Download Long rise times of sound pulses in grasshopper songs improve the

J Comp Physiol A (1993) 173:425-434
Journal of
Comparative
h iok, gy A
Neu~'al,
and
9 Springer-Verlag 1993
Long rise times of sound pulses in grasshopper songs improve the
directionality cues received by the CNS from the auditory receptors
R. Krahe, B. Ronacher
Institut ffir Zoologie II, Universit~it Erlangen, Staudtstrasse 5, D-91058 Erlangen, Germany
Accepted: 2 July 1993
Abstract. Auditory receptors of the locust (Locusta migratoria) were investigated with respect to the directionality
cues which are present in their spiking responses, with
special emphasis on how directional cues are influenced
by the rise time of sound signals. Intensity differences
between the ears influence two possible cues in the receptor responses, spike count and response latency. Variation in rise time of sound pulses had little effect on the
overall spike count; however, it had a substantial effect
on the temporal distribution of the receptor's spiking response, especially on the latencies of first spikes. In particular, with ramplike stimuli the slope of the latency vs.
intensity curves was steeper as compared to stimuli with
steep onsets (Fig. 3). Stimuli with flat ramplike onsets
lead to an increase of the latency differences of discharges
between left and right tympanic receptors. This type of
ramplike stimulus could thus facilitate directional hearing. This hypothesis was corroborated by a Monte Carlo
simulation in which the probability of incorrect directional decisions was determined on the basis of the receptor latencies and spike counts. Slowly rising ramps significantly improved the decisions based on response latency, as compared to stimuli with sudden onsets (Fig. 4).
These results are compared to behavioural results obtained with the grasshopper Ch. biguttulus. The stridulation signals of the females of this species consist of ramplike pulses, which could be an adaptation to facilitate
directional hearing of phonotactically approaching
males.
Key words: Grasshoppers - Auditory receptors - Directional hearing - Envelope rise time
Abbreviations: HFR, high frequency receptor; ILD, interaural level
difference; LFR, low frequency receptor; SPL, sound pressure level;
WN, white noise
Correspondence to: Dr. B. Ronacher
Introduction
In many grasshopper species acoustic communication
guides the meeting of sexual partners. It plays a key role
in preventing interspecific hybridization. The animals
have to solve two basic problems, that is, first to recognize a conspecific's song, and then to localize the potential mate. In the grasshopper Chorthippus biguttulus both
sexes stridulate, and it is mainly the task of the males to
localize and to approach a rather stationary female, on
the basis of the female's response song (for reviews, see
Elsner and Popov 1978; von Helversen and yon Helversen 1987). The songs of males and females show the
same basic pattern but differ in the rise time of sound
pulses (von Helversen and von Helversen 1983; von Helversen 1993). The song of a male consists of sound pulses
with very short rise times (in most cases less than 1 ms).
In contrast, the female's song consists of sound pulses
that rise and fall slowly (rise times of 4-7 ms, Fig. lb).
This difference in the steepness of ramps is a decisive cue
for determining a conspecific's sex, and Ch. biguttulus
males show phonotactic behaviour only to signals with
slowly rising ramps (von Helversen 1993).
Males probably can only 'lateralize' a sound source,
i.e. they determine whether the sound source is located on
their left or on their right side (Rheinlaender 1984; von
Helversen and Rheinlaender 1988). The phonotactic approach is based on a repetition of such left/right decisions. Because males are small (distance between the ears
less than 2 mm), it is very unlikely that they can evaluate
the physical interaural time differences (differences of 5-6
~ts at most). Instead, they must rely on interaural level
differences (ILD) that result from the diffraction of sound
waves around the body and the pressure gradient properties of their ears (for reviews see Michelsen 1979, 1983;
Lewis 1983). In detecting ILDs as small as 0.5 dB (yon
Helversen and Rheinlaender 1988), however, the
grasshopper males are superior to most vertebrates. A
difference of only 2 dB allows an errorless decision towards the louder side (von Helversen and Rheinlaender
1988).
426
R. Krahe, B. Ronacher: Directionality cues in grasshopper's auditory receptor responses
I L D s between the two ears have a twofold effect u p o n
the t y m p a n i c receptor discharges: (i) The receptors of the
ear stimulated with lower intensity will respond with a
lower spike rate. (ii) In addition, the latency of the first
spike will be increased, due to the intensity dependence of
the receptor's latency ( M 6 r c h e n et al. 1978). In principle,
the C N S of the animals might evaluate b o t h cues for
directional hearing, spike c o u n t differences as well as response latency (see M 6 r c h e n et al. 1978; M 6 r c h e n 1980;
Rheinlaender and M 6 r c h e n 1979; Rheinlaender and
R 6 m e r 1980). Since the animals have no knowledge
a b o u t the stimulus onset apart from their receptor responses, they c a n n o t determine latency differences but
rather physiological time differences. N o t w i t h s t a n d i n g
this reservation we will use the widely used term "latency
difference". Behavioural tests have s h o w n that grasshoppers are indeed able to use artificially generated - interaural time differences (without I L D ) as a cue for orientation (yon Helversen and v o n Helversen 1983; von Helversen and Rheinlaender 1988). It was also possible to
d e m o n s t r a t e time-intensity trading in behavioural tests
(D. von Helversen, pers. comm.).
As the males d e p e n d on the female's stridulation signals for localizing the s o u n d source, this study addressed
the question of whether the shape of the female's signal,
with its slowly rising ramps, could improve neuronal cues
used for directional hearing. At first glance this appears
counterintuitive, because the temporal precision of the
spiking response p r o b a b l y would be reduced as c o m pared to rectangularly m o d u l a t e d signals. However, as
suggested by A d a m (1977), a slowly rising signal could
indeed be a d v a n t a g e o u s by virtue of p r o d u c i n g an additional gain in latency difference between the ears (shown
schematically in Fig. la).
The o u t s t a n d i n g precision of s o u n d lateralization of
Ch. biguttulus males, of course, must have its basis in the
directionality cues which are present in the responses of
a u d i t o r y receptors from left and right ear. As a first step
t o w a r d s u n d e r s t a n d i n g the capacities for directional
hearing of grasshoppers, one has to assess quantitatively
the directional cues present in receptor cell responses to
different shapes of the s o u n d signals, as are found in the
c o m m u n i c a t i o n signals.
In this study we used M o n t e Carlo simulations with
data from recordings from single a u d i t o r y receptors to
investigate the possible contributions of response latency
and spike c o u n t cues to directional hearing.
Material and methods
Animals. The animals used in the experiments were locusts (Locusta
migratoria), preferentially males, which were obtained from a commercial supplier. The locust's auditory receptors are used as a model system for the receptors of Ch. biguttulus (see Discussion).
Electrophysiological recordings and stimulation apparatus. The animals were briefly anaesthetized with CO2 and were attached to a
free-standing holder (thickness 4 mm) by a wax-resin mixture.
Head, legs, wings and gut were removed. The thorax was opened
dorsally and the metathoracic ganglion was exposed and partially
desheathed. In most experiments the ganglion was stabilized by
ipsi
-~--
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threshold
......
a
b
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50
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Fig. 1. a Schematic demonstration of the effects of stimulus rise time
on latencies of ipsilateral and contralateral receptors. Dotted lines
indicate an hypothetical receptor's threshold, arrows indicate crossing of threshold by the rising intensities of stimuli, b Pulse shape in
stridulation signals of male (upper) and female (lower) Ch. biguttulus.
Scale bar 50 ms. (Courtesy of D. and O. von Helversen). e Frequency
spectra of left and right speaker
minute needles. The whole torso was filled with locust Ringer solution (Pearson and Robertson 1981).
The experiments were performed in an anechoic Faraday-cage
at room temperature (22-25~ The recorded signals were amplified by a LIST LM-1 electrode amplifier and were stored on magnetic tape (RACAL store 4DS). The stimuli were delivered via two
MOTOROLA speakers (PH10, 2.5-40 kHz) located 35 cm from the
preparation on the left and right side. A computer (AIM 65,
ROCKWELL) modulated the amplitudes of the white noise (WN;
Fa. NOIZEG, 100 Hz-100 kHz) or sine wave stimuli. Sound intensities were adjusted with a Briiel & Kj~ier condenser microphone
(1/2 inch) located at the site of the preparation and with a Brfiel &
Kjfier measuring amplifier type 2209, and are given in dB re 2 • l0 s
N/m 2 (SPL). Figure lc shows the frequency spectra of both speakers. For further details see Stumpner and Ronacher (1991).
R. Krahe, B. Ronacher: Directionality cues in grasshopper's auditory receptor responses
Intracellular or quasi-intracellular recordings were made with
thin-walled borosilicate-glass microelectrodes, whose tips were
filled with a 3-5% solution of Lucifer Yellow (ALDRICH) in 0.5 M
LiCk After an experiment the thoracic ganglia were fixed in 4%
paraformaldehyde, dehydrated and cleared in methylsalicylate. The
wholemount with the stained cell was viewed under a fluorescence
microscope, photographed and drawn via a drawing tube.
Auditory receptor fibres were recorded at the entrance of nerve
6 into the metathoracic ganglion complex. After penetration of a
fibre, thresholds to W N and sine wave stimuli (2-25 kHz) were
monitored. Receptors were classified according to R6mer's (1976)
criteria. In order to compare thresholds with R6mer's data,
thresholds were determined using rectangularly modulated stimuli
(100 ms; WN or sinus). For all further tests sawtooth-shaped stimuli
(WN) were presented, each 10 ms in duration, with an interval of
100 ms. Two stimulus types were used: one had the shape of a rising
ramp, with steep cutoff, the second was a 'mirror image', i.e. it had
a sudden onset and declined gradually (cf. insets in Fig. 2a). These
two stimuli were chosen in order to have equal energy and frequency content. The shape and spectra of the stimuli as produced by the
loudspeakers were controlled in microphone recordings and subsequent signal analysis. The power spectra of the two signals were
virtually indistinguishable. The rise time of the steep onset was less
than 0.5 ms. Intensities were varied in 5 dB steps, beginning at 5 dB
or 10 dB, up to 40 dB above the receptor's threshold. Fifty stimuli
of each type were presented at each intensity. If possible the same
stimulation sequence was repeated via the loudspeaker located contralateral to the recording site. In some experiments longer 'song
models' were used that were composed of 6 'syllables' separated by
pauses of 25 ms to mimic stimuli used in behavioural experiments
(yon Helversen, pers. comm.). Each 'syllable' consisted of six 10
ms-pulses, either with a rising ramp, or with a steep onset and
falling ramp (same as above).
Data evaluation. The recorded signals were transferred to a personal
computer (Tandon AT 386 DX) via an AD-converter (DATA
T R A N S L A T I O N DT 2821) and the program T U R B O L A B
(STEMMER), and further analyzed with the program N E U R O LAB (Hedwig and Knepper 1992). The results are shown in form of
latency diagrams and post-stimulus-time histograms.
Monte Carlo simulations. In order to quantify the directional cues
present in the responses of a single pair of receptor cells, we compared latencies and spike counts for stimulation with ipsilateral vs.
contralateral sound incidence (90 ~ vs. 270~ The procedure shall be
exemplified for the evaluation of response latency: The basis for a
Monte Carlo simulation were two data sets of latencies of the first
spikes, which were obtained at a given intensity (50 stimulus presentations for both directions, 90 ~ and 270~ Then one value out of 50
was randomly drawn from each of these two latency distributions,
and the two values were compared. If the ipsi-latency was larger
than the contra-latency this was scored as an 'error', if it was
smaller, it was counted as 'correct'. There were also cases where the
two values were exactly the same (within the limits of acuity of the
data sampling (50 gs); see Discussion). This would correspond to an
undetermined situation. One half of the 'undetermined cases' was
added to the errors. These cases were very rare for latency evaluation, and did not influence the results. This procedure was repeated
1000 times, and the 'error' probabilities were assessed on this basis
(see Figs. 4, 5).
A similar evaluation was performed for the spike count data. An
'error' was assumed if the ipsi-spike count (spikes/stimulus) was
smaller than the contra-spike count. With these data there was a
higher probability of the two values being equal, which would lead
to an undetermined situation. Again, one half of the undetermined
cases was added to the errors (cf. also Rheinlaender and R6mer
1980).
The ILDs found in behaviourat tests with Ch. biguttulus for ipsi
vs. contra stimulation with natural signals are 7-9 dB (yon Helversen 1984). However, a 90 ~ incidence of sound is the maximum,
and a rather unlikely situation for localizing a sound source. More-
427
over, grasshoppers can use much smaller ILDs for a correct lateralization (see Introduction). We therefore also simulated smaller angles of sound incidence by comparing responses at smaller ILDs.
Such values were obtained from the curves for ipsilateral stimulation by comparing, for example, latency (or spike count) data sets 5
dB apart from each other. In order to simulate even smaller ILDs
of 1 or 2 dB (Figs. 4, 6), we obtained data sets by interpolation
between measured data sets. To obtain the latency values, we linearly interpolated between the mean values of the measured data sets
and moved the data set of the lower intensity along this axis towards the data set of the higher intensity. The generation of intermediate spike count distributions is more complicated. One has to
generate new sets of whole numbers normally distributed around
the linearly interpolated mean values.
These simulations assumed that a comparison would take place
between only two receptors from two ears with identical characteristics. In the next step, error probabilities were calculated on the
basis of the evaluation of several parallel receptors (Fig. 6). The
basis for these calculations were the data from 6 receptor cells that
were recorded on one side in one animal. From this pool for example 15 latency values were drawn randomly from the 6 distributions
at the higher and at the lower intensity (with the constraint that
intensity-pairs from the same distribution were compared), and for
each pair of latencies it was determined whether it would lead to a
'correct' or a 'wrong' decision. If the majority of decisions were
correct this was counted as a correct decision of the animal. This
procedure was repeated 1000 times. In order to reduce the chances
of equal numbers of correct and wrong decisions (and therefore
undetermined situations), we present data for odd numbers of receptors (see Fig. 6). Results were similar for even numbers, if the
undetermined situations were partitioned 50:50 between correct
and wrong decisions.
Results
Receptor responses
I n o r d e r to c o m p a r e s t i m u l i o f e q u a l e n e r g y a n d f r e q u e n cy c o n t e n t , o n l y t h e r e s p o n s e s to " t r i a n g u l a r l y - s h a p e d "
s t i m u l i are p r e s e n t e d . T h e i n t e n s i t y r e s p o n s e c u r v e s alm o s t c o i n c i d e for t h e t w o s t i m u l u s t y p e s ( s l o w l y a n d
s t e e p l y rising r a m p s , Fig. 2a). C o n t r a l a t e r a l s t i m u l a t i o n
r e s u l t e d in a p a r a l l e l shift o f the i n t e n s i t y r e s p o n s e c u r v e s
b y a b o u t 8 d B ( r a n g e : 6 - 1 2 dB) as c o m p a r e d to i p s i l a t e r a l
s t i m u l a t i o n (Fig. 2a). T h e n u m b e r o f s p i k e s in r e s p o n s e to
t h e t w o s t i m u l u s t y p e s at a g i v e n i n t e n s i t y w a s a l m o s t t h e
same within the dynamic range of the receptor's responses. O n l y at h i g h intensities, i.e. close to t h e cell's s a t u r a t i o n r a n g e , t h e s p i k e c o u n t t e n d e d to b e s o m e w h a t h i g h e r
for s l o w l y r i s i n g r a m p s (Fig. 2a,b). I n c o n t r a s t , in t h e t e m p o r a l d i s t r i b u t i o n s o f s p i k e s a d i s t i n c t d i f f e r e n c e w a s visible ( P S T - h i s t o g r a m s in Fig. 2c). W i t h t h e s l o w l y r i s i n g
r a m p , t h e first s p i k e o c c u r r e d later, a n d t h e t e m p o r a l
scatter of spikes was higher.
T y p i c a l d a t a o n t h e l a t e n c i e s o f a r e c e p t o r fibre a r e
g i v e n in Fig. 3a for d i f f e r e n t intensities. F o r t h e s t i m u l i
w i t h s u d d e n o n s e t s t h e l a t e n c y c u r v e b e c o m e s v e r y flat at
i n t e n s i t i e s h i g h e r t h a n 1 5 - 2 0 d B a b o v e t h e cell's
t h r e s h o l d ; s t a n d a r d d e v i a t i o n s a r e v e r y small, in m o s t
cases less t h a n 0.5 m s (Fig. 3b). F o r t h e s l o w l y r i s i n g
r a m p , in c o n t r a s t , t h e m e a n v a l u e s o f l a t e n c i e s a r e l a r g e r ,
a n d t h e c u r v e s h o w s a d i s t i n c t l y s t e e p e r slope. I n g e n e r a l ,
the respective standard deviations were also significantly
l a r g e r for t h e s l o w l y rising r a m p (Fig. 3b). T h e s t e e p e r
428
R. Krahe, B. Ronacher: Directionality cues in grasshopper's auditory receptor responses
25
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Fig. 2. a Intensity response curve of a type 1 receptor to ipsilateral
and contralateral stimulation with WN-sound pulses of different
shape (see insets). Pulse duration 10 ms, rise time 10 ms or 0 ms.
n = 50 per data point, bars indicate largest standard deviations. At
76 dB and at 81 dB (ipsi) and at 86 dB (contra) the slowly rising
ramp evoked significantly more spikes (P <0.01). b Pairwise comparison of the number of spikes elicited by ramp stimuli (abscissa)
and stimuli with steep onsets (ordinate). Data of 8 cells, stimulated
70
i
80
ipsi
i
go
INTENSITY[dB]
Fig. 3. a Intensity dependence of latencies of a low frequency receptor (type 1 or 3), for sound pulses of different shape (insets). Bars
indicate standard deviations, h Comparison of standard deviations
for these two stimuli. All differences are significant (P < 0.01 for 76
dB, P<0.001 for all others); n = 50. e Latency curves of a type
l-low frequency receptor, for ipsilateral and contralateral stimulation (same cell as in Fig. 2a). Arrows indicate the respective ipsi-contra differences. Bars: SD, n = 50
<
at different intensities. Stippled: bisectrix, thick: regression line. Correlation coefficient r = 0.989. e PST histograms of spike responses
at three intensities (different cell than in a). Abscissa: time after
stimulus onset, bin width 0.5 ms; ordinate: spikes per bin and stimulus presentation. 50 stimulus presentations per diagram
R. Krahe, B. Ronacher: Directionality cues in grasshopper's auditory receptor responses
slope of the upper curve in Fig. 3a corresponds to the
above mentioned gain in latency difference (Fig. la),
which could improve directional hearing. For an intensity decrease of, say, 5 dB the upper curve yields a larger
difference in latency than the lower curve. However, the
larger standard deviations would, at least partly, reduce
this gain. In order to ascertain how these two opposing
effects interact, we show in Fig. 3c latency curves for ipsiand contralateral stimulation. The distance between ipsia n d contra-curves is considerably larger for the stimulus
with slowly rising ramp (arrows in Fig. 3c), and, most
importantly, there is a better separation of the respective
confidence intervals. This is especially obvious at high
intensities, where steep ramps yield almost identical latencies.
Determination of error probabilities based on the
responses of a single pair of receptors
These data suggest that slowly rising ramps increase the
probability for correct right-left decisions. We tested this
hypothesis by calculating the probabilities for incorrect
directional decisions from the respective distributions of
latencies in a Monte Carlo simulation (cf. Methods). As a
first step it was assumed that the CNS would evaluate the
responses of only one pair of receptor cells. This situation
was approximated in the neurophysiological experiment
by stimulating the receptor under study via the ipsilateral
or via the contralateral loudspeaker (see Fig. 3c). The resuits of this simulation describe what information on
sound direction can be drawn from a pair of left and right
receptors, under optimal conditions (see Discussion).
A first result of the Monte Carlo simulations is shown
in Fig. 4a. With intensities up to 20 dB above the receptor's threshold the two types of stimuli yield similarly low
error probabilities. However, at higher intensities the
slowly rising ramps yield a next to zero probability of
false decisions, while for steep ramps the error probabilities increase to values as high as 0.25. An evaluation of
other receptor cells, including those with lower
thresholds (type 2, 3 receptors), yielded very similar resuits. Thus, with slowly rising ramps the intensity range
could be expanded over which directional cues are
present in a bilateral pair of receptors. It has to be emphasized that the values used so far for the calculation of
error probabilities characterize the optimal situation for
directional hearing, i.e. stimuli delivered from a sound
source located perpendicular to the animal's body axis.
Grasshopper males, however, can use much smaller intensity differences for sound lateralization (see Introduction and von Helversen and Rheinlaender 1988). A similar calculation of error probabilities corresponding to an
assumed interaural level difference of 2 dB is shown in
Fig. 4b. In this case the probability of errors is substantially increased with both types of stimuli. The error
probabilities were relatively constant over the intensity
range tested (this applied also to other cells, except in
some cases for very low and very high intensities). Stimuli
with ramplike onsets are superior, yielding lower error
probabilities. Figure 4c shows a pairwise comparison of
429
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Fig. 4. a Probabilities of incorrect lateralization ('errors') calculated
by a Monte Carlo simulation from the latencies of a single low
frequency receptor to ipsilateral and contralateral stimulation (see
text and Methods) 9 Same cell as in 3c. b Same calculation based on
an assumed interaural level difference (ILD) of 2 dB. c Pairwise
comparison of the error probabilities for the two stimulus types
(ILD = 2 dB); 8 different receptors (6 type 1 and 2 type 3 receptors).
Stippled: bisectrix. Crosses and bars near the axes indicate the respective mean values _ SD for ramp stimuli (ordinate) and steep
onsets (abscissa)
the error probabilities for the two types of stimuli, for 8
different cells (at 4-6 intensities, each). The data do not
cluster around the bisectrix, but are shifted to the right.
In only 4 cases did the stimulus with a steep ramp yield a
lower error probability than the stimulus with a slowly
430
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R. Krahe, B. Ronacher: Directionality cues in grasshopper's auditory receptor responses
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Figure 5 compares, for an ILD of 5 dB, the error probabilities resulting from an evaluation of spike count, of
latency cues, and of a combined evaluation of both cues.
Spike count evaluation yields similar values for slowly
rising and steep ramps (Fig. 5a). This is expected because
the intensity response functions are similar for both stimulus types (see Fig. 2a). For stimuli with sudden onsets,
both spike count as well as response latency yield similarly high error probabilities (compare Fig. 5a and b). However, for ramp stimuli an evaluation of latency cues results in substantially lower error probabilities than spike
counts (Fig. 5a,b). A correlated analysis of both cues
yields no improvement in case of slowly rising ramps,
while there is a moderate improvement for the other
stimulus type (Fig. 5c).
j~/~j
0.25
,,
0.00
60
65
70
75
80
85
I I
INTENSITY
[dB]
Fig. 5. Error probabilities for an assumed interaural level difference
of 5 dB, based on spike count alone (a), response latency (b), and a
correlated analysis of both (e), calculated from the data of a single
pair of receptors. In e open symbols indicate error probabilities
based on latency alone, filled symbols indicate those based on both
cues
rising ramp, and in 30 cases the reverse was true
(P~0.001, sign test). In these 4 cases the data were obtained near the threshold of the respective cell. Moreover,
the mean error probabilities (bars in Fig. 4c) differed in a
highly significant way (0.252 ___ 0.083 vs. 0.400 -t- 0.077,
P~O.O01).
As mentioned in the Introduction, differences in spike
count might also be used as a cue for sound direction.
The results of Figs. 4 and 5 suggest that the information
provided by a single pair of receptors is not sufficient to
explain the accuracy of turning behaviour observed in
behaving grasshopper males. Two possible mechanisms
for reducing error probability are obvious:
(i) Since the auditory organ of grasshoppers contains
about 90 to 100 receptor cells (Gray 1960; Michel and
Petersen 1982), the CNS could assess response latency
and/or spike count from these parallel fibres, and thereby
reduce the error probabilities.
(ii) The animals might sample over a longer period of
time. Indeed, the stridulation signals of Ch. biguttulus, on
which the behavioural data were obtained, consist of
longer series of "syllables" (composed of 6 to 8 pulses),
which are separated by pauses of 15 to 25 ms (values
depending on temperature, cf. von Helversen 1972; von
Helversen and von Helversen 1987). The total duration of
female stridulation sequences ("songs") usually is approximately 1 s (songs of males are longer, von Helversen and
von Helversen 1975). In experiments with model songs,
however, males also show their typical turning response
to songs that were artificially shortened to 450 ms duration.
Figure 6 shows the reduction of error probabilities
that could, in principle, be achieved by evaluation of information from several parallel receptors. Again, the best
case has been taken as a basis, by comparing receptor
fibres of equal sensitivity from left and right ear. A decision was counted as incorrect if in more than half of the
cases the ipsi-latencies were larger than the contra-latencies (sampling accuracy: 50 ~ts; see Methods). The resulting error probabilities show a steep decrease between 1
cell and 10 cells, and a flatter decrease between 10 and 30
cells evaluated in parallel. The data of Fig. 6 do not follow a simple squareroot of N relationship. The curves for
the two stimulus types are clearly separated. Most interestingly, the error probabilities for an evaluation of more
than 30 receptor fibres approximate the values found in
behaviour, but only for the stimuli with slowly rising
ramp (error probabilities are below 0.01). The stimuli
with steep onset still lead to an error probability of 0.1.
R. Krahe, B. Ronacher: Directionality cues in grasshopper's auditory receptor responses
>I-
0.50
p r o b a b l y cannot be explained on the basis of information
provided by a single pair of receptors. Therefore, in the
third section we will try to give an estimate of the possible
i m p r o v e m e n t of directionality cues that could be attained
by the evaluation of parallel receptors.
D
ID
<
W
0
nrt
nO
nnLU
431
0.25
Directionality cues present in the responses of auditory
receptors
0.00
0
10
NUMBER
20
OF
20
40
CELLS
Fig. 6. Decrease of error probabilities by evaluation of N parallel
receptor fibres (abscissa), for an assumed interaural level difference
of 2 dB. N varied from 1 to 31. Ordinate: error probability, as in
Fig. 4. See text for details of the evaluation. Data are mean values
over an intensity range of 36 dB. Bars indicate standard deviations.
Curves based on the data of 6 different receptors recorded in one
hemiganglion of a locust (5 type 1 and 1 type 3 receptors)
With longer song models the latency cues do not
change substantially: We measured the latencies for the
first spike response to each syllable (in a 6 syllable song,
cf. Methods). There was a small increase in latencies,
mainly between the first and the second syllable, and the
variances of latencies were somewhat higher for the 6th
syllable than for the first. As in the simulations shown
above, the stimuli with slowly rising r a m p still yielded
smaller error probabilities. But, for a comparison of two
single latencies at 2 dB difference, error probabilities were
still in the range of 0.25 (or even higher in case of stimuli
with sudden onsets). Because we do not know how the
CNS would evaluate the latency cues in a longer song
model, a tentative approximation would be to assume a
kind of 'majority vote', like that used for the curves of
Fig. 6 (cf. Methods). As can be seen from that figure, the
latency evaluation of six to ten elements (first spikes to
syllable onsets) would not reduce the error probabilties
to the desired degree. As concerns spike count, this cue
indeed improves with longer stimuli. Again the two types
of stimuli yielded similar intensity response curves, and
consequently the error probabilities were also similar for
both stimuli. However, in a spike count evaluation for a
model song of 480 ms duration (see above) the error
probabilities for an assumed interaural level difference of
2 dB were reduced only to around 0.1, and thus did not
attain the range found in behavioural experiments.
Discussion
The aim of this paper was to investigate the cues for
directional hearing that are available for the CNS of a
grasshopper from the responses of auditory receptors,
with special emphasis on stimulus rise-times. There are
two main results of this study which shall be discussed in
turn: (i) Ramplike stimuli yield improved latency cues
c o m p a r e d to stimuli with steep onsets. (ii) The precision
of lateralization found in behavioural experiments most
The data presented here (Figs. 3-5) show that stimuli
with ramplike onsets can be advantageous for directional
hearing in grasshoppers, and p r o b a b l y also in other animals with small interaural disparities and negligible
physical time differences. Although with slowly rising
ramps the spiking responses are triggered less precisely
(Figs. 2c, 3b), this stimulus type yields an 'additional gain'
in latency differences that outweighs the former effect.
This has been demonstrated quantitatively by Monte
Carlo simulations (Fig. 4) in which the opposing contributions of b o t h effects can be assessed. Thus A d a m ' s
(1977) suggestion of the advantage of ramplike stimuli for
directional hearing could be confirmed, and defended
against a m a j o r objection raised against it: i.e. that the
hypothetical gain in latency difference would be destroyed by an increase in variance.
Slowly rising ramps a p p e a r to be especially advantageous at small interaural level differences (Fig. 4b,c). Interestingly, for small interaural level differences the error
probabilities were rather independent of intensity, especially for the ramplike stimuli (Fig. 4b, 5b). In Fig. 3a,c
the slope of the latency vs. intensity curves decreases with
increasing intensity. The rather constant error probabilities of Fig. 4b thus indicate that the decrease in latency
difference, which results from this shape of the curves, is
compensated over a wide range by an equidirectional
change in the standard deviations (Fig. 3b).
The other available cue, spike count, yields similar
values for both stimulus types (Fig. 5a). This means, however, that the use of ramplike communication signals
would improve latency cues while not deterioriating the
other possible directional cue, spike count.
In the above simulations it was assumed that even a very small
latency difference could be evaluated by auditory interneurones
within the grasshopper's CNS. It is conceivable, however, that in the
CNS time differences of a few hundred microseconds would perhaps
lead to an ambiguous situation. Taking this into account, we performed the same simulation and assumed a threshold for the evaluation of latency differences (threshold values were varied between
0.1 and 0.5 ms). This additional assumption, however, does not
improve the situation. Though the probabilities of incorrect decisions were reduced, the proportion of undetermined situations increased drastically, up to 100% at higher intensities for the stimulus
with steep rise. Again, this increase was much less pronounced for
ramplike onsets (data not shown).
M6rchen et al. (1978) and M6rchen (1980) also give data on the
latencies of auditory receptors of locusts. They report differences of
up to 5 ms in latencies to ipsi- and contra-stimulation, even for
stimuli with steep onsets (cf. Fig. 3c). However, these values were
obtained with 25 kHz stimuli, which lead to a distinctly higher
interaural level difference of approximately 20 dB (see also R6mer
1976). In addition, the latency vs. intensity-curves given in M6rchen
et al. (1978) and R6mer (1976) - compared with the values of Fig. 3
432
R. Krahe, B. Ronacher: Directionality cues in grasshopper's auditory receptor responses
- show a steeper slope in the near threshold range, which is accompanied by an enormous increase in standard deviations. However,
this apparent difference is solely a consequence of stimulus duration: M6rchen used 22 ms tone pulses, R6mer used 20 or 100 ms
stimuli, and with longer stimuli at very low intensities there is an
increased probability for first spikes to have long latencies: At very
low intensities a short (e.g. 10 ms) stimulus will often not evoke any
spike. In contrast, with a longer stimulus there is still a chance that
a spike will occur, even if none was elicited during the first 10 to 15
ms. Because of the drastic increase of standard deviations of latencies, the steeper slope of the curves in the near threshold range in
M6rchen et al. (1978) would not yield a reduction in error probabilities.
Comparison of neurophysiological data with behavioural
results
In behavioural tests with Ch. biguttulus it has been shown
that grasshoppers can use intensity differences as well as
time differences for directional hearing (von Helversen
and von Helversen 1983; von Helversen and Rheinlaender 1988). Although the relevant behavioural data were
obtained with Ch. biguttulus, we decided to use L. migratoria for neurophysiological recordings, mainly because
of the advantages in recording from and culturing of locusts. The use of locust's auditory receptors as a model
for receptors of other acridid grasshoppers was justified
by earlier investigations in which essentially no differences were found at the level of tympanic receptor cells
between L. migratoria and Ch. biguttulus, apart from a
slight shift in characteristic frequencies (Ronacher and
R 6 m e r 1985; Stumpner 1988; Stumpner and Ronacher,
unpubl.). Even the m o r p h o l o g y and physiology of the
auditory interneurones are very similar in both species
(R6mer et al. 1988; Stumpner and Ronacher 1991).
Therefore, it seems justified to compare the electrophysiological data presented here with behavioural results obtained on Ch. biguttulus.
A more critical point for a quantitative comparison
could be that the behavioural experiments were performed at higher temperatures (around 30~
Higher
temperatures influence thresholds, spike count, and latencies of neurons (Heitler et al. 1977; Abrams and Pearson 1982; Ronacher and R 6 m e r 1985; Wolf 1986a). However, the shape of latency curves obtained at high temperatures (with rectangularly modulated signals) is very similar to the shape of latency curves obtained at r o o m temperature, except for a shift to lower values (Ronacher,
unpubl.). We therefore are confident that the differences
in experimental temperatures do not affect our model
calculations too much for a comparison with behavioural
data.
As mentioned before, Ch. biguttulus males can lateralize a sound source at very small ILDs. An I L D of only 2
dB leads to a virtually errorless decision towards the
louder side (von Helversen and Rheinlaender 1988). This
difference would correspond to a sound source located
approximately 10-15 ~ from the animal's longitudinal
axis (Rheinlaender 1984; Wolf 1986b). Comparing these
values with the error probabilities derived from the responses of a single pair of receptors, it becomes obvious
that neither the evaluation of the latencies of the first
spikes, nor an evaluation of spike counts, nor a correlated analysis of both cues yields the necessary accuracy for
directional decisions (Figs. 4, 5). We conclude that the
animals must use redundant cues. This could be achieved
by using information from m a n y parallel receptors and/
or by sampling over a longer time period.
According to our data there was not a sufficient improvement of the latency cue with longer song models.
The spike count difference showed some improvement
with these models (480 ms duration, see above), but the
error probabilities were still around 0.1, which is approximately an order of magnitude too high. It has to be
mentioned, however, that the accuracy of lateralization
with shortened model songs has not yet been tested. Further behavioural studies must now follow, in order to
know how m a n y syllables must be present in a song model to attain the above mentioned precision of lateralization behaviour.
An evaluation of the response latencies of parallel
receptor fibers might explain the directional sensitivity of
behaving animals
Each tympanal organ of L. migratoria accommodates 90
to 100 receptor cells (Michel and Petersen 1982), which
can be classified morphologically into 4 types on the basis of their attachment sites in Mfiller's organ (Gray 1960;
Michelsen 1971a,b; Stephen and Bennet-Clark 1982;
Breckow and Sippel 1985). Receptor types differ considerably in their tuning and thresholds (Michelsen 1971a;
R 6 m e r 1976). As the dynamic range of single receptors is
restricted (20-25 dB), these differences in thresholds expand the dynamic range of the auditory organ ('range
fractionation', Cohen 1964; Rheinlaender 1975). According to Michel and Petersen (1982) there exist approximately 20 low frequency receptors (LFR) of the most
sensitive type (type 2 according to R 6 m e r 1976), and 60
LFR, belonging to type 1 and 3; G r a y (1960) reports 35
a-cells (type 1) and 12 b-cells (type 3), see Breckow and
Sippel (1985) for the synonymization. Only 8-10 high frequency receptors (HFR, type 4) were found. The receptor
types also differ somewhat in their shortest latencies
(R6mer 1976; Halex et al. 1988). Type 1 L F R with high
thresholds show the shortest latencies, while H F R have
the longest latencies (R6mer 1976).
If the CNS evaluates information from parallel receptors a major problem has to be solved: Because of the
differences in best frequencies and thresholds of receptors, stimuli at medium to higher intensities must lead to
considerable differences in latencies and spike count in
receptors belonging to different types. H o w m a n y receptors of the 4 groups will be excited will depend on the
sound intensity and the frequency content of the signal.
By sampling from all receptor types, the signal to noise
ratio would be reduced, especially at higher intensities,
where the most sensitive receptors are in their saturation
range. This limitation applies to both cues, response latency and spike count. A solution to avoid these problems would be the existence of different interneurones,
each evaluating only a subset of receptors belonging to
R. Krahe, B. Ronacher: Directionality cues in grasshopper's auditory receptor responses
one type. A possible n e u r o a n a t o m i c a l basis for such a
receptor-type specific sampling are the t o n o t o p i c projection areas of different receptor types in the a u d i t o r y neuropile of the m e t a t h o r a c i c ganglion ( R 6 m e r 1985; R 6 m e r
et al. 1988; Halex et al. 1988). Unfortunately, the n u m b e r
of individual receptor cells that c o n n e c t to any particular
a u d i t o r y interneurone is u n k n o w n . N e u r o a n a t o m i c a l
d a t a and short synaptic delays indicate that SN1, SN2,
BSN1, and T N 1 are m o n o s y n a p t i c a l l y connected to receptors ( M a r q u a r t 1985; R 6 m e r and M a r q u a r t 1984;
R 6 m e r et al. 1988; see also Lakes et al. 1990; S t u m p n e r
1988; S t u m p n e r and R o n a c h e r 1991), while m o s t ascending n e u r o n s apparently have no direct c o n t a c t with receptors ( R 6 m e r and Rheinlaender 1983; R 6 m e r et al.
1988); two exceptions are A N 1 0 a n d T N 3 (Pearson et al.
1985). Further studies m u s t n o w follow to ascertain h o w
directionality cues are further processed by a u d i t o r y interneurones of the m e t a t h o r a c i c ganglion complex.
Behavioural tests with Ch. biguttulus have d e m o n strated that the rise time of c o m m u n i c a t i o n signals is
i m p o r t a n t for pattern recognition, and especially for determining the sex of a conspecific signaller (von Helversen 1993). The present d a t a on a u d i t o r y receptor responses suggest that an additional function of this shape
of stridulation signals p r o d u c e d by the females could be
to i m p r o v e latency cues for directional hearing and thus
facilitate the male's search and approach. It w o u l d be
interesting to k n o w whether similar m e c h a n i s m s are also
used by other species. In several treefrog species, for example, the pulse shape (rise time) of vocalizations is also
i m p o r t a n t for species recognition ( G e r h a r d t and D o h e r t y
1988; see also G e r h a r d t 1982, 1988; D o h e r t y and Gerh a r d t 1984; for electrophysiological d a t a see e.g. Hall and
Feng 1988; Feng et al. 1990, 1991; C o n d o n et al. 1991;
G o o l e r and Feng 1992). It seems likely that in some of
these species the shape of the c o m m u n i c a t i o n signals
could also contribute to p r o d u c e physiological time differences between afferent discharges, a n d thus facilitate
the localization of the s o u n d source (cf. e.g. Feng and
C a p r a n i c a 1976; Jorgensen and G e r h a r d t 1991; K l u m p
a n d G e r h a r d t 1989; Melssen a n d E p p i n g 1992; Rheinlaender et al. 1979; Rheinlaender and K l u m p 1988;
Schmitz et al. 1992).
Acknowledgements. We thank G. Rammes for providing some data
and U. Habbe for his most valuable help with the Monte Carlo
simulation programs. Carl Gerhardt, Ulrich Habbe, Dagmar von
Helversen, Andreas Stumpner, and two anonymous referees gave
helpful comments on the manuscript which are appreciated.
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