Mechanisms underlying phonotactic steering in the cricket Gryllus bimaculatus revealed with a fast trackball system
University of Cambridge, Department of Zoology, Downing Street, Cambridge CB2 3EJ, UK
* Author for correspondence (e-mail: bh202{at}cam.ac.uk)
Accepted 13 December 2004
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Summary |
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Key words: cricket phonotaxis, track ball system, sound localisation, steering, pattern recognition
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Introduction |
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The existence of two bilaterally paired recognisers that allow crickets to
chose between two sound patterns was first proposed by Pollack
(1986). In two-stimulus
situations crickets (Teleogryllus oceanicus) preferred the
conspecific pattern to a heterospecific song, which was seen as the result of
two interacting recognisers. Stabel et al.
(1989
) and Wendler
(1990
) exposed walking
crickets to two sounds simultaneously and demonstrated that the animals walk
towards the side where the sound pattern is better represented in the activity
of ascending auditory neurons. They concluded that the recognition process is
based on the temporal pattern of the neuronal activity and postulated that
recognition and localization are performed sequentially with two central
nervous recognisers, one on each side of the body, whose output is compared
either in the brain or at the thoracic motor networks. The selective response
of identified auditory brain neurons to temporal patterns indicated that
corresponding pattern recognition networks might be located in the
protocerebrum (Schildberger,
1984
,
1994
). This model has become
an accepted view on pattern recognition and localization in the crickets
G. bimaculatus and G. campestris
(Horseman and Huber, 1994
;
Helversen and Helversen, 1995
;
Pollack, 1998
,
2000
;
Stumpner and Helversen, 2001
;
Hennig et al., 2004
).
Consequently, when simultaneously exposed to two sound sources crickets are
expected not just to turn to the louder side but to the better pattern
(Helversen and Helversen 1995
;
Helversen 1997
).
The cricket's ability of pattern recognition is always deduced from the
animals' steering or orientation behaviour in flight (Ulagarai and Walker,
1973; Nolen and Hoy, 1986;
Pollack and Hoy, 1979
) or
walking (Murphey and Zaretsky,
1972
; Popov and Shuvalov,
1977
). Major experiments in walking crickets were based on female
phonotaxis performed on treadmills that provided the mean walking velocity and
the overall path of the walking cricket, but due to low resolution could not
reveal information about the rapid dynamics of the underlying steering
behaviour (Weber et al., 1981
;
Schmitz et al., 1982
;
Doherty and Pires, 1987
;
Doherty 1991
). We recently
developed a highly sensitive trackball system, which allowed us to measure
cricket walking behaviour at the level of the animals stepping cycle
(Hedwig and Poulet, 2004
), an
accuracy not achieved in previous experiments. With this system we analysed
the fast dynamics of cricket auditory steering and investigated the impact of
intensity differences, time differences and split-song paradigms on cricket
auditory orientation and the implication for pattern recognition.
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Materials and methods |
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Trackball system
A trackball, with a diameter of 56.5 mm and a weight of 3.0 g, was
manufactured out of Rohacell 31 (Röhm KG, Darmstadt, Germany). The
surface of the ball was speckled with black ink to enhance its optical
contrast. The ball fitted into a transparent acrylic half-sphere, which
contained 24 holes and was mounted on top of a small cylinder. The cylinder
was connected to a constant air supply and the air pressure was adjusted so
that the trackball was gently lifted and was free to rotate with minimal
friction. An optical sensor (ADNS-2051, 2D Optical Mouse Sensor; Agilent,
Farnell Electronics, Oberhaching, Germany) was aligned opposite the south pole
of the trackball. The LED of the sensor illuminated the lower area of the
trackball through the acryl sphere. The optical pattern reflected from the
surface of the trackball allowed the sensor to monitor any trackball movements
in the forwardbackward and leftright direction simultaneously.
The output of the sensor chip was processed on-line with a quadratur to pulse
converter, which generated two data channels and produced for every movement
increment of 127 µm in the forwardbackward and leftright
direction a coding pulse of 150 µs duration and 1.5 V amplitude,
respectively. Positive coding pulses indicated forward or left increments, and
negative pulses indicated movements to the back or right.
Data evaluation
The coding pulses of the two movement components and the envelope of the
sound stimuli were sampled online at 10 kHz per channel using an A/D board
(PCI-Mio 16-E-4; National Instruments, Newbury, UK) controlled by software
programmed in LabView 5.01. Data were stored on the hard disk of a PC for
later off-line analysis with custom-made software. From the repetition rate of
the coding pulses the velocity of both movement components was derived. The
forwardbackward and leftright velocities were then used to
calculate the translation velocity of the animal and were 250 Hz low-pass
filtered. Velocity signals were integrated to reveal the overall lateral
deviation and the path length covered by the walking cricket
(Fig. 1B). Measurements of
overall lateral deviation and path length were exported to Excel for pooling
and statistical analysis. We refrained from any binning of the coding pulses
to maintain maximum temporal and spatial sensitivity of the measurements. With
an A/D sampling rate of 10 kHz, the maximum rate of coding pulses (150 µs)
that could be resolved was about 300 Hz. With the given specification of the
sensor chip the system should perform linearly up to trackball speeds of 38 cm
s-1 in either direction.
Sound stimulation
The speakers and trackball system were located inside a sound proofed
chamber (L150 cm, W100 cm, H70 cm) lined with Illsonic tiles (Sonex 65/125;
Illbruck, Bodenwöhr, Germany). The noise level inside the chamber
measured at the top of the trackball was 38 dB SPL rel. 10-5 N
m2 (band pass filter 200200,000 Hz) when the air supply for
the trackball was turned on. The standard sound pattern had a frequency of 4.8
kHz, syllable duration of 21 ms (including 2 ms rise and fall times), a
syllable period of 42 ms, chirp duration of 250 ms and a chirp period of 500
ms, and corresponded to an syllable repetition interval pattern (SRI 42) that
Thorson et al. (1982) used in
previous phonotactic experiments. Sound stimuli were digitally generated at
22.05 kHz sampling rate (Cool Edit 2000; Syntrillium, Phoenix, USA) and were
presented by PC audio boards via 2 active speakers (SRS A57; Sony,
Tokyo, Japan). These were positioned at a distance of 87 cm frontal to the
cricket each at an angle of 45° to the animal's length axis
(Fig. 1A). Sound intensities
were calibrated with an accuracy of 0.5 dB at the position of the cricket
using a Bruel and Kjaer (Nærum, Denmark) free field microphone (Type
4191) and measuring amplifier (Type 2610). To analyse phonotactic walking,
sound patterns were generally presented from the left and/or right speaker for
durations of 30 s. An electronic circuit produced the envelope of the sound
pattern with a RMS chip (Type 637; Analog Devices, Walton-on-Thames, UK) set
to a time constant of 0.5 ms.
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Results |
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In one set of experiments we measured with an optoelectronic camera
(Hedwig, 2000) the stepping
cycle of one front leg simultaneously with the trackball rotations of the
walking animal. These recordings revealed that the translation velocity was
modulated in phase with the animal's stepping
(Fig. 1C). Due to the tripod
gait of insects, which moves a set of three legs at any time, the recording
showed regular oscillations in the amplitude of the translation velocity with
twice the frequency of the front leg movements. Thus, the track ball system
actually resolved the cricket walking velocity components at the level of the
stepping cycle.
Intensity function of phonotactic steering
During the experiments, sound was played from a left or right speaker each
positioned frontally at 45° from the animal's length axis. Since the
crickets could not alter their orientation towards the speakers the acoustic
stimulus conditions remained constant. The sound pattern used to test the
animals had been effective at eliciting phonotaxis in previous experiments
(Thorson et al., 1982). It had
a syllable duration of 21 ms and a syllable interval of 21 ms. Six syllables
were grouped into a chirp and were repeated every 500 ms. Sound intensity was
increased from 45 dB SPL in steps of 5 dB to 85 dB SPL. Each pattern was
presented for 30 s from the left and right side, respectively.
When tethered on top of the trackball most crickets started walking spontaneously. Without acoustic stimulation the animals walked and randomly deviated towards the left or right side. When the sound pattern was presented the crickets started steering towards the active speaker (Fig. 2A) and upon each change in the side of sound presentation the animals changed their walking direction correspondingly. We calculated the lateral deviation from a straight path as a measure of the animal's steering towards a sound source and the animal's translation velocity within the test time interval of 60 s (Fig. 2B). With increasing sound intensity the lateral deviation towards the sound source and the walking velocity increased. For 17 crickets we quantified the behaviour for all sound intensities tested. Phonotactic steering significantly started at 45 dB SPL with a mean deviation of 8.4 cm min-1 and increased linearly with sound intensity to 51.0 cm min-1 at 75 dB SPL. Further increase in sound intensity led to a saturation of auditory steering and at 85 dB SPL the mean lateral deviation (52.0 cm min-1) was not significantly different from the value at 75 dB SPL. By comparison, the overall path length increased from 161.8 cm min-1 at 45 dB to 280.8 cm min-1 at 85 dB SPL. Between 45 and 75 dB the overall lateral deviation increased 6.1-fold whereas the path length increased only by a factor of 1.7. From these experiments we conclude that the animals performed phonotactic behaviour when walking on the trackball. The low auditory threshold and the reliable steering manoeuvres after changes in sound direction indicated that the behaviour was not impeded by the experimental situation.
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We took advantage of the high temporal and amplitude resolution, and analysed the dynamics of phonotactic steering for responses towards the 75 dB sound patterns. The lateral steering velocity demonstrated that the animals do not steer with constant amplitude, but produced steering transients triggered by the sound pattern (Fig. 3A). Consequently each chirp shifted the animal's path to the left by about 45 mm. Compared with the steering velocity, the forwardbackward velocity component was only weakly modulated by the acoustic stimulus. Averaging the velocity components (Fig. 3B) demonstrated that the lateral steering velocity started to increase after the second sound pulse of a chirp. It reached 2.6 cm s-1 after the end of the chirp and then decreased again. The average forward velocity remained at a high constant level and exhibited a transient minimum at the beginning of each steering response. These averaged profiles of the forward velocity components were different in individual crickets. In some steering animals the forward velocity component was modulated only to a very small degree. This could indicate separate mechanisms for the control of lateral steering and forward speed. Animals that showed a good phonotactic performance were used for further experiments.
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Steering towards bilateral intensity differences
For auditory orientation animals can exploit interaural intensity
differences and/or interaural latency differences. A basic rule for cricket
phonotactic walking was `turn towards the louder side'
(Huber et al., 1984;
Schildberger, 1994
). This
parsimonious explanation of cricket orientation has never been analysed with a
trackball system and there is no information, to what degree crickets are able
to exploit leftright intensity differences for phonotactic steering. We
presented identical sound patterns simultaneously from both speakers at an
intensity of 60 dB SPL. During the test the intensity of one speaker was
consecutively increased by 1, 2, 3, 4, 5, 10 and 15 dB. Each intensity
difference was presented for 30 s from the left and right side, respectively.
For 12 crickets the overall lateral deviation was calculated and is given
relative to the phonotactic response of the animals to a 75 dB SPL stimulus
used as a 100% reference response (Fig.
4).
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When exposed to the test paradigm without any intensity differences (Fig. 4A) the animals steered to the left and right side with the same intensity and consequently walked straight ahead. At intensity differences of just 12 dB, the animals started orientated behaviour and steered towards the louder speaker. With increasing intensity difference the deviation towards the louder side gradually increased (Fig. 4A). However, even at 10 and 15 dB intensity differences the lateral deviation was not as straight as during the threshold tests (compare with Fig. 2) and lateral deviation appeared less precise. Quantitative analysis demonstrated that at 1 dB intensity difference the deviation from the midline was 12.0% of the lateral deviation to a 75 dB unilateral sound and was just significant at 97% level. Averaging the steering response towards the 1 dB louder speaker (Fig. 4C, top) demonstrated that the mean steering velocity was slightly shifted towards the louder speaker. At higher intensity differences the animals' performance increased. At 2 dB intensity difference it reached 24.0% of the standard response (Fig. 4B) and the averaged steering velocity exhibited a clear response towards the louder speaker (Fig. 4C, middle). At 10 dB difference the orientation towards the louder sound corresponded to 74.4% of the reference value (Fig. 4B) and caused a clear turning reaction as revealed by the averaged steering signal (Fig. 4C, bottom). Finally at 15 dB difference, with one speaker at 65 dB SPL and the other at 80 dB SPL, the orientation towards the louder speaker reached 98.0% of the standard response.
Calculating the overall path length walked during this test (Fig. 4D) demonstrated that all animals walked about 205 cm min-1 and that the results are not biased by preferences towards particular combinations of intensities. We therefore conclude that crickets are sensitive to bilateral intensity differences of at least 2 dB and that they are able to exploit these minute acoustic cues for auditory steering. The steering amplitude, however, is intensity dependent with larger differences in sound intensity leading to larger steering responses.
Steering towards bilateral time differences
The exploitation of interaural time differences for auditory orientation
may be challenging for the cricket G. bimaculatus. The distance
between the bilateral spiracle openings is about 5 mm and the distance between
the ears in the front legs is about 9 mm. Thus, the interaural time difference
for impinging sound waves corresponds to about 1530 µs and insect
ears are limited to exploit these interaural time differences for directional
processing (Lewis, 1983;
Michelsen, 1998
). We
experimentally introduced a time difference in the range of 212 ms
between the sound patterns presented from the left and right side. Due to the
stimulus amplitude of 75 dB in these experiments the leading sound pulse will
also activate the afferents at the contralateral side before the delayed sound
pulse starts. Such a situation may arise when a female is exposed to the songs
of many males singing with slightly different chirp or syllable rates. We
analysed to what degree females may exploit these time differences for
auditory orientation and exposed 11 females to identical sound patterns of 75
dB SPL in amplitude with one pattern consecutively leading the acoustic
stimulation by 2, 4, 6, 8, 10 and 12 ms. Each time difference was presented
for 30 s from each side of the animals and phonotactic steering was plotted
and evaluated (Fig. 5).
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The walking paths encountered when the animals were exposed to time differences were strikingly different to those in response to intensity differences. Although one might expect a clear orientation towards the leading sound pattern, a typical example of the phonotactic performance of a cricket (Fig. 5A) demonstrated that the females hardly steered towards leading pattern. Only at time differences of 4 and 8 ms the animals preferred the leading sound pattern. When we pooled the responses of all females tested, this weak reaction towards the leading sound pattern became statistically evident.
At a time difference of 2 ms the crickets actually orientated towards the delayed sound pattern by 7.1% of the standard response, i.e. the turned away from the leading pattern. The orientation towards the leading pattern at differences of 6 ms and 12 ms corresponded just to 5.7% and 1.7% and was not significantly different from walking straight ahead. The animals demonstrated a weak, but significant, steering towards the leading sound pattern only at differences of 4 ms (26.3%), 8 ms (15.2%) and 10 ms (14.8%). However, even at these delays averaging the steering velocity did not reveal a clear phasic turning response towards the leading pattern (Fig. 5C). Instead, there was only a weak general shift towards the direction of the leading speaker, similar to responses we observed for intensity differences of about 2 dB (compare with Fig. 4C). Although the experimentally induced time differences are well within the physiological range of synaptic processing and should easily be resolved in the CNS, the experimental data indicate that crickets may not or only weakly exploit time differences for auditory localization.
The impact of bilateral syllable numbers on phonotactic steering
Neurobiological experiments by Nabatiyan et al.
(2003) on discharge rate
coding by auditory interneurons pointed towards the importance of single sound
pulses for phonotaxis. With split-song paradigms
(Weber and Thorson, 1988
) we
tested to what degree single syllables have an impact on phonotactic steering
and generated sound patterns with a systematic variation in the number of
sound pulses presented from the left and right side. We started with the
standard six syllable chirp and we gradually reduced the number of syllables
played from one side from 6 to 0 and at the same time gradually increased the
number of syllables presented at the other side from 0 to 6
(Fig. 6A,B). For each
combination it was always the last syllable of a chirp that was altered and
each paradigm was played for 30 s from each side of the animal (see
Fig. 7 for details of the sound
pattern). Between the tests was a silent period of 10 s.
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Like all other crickets, the animal in Fig. 6A steered best when all six sound pulses were presented from one side (6:0 and 0:6). However, when we played the last sound pulse of the chirps from the contralateral side (5:1), a considerable reduction of the steering response towards the five-syllable chirp occurred. This effect increased with the increasing number of syllables presented from the contralateral side. When the first three and last three pulses of the chirps were presented from opposite sides, the overall deviation to any side became small, but still the animals generally orientated stronger towards the leading syllables. Also the pattern 2:4 elicited orientation towards the left side where only two pulses of a chirp were presented. In this case, even after the consecutive switch, when four syllables from the right preceded two syllables from the left, the animal kept walking to the left. When the pattern 1:5 was given the overall response was dominated by orienting towards the five syllables. We quantified the response for 12 crickets and found a close correlation between the number of syllables presented from each side and orientation (Fig. 6B). With the decreasing ratio of pulses presented from the left and right side the orientation of the animals towards the left side gradually decreased from 89.5% at 6:0 to 73.9% at 5:1, then to 53.2% at 4:2 and finally 26.4% at a syllable ratio of 3:3. Orientation then changed towards the right with -26.0% at 2:4, -82.4% at 1:5 and -91.6% at 0:6. Although there was always a slight bias towards the side presenting the start of a chirp, each change in the ratio of pulses presented, caused a stepwise change in the lateral deviation. The overall phonotactic performance was good in all animals tested (Fig. 6C). The path length was at a maximum when the animals were exposed to the 3:3 pattern. The gradually reduced lateral orientation could be interpreted in a way that the attractiveness of the sound pattern was affected by changing the number of syllables presented from both sides and that, therefore, the animals turned less when exposed to this pattern. However, as another possibility the animals might steer towards individual sound pulses and in fact might have turned to the pulses presented from both sides in the same way. In both cases the dynamics of the underlying steering responses would be fundamentally different. To distinguish between both possibilities, i.e. reduced attractiveness or steering towards individual sound pulses we analysed the dynamics of the animals steering behaviour.
Temporal dynamics of lateral steering
The trackball system used demonstrated that phonotactically walking
crickets do not steer with a constant lateral velocity. Moreover, they
consecutively produce lateral steering movements with considerable amplitudes
of 27 cm s-1 although their overall lateral deviation
indicates a directed walking path when analysed at low spatial resolution
(Fig. 2A top,
6A top). To demonstrate the
dynamics underlying the auditory steering responses we averaged the lateral
steering velocity evoked by the acoustic test patterns presenting different
syllable numbers (Fig. 7).
When all six sound pulses were presented from the left (Fig. 7A), the animals started steering towards the left at 5560 ms after chirp onset, i.e. just before the end of the second sound pulse. Steering reached a mean maximum amplitude of 2.2 cm s-1, it lasted for the duration of the chirp and then gradually decayed to 0.5 cm s-1 (compare with Fig. 3B). The time course of this response already indicates, that the animals did not evaluate the temporal pattern of the whole chirp until steering started. Instead steering was already initiated, while the second sound pulse was still playing. When we presented the stimulus pattern 5:1 (Fig. 7B) steering to the left started again during the second sound pulse. However, due to the single pulse presented from the right, steering to the right commenced earlier, faster and to an average steering velocity of 0.0 cm s-1 between the chirps. Note: as a reference, the response to six pulses presented from the left is always indicated in blue. Turning towards the right side gradually increased with the number of sound pulses presented from the right (Fig. 7C). When the last three pulses were presented from the right (Fig. 7D) the animals started to turn right during the chirp, i.e. after the 2nd pulse from the right. The overall steering response towards the right sound pulses compensated the initial steering towards the leading left pulses. It brought the mean steering velocity to zero but it was not strong enough to actually turn the animal to the right. As a consequence, the cricket still orientated to the side of the leading pattern (see Fig. 6A at 3:3). The steering response to the initial sound pulses actually has to be overcome by a stronger response to the following pulses. In this case, even at 2:4 (Fig. 7E), the animal clearly responded to the four sound pulses presented from the right. However, this response was not strong enough to overcome the initial response to the two pulses from the left. Consequently the orientation of the cricket was still to the left (see Fig. 6A at 2:4). The initial response towards the single pulse presented from the left was only overcome by consecutive steering towards the five pulses from the right in the 1:5 trial (Fig. 7E) and the orientation of the animal was to the right. These averages of the steering velocity clearly indicate that the animals steer towards individual sound pulses and that steering changes even during ongoing chirps. Therefore, orientation cannot be not based on an evaluation of the chirp pattern. It also indicates that by evaluating a cricket's walking path or its direction with low temporal and spatial resolution only, the underlying steering and auditory processing mechanisms cannot be revealed.
Pattern recognition and orientation
In crickets, the final walking direction chosen may depend on a pattern
recognition process analysing the `quality' of the perceived stimulus pattern.
It has been proposed (Pollack,
1986; Stabel et al.,
1989
; Helversen and Helversen,
1995
) that crickets use a left and right recogniser in their CNS
to compare the perceived patterns at both sides and finally steer towards the
better pattern, i.e. there is a serial processing of pattern recognition and
localization. Our previous experiments demonstrated that crickets even steer
towards individual sound pulses and start steering after 5560 ms. These
rapid steering responses question whether steering is based on a comparison of
the quality of auditory patterns perceived at the left and right side. To
analyse this matter more closely we took the split-song paradigm to the
extreme (Hedwig and Poulet,
2004
) and presented every other sound pulse of the chirp pattern
from the opposite side (Fig.
8).
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When exposed to these split sound patterns, the crickets perceived the same number of sound pulses from the left and right side. Correspondingly, they generally walked straight ahead (Fig. 8A), or could show a slight bias towards the side presenting the first pulse. This may be interpreted as if the animals kept a course between both speakers where the perceived pattern was optimal. The lateral steering velocity signal demonstrated, however, that the animals permanently produced steering transients to the left and the right side. These transients in the lateral steering velocity were linked to the individual sound pulses (Fig. 8B). Superimposing the steering velocity signal (Fig. 8C) revealed that the animals rapidly and reliably steered towards the left and right side and altered their turning direction corresponding to the split-song pattern. We averaged the lateral steering velocity signal for the duration of a split-song chirp and revealed the time course of these steering transients (Fig. 8D). This demonstrated that the crickets alternating steered to the sound pulses presented from the left and right side, corresponding to the presentation of the split-song sound pulses. Even under these extreme circumstances the animals steered towards the individual sound pulses. Steering again occurred with a latency of 5560 ms. During this rapid steering behaviour, responses to the left (i.e. the first) pulses were at least compensated by responses to the right (i.e. the following) pulses and at the end of a chirp the responses to the last pulse dominated the steering response. As a consequence, cricket orientation was straight ahead or slightly biased towards the side with the leading pulses. These experiments finally demonstrated that crickets rapidly steer towards individual sound pulses. The intensity of the steering responses could vary in the course of a walking sequence and from animal to animal. Since these auditory steering responses occurred with a rate of 24 Hz it appears that leg movements underlying walking behaviour were modulated in a reflex-like way.
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Discussion |
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Technical considerations of the trackball systems
The design of the trackball system allowed a single 2D sensor chip to
monitor the cricket's walking path. The sensor detected any
forwardbackward and leftright movements of the trackball with a
spatial resolution of just 127 µm and should work linearly to velocities of
38 cm s-1. Since the sensor data were processed without any
temporal averaging, the data resolved single steps of the walking pattern and
fine temporal details of the steering behaviour. The temporal and spatial
resolution of our system is superior to previous open loop
(Doherty and Pires, 1987;
Schildberger and Hörner,
1988
; Stabel et al.,
1989
) and closed loop systems
(Weber et al., 1981
;
Schmitz et al., 1982
) used to
analyse cricket phonotactic walking. The closed loop Kramer treadmill system
was adjusted to compensate the mean speed of the walking cricket. Its dynamic
performance was not sufficient to capture the velocity modulation
corresponding to the animal's tripod gait or rapid changes in the velocity
components during steering or at the start and end of walking bouts (see
Weber et al., 1981
, their fig.
4). For data analysis the velocity signal generally was binned and calculated
only during certain time windows or path length, e.g. every 500 ms by Schmitz
et al. (1982
) or over 1 s by
Doherty and Pires (1987
). Based
on our presented data we conclude that temporal and spatial details of the
crickets steering behaviour could not be resolved with such methods. Our track
ball system generated low background noise (38 dB SPL) as compared with 58 dB
SPL of the compensated walking sphere
(Schmitz et al., 1982
).
Phonotactic steering therefore could be elicited even at 45 dB SPL, it
increased up to 75 dB and, as in G. campestris
(Schmitz et al., 1982
),
saturated at higher intensities.
During turning movements, tethered animals are expected to have problems
controlling the inertia of the trackball if the trackball is larger than 1.5
times of the animal's mass (Weber et al.,
1981). A female cricket weighted about 12001300 mg. The
effective mass the crickets had to control when rotating the trackball was
1200 mg (2/5 of the total sphere mass) and, thus, closely corresponded to the
animal's body mass.
Open loop trackball systems may be regarded as restrictive to the animal's behaviour. However, the low threshold for the release of phonotaxis and the dynamic of the steering behaviour observed indicate that in our system walking was not impeded. The considerable advantage of our open loop system is that the animal's turning responses do not alter the conditions of acoustic stimulation. Since the crickets remained at a constant position relative to the speakers their steering responses could be measured and quantified, with high temporal and spatial resolution.
The effect of bilateral intensity differences on phonotactic steering
A major rule for cricket phonotaxis has been `turn towards the louder side'
(Huber et al., 1984;
Schildberger, 1994
). A direct
analysis of the crickets' actual ability to exploit bilateral intensity
differences, however, had not been obtained. When we exposed phonotactically
walking crickets to bilateral sound patterns of different intensity, the
animals significantly steered towards the side of the louder sound source as
soon as the intensity difference was greater than 1 dB SPL. However, during
bilateral stimulation even at intensity differences of 15 dB their steering
behaviour appeared to be noisier and the lateral deviation less accurate as
during unilateral stimulation. A sensitivity of crickets towards binaural
intensity differences of at least 2 dB had been inferred from auditory
lateralization experiments by Rheinlaender and Blätgen
(1982
). Our measured
sensitivity supports this conclusion. The crickets' sensitivity is thus
similar to the performance of the grasshopper Chorthippus biguttulus
(Helversen and Rheinlaender,
1988
) and the bush cricket Gampsocleis (H. Römer,
personal communication). In these species turning behaviour towards the louder
of two stimuli is reliably correct as soon as the interaural intensity
differences are 12 dB.
The effect of bilateral latency differences on phonotactic steering
When both ears of walking crickets were exposed to identical sound patterns
shifted in time, the animals only weakly steered towards the leading sound
pattern. Even the best response at 4 ms was comparably poor and was similar to
a response to bilateral intensity differences of just 2 dB. This was
unexpected since in flying crickets a delay of 475 ms between
ultrasound pulses causes a clear precedence effect with the animals steering
away from the leading sound pulse. Only between 02 ms is the direction
of the turn arbitrary relative to the sound pulse
(Wyttenbach and Hoy, 1993).
Rheinlaender and Mörchen
(1979
) demonstrated that
during binaural stimulation of a locust directionally sensitive auditory
interneurone, a time difference of just 4 ms is sufficient for the leading
stimulus to completely suppress the response towards the sound following from
the contralateral side. In behavioural experiments, grasshoppers reliably
orientate towards the leading of two identical sound patterns, as soon as the
delay between the patterns reaches 1 ms
(Helversen and Rheinlaender,
1988
). A network for bilateral auditory contrast enhancement
operates in the auditory pathway of crickets. The mutual inhibitory network of
the Omega neurons seems to be designed for the processing of directional
information (see Hennig et al.,
2004
, for review). We therefore had expected a clearer orientation
of the crickets towards the leading sound. One possibility for the poor
directional responses could be a direct unilateral effect of the auditory
input onto the ipsilateral motor networks. Under these circumstances, the
motor effects evoked at both sides would cancel. However, the averages of the
steering responses should have revealed an initial phasic steering response
towards the side of the leading sound pattern. Such a response was not evident
in the averages. We therefore also consider that superimposing two effective
patterns may have reduced the effectiveness of the resulting pattern, either
within the peripheral auditory system due to detrimental phase shifts of the
sound waves [which may have led to a loss of directionality
(Michelsen and Löhe,
1995
)], or due to deteriorating the overall temporal structure of
the song for the recognition process. However, our data are in agreement with
auditory steering in flying crickets, which also depends on intensity
differences of auditory afferent activation rather than latency differences
(Pollack, 2003
).
Rapid steering to single sound pulses, and concepts of pattern recognition and orientation
After a change of sound direction, previous studies have reported that
crickets change their walking direction within 1500 ms
(Schmitz et al., 1982) or
after 5001000 ms (Schildberger and
Hörner, 1988
). These values may indicate that the crickets
turning response is based on the evaluation of the chirp pattern but rather
may be due to the low temporal resolution of the treadmills. Our highly
sensitive trackball system revealed latencies for turning 20 times faster. In
our split song paradigms, crickets changed their walking direction even within
a chirp and steered towards single sound pulses with a latency of just
5560 ms. These rapid steering responses have important consequences for
the currently proposed concepts of pattern recognition and orientation.
Auditory steering within 55 ms poses the question about whether such
responses can be mediated with the participation of temporal filtering
circuits in the brain. The band-pass circuits in the brain seem to be tuned
towards the species-specific syllable rate and are regarded as central
elements for pattern recognition
(Schildberger, 1984). A simple
calculation provides the processing time for the proposed type of pattern
recognition required. At 70 dB SPL, the cephalic arborisations of the
ascending interneurone AN1 responds after about 20 ms. The band-pass neurons
BNC2, which are assumed to be central to pattern recognition, are activated
with a latency of about 45 ms
(Schildberger, 1984
). A band
pass network has to process at least two syllables to evaluate the syllable
rate and to activate the proposed band-pass recognition process. With the
SRI42 sound pattern used here this corresponds to 63 ms. After activation of
BNC2 another 5 ms will be needed to transmit any resulting steering command
towards the thoracic system and we may assume an additional 30 ms to generate
the motor activity. Thus, a steering command that is based on the output of
the proposed band-pass filter in the brain will need about 143 ms to evoke a
motor response. The rapid turning behaviour towards individual syllables
(5560 ms) therefore leaves no time for the band-pass pattern
recognition process to be involved in the encountered rapid phonotactic
steering. Conversely, Schildberger and Hörner
(1988
) describe changes in
walking direction upon modulating the activity of ascending auditory neurons
but unfortunately do not give the latency of these responses. Some descending
brain neurons respond to sound and appear to be involved in the control of
walking (Böhm and Schildberger,
1992
). They respond to high intensity sound after a latency of
2540 ms (Staudacher,
2001
). The auditory response of these descending brain neurons was
not very regular and the neurons were activated by other sensory modalities as
well. The auditory response latency of some of these neurons may just be short
enough so that they could be directly involved in the control of rapid turning
responses, however the pathways by which they are activated are not yet
known.
A generally accepted concept for cricket phonotaxis suggests a serial
organisation of pattern recognition and localization. It is proposed that two
bilateral recognisers in the cricket CNS first filter the ascending
information and that the output of these two recognisers is then compared to
allow the animal to steer towards the `better' of two patterns
(Pollack, 1986;
Stabel et al., 1989
;
Wendler, 1990
;
Helversen and Helversen,
1995
). The rapid steering responses towards single sound pulses,
however, demonstrate that the overall temporal structure of the sound pattern
is not evaluated for steering. Our behavioural data therefore refute the
proposed serial organisation of the recognition and localization process.
During phonotactic walking each sound pulse presented from one side of the
cricket generated a steering response towards that side. There was a clear
dependence between the number of syllables presented from one side and the
overall lateral deviation of the animals. The relation between the number and
the intensity of sound pulses perceived at each ear determined the overall
direction of walking. As a consequence cricket auditory orientation emerges
from singular steering events and not from the calculation of a steering
direction. The cricket G. bimaculatus solves the complex task of
auditory orientation with a most simple algorithm by turning towards
individual sound pulses (Hedwig and Poulet,
2004
). Female G. campestris, when exposed to sound
patterns interleaved from a left and right speaker, walked in a direction
between the speakers (Weber and Thorson,
1988
). This may be due to an optimum zone for recognition and
tracking, but may also be the consequence of symmetrical steering responses to
both speakers, which led to an intermediate walking path involving steering
responses that were not resolved by the treadmill system.
Is there a thoracic pathway for steering?
The rapid auditory steering responses may be controlled by the brain and/or
they may be mediated directly to the walking motor network at the thoracic
level. Considering the evolutionary history of the cricket auditory organ may
support the second assumption. In insects, hearing organs have evolved from
chordotonal organs providing proprioceptive feedback to the CNS. In crickets
and bushcrickets, in particular, the chordotonal organ in the front leg has
evolved to a hearing organ (Fullard and
Yack, 1993). In acridid Orthoptera, the homologous chordotonal
organ in the forelegs is involved in mediating fast proprioceptive feedback to
motor networks controlling leg position and walking
(Burrows, 1996
). Although in
the cricket a postsynaptic thoracic pathway has evolved for the processing of
sound, at least part of the `old' proprioceptive network linked to motor
control may have been conserved (Dumont and
Robertson, 1986
) and may still provide a fast and effective
auditory-to-motor interface. Thus, a direct reflex-like link may allow
integrating rapid responses to sound pulses into the walking motor pattern.
Evidence for these still speculative thoughts may be gained from further
analysis of the auditory steering responses.
Future analysis: interaction of pattern recognition and steering
If phonotaxis is strictly based on responses to individual sound pulses,
then G. bimaculatus should indiscriminately steer towards any
auditory pattern with an appropriate carrier frequency. Phonotactic walking,
however, depends on the temporal structure of the sound
(Weber et al., 1981). Thus,
pattern recognition is necessary for phonotaxis to occur. However, the
functional relationship between the recognition and localization process may
be dynamic and both may even have different selectivity for temporal patterns.
Steering towards non-attractive patterns occurred temporarily after crickets
were exposed to attractive songs (Weber et
al., 1981
), and steering could even be elicited when
non-attractive patterns were combined with an attractive pattern resembling
the species-specific songs (Doherty,
1991
). These experiments indicate that a recognition process may
control and activate a separate localization process. However, to understand
further the organisation of cricket phonotaxis we propose that a thorough
re-evaluation of pattern recognition and its impact on localization is
required.
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