
targets, and
fluctuations
in echo amplitude
from moment to moment also
appear important
for the bat to make more subtle distinctions
(Griffin et al., 1965; Griffin, 1967; Simmons and Vernon, 1971;
Neuweiler
et al., 1980; Schnitzler and Henson, 1980).
The definitions
of the four proposed acoustic stages of pursuit
shown in Figures 4 and 5E are apparent
from the curves in
Figure 5 (A to D). The original definitions
of the search and
terminal
stages refer, respectively,
to the bat not giving any
sign of having detected the target, and to the bat’s energetic
efforts to intercept and seize the target in the final instant of
the whole maneuver (Griffin,
1958; Griffin et al., 1960). These
two definitions
seem obvious and straightforward.
Now that we
know that the bat initially detects insect-sized targets at longer
ranges than 1 to 1.5 m (Kick, 1982), we ought to move the
search stage to an earlier period which ends with the reception
of the first echoes from the target above the threshold for echo
detection. The search stage thus would end at a distance which
depends upon the target’s size and the relationship
of its echoes
to the data shown in Figure 3. Large insects would be detected
at 5 m or more, medium-sized
insects at distances of 2 to 4 m,
and small insects at distances of 1 to 2 m. There appears to be
a minimum
size to the targets which the bat can detect in the
pursuit process. The bat’s rising threshold for detecting earlier
echoes will keep targets that are below threshold at 1 m below
threshold at shorter ranges, too. Individual
spherical targets as
small as 1 mm in diameter would thus never be detected by E.
fuscus. Clusters of such small targets might be detected, however, since the aggregate echo ought to exceed the bat’s thresh-
Vol. 4, No. 11, Nov. 1984
old as the bat flies nearer. Myotis can in fact capture spherical
targets as small as 1.6 mm in diameter from airborne clusters
(Webster and Brazier, 1965; Webster, 1967), but smaller targets
appear not to be detected.
The original definition
of the approach stage of pursuit was
based upon the overt responses which bats consistently
make
to the presence of a target when they reach a distance of roughly
1.5 m (Griffin,
1958; Griffin et al., 1960). The data shown in
Figure 3 and the curves in Figure 5 make it clear that the bat’s
activities beginning at a distance of about 1.5 m are very special.
The bat begins to track the target in range with its middle ear
muscle contractions,
in horizontal
and vertical direction with
its head aim response, and in terms of its acoustic images by
changing the characteristics
of its sonar signals (Simmons et
al., 197913). The approach stage here describes the bat’s behavior
after the target is detected but before any of these tracking
mechanisms come into operation at a range of about 1.5 m.
A flying insect beats its wings and twists and turns in the
air, offering to the bat relatively
large changes in its acoustic
reflective characteristics
from one echo to the next (Griffin et
al., 1965; Griffin,
1967; Schnitzler,
1983). Once the target is
detected, the bat would have the opportunity
to observe these
target-related
changes in amplitude
from one echo to another.
This is particularly
true for the tracking stage because other,
larger changes in amplitude
are removed by the automatic gain
control
and tracking
filter system. Echo-to-echo
amplitude
variations
in different frequency bands also may be an important cue for the bat to use in discriminating
the shape of
airborne targets (Griffin,
1967). The bat may wait until the
target is within 1.5 m or so, and the gain control is active, to
begin seriously examining the target to identify it, and we know
that the bat probably
makes decisions concerning
the target
during the tracking
stage (Griffin
et al., 1965). The bat’s
deferred reaction to the target, from detection at several meters
to overt reaction at roughly 1 to 1.5 m (Griffin, 1958; Schnitzler
and Henson, 1980; Kick, 1982), may represent a range gating
mechanism linked to activation of the gain control mechanism.
The consistent triggering
of the tracking stage’s characteristic
behavior pattern at a distance of about 1.5 m seems related to
target range rather than to target detection now that we know
detection to occur substantially
earlier.
During the approach stage the bat receives a series of echoes
which increase progressively
in amplitude
from the region of
threshold at 0 dB SPL to a level of about 20 dB above threshold.
Substantial
further increases do not become manifest at the
inner ear due to the gain control system coming into effect
during the tracking stage. Most of the approach stage thus is
characterized
by reception of echoes at such low sensation levels
that the bat may form only an imprecise acoustic image of the
target. Furthermore,
in some species of bats the signals emitted
during this approach stage are still essentially detection signals;
they are narrow in bandwidth
(Simmons
et al., 1979b) and
cannot provide the bat with much detailed information
about
the target. Only during the tracking stage do these bats begin
to use sonar signals of broader bandwidth
that can convey
precise information
about a target’s location, and only during
the tracking
stage will echoes of these signals probably
have
sufficient amplitude
relative to threshold for the bat to extract
accurate information
about the target’s location. The approach
stage would be shorter for smaller targets, since these would be
detected at closer range, while the end of the approach stage is
fixed by the stereotyped reactions that mark the tracking stage
at a distance of about 1.5 m. Spherical targets with diameters
smaller than 3 mm would evoke the reactions of the tracking
stage only after the bat has approached
nearer than 1.5 m;
detection
would take place so close to the target that the
tracking response would begin at once. In these conditions the
perceptual
qualities of the approach and tracking stages over-
The Journal
of Neuroscience
Echo Gain Control
and Neuroethology
lap, as indicated
in Figure 4 by the arrows extending
the
approach stage past image 7.
Physiological
consequences of stabilization
of echo amplitude.
Stabilization
of the amplitude
of stimulation
of the cochlea by
echoes has two extremely
important
consequences for neural
activity evoked by echoes in the auditory nerve. Bats perceive
the distance to a target from the arrival time of echoes (Simmons, 1973), and the limiting accuracy with which bats perceive
echo arrival time is partly determined
by the acoustic waveform
of the sonar signals and echoes (Simmons, 1979) and probably
also by the signal-to-noise
ratio of echoes (Skolnik,
1962;
Woodward,
1964; Schnitzler
and Henson, 1980). Neurophysiological experiments
indicate that the representation
of the time
of occurrence of FM signals such as echolocation
sounds in the
most peripheral
parts of the auditory
nervous system is in
terms of the time of occurrence of nerve discharges in fibers
tuned to individual
frequencies
occurring
in the FM sweep
(Suga, 1973; Pollak et al., 1977). The latency of discharges for
neurons in the auditory
system is dependent
upon stimulus
amplitude;
changes in the amplitude
of echoes stimulating
the
bat’s cochlea produce shifts in the timing of nerve impulses. A
change of 30 to 40 dB in echo amplitude
can produce a shift in
the timing of nerve discharges of several milliseconds,
and even
the smallest shifts observed are about 1 msec (Suga, 1970;
Pollak et al., 1977; Pollak, 1980). To the bat, 1 msec corresponds
to a change of 17 cm in echo range, which is many times larger
than the smallest shift in range which the bat can directly
perceive (Simmons, 1973). In fact, 17 cm is the minimum
range
shift that neurophysiological
data lead us to expect that a 30to 40.dB shift in echo amplitude
would produce in the bat’s
perception
of target range. Bats usually capture insects in the
wing or tail membranes
(Webster and Griffin, 1962), and they
would certainly fail to do so quite frequently
if their perception
of the target’s distance were perturbed
by as much as 17 cm.
The regulation
of echo amplitude
at the cochlea to a stable
level by the middle ear system would prevent large shifts in
echo amplitude
from appearing in the stimuli delivered to the
cochlea while the bat approaches
nearer to a target from an
initial distance of 1 to 1.5 m. Large intensity-related
changes
in neural response latency would thus not occur during the
tracking stage.
Most of the insects pursued by bats such as E. fuscus are
relatively
small sonar targets-mayflies,
June beetles, and
small flies and moths are fairly representative
of the sizes
frequently captured (Griffin, 1958; Novick, 1977; Fenton, 1982).
These insects have acoustic cross-sections roughly comparable
to spheres with diameters of 0.2 to 2 cm, although the insects
will have quite different apparent sizes or cross-sections
from
different
aspects (directions)
and from moment to moment
(Griffin et al., 1965; Griffin, 1967; Schnitzler,
1983). The intensities of echoes from such small targets during the tracking
stage will probably range from about 0 to 35 dB SPL peak to
peak (Griffin,
1958; Kick, 1982). From Figure 3, targets with
echoes,of this amplitude at distances of 1 to 1.5 m will therefore
have echoes only 0 to 35 dB above the bat’s threshold of hearing.
Stimulation
by echoes reaching the bat during the pursuit of
prey would thus activate auditory nerve fibers only in the socalled “tip” region of the tuning curves for these fibers.
The most salient feature of the response of auditory
nerve
fibers in mammals to higher-frequency,
brief sounds delivered
at low intensities and at frequencies within the tip of the fiber’s
tuning curve is that the response usually consists of a single
discharge which marks the time of occurrence of the onset of
the sound (Kiang,
1965). At stimulus levels between 0 and
perhaps 20 dB above the fiber’s threshold there is not even an
increase in the total number of discharges per unit time above
the spontaneous
firing rate, just a grouping in time or synchronization
of the same number
of discharges to the times of
of Echolocation
2735
repeated stimulation
(Johnson, 1980). At stimulus levels above
the threshold
for actually increasing
the total number of discharges per unit time above the spontaneous level, usually there
still will only be a single discharge marking the time of occurrence of a brief stimulus such as the very transient
sweep of a
bat’s FM sound through the excitatory area of the tuning curve
(Pollak et al., 1977). More than one discharge for each stimulus
only occurs when such transients are strong enough to activate
the neuron in regions of the tuning curve considerably
elevated
from the tip. As a result of all this, the auditory nerve of a bat
approaching
an insect most conspicuously
will carry information about the time of occurrence of individual
frequencies in
the FM sweeps of echoes. Intensity information
is unlikely to
be richly represented by the total number of impulses in each
fiber evoked as a burst of activity by each echo. It is more likely
to be represented by the differing sensitivities
of neurons tuned
to the same frequency, with only the most sensitive neurons
responding
to the weakest echoes. Models of echolocation
that
are based upon spectrogram-like
neural representations
of
acoustic waveforms seem most useful to pursue at this juncture
(Suga, 1973; Altes, 1980; Simmons, 1980).
Internal noise and detection of echoes. The bat’s threshold for
detecting echoes is determined
ultimately
by the strength of
echoes relative to noise (Skolnik, 1962; Woodward,
1964). This
noise could be acoustic noise originating
externally
in the
environment,
or it could be noise originating
within the bat’s
auditory
system. Because external noise passes through
the
middle ear system along with echoes and is attenuated as well
as echoes by contraction
of the middle ear muscles, the data in
Figure 3 show that the bat’s ability to detect echoes (at least in
the conditions of these experiments)
is limited by internal noise,
not external noise. The signal-to-noise
ratio of echoes to external noise ought to remain unaffected by middle ear attenuation,
whereas attenuation
of echoes by the middle ear would weaken
echoes with respect to noise manifested in the inner ear or the
auditory nervous system. This internal noise seems unlikely to
be of an acoustic nature since it would have to be ultrasonic
in
frequency; it may originate
instead in the transduction
processes of the inner ear-in
the hair cells of the organ of Corti or
in their synaptic connections
with auditory nerve fibers.
During the approach stage, as the signal-to-noise
or signalto-threshold
ratio of echoes progressively
increases from 0 to
25 dB (in the example shown in Fig. 5), the bat would become
increasingly
accurate in perceiving
the time of occurrence of
echoes (Schnitzler
and Henson, 1980). Perceptions
of target
range, horizontal
direction,
and vertical direction,
which may
be based in part on temporal cues (Simmons, 1979; Lawrence
and Simmons,
1982b; Simmons et al., 1983), would become
increasingly
acute as echoes increase in strength
over the
internal noise of the bat’s sonar receiver. If the bat relies upon
the timing of echoes and temporal
information
in echoes to
perceive the target’s location
in three dimensions
and the
intensity
of echoes to distinguish
the target, the bat may
effectively
isolate even the cues for target location from the
cues for target identity,
using the spatial tracking
filter to
improve the quality of both kinds of information.
The echo
signal-to-noise
ratio apparently
becomes good enough during
the tracking stage for the bat to enter the target’s range on a
neural map of distances in the auditory
cortex (Suga and
O’Neill,
1979). It is interesting
that the neural map becomes
most organized and well defined for targets at distances of 1.5
m and less, the zone within which echo gain control operates.
Perhaps the range gate mechanism for initiating
the tracking
stage may be located in, or at least activated by, the 1.5-m site
on the cortical map.
The bat’s spatial tracking filter system is composed of the
external ear, the middle ear, and such behavioral
responses as
the aim of the bat’s head and the changes in sonar emissions
Kick and Simmons
2’736
occurring during the tracking stage of pursuit. It has proven
necessary for us to have the behavioral
data shown in Figure 3
to discern the existence of the system, even though sufficient
physiological
data have been available for one or two decades.
We could ask for no more satisfying a demonstration
of the
central role of ethological
and behavioral
research in the neurosciences, not merely to isolate and define problems which
can then be approached
with the modern technical arsenals of
anatomy and physiology,
but to tell us what the results of this
approach will mean.
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