1. The auditory threshold curve of averaged evoked potentials of
the colliculus inferior in Rhinolophus /errum equinum to pure tone stimulation
from 1 to 100 kHz is presented (Fig. 1). For pure tone frequencies lower than
14 ktIz thresholds steeply rise from 20 to 110 db. The steepness of the acoustical
filter for 83.3 kHz signals and the frequency of the echoes heard by Greater Horseshoe
Bats is accentuated by averaging methods. Because of averaging, evoked
potentials thresholds are lowered by about 20 db compared to those obtained by
non-averaging methods.
2. Prominent off-responses in evoked potentials appear for three stimulus
frequency ranges: 3-10 kHz with a peak at 5 ktIz, 20-40 kHz with a peak at
20 kHz and 80.0-82.6 kHz with a peak at 81.5 kHz (Fig. 2).
3. It is unlikely that beat note frequencies play any role for echolocation.
4. The relevance of these results to echolocation in Horseshoe Bats is discussed,
especially as to Doppler shift information contained in the constant frequency
part of echoes

Neuweiler, Gerhard

Schnitzler, Hans-Ulrich

Schuller, Gerd

English

Universität München: Elektronischen Publikationen

Z. vergl. Physiologie 74, 57-63 (1971) 
9 by Springer-Verlag 1971 
On- and Off-Responses 
in the Inferior Colliculus 
of the Greater Horseshoe Bat to Pure Tones* 
GEICttAI~D NEUWEILEtr GEliD SCHULLEI~, and  HANs-ULI~ICH SCH/qlTZLEI~ 
Zoophysiologisches Institut der Universit~t Tiibingen 
Received May 14, 1971 
Summary. 1. The auditory threshold curve of averaged evoked potentials of 
the colliculus inferior in Rhinolophus /errum equinum to pure tone stimulation 
from 1 to 100 kHz is presented (Fig. 1). For pure tone frequencies lower than 
14 ktIz thresholds steeply rise from 20 to 110 db. The steepness of the acoustical 
filter for 83.3 kHz signals and the frequency of the echoes heard by Greater Horse- 
shoe Bats is accentuated by averaging methods. Because of averaging, evoked 
potentials thresholds are lowered by about 20 db compared to those obtained by 
non-averaging methods. 
2. Prominent off-responses in evoked potentials appear for three stimulus 
frequency ranges: 3-10 kHz with a peak at 5 ktIz, 20-40 kHz with a peak at 
20 kHz and 80.0-82.6 kHz with a peak at 81.5 kHz (Fig. 2). 
3. I t  is unlikely that  beat note frequencies play any role for echolocation. 
4. The relevance of these results to echolocation in Horseshoe Bats is discussed, 
especially as to Doppler shift information contained in the constant frequency 
part of echoes. 
In t roduct ion  
Horseshoe  Ba ts  emi t  long u l t rasonic  o r ien ta t ion  sounds  of cons tan t  
f r equency  wi th  a t e rmina l  f r equency-drop  of a b o u t  14-16 kHz.  F ly ing  
ba t s  lower the  f requency  of the  cons t an t  f requency  p a r t  (CF) b y  an 
a m o u n t  which compensa tes  for Dopp le r  shifts caused b y  the  f l ight  
veloci ty .  The  f requency  is therefore  k e p t  cons tan t  a t  a b o u t  83.3 k H z  
which is the  f requency  of res t ing  ba t s  (Schnitzler ,  1968). A t  this  f requency  
the  a u d i t o r y  th re sho ld  of on-responses  of coll icular  evoked  po ten t i a l s  
has  a m i n i m u m  and  rises s t eep ly  a t  the  frequencies below a n d  above  
(Neuweiler,  1970). This  f i l ter  for 83.3 k H z  s t imul i  m a y  be real ized b y  
per iphera l ,  basf lar  or nervous  processes or combina t ions  of them.  I n  
th is  p a p e r  we r e p o r t  col l ieular  off-responses to  pure  tone  s t imu la t ion  
occurr ing in  res t r i c t ed  f r equency  ranges  which m a y  ind ica te  t ha t ,  a t  
leas t  pa r t i a l ly ,  cen t ra l  nervous  processes are  invo lved  in  the  f i l ter  for 
83.3 kHz .  
* This study was supported by Stiftung Volkswagenwerk, grant No. 110771 
and DFG, grant :No. Va 22/4. 
58 G. Neuweiler, G. Schuller, and H.-U. Sehnitzler: 
The Doppler shift compensation in connection with the acoustical 
filter diminishes the problem of masking of overlapping outgoing pulses 
and returning echoes. According to a theory of J. D. Pye (1960, 1961) 
and L. Kay  (1961, 1962) the overlapping would account for a different 
way of evaluating frequency shifts caused by Doppler effects. In  their 
theory, the simultaneous hearing of emitted sound and returning echo 
would produce a beat note, the frequency of which is proportional to 
the flight velocity of the bat relative to the target. The frequency of the 
beat note may range from a few Hz to 3 kHz. Pye assumes that  the 
source of nonlinearity for creation of beat notes are the middle ear 
muscles. In  that  case the auditory system of Horseshoe Bats should be 
sensitive to low frequency stimuli. We therefore extended the stimulus 
frequency range for threshold measurements in the colliculus inferior 
into the audible range down to 1 kHz. 
Methods 
Auditory evoked potentials from 7 Nembutal-anesthetized Rhinolophus/errum 
equinum were recorded in the eollieulus inferior using Ag-AgCl-eleetrodes. Thresholds 
of on-responses were determined for pure tone stimulation from 1 to 100 kttz. The 
experimental procedure is basically the same as described in Neuweiler (1970). 
For stimulation in the range from 1-20 kHz we used a Valvo AD 1260 M-5 
loudspeaker and for ultrasonic frequencies a condensator loudspeaker of our own 
design. 
For each set of stimulus parameters 100 evoked potentials were averaged by a 
Didae-800 computer (Interteehnique). Stimulus repetition rate was 8-9/see while 
stimulus duration lasted 30 msee with a rise- and fall-time of 2 msec. Stimulus 
intensity is expressed in db re 0.0002 dyn/cm 2. The analysis time for 800 channels 
was 96 msee. Thresholds were measured by lowering the sound intensity in 5 db 
steps and determined by the intensity at which a response was no longer visible. 
The amplitude of the averaged evoked responses was left unealibrated. 
Results 
Threshold.s o/On.Response8 
Compared to the conventional method used in the previous study 
(•euweiler, 1970) the averaging method results in an overall decrease 
of detectable eollicular thresholds for pure tone stimulation of about 
20 db. Fig. 1 shows a representative example of the recorded threshold 
curves. The lowest threshold in the ultrasonic frequency range extends 
to --  5 db as compared to 30-25 db in nonaveraged studies. 
Invariably in all threshold curves a narrowly tuned filter ~or 83.3 kHz 
signals appears with a steeply rising slope for lower frequencies down 
to 81.5 kHz (see inset in Fig. 1). The frequencies of highest and lowest 
thresholds are consistently 81.5-81.8 kHz and 83.3-83.5 kHzrespectively. 
By the averaging method the threshold difference between 81.5 and 
Responses in Inferior Colliculus of Horseshoe Bats 59 
100 
90 
80 
70 
60 
50 
40 
30 
20 
10 
0 
'db re 0.0002dyn/cm 2 
\ 
\ 
\ 
\ 
\ 
\ 
r  ' ' I [ I , I 
. . . .  ' 
c _ _  
: 2 o , ,  , L r  , , , , / 
0 ~ 
80182 81 86 8~kHgzO 
~V 
" / ~  / /  V 
3 4 5 6 8 10 20 30 40 5060 80100kHz 
Fig. 1. Threshold curve of averaged evoked potentials of the inferior colliculus 
in Rhinolophus/errum equinum (RF 5/14/7). Abscissa: stimulus frequency; ordinate: 
threshold in db re 0.0002 dyn/cm 2. Stimulus: pure tone, 30 msec duration, 2 msec 
rise/fall time, 8-9/see repetition rate. Inset: Enlarged section of the threshold curve 
for stimulus-frequencies from 80.0 to 90.0 kHz 
83.3 kHz signals is accentuated compared to those of unaveraged 
responses. The threshold for 81.5 kHz tones always is 50-60 db and 
for 83.3 kHz tones 10-5 db. This amounts to an average threshold slope 
of 40-55 db/1.8 kHz compared to a 33 db /1 .8kHz  slope in former 
experiments (Neuweiler, 1970). At frequencies higher than 83.3-83.5 kHz 
thresholds again rapidly increase but  less steeply than  those for lower 
frequencies. 
Low thresholds of frequencies other than 83.3 kHz are more variable. 
An absolute minimum of threshold for stimuli between 20 and 30 kI tz  
exists in most threshold curves (see Fig. 1). In  two eases however this 
minimum occurred for frequencies between 60 and 70 kHz. Invar iably  
there appears a small maximum of threshold for 40 kI Iz  tones. 
As stimulus frequency is lowered from 20 to 10 kHz thresholds of 
eollieular evoked potentials increase by  20-30 db (see Fig. 1). The low 
thresholds for 10 kHz tones recorded in the previous paper  (Neuweiler, 
1970) most  probably result from stimulus distortions caused by the 
loudspeaker for frequencies below 20 kHz. 
From 8 to 5 kI tz  the threshold curve remains flat at  a high level 
of 60-70 db. For still lower frequencies down to 1 k I lz  the thresholds 
rise again by  25-40 db and reach a value of 110 db which is the highest 
intensity available in our loudspeaker. In  two bats the maximal  intensity 
was not sufficient to elicit any  collicular response for 1 and 2 kHz tones. 
60 G. Neuweiler, G. Schuller, and H.-U. Schnitzler: 
/z_ _',,/_ 
/ ,  
2 3 4 5 6 
!Ji I lllH 
,IJ/ll/I I I IIIIZI 
01,/I i I~J_.,rl i I ,t I I  I I IIIIq 
80 82-84. I 86ki8 I i I IllII 
II IIIII 
I I I 1  LIII I \1 I I/ [1_1 
8 10 12 16 20 30 40 60 80100kHz 
Fig. 2. Amplitude of off-responses in averaged collieular evoked responses of 
Rhinolophus ]errum equinum. Each point is the average of 3 experiments. Abscissa: 
stimulus frequency; ordinate: amplitude of the off-response in arbitrary units. 
Stimulus: pm'e tone, 30 msec duration, 2 msec rise/fall time, intensity 70 db re 
0.0002 dyn/cm 2, 8-9 see repetition rate. Inset: Enlarged section of the amplitude 
cum~e for stimulus frequencies from 80.0 to 90.0 kHz 
If  one interprets thresholds of collicular responses as correlates of 
hearing thresholds, Horseshoe Bats may detect auditory signals in the 
frequency range of 12-5 kHz only at high intensities and frequencies 
below 4 kHz will not be heard under natural conditions. 
OH-Responses 
Off-responses to pure tone stimulation are an uncommon feature in 
the auditory system of mammals. In  bats they only occur in species 
which emit a CF-part in their echolocation pulses (Grinnell, 1970). 
Horseshoe Bats are no exception to Grinnell's statement since at 
certain frequency bands prominent off-responses appear in the evoked 
potentials of the colliculus inferior. Fig. 2 shows the mean amplitude of 
off-responses plotted as a function of stimulus frequency from 3 bats. 
Stimulus intensity was 70 db. There are three distinct maxima of off- 
responses, the first from 3-10 kHz, with a peak at 5 kHz, the second 
from 20 to 40 kHz with peak amplitude at 20 kHz and the third from 80.0 
to 82.6 kHz with peak amplitude at 81.5 kHz. Viewed on a logarithmic 
scale the frequency range for off-responses gets narrower with increasing 
stimulus frequency and the amplitude peak quickly increases from low 
to high frequency range. 
If  one takes the lowest frequency producing a maximal off-response 
as the fundamental one, it seems that  the maxima of off-responses occur 
at harmonics of the basic frequency. 
Responses in Inferior Collieulus of Horseshoe Bats 61 
The most interesting feature of the off-effects again appears in the 
frequency range of the echolocation pulses (see inset in Fig. 2). The 
maximal off-amplitude occurs exactly at  81.5 kHz, the frequency of 
highest threshold for on-responses. With increasing frequency the off- 
responses rapidly decline and reach a minimum at the eehofrequency 
of 83.0-83.3 kHz where threshold of on-responses is minimal. At this 
frequency for very high sound pressure levels only a small off-effect may 
be obtained. For stimulus frequencies from 84-88 kHz the off-responses 
increase again but  never reach the amplitude of those for 81.5 kHz 
stimuli. 
Off-responses may be elicited by stimulus frequencies other than 
those in the three frequency ranges mentioned, but  then extremely 
high intensities have to be applied. For 50 and 60 kHz stimuli we never 
obtained off-responses even at  110 db, the highest intensity available. 
Discussion 
This s tudy confirms and validates the existence of an acoustical 
filter at the frequency of the CF-part of the echo heard by a Greater 
Horseshoe Bat. The significance of this filter for echolocation in cor- 
roboration with Doppler shift compensation has been discussed else- 
where (Neuweiler, 1970). The main points are shortly summarized here: 
Flying bats lower the frequency of the CF-part of the emitted sound 
in order to compensate for Doppler shifts. This frequency therefore 
varies between 81.0 and 83.3 kHz dependent on flight velocity whereas 
the echofrequency is kept constant at  83.3 kHz (Schnitzler, 1968). By 
using a narrowly tuned filter for this echo-frequency of 83.3 kHz, 
collicular thresholds for the CF-part of the echo are very low whereas 
thresholds for the frequencies of the emitted sounds are high (see inset 
in Fig. 1). Thus masking of the echo by ongoing sound emission may be 
avoided. 
Doppler shifts are most prominent for echoes returning from flight 
direction (0~ They decrease by the cosinus for other angles of incidence 
and are zero for echoes returning perpendicular to flight direction. Since 
the emitted frequency is regulated for maximal Doppler shifts in the 
echoes, i.e. for echoes from 0~ the frequencies of the echoes 
from greater angles are lower than 83.3 kHz and fall in an area of high 
hearing thresholds. Therefore the acoustical filter results in a preferred 
processing of echoes returning from straight ahead. 
The most surprising feature of the Horseshoe Bat's threshold curve 
is not the low threshold for the echo-frequency at  83.3 kHz but  the 
very high one for the frequency range of the emitted sounds at  81.5 kItz. 
This "sharply t uned"  frequency range of high thresholds separates 
62 G. Neuweiler, G. Schuller, and It.-U. Schnitzler: 
hearing of the CF-part of the echoes from hearing of any lower frequency. 
How is this high threshold established ? Since it  is so narrowly tuned to 
81.5 kHz (Q-value 81.5), it  is tempting to postulate neural inhibition. 
If one considers off-responses as rebound from inhibition this postulate 
is strengthened by the very fact that  the most prominent off-responses 
exactly appear for frequencies around 81.5 kHz whereas for 83.3 kHz 
off-effects reach a minimum or are absent. A drawback, however, is that  
off-responses also occur at  20 and 5 kHz where neural inhibition seems 
to be unnecessary. 
Grinnell (1970) described prominent off-responses in Chilonycteris 
rubiginosa, a bat emitting a long CF-part of 64 kHz. Just  below the 
frequency of the bat 's greatest sensitivity a sharply tuned off-maximum 
at 60-62 kHz exists which again coincides with a maximum of threshold 
for on-responses. As Chilonycteris rubiginosa compensates for Doppler- 
shifts (Schnitzler, 1970), it  appears that  this bat also has an acoustical 
filter tuned to its echo frequency of 64 kHz. 
Grinncil interprets the off-responses of the CF-part as time markers 
which enable a bat  emitting long pure tone pulses to measure the time 
difference between sound emission and echo for detection of target 
range. This interpretation does certainly not apply to Horseshoe Bats 
since in these animals there exists an absolute minimum of off-responses 
for the very echo frequency of 83.3 kHz (see inset in Fig. 2). On the 
basis of the available experimental data we consider off-responses in 
the colliculus inferior to pure tone stimulation as a manifestation of 
neural inhibition. 
Information contained in Doppler shifts may be carried by beat 
notes produced by simultaneous hearing of emitted frequency and the 
Doppler shifted echo (Pye, 1960, 1961 ; Kay, 1961, 1962). For Horseshoe 
Bats this theory seemed plausible since emitted echolocation sound and 
returning echo overlap for target ranges within about 10 m. Pye considers 
this to be caused by nonlinearity in the middle ear (muscle activity) 
which produces a difference tone from the two primary frequencies. In 
this case Horseshoe Bats should have low hearing thresholds for fre- 
quencies of a few Hz to 3 kHz. As Fig. 1 shows thresholds in fact are 
very high at  low frequencies. Only when the site of nonlinearity is 
shifted to the basilar membrane (Tonndorf, 1959) hearing of beat note 
frequencies seems possible. If the insensitivity to low frequencies, as 
shown in the threshold curve, is caused by a high pass filter in the sound 
transmitting system of the middle ear, this barrier for low frequencies 
may be overcome by beat notes produced at the basilar membrane. 
According to Tonndorf (1959) similar high intensities of the primary 
frequencies are required if a beat note is to be produced at the basilar 
Responses in Inferior Colliculus of Horseshoe Bats 63 
membrane .  U n d e r  these specific condi t ions  only  hear ing of bea t  notes  
seems possible  a t  al l  in Horseshoe Bats .  
The  high thresholds  for low pure  tone  frequencies  which res t r ic t  the  
hear ing  of bea t  notes  to  h igh ly  specified condi t ions ,  the  mere  exis tence 
of the  Dopp le r  effect compensa t ion  and  the  e labora te  acoust ica l  f i l ter  
for  echo frequencies a t  83.3 k H z  make  i t  un l ike ly  t h a t  bea t  note  fre- 
quencies are  processed for echolocat ion.  
References 
Grinnell, A. D.: Comparative auditory neurophysiology of neotropical bats em- 
ploying different echolocation signals. Z. vergl. Physiol. 68, 117-153 (1970). 
Kay, L.: Perception of distance in animal echolocation. Nature (Lond.) 190, 
361-362 (1961). 
- -  A plausible theory of the bat 's echolocation acuity. Animal Behav. 10, 34-41 
(1962). 
Neuweiler, G. : Neurophysiologisehe Untersuehungen zum Echoortungssystem der 
GroBen Hufeisennase Rhinolophus/errum equinum. Z. vergl. Physiol. 67, 273-306 
(1970). 
Pye, J. D.: A theory of echolocation by bats. J. Laryng. Otol. 74, 718-729 (1960). 
- -  Perception of distance in animal echolocation. Nature (Lond.) 190, 362-363 
(1961). 
Schnitzler, H. U. : Die Ultraschall-Ortungslaute der Hufeisen-Flederm~use in ver- 
schiedenen Orientierungssituationen. Z. vergl. Physiol. 57, 376-408 (1968). 
- -  Echoortung bei der ]?ledermaus Chilonycteris rubiginosa. Z. vergl. Physiol. 68, 
25-38 (1970). 
Tonndoff, J. : Beats in cochlear models. J. acoust. Soe. Amer. 31, 608-619 (1959). 
Dr. Gerhard Neuweiler 
Zoophysiologisches Institut der Universitiit 
BRD-7400 Tfibingen, KSllestr. 23 
Germany 


On- and Off-Responses in the Inferior Colliculus of the Greater Horseshoe Bat to Pure Tones

Open Access LMU ( Ludwig-Maximilians-Univ. München)

Z. vergl. Physiologie 74, 57-63 (1971) 9 by Springer-Verlag 1971 On- and Off-Responses in the Inferior Colliculus of the Greater Horseshoe Bat to Pure Tones* GEICttAI~D NEUWEILEtr GEliD SCHULLEI~, and HANs-ULI~ICH SCH/qlTZLEI~ Zoophysiologisches In titut der Universit~t Tiibingen Received May 14, 1971 Summary. 1. The auditory threshold curve of averaged evoked potentials of the colliculus inferior in Rhinolophus /errum equinum to pure tone stimulation from 1 to 100 kHz is presented (Fig. 1). For pure tone frequencies lower than 14 ktIz thresholds steeply rise from 20 to 110 db. The steepness of the acoustical filter for 83.3 kHz signals and the frequency of the echoes heard by Greater Horse- shoe Bats is accentuated by averaging methods. Because of averaging, evoked potentials thresholds are lowered by about 20 db compared to those obtained by non-averaging methods. 2. Prominent off-responses in evoked potentials appear for three stimulus frequency ranges: 3-10 kHz with a peak at 5 ktIz, 20-40 kHz with a peak at 20 kHz and 80.0-82.6 kHz with a peak at 81.5 kHz (Fig. 2). 3. I t  is unlikely that beat note frequencies play any role for echolocation. 4. The relevance of these results to echolocation i Horseshoe Bats is discussed, especially as to Doppler shift information contained in the constant frequency part of echoes. Introduction Horseshoe Bats emit  long ultrasonic or ientat ion sounds of constant frequency with a terminal  f requency-drop of about  14-16 kHz. F ly ing bats lower the frequency of the constant frequency par t  (CF) by an amount  which compensates for Doppler  shifts caused by  the fl ight velocity. The frequency is therefore kept  constant at  about  83.3 kHz which is the frequency of resting bats (Schnitzler, 1968). At  this frequency the audi tory  threshold of on-responses of coll icular evoked potent ia ls  has a min imum and rises steeply at  the frequencies below and above (Neuweiler, 1970). This f i lter for 83.3 kHz  st imuli  may be realized by  peripheral,  basflar or nervous processes or combinat ions of them. In  this paper  we report  coll ieular off-responses to pure tone st imulat ion occurring in restr icted frequency ranges which may indicate that ,  at  least part ia l ly,  central  nervous processes are involved in the fi lter for 83.3 kHz. * This study was supported by Stiftung Volkswagenwerk, grant No. 110771 and DFG, grant :No. Va 22/4. 58 G. Neuweiler, G. Schuller, and H.-U. Sehnitzler: The Doppler shift compensation i connection with the acoustical filter diminishes the problem of masking of overlapping outgoing pulses and returning echoes. According to a theory of J. D. Pye (1960, 1961) and L. Kay (1961, 1962) the overlapping would account for a different way of evaluating frequency shifts caused by Doppler effects. In their theory, the simultaneous hearing of emitted sound and returning echo would produce a beat note, the frequency of which is proportional to the flight velocity of the bat relative to the target. The frequency of the beat note may range from a few Hz to 3 kHz. Pye assumes that the source of nonlinearity for creation of beat notes are the middle ear muscles. In that case the auditory system of Horseshoe Bats should be sensitive to low frequency stimuli. We therefore xtended the stimulus frequency range for threshold measurements in the colliculus inferior into the audible range down to 1 kHz. Methods Auditory evoked potentials from 7 Nembutal-anesthetized Rhinolophus/errum equinum were recorded in the eollieulus inferior using Ag-AgCl-eleetrodes. Thresholds of on-responses were determined for pure tone stimulation from 1 to 100 kttz. The experimental procedure isbasically the same as described inNeuweiler (1970). For stimulation in the range from 1-20 kHz we used a Valvo AD 1260 M-5 loudspeaker and for ultrasonic frequencies a condensator loudspeaker of our own design. For each set of stimulus parameters 100 evoked potentials were averaged by a Didae-800 computer (Interteehnique). Stimulus repetition rate was 8-9/see while stimulus duration lasted 30 msee with a rise- and fall-time of 2 msec. Stimulus intensity is expressed in db re 0.0002 dyn/cm 2.The analysis time for 800 channels was 96 msee. Thresholds were measured by lowering the sound intensity in 5 db steps and determined by the intensity at which a response was no longer visible. The amplitude of the averaged evoked responses was left unealibrated. Results Threshold.s o/On.Response8 Compared to the conventional method used in the previous study (•euweiler, 1970) the averaging method results in an overall decrease of detectable ollicular thresholds for pure tone stimulation of about 20 db. Fig. 1 shows a representative example of the recorded threshold curves. The lowest threshold in the ultrasonic frequency range extends to -- 5 db as compared to 30-25 db in nonaveraged studies. Invariably in all threshold curves a narrowly tuned filter ~or 83.3 kHz signals appears with a steeply rising slope for lower frequencies down to 81.5 kHz (see inset in Fig. 1). The frequencies of highest and lowest thresholds are consistently 81.5-81.8 kHz and 83.3-83.5 kHzrespectively. By the averaging method the threshold difference between 81.5 and Responses in Inferior Colliculus of Horseshoe Bats 59 100 90 80 70 60 50 40 30 20 10 0 'db re 0.0002dyn/cm 2 \ \ \ \ \ \ r  ' ' I [ I , I . . . .  ' c__  :2o , ,  , L r  , , , , / 0 ~ 80182 81 86 8~kHgzO ~V " /~ / /  V 3 4 5 6 8 10 20 30 40 5060 80100kHz Fig. 1. Threshold curve of averaged evoked potentials of the inferior colliculus in Rhinolophus/errum equinum (RF 5/14/7). Abscissa: stimulus frequency; ordinate: threshold in db re 0.0002 dyn/cm 2.Stimulus: pure tone, 30 msec duration, 2 msec rise/fall time, 8-9/see repetition rate. Inset: Enlarged section of the threshold curve for stimulus-frequencies from 80.0 to 90.0 kHz 83.3 kHz signals is accentuated compared to those of unaveraged responses. The threshold for 81.5 kHz tones always is 50-60 db and for 83.3 kHz tones 10-5 db. This amounts to an average threshold slope of 40-55 db/1.8 kHz compared to a 33 db/1.8kHz slope in former experiments (Neuweiler, 1970). At frequencies higher than 83.3-83.5 kHz thresholds again rapidly increase but less steeply than those for lower frequencies. Low thresholds of frequencies other than 83.3 kHz are more variable. An absolute minimum of threshold for stimuli between 20 and 30 kItz exists in most threshold curves (see Fig. 1). In two eases however this minimum occurred for frequencies between 60 and 70 kHz. Invariably there appears a small maximum of threshold for 40 kI Iz tones. As stimulus frequency is lowered from 20 to 10 kHz thresholds of eollieular evoked potentials increase by 20-30 db (see Fig. 1). The low thresholds for 10 kHz tones recorded in the previous paper (Neuweiler, 1970) most probably result from stimulus distortions caused by the loudspeaker for frequencies below 20 kHz. From 8 to 5 kItz the threshold curve remains flat at a high level of 60-70 db. For still lower frequencies down to 1 kI lz  the thresholds rise again by 25-40 db and reach a value of 110 db which is the highest intensity available in our loudspeaker. In two bats the maximal intensity was not sufficient o elicit any collicular response for 1 and 2 kHz tones. 60 G. Neuweiler, G. Schuller, and H.-U. Schnitzler: /z_ _',,/_ / ,  2 3 4 5 6 !Ji I lllH ,IJ/ll/I I I IIIIZI 01,/I i I~J_.,rl i I ,t I I  I I IIIIq 80 82-84. I 86ki8 I i I IllII II IIIII I I I 1  LIII I \1 I I/ [1_1 8 10 12 16 20 30 40 60 80100kHz Fig. 2. Amplitude of off-responses in averaged collieular evoked responses ofRhinolophus ]errum equinum. Each point is the average of 3 experiments. Abscissa: stimulus frequency; ordinate: amplitude of the off-response in arbitrary units. Stimulus: pm'e tone, 30 msec duration, 2 msec rise/fall time, intensity 70 db re 0.0002 dyn/cm 2,8-9 see repetition rate. Inset: Enlarged section of the amplitude cum~e for stimulus frequencies from 80.0 to 90.0 kHz If one interprets thresholds of collicular responses as correlates of hearing thresholds, Horseshoe Bats may detect auditory signals in the frequency range of 12-5 kHz only at high intensities and frequencies below 4 kHz will not be heard under natural conditions. OH-Responses Off-responses to pure tone stimulation are an uncommon feature in the auditory system of mammals. In bats they only occur in species which emit a CF-part in their echolocation pulses (Grinnell, 1970). Horseshoe Bats are no exception to Grinnell's statement since at certain frequency bands prominent off-responses appear in the evoked potentials of the colliculus inferior. Fig. 2 shows the mean amplitude of off-responses plotted as a function of stimulus frequency from 3 bats. Stimulus intensity was 70 db. There are three distinct maxima of off- responses, the first from 3-10 kHz, with a peak at 5 kHz, the second from 20 to 40 kHz with peak amplitude at 20 kHz and the third from 80.0 to 82.6 kHz with peak amplitude at 81.5 kHz. Viewed on a logarithmic scale the frequency range for off-responses gets narrower with increasing stimulus frequency and the amplitude peak quickly increases from low to high frequency range. If one takes the lowest frequency producing a maximal off-response as the fundamental one, it seems that the maxima of off-responses occur at harmonics of the basic frequency. Responses in Inferior Collieulus of Horseshoe Bats 61 The most interesting feature of the off-effects again appears in the frequency range of the echolocation pulses (see inset in Fig. 2). The maximal off-amplitude occurs exactly at 81.5 kHz, the frequency of highest threshold for on-responses. With increasing frequency the off- responses rapidly decline and reach a minimum at the eehofrequency of 83.0-83.3 kHz where threshold of on-responses i minimal. At this frequency for very high sound pressure levels only a small off-effect may be obtained. For stimulus frequencies from 84-88 kHz the off-responses increase again but never reach the amplitude of those for 81.5 kHz stimuli. Off-responses may be elicited by stimulus frequencies other than those in the three frequency ranges mentioned, but then extremely high intensities have to be applied. For 50 and 60 kHz stimuli we never obtained off-responses ven at 110 db, the highest intensity available. Discussion This study confirms and validates the existence of an acoustical filter at the frequency of the CF-part of the echo heard by a Greater Horseshoe Bat. The significance of this filter for echolocation i  cor- roboration with Doppler shift compensation has been discussed else- where (Neuweiler, 1970). The main points are shortly summarized here: Flying bats lower the frequency of the CF-part of the emitted sound in order to compensate for Doppler shifts. This frequency therefore varies between 81.0 and 83.3 kHz dependent on flight velocity whereas the echofrequency is kept constant at 83.3 kHz (Schnitzler, 1968). By using a narrowly tuned filter for this echo-frequency of 83.3 kHz, collicular thresholds for the CF-part of the echo are very low whereas thresholds for the frequencies of the emitted sounds are high (see inset in Fig. 1). Thus masking of the echo by ongoing sound emission may be avoided. Doppler shifts are most prominent for echoes returning from flight direction (0~ They decrease by the cosinus for other angles of incidence and are zero for echoes returning perpendicular to flight direction. Since the emitted frequency is regulated for maximal Doppler shifts in the echoes, i.e. for echoes from 0~ the frequencies of the echoes from greater angles are lower than 83.3 kHz and fall in an area of high hearing thresholds. Therefore the acoustical filter results in a preferred processing of echoes returning from straight ahead. The most surprising feature of the Horseshoe Bat's threshold curve is not the low threshold for the echo-frequency at 83.3 kHz but the very high one for the frequency range of the emitted sounds at 81.5 kItz. This "sharply tuned" frequency range of high thresholds eparates 62 G. Neuweiler, G. Schuller, and It.-U. Schnitzler: hearing of the CF-part of the echoes from hearing of any lower frequency. How is this high threshold established ? Since it is so narrowly tuned to 81.5 kHz (Q-value 81.5), it is tempting to postulate neural inhibition. If one considers off-responses as rebound from inhibition this postulate is strengthened by the very fact that the most prominent off-responses exactly appear for frequencies around 81.5 kHz whereas for 83.3 kHz off-effects reach a minimum or are absent. A drawback, however, is that off-responses also occur at 20 and 5 kHz where neural inhibition seems to be unnecessary. Grinnell (1970) described prominent off-responses in Chilonycteris rubiginosa, a bat emitting a long CF-part of 64 kHz. Just below the frequency of the bat's greatest sensitivity a sharply tuned off-maximum at 60-62 kHz exists which again coincides with a maximum of threshold for on-responses. As Chilonycteris rubiginosa compensates for Doppler- shifts (Schnitzler, 1970), it appears that this bat also has an acoustical filter tuned to its echo frequency of 64 kHz. Grinncil interprets the off-responses of the CF-part as time markers which enable a bat emitting long pure tone pulses to measure the time difference between sound emission and echo for detection of target range. This interpretation does certainly not apply to Horseshoe Bats since in these animals there exists an absolute minimum of off-responses for the very echo frequency of 83.3 kHz (see inset in Fig. 2). On the basis of the available experimental data we consider off-responses in the colliculus inferior to pure tone stimulation as a manifestation of neural inhibition. Information contained in Doppler shifts may be carried by beat notes produced by simultaneous hearing of emitted frequency and the Doppler shifted echo (Pye, 1960, 1961 ; Kay, 1961, 1962). For Horseshoe Bats this theory seemed plausible since emitted echolocation sound and returning echo overlap for target ranges within about 10 m. Pye considers this to be caused by nonlinearity in the middle ear (muscle activity) which produces a difference tone from the two primary frequencies. In this case Horseshoe Bats should have low hearing thresholds for fre- quencies of a few Hz to 3 kHz. As Fig. 1 shows thresholds in fact are very high at low frequencies. Only when the site of nonlinearity is shifted to the basilar membrane (Tonndorf, 1959) hearing of beat note frequencies eems possible. If the insensitivity to low frequencies, as shown in the threshold curve, is caused by a high pass filter in the sound transmitting system of the middle ear, this barrier for low frequencies may be overcome by beat notes produced at the basilar membrane. According to Tonndorf (1959) similar high intensities of the primary frequencies are required if a beat note is to be produced at the basilar Responses in Inferior Colliculus of Horseshoe Bats 63 membrane.  Under  these specific condit ions only hearing of beat  notes seems possible at  all in Horseshoe Bats. The high thresholds for low pure tone frequencies which restr ict  the hearing of beat  notes to highly specified conditions, the mere existence of the Doppler effect compensat ion and the elaborate acoustical f i lter for echo frequencies at  83.3 kHz make it unl ikely that  beat  note fre- quencies are processed for echolocation. References Grinnell, A. D.: Comparative auditory neurophysiology of neotropical bats em- ploying different echolocation signals. Z. vergl. Physiol. 68, 117-153 (1970). Kay, L.: Perception of distance in animal echolocation. Nature (Lond.) 190, 361-362 (1961). - -  A plausible theory of the bat's echolocation acuity. Animal Behav. 10, 34-41 (1962). Neuweiler, G. : Neurophysiologisehe Untersuehungen zum Echoortungssystem der GroBen Hufeisennase Rhinolophus/errum equinum. Z vergl. Physiol. 67, 273-306 (1970). Pye, J. D.: A theory of echolocation by bats. J. Laryng. Otol. 74, 718-729 (1960). - -  Perception of distance in animal echolocation. Nature (Lond.) 190, 362-363 (1961). Schnitzler, H. U. : Die Ultraschall-Ortungslaute der Hufeisen-Flederm~use in ver- schiedenen Orientierungssituationen. Z. vergl. Physiol. 57, 376-408 (1968). - -  Echoortung bei der ]?ledermaus Chilonycteris rubiginosa. Z. vergl. Physiol. 68, 25-38 (1970). Tonndoff, J. : Beats in cochlear models. J. acoust. Soe. Amer. 31, 608-619 (1959). Dr. Gerhard Neuweiler Zoophysiologisches In titut der Universitiit BRD-7400 Tfibingen, KSllestr. 23 Germany 

A plausible theory of the bat's echolocation acuity.

A theory of echolocation by bats.

Beats in cochlear models.

Comparative auditory neurophysiology of neotropical bats employing different echolocation signals.

Die Ultraschall-Ortungslaute der Hufeisen-Flederm~use in verschiedenen Orientierungssituationen.

Echoortung bei der ]?ledermaus Chilonycteris rubiginosa.

Neurophysiologisehe Untersuehungen zum Echoortungssystem der GroBen Hufeisennase Rhinolophus/errum equinum.

Perception of distance in animal echolocation.

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On- and Off-Responses in the Inferior Colliculus of the Greater Horseshoe Bat to Pure Tones

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