Doppler-shift compensation behavior in horseshoe bats revisited: auditory feedback controls both a decrease and an increase in call frequency
1 Department of Biology, University of California at Riverside, Riverside,
CA 92521-0427, USA
2 Institute of Zoology, Chinese Academy of Sciences, 19 Zhongguancun Road,
Beijing 100080, China
* Present address: Department of Physiological Science, University of California
at Los Angeles, Los Angeles, CA 90095-1606, USA
(e-mail: metzner{at}ucla.edu )
Accepted 20 March 2002
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Summary |
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Key words: horseshoe bat, Rhinolophus ferrumequinum, hearing, echolocation, audio-vocal feedback, Doppler-shift compensation behaviour
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Introduction |
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Although auditory feedback does not seem to affect vocalizations in various
adult non-human primates and in adult cats
(Janik and Slater, 1997;
Jürgens, 1998
), it is
essential in bats (Griffin,
1958
). Horseshoe bats, for instance, specialize in adjusting the
frequency of their calls depending on the pitch of the echo signal. During
flight, the dominant constant-frequency component of their distinctive calls
is shifted as a result of Doppler effects. The bats compensate for these
shifts by adjusting the frequency of their subsequent calls
(Schnitzler, 1968
). This
ensures that the echo of interest remains within a narrow frequency range
stimulating a region of the cochlea innervated by a disproportionately large
neuronal population with exceptionally sharp tuning properties, termed the
`auditory fovea' (Schuller and Pollak,
1979
) (see Fig. 1).
This so-called Doppler-shift compensation (DSC) behavior
(Schnitzler, 1968
) represents
one of the most precise forms of sensory-motor integration known. It has been
compared with visual fixation, in which eye movements keep an image of
interest centered on the fovea, a region of the retina with densely packed
receptors and neurons with small receptive fields
(Schuller and Pollak, 1979
).
DSC behavior can even be elicited in stationary horseshoe bats by presenting
echo mimics, i.e. electronically delayed and frequency-shifted playbacks of
the bat's own calls (Schuller et al.,
1974
,
1975
). DSC behavior is not
limited to horseshoe bats. The Central and South American mustache bat
Pteronotus parnellii produces echolocation calls that are very
similar to those of horseshoe bats and also compensates for Doppler-shifted
echoes (Henson et al., 1985
;
Keating et al., 1994
).
|
For the past three decades, we have commonly believed that in both groups
of bats only echo frequencies returning above the bat's resting frequency (RF;
i.e. the frequency the bat emits and hears when not flying) affect DSC
behavior, causing the bat to lower its vocalization frequency (horseshoe bats,
e.g. Schnitzler, 1968,
1973
; Schuller et al.,
1974
,
1975
;
Simmons, 1974
; Metzner,
1989
,
1993b
,
1996
;
Tian and Schnitzler, 1997
;
Pillat and Schuller, 1998
;
Behrend and Schuller, 2000
;
mustache bats, e.g. Henson et al.,
1985
; Suga et al.,
1987
; Pollak and Casseday,
1989
; Gaioni et al.,
1990
; Suga, 1990
;
Keating et al., 1994
). Echo
frequencies returning below the RF, where auditory thresholds are up to 30 dB
higher (see Fig. 1), were
believed to provide no auditory feedback and only allow the call frequency to
return passively to the RF. This appeared plausible since under natural
conditions, when horseshoe (or mustache) bats approach a background target,
the bats experience only positive Doppler shifts. However, the literature also
contains some, though mostly neglected, evidence that echo frequencies below
the RF might also drive DSC behavior. Schnitzler himself in his original
publication (Schnitzler, 1968
)
shows a horseshoe bat lowering and raising its call frequency below and above
the RF (his Fig. 12), in response to a large ball swinging in front of the
bat. Similarly, when Gaioni et al.
(1990
) tested DSC behavior in
mustache bats by swinging the bats on a pendulum, two bats raised their call
frequencies by 200-400 Hz above the RF during the backward swing (their
Fig. 1). Nevertheless, they
state that mustache bats `did not show DSC on the backswing'
(Gaioni et al., 1990
). Finally,
results from deafening experiments in horseshoe bats suggested that, to
maintain RF in normal hearing bats, auditory feedback was required from
frequencies not only above but also below the RF
(Rübsamen and Schäfer,
1990
). Therefore, it appears that the literature does indeed
contain some conflicting reports on whether bats compensate for echo
frequencies below the RF.
The present study was designed to re-assess the range of echo frequencies eliciting DSC behavior. This information is indispensable in evaluating the circuitry and neural mechanisms for auditory feedback control of DSC behavior.
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Materials and methods |
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The following gives a brief theoretical outline of how double heterodyning
and filtering yields frequency-shifted playback signals (for further details,
see Schuller et al., 1974,
1975
). In the first
heterodyning step, the bat's call is recorded (say call frequency is at 80
kHz) and `mixed' (electronic multiplication) with one pure-tone signal (say 60
kHz) resulting in two signals, one at 140 kHz (=80+60 kHz) and one at 20 kHz
(=80-60 kHz). This output consisting of signals at 20 and 140 kHz is
highpass-filtered at 99 kHz, resulting in cancellation of the 20 kHz
component. In the subsequent second heterodyning step, the remaining 140 kHz
component is then mixed with a second pure-tone signal (say 62 kHz). The
outcome is a signal composed of components at 202 kHz and 82 kHz.
Lowpass-filtering at 99 kHz cancels the high-frequency component (202 kHz) and
transmits the signal at 82 kHz, which is the frequency of the playback signal
delivered to the bat. Hence, it stimulates an echo that is shifted 2 kHz above
the bat's own call frequency. The difference between the first and second
pure-tone signals used for heterodyning therefore determines the size of the
frequency shift induced in the playback signal. Since each heterodyning step
results in two components that are far more than one octave apart (20
versus 140 kHz, and 82 versus 202 kHz, respectively), they
can be easily and reliably separated by filtering.
Call frequency, call amplitude and time course and the size of the induced frequency shift in the echo mimic were analyzed using commercially available signal-analysis statistics software (`Signal' Engineering Design, Belmont, MA, USA; SigmaStat and SigmaPlot, Jandel Corp., San Rafael, CA, USA).
Experiments were performed in an anechoic chamber (28°C, >50%
relative humidity) where echoes reflected from the walls were below the noise
level of our recording system (i.e. <45 dB SPL). The bats' calls were
recorded by a -inch ultrasonic microphone and amplifier (Brüel
& Kjær; Nærum, Denmark) positioned 15 cm in front of the bat's
nostrils, electronically delayed by 4 ms (custom-built delay line),
heterodyned (model DS335 function generators, accuracy greater than 0.01 Hz at
80 kHz; Stanford Research Systems, Sunnyvale, CA, USA), high- and subsequently
lowpass-filtered (99 kHz each; digital two-channel filter, model SR650,
roll-off 115 dB per octave; Stanford Research Systems, Sunnyvale, CA, USA) and
then played back via a power amplifier (Krohn-Hite, model 7500, Avon,
MA, USA) and a condenser-type ultrasonic loudspeaker (Panasonic Inc.;
Secaucus, NJ, USA).
The loudspeaker was positioned at a distance of 15 cm from the bat's right
or left pinna and at angles of approximately 30° lateral from (azimuth)
and 15° below (elevation) the midline, roughly corresponding to the best
direction of hearing in these bats
(Grinnell and Schnitzler,
1977). Bats could move their head freely. The transfer function of
the loudspeaker allowed the delivery of pure-tone pulses of up to 122 dB SPL
measured at the position of the bats' pinnae and ±5 kHz around the
bats' RFs, which ranged from 76.5 to 78.8 kHz. A spectrographic analysis
revealed that the amplitude of harmonics for pure-tone signals in this
frequency range was less than 60 dB SPL. Calibration of the playback system
was performed with a
-inch ultrasonic microphone and power amplifier
(Brüel & Kjær) using commercial signal-analysis software
(`Signal', Engineering Design, Belmont, MA, USA). The frequency and amplitude
of the bats' calls were extracted from a custom-built frequency-to-voltage and
a.c./d.c. converter, respectively. The accuracy for determining call frequency
and amplitude was ±24 Hz and ±3 dB, respectively. Call
frequency, call amplitude and time course and the size of the induced
frequency shift in the echo mimic were continuously monitored and recorded on
video tape using a recording adapter (Vetter 3000A, Rebersburg, PA, USA;
sample rate 40 kHz per channel).
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Results |
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Another more dramatic difference between compensation for positive and
negative shifts was that the bats never fully compensated for negative shifts
(Fig. 2B-D). The greatest
increase in call frequency observed was +1.51 kHz in response to a -4.5 kHz
shift in the artificial echo, and the mean maximum compensation performance
was 22.0% (N=500 cycles), 16.9% (N=500 cycles) and 14.9%
(N=200 cycles) of the maximum frequency shifts of -1.5, -3 and -4.5
kHz, respectively. Nevertheless, the overall changes in call frequency in
response to the three different echo frequency shifts tested were
significantly different (Fig.
2D). For comparison, call frequencies emitted at rest by an
individual bat show standard deviations of only approximately ±50 Hz,
which is less than 0.1% of RF (Schuller et
al., 1974).
In this first experimental paradigm, horseshoe bats compensated only for up
to 22% of the frequency range covered by negative shifts
(Fig. 2B-D), whereas they
compensated for 95% of positive shifts
(Fig. 2A)
(Schnitzler, 1968;
Schuller et al., 1974
;
Tian and Schnitzler, 1997
).
This asymmetry was not based upon a lack of auditory input from echo
frequencies below RF since different modulation depths below RF had
significantly different effects on DSC behavior
(Fig. 2B-D). Instead, this
difference appears to be caused by limitations on the (pre)motor control side,
since even electrical stimulation of the superior laryngeal nerve, which is
the motor nerve innervating the larynx and controlling call frequency
(Schuller and Rübsamen,
1981
), was unable to raise call frequencies by more than 1.2 kHz
for a stimulation near saturation of the firing rate of the nerve
(Schuller and Suga, 1976b
).
The peculiar mechanics of sound production in the larynx of bats probably
causes such a constraint (Suthers and
Fattu, 1982
): in bats, the precise timing between glottal activity
and the activity of the cricothyroid muscle, which is particularly important
for producing high-pitched vocalizations, limits the generation of increases
in call frequencies.
The results presented in Fig. 2 therefore indicate (i) that, in addition to frequencies above RF (Fig. 2A), those below RF (Fig. 2B-D) also provide auditory feedback for the control of DSC behavior, and (ii) that horseshoe bats can systematically increase their vocalization frequency even above the RF (Fig. 2B-D).
To verify the former point, the time courses were measured for decreases
and increases in vocalization frequency during stepwise positive (up to 4.5
kHz above RF) and negative (return to RF) shifts in echo frequency,
respectively (Fig. 3A). This
paradigm had previously been used to yield important insights into, for
instance, the effects of varying step size on the time course of compensation
and to compare the speed of compensation for positive with that for negative
steps (Simmons, 1974;
Schuller et al., 1975
;
Schuller and Suga, 1976a
).
These studies demonstrated that compensation became faster with increasing
step size and that, for the same absolute intensity level, responses to
positive steps were faster than those to negative steps. The results also
showed that information about the size of the frequency shift in the last echo
heard could be stored for several minutes, being significantly reset only when
a new call had been emitted and the corresponding echo signal had been heard
at a different frequency (the `sample-and-hold' analogy of
Schuller and Suga, 1976a
).
What had been missing so far, however, was information on how varying
intensity levels for positive and negative steps affect the speed of
compensation. Hence, in our second series of experiments, we tested four
different intensities ranging, in steps of 10 dB, from 0 to 30 dB attenuation
relative to the bat's own call (corresponding to intensities of approximately
85-115 dB SPL). If, as indicated by the results from our first experimental
paradigm (see Fig. 2), both
frequency ranges provide auditory feedback, call frequencies during both
positive and negative shifts in stimulus frequency should change more rapidly
with increasing intensity. This was indeed the case in all three bats tested
(Fig. 3C,D; a representative
example is given in Fig. 3B).
The median time constants for negative shifts shortened from 2.28 s at 30 dB
attenuation to 0.89 s at 0 dB attenuation
(Fig. 3B,C); for positive
shifts, the median time constants shortened from 1.64 s at 30 dB to 0.75 s at
0 dB attenuation (Fig. 3D).
While the time courses of responses to positive steps were slightly more
variable (S.D. ranging from 1.37 to 0.22 s) than those for negative steps
(S.D. between 0.38 and 0.17 s), the trend was nevertheless significant (all
pairwise multiple comparison procedure, Dunn's method, P<0.05).
The speed of DSC responses was directly correlated with the size of the
initial change in call frequency: the first call during faster DSC responses
to positive steps, for instance, was emitted at lower frequencies than during
slower responses (data not shown; see also
Schuller, 1986).
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Discussion |
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It is apparent that horseshoe bats approaching a background target should
compensate for flight-induced increases in the echo frequency to maintain
echoes within their auditory fovea. But what is the purpose of compensating
for negative frequency shifts? Normally, only echoes returning from larger
background targets and not those from small prey objects are loud enough to
elicit DSC behavior (e.g. Schnitzler,
1968,
1973
;
Trappe and Schnitzler, 1982
).
Thus, it has commonly been believed that only frequencies above RF are
encountered naturally (Schnitzler,
1968
; Schuller et al.,
1974
,
1975
;
Schuller and Suga, 1976b
;
Schuller, 1986
; Metzner,
1989
,
1993b
;
Tian and Schnitzler, 1997
;
Pillat and Schuller, 1998
).
Although some of the data originally describing DSC behavior in horseshoe and
mustache bats indeed showed that these bats could also compensate for negative
shifts (see Fig. 12 in Schnitzler,
1968
; see Fig. 1 in
Gaioni et al., 1990
), this
observation had soon been discounted. This failure to notice the importance of
feedback from echo frequencies below RF did not change when results from
deafening experiments demonstrated that the RF of deaf horseshoe bats changed
`unsystematically, and some even nearly maintain the presurgical values'
(Rübsamen and Schäfer,
1990
). The authors suggested that, to maintain RF, auditory
feedback was required not only from frequencies above but also from those
below RF since the absence of negative feedback only from frequencies above RF
should have caused deafened bats to produce call frequencies that were
different from the predeafened value.
However, there are some circumstances during normal echolocation behavior
when echo frequencies could return below the RF and elicit compensation
behavior. For instance, during final target approach, such as before landing
on a cave wall, flight speed is gradually reduced, which causes echo
frequencies to fall below RF as a result of `overcompensation' by the bat.
Hence, bats start to increase their call frequencies. During these final
approach stages, calls are still emitted at very high levels of approximately
120 dB SPL, and thus echo intensities also remain high
(Tian and Schnitzler, 1997).
Even when adding a transmission loss of up to 20 dB for the corresponding
target distances (Lawrence and Simmons,
1982
), these calls generate echoes returning at least 70 dB above
the auditory threshold for these frequencies
(Fig. 1, light gray area). This
corresponds to intensities that also elicit the lowering of call frequencies
in response to positive Doppler shifts
(Schuller et al., 1974
)
(Fig. 1, dark gray area).
Active compensation for these negative frequency shifts during final target
approach would enable the bat to increase its call frequency faster, and thus
more efficiently, than with a purely passive mechanism
(Schuller, 1986
).
Another instance when horseshoe bats might experience echo frequencies shifting below RF is during somersault landings, which they quite frequently perform (W. M. and S. Z., personal observations). During such flight maneuvers, the position of the bat's head and ears changes rapidly relative to a stationary background, such as a cave wall, and this might be sufficient to induce small negative Doppler shifts. However, in the absence of any documented echo signals recorded during natural flight maneuvers in Doppler-compensating bats, these scenarios have to be considered speculative.
What are the consequences for the neural substrates and sensory feedback
mechanisms involved in controlling DSC behavior? The observation that
horseshoe bats actively compensate for both positive and negative shifts in
echo frequency suggests that DSC behavior is not controlled by a
unidirectional audio-vocal feedback mechanism, as has been assumed over the
past three decades (Schnitzler,
1968,
1973
,
1986
; Schuller et al.,
1974
,
1975
;
Simmons, 1974
;
Schuller and Suga, 1976b
;
Metzner, 1989
,
1993b
;
Tian and Schnitzler, 1997
;
Pillat and Schuller, 1998
).
Since echo frequencies below RF also elicit DSC behavior, one can no longer
assume that only populations of neurons tuned to frequencies above RF are
potential candidates for audio-vocal interfaces (Metzner,
1989
,
1993b
,
1996
;
Pillat and Schuller, 1998
;
Behrend and Schuller, 2000
).
Neurons tuned to frequencies below RF obviously play a role as well.
More importantly, however, the findings described here revise our current
understanding of the audio-vocal feedback mechanism that controls DSC
behavior. Previously, a single inhibitory (Metzner,
1989,
1993b
,
1996
;
Pillat and Schuller, 1998
;
Behrend and Schuller, 2000
) or
excitatory feedback mechanism was considered to be sufficient to account for
the lowering of call frequencies in response to positive Doppler shifts.
However, the active response to both positive and negative Doppler shifts
(Figs 2,
3) suggests that a single
inhibitory or a single excitatory feedback mechanism is insufficient. This is
illustrated in Fig. 4. The
motor command for generating different call frequencies appears to be the same
in all mammals studied so far, including humans
(Fig. 4A). As indicated by a
white arrow, lower vocalization frequencies (VF1 in
Fig. 4A) are caused by a lower
level of activity of the motor output, e.g. the superior laryngeal nerve (see
the corresponding motor activity level MA1 in
Fig. 4A)
(Schuller and Suga, 1976b
;
Schuller and Rübsamen,
1981
; Yajima and Hayashi,
1983
; Larson et al.,
1987
). Conversely, higher premotor activity (MA2)
generates higher call frequencies (VF2), as shown by a black arrow.
Any sensory feedback mechanism must ultimately conform to this relationship,
i.e. sensory information about different echo frequencies must converge at the
level of the sensory-motor interface in such a way as to allow the motor
pattern described above to be generated in response.
|
The three simplest scenarios for such an integration of echo frequencies and the resulting auditory feedback control of call frequencies during DSC behavior are depicted in Fig. 4B-D. Generally, during DSC behavior, echo frequencies above RF (such as EF1 in Fig. 4B-D; white arrows) generate lower vocalization frequencies (VF1 in Fig. 4A), as is seen in any `normal' DSC behavior (see Fig. 2A). However, auditory feedback from frequencies below RF (EF2 in Fig. 4B-D; black arrows) produces call frequencies above RF (VF2 in Fig. 4A), as we have shown in Fig. 2B-D (`inverse' DSC behavior).
Let us now consider how these different echo frequencies above and below RF
(EF1 and EF2) yield call frequencies below and above RF,
respectively, assuming that a purely inhibitory feedback mechanism is at work
at the level of the sensory-motor interface
(Fig. 4B). We had originally
suggested this scenario largely on the basis of neurophysiological data
(Metzner, 1989,
1993b
). First, let us look at
echo frequencies above RF, such as EF1 in
Fig. 4B. We know that they
lower call frequencies (such as VF1 in
Fig. 4A) and we also know that
a lowering of call frequency requires a decrease in motor activity
(Fig. 4A, white arrow).
Assuming purely inhibitory feedback, reduced motor activity can be caused only
by inhibition that is stronger than at rest. The corresponding echo
frequencies above RF can create such stronger inhibition only when sensory
activity levels increase with increasing echo frequencies (white arrow in
Fig. 4B). Conversely, lower
echo frequencies (black arrow in Fig.
4B) exhibit a lower level of sensory activity, leading to less
inhibition of the motor side and thus causing call frequencies to rise (black
arrow in Fig. 4A).
If we assume instead an all-excitatory feedback mechanism (Fig. 4C), the relationship between varying echo frequencies and the resulting changes in sensory activity levels simply have to be reversed to yield the appropriate motor commands (Fig. 4A).
Audio-vocal feedback control during DSC behavior inevitably requires convergence and pooling of frequency information from all frequency channels involved. As a corollary, firing rates in neurons integrating this frequency information become ambiguous: their level of activity is determined by the size of the frequency shift (as deduced above) but also, much as in individual auditory neurons, by the intensity of the echo. Hence, during auditory feedback control, frequency information is at least to a certain degree traded for intensity information and vice versa. This is essential when analyzing the effects we observed while varying intensity levels during stepwise changes in echo frequency (see Fig. 3) in the light of an all-inhibitory (Fig. 4B) or a purely excitatory (Fig. 4C) feedback mechanism. These experiments demonstrated that after both positive and negative steps higher echo intensities caused call frequencies between successive calls to change faster, resulting in shorter time constants of the DSC responses (Fig. 3B,C). However, neither a purely inhibitory nor a purely excitatory scenario is consistent with these results, as outlined below.
If auditory feedback control were purely inhibitory, as assumed in Fig. 4B, louder echoes at any frequency (above or below RF), by pushing the sensory activity to higher levels, would result in stronger inhibition of the motor side over the entire frequency range (below and above RF, respectively). An overall stronger inhibitory effect on the motor side, however, had opposite consequences on the raising and lowering of call frequencies: louder echoes at frequencies above RF would cause call frequencies to drop faster because of stronger inhibition (in Fig. 4A, the new motor activity level would fall below MA1). Louder echoes below RF, however, which also exert more inhibition on the motor side, would result in a slower rise in call frequency (see Fig. 4A: the new motor activity level would fall below MA2 as well). This, however, is contradicted by our experimental results (Fig. 3B,C). Our results are also inconsistent with a purely excitatory feedback mechanism (Fig. 4C), which predicts that louder echoes below RF should accelerate the DSC response whereas echoes above RF should slow it down.
Only an antagonistically acting control mechanism, combining excitatory and inhibitory feedback as depicted in Fig. 4C, is fully consistent with our experimental results. In such a `push/pull' operational mode, inhibitory feedback would originate from a neuronal population encoding for positive Doppler shifts (Fig. 4C, right portion) and excitatory feedback from another neuronal population encoding for negative Doppler shifts (Fig. 4C, left portion). Hence, call frequencies would decrease and increase, respectively, by modulating the motor activity around an intermediate level corresponding to the RF (Fig. 4A).
Indeed, our recent results from pharmacological studies indicate that a
small brainstem area controls DSC behavior via such an
antagonistically acting mechanism utilizing inhibitory feedback from
frequencies above RF mediated by -aminobutyric acid (GABAA)
and excitatory feedback from frequencies below RF mediated by glutamate (AMPA)
(Smotherman and Metzner,
2000
).
`Push/pull' operational modes appear to control a variety of behaviors,
such as compensatory eye movements in both vertebrates and invertebrates
(Moschovakis et al., 1996),
antagonistically acting motor outputs during various forms of locomotion
(Stein et al., 1997
;
Shaw and Kristan, 1999
) and an
electromotor behavior related to orientation and object detection in weakly
electric fish, the `jamming avoidance response' in Eigenmannia
(Metzner, 1993a
). DSC behavior
might therefore reflect general principles of sensory-motor control of motor
outputs. It may even share basic aspects with audio-vocal feedback controlling
the pitch of vocal utterances in other mammals
(Janik and Slater, 1997
;
McCowan and Reiss, 1997
),
including the involuntary response to `pitch-shifted feedback' in humans
(Burnett et al., 1998
;
Houde and Jordan, 1998
;
Jones and Munhall, 2000
).
However small a potential adaptive advantage of compensating for negative
frequency shifts might have been, it is evolutionarily probably more
appropriate to consider that, as long as maintaining a presumably universal
neural basis did not place the system at any disadvantage, there was also no
selective pressure acting to eliminate it.
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Acknowledgments |
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