Infrasound initiates directional fast-start escape responses in juvenile roach Rutilus rutilus
1 Institute of Biology, University of Oslo, Blindern N-0316,
Norway
2 Vision Touch and Hearing Research Centre, School of Biomedical Sciences,
University of Queensland 4072, Australia
* Author for correspondence (e-mail: h.e.karlsen{at}bio.uio.no)
Accepted 6 September 2004
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Summary |
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Key words: fish, Rutilus rutilus, startle response, C-escape response, S-escape response, predator avoidance, infrasound, acceleration, compression, rarefaction, Mauthner neuron
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Introduction |
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The otolith organs of the inner ears in fish are inertial motion detectors
directly stimulated by the particle accelerations of a sound wave, and fish
may use these organs to determine the three-dimensional directionality of an
incident sound wave (see review by Sand,
2002). Upon exposure to sound, the surface of a swim bladder may
show amplified radial motions that are transmitted to the inner ear, providing
an auditory gain to the fish (see review by
Popper et al., 2003
). Thus,
fish with a swim bladder are sensitive to both the kinetic and pressure
components of sound. By decoding the phase difference between these
components, fish may be able to discriminate between opposing sound sources
(180° apart) (Schuijf,
1975
,
1981
;
Buwalda et al., 1983
;
Schellart and de Munck,
1987
).
The phase comparison theory for sound source localization in fish has
recently been extended to a neural model (called the XNOR-model) for how the
different elements of the neural escape network may perform the
leftright sound discrimination evident in acoustic startle behaviour
(Eaton et al., 1995;
Guzik et al., 1999
). In
essence, the model predicts that directionality is determined by a time domain
neural analysis of the initial polarities of the sound pressure and
acceleration. Thus, an attack from the right will produce an initial right to
left acceleration combined with a pressure increase, while a suction type of
predator at this position will cause left to right acceleration and a
rarefaction. Crucial assumptions of the model are that both these initial
combinations of sound pressure and acceleration should inhibit the left and
activate the right side Mauthner cell system, in order to elicit the
appropriate escape to the left.
Numerous neurophysiological and behavioural studies have been conducted to
clarify the sensory modalities involved in startle behaviours in fish.
However, most of the behavioural studies performed to date have been hampered
by insufficient control of the stimulus parameters. One of the few studies
with a carefully controlled stimulus design is that of Blaxter et al.
(1981), who found that herring
Clupea harengus L. were able to perform C-starts away from an
underwater sound source independently of whether the first sound cycle started
with compression or rarefaction. However, the stimulus frequencies used were
too high (26160 Hz) to conclude whether the C-starts were elicited by
sound compression, rarefaction, or both. Thus, behavioural data relevant for
testing the validity of the XNOR-model is still lacking, as is also
electrophysiological data. By performing intracellular recordings from M-cells
in the goldfish, Canfield and Eaton
(1990
) showed that sound
pressure was the salient stimulus for activation, but independent effects of
sound compression versus rarefaction were not studied. In the later
study by Casagrand et al.
(1999
), sound acceleration and
pressure were found to be effective stimuli of both M-cells and other M-cell
homologs in the brain stem. However, the frequencies used were again too high
(1002000 Hz) to reveal the relative effects of sound compression and
rarefaction. In addition, the acceleration and pressure components were tested
separately and not jointly in a manner comparable to natural conditions.
In earlier studies of acoustic escape responses in fish, the focus has
mainly been on frequencies above 100 Hz. However, a typical head-on attack by
a predatory fish produces complex hydrodynamic and acoustics stimuli with
frequency components mainly below 100 Hz
(Bleckmann et al., 1991). In
fact, a swimming goldfish generates a hydrodynamic flow field with the main
acceleration components below 1020
Hz(Enger et al., 1989
). The
possible significance of such low frequency stimuli for escape behaviour is
still unknown. We have previously shown that the otolith organs in fish are
highly sensitive to the acceleration component of infrasound down to at least
0.1 Hz (Sand and Karlsen,
1986
; Karlsen,
1992a
,b
).
Typical behavioural threshold values are in the range of 105
m s2, or 4 orders of magnitude less than for detection of
linear accelerations in humans. At higher intensities around
102 m s2, infrasound can initiate strong
avoidance responses in fish (see review by
Sand et al., 2001
). For a prey
fish, such sounds could indicate an approaching predator. We thus predicted
that also infrasound might excite Mauthner neurons, and we have tested this
assumption by using juveniles of the ostariophysan species roach Rutilus
rutilus L. The fish were tested in a swing apparatus in which a suspended
chamber was used to accelerate both the fish and surrounding water linearly in
a quantifiable way (Karlsen,
1992b
). Infrasonic accelerations did evoke C- and S-type startle
responses. The responses were directional, and on average in the same
direction as the initial phase of acceleration. In contrast to the
postulations of the XNOR-model, only fish subjected to the combination of
acceleration and compression readily responded, while those experiencing
acceleration and rarefaction did not.
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Materials and methods |
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Experimental apparatus
The test apparatus was a swing system previously employed to study
infrasound hearing in fish (see diagram in
Karlsen, 1992b). In short, a
Perspex chamber filled with water was suspended by four steel strings from a
solid steel framework attached to a 150 kg concrete block. The block rested on
a 20 cm layer of dry sand poured directly on the concrete basement floor. The
horizontal background acceleration noise level measured at the chamber wall
was less than 106 m s2 in the frequency
range 0.1200 Hz. The dimensions of the chamber were 40 cm x20 cm
x15 cm, corresponding to a volume of 12 l. The test chamber was
accelerated by a Derritron VP3 vibrator (Riverside, CA, USA) secured to the
concrete block and connected to the end wall of the suspended chamber by a
horizontally aligned metal shaft. The displacement and acceleration of the
chamber during testing were monitored by a linear variable differential
transformer (LVDT) (Shaevitz 100 DC-D, Hampton, VA, USA) and an accelerometer
(Entran EGCS-A2-2, Les Clayes-sous-Bois, France) attached to the chamber wall
opposite to the vibrator. The pressures at different positions inside the
chamber were measured using a hydrophone (Brüel & Kjær 8104,
Nærum, Denmark). The sinusoidal driving voltage to the vibrator was
produced by a function generator (Wavetek 186, Norwich, UK) and consisted of a
single cycle. In order to avoid acceleration transients at the onset of the
stimulus, the waveform was d.c.-shifted one peak value and phase shifted to
start at 90° (Fig.
1). The waveform was pulse triggered and passed through an
attenuator and a power amplifier before reaching the vibrator. The pulse
triggering the function generator was initiated manually using a stimulator
(Grass S4, West Warwick, RI, USA).
|
The behaviour of the fish was monitored by video recording at 25 frames s1 using a Sony DCR-VX 1000E video camera looking down at the fish through the transparent roof of the test chamber. The bottom of the tank was light grey, in order to make the darker fish stand out when seen from above, and marked with thin centre lines. The behaviour of the fish was observed in real time on a TV screen, and the video recordings were simultaneously stored on a Hitachi Super VHS video recorder. A small red LED display driven by the triggering pulse to the function generator was placed at the corner of the camera view. A digital oscilloscope was used to simultaneously record the driving voltage to the vibrator and the outputs from the LVDT, accelerometer and hydrophone. Hard copies of the respective waveforms were obtained using an x,y plotter connected to the oscilloscope.
Stimulus waveform
The waveforms of the driving voltage to the vibrator and the outputs from
the different transducers are compared in
Fig. 1. The shape of these
waveforms were inverted, but otherwise unaffected, by changing the initial
acceleration from push to pull mode. Evidently, the simple one cycle, phase-
and d.c.-shifted driving voltage induced chamber accelerations and
displacements of rather complex waveforms. However, the escape responses were
evoked during the period between stimulus onset and the initial acceleration
peak. Within this period, the acceleration approached the initial half-cycle
of a sinusoidal waveform of 1.7 x the driving frequency, starting at
90°. Hence, assuming that acceleration was the relevant stimulus
parameter, the effective stimulus frequency was about 1.7 x the
frequency of the driving voltage to the vibrator. The frequency of the
corresponding initial compression or rarefaction inside the chamber was
approximately 2.1 x the driving frequency. In the result section, the
stimulation frequency is presented as the frequency of the initial
acceleration. In most of the tests, the driving frequency was 4 Hz, and the
frequency of the initial acceleration was then approximately 6.7 Hz.
Testing procedure
Before testing began, about eight fish at a time were transferred gently to
the test chamber and allowed to rest for at least 8 h, usually overnight,
before the first stimulus. Care was taken to ensure that no air bubbles
remained in the chamber after transfer of the fish. The test chamber was
normally filled with water from the lake. However, in some tests the lateral
line was blocked by adding 0.1 mmol l1 Co2+ to
virtually Ca2+-free artificial freshwater. This procedure
completely abolishes the mechanosensitivity of the lateral line system in
roach without affecting the inner ear
(Karlsen and Sand, 1987). A
total of 54 fish were tested in the main series of experiments, employing the
6.7 Hz stimulus at 15 dB above threshold, and each group of 78 fish in
the chamber was stimulated four times. The test fish were not tagged, and we
were thus unable to examine the responses and responsiveness of each
individual fish. All experiments were recorded on videotape, and a resting
period of minimum 30 min was allowed between tests. The swing apparatus was
kept in a separate room isolated from the control room, in which the
investigators were conducting the experiments. All the electronic instruments,
apart from the camera, the vibrator and the transducers attached to the
chamber, were also kept in the control room.
Data analysis
During playback analysis, the frame-by-frame movement of each fish in a
given trial was traced by hand onto a clear plastic film taped to the front of
the TV monitor. The frame corresponding to stimulus onset was identified by
the flashing LED. Tracing was done for 5 frames, or 200 ms, starting at the
frame before stimulus onset. A distance calibrator within the chamber made it
possible to calculate the swimming distances and velocities between frames.
For plots of startle trajectories, the position of the head of the fish in
each frame was converted into x,y coordinates, starting at (0,0) for
the frame before stimulus onset. Coordinates were entered into a computer and
the trajectories were plotted using the program Sigmaplot 2000. The final
escape angle relative to the direction of acceleration was calculated using
the head coordinates of last two frames of the 5-frame sequence.
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Results |
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The fish did show some variability in the apparent latency of the response. This was mainly due to lack of synchronization between the video frame timing and the manually initiated stimulus. The frame containing the LED monitor flash was termed frame 0. The starts of the 84 escapes were distributed as follows: frame 0, 1; frame 1, 30; frame 2, 43; frame 3, 7; frame 4, 1; frame 5, 2. To be sure that the fish were responding to the initial phase of acceleration at 6.7 Hz, and to minimize the chance of secondary responses to other responding fish, the 10 startle responses occurring in frames 35 were excluded when response latencies and final escape angles were estimated and when escape trajectories were traced. The average latency of the remaining 74 responses was approximately 63 ms. These responses were initiated within the duration (about 80 ms) of the initial compression or rarefaction in the chamber (Fig. 1).
We also made a series of preliminary experiments on the threshold of the acceleration response as a function of frequency. Each frequency was calculated from the rise time of the accelerometer waveform. Our tentative conclusion was that the threshold acceleration needed to trigger the response became higher as frequency was decreased within the tested range between 3.4 and 32 Hz.
Polarity of the response
During the early stages of the project, we noticed that the fish showed a
tendency to jump or shoot in the same direction as the initial acceleration of
the swing. To study this further, we changed the polarity of the initial swing
movement between push and pull, in a quasi-random fashion. The frequency of
the initial acceleration was 6.7 Hz and the stimulus level was approximately
15 dB above the response threshold. Fig.
2 shows the resulting flight trajectories of the response to
initial movements of the test chamber from right to left, push-mode (A), and
from left to right, pull-mode (B). The direction of the flight trajectories
showed a wide scatter, but the average direction coincided with the direction
of the initial acceleration. The final escape angle relative to the stimulus
direction, as defined by Domenici and Blake
(1993), approximated a
symmetric and unimodal distribution as shown in
Fig. 3. There was no obvious
difference between the average response direction of the first fish responding
in a group and the more delayed startle responses, strengthening the
assumption that all the analysed responses were to the initial stimulus and
not secondary to other responding fish.
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For initial accelerations in both push and pull modes, it was noticed that nearly all escape responses occurred in the trailing half of the chamber, where the initial acceleration was associated with a pressure increase. Only 3 of the 74 startle responses studied in detail occurred in the leading half of the chamber, where the initial acceleration coincided with a pressure decrease. A summary of these data is shown in Fig. 4. In preliminary tests, the ambient pressure within the tank in the absence of acceleration was abruptly increased by rapidly lifting the outlet tube. Such treatment had no behavioural effects at all, even for sudden pressure elevations much larger than those encountered in the acceleration studies, suggesting that the observed responses were not induced by increased pressure alone. In the future, experiments allowing independent control of acceleration and pressure changes of variable waveforms will be performed.
|
Control for involvement of the lateral line or visual cues
The swing system used in the experiments was designed to move the fish and
the surrounding water together as a unit, in order to minimize the possibility
of lateral line activation (Karlsen,
1992b). To completely eliminate the possible involvement of this
sensory modality in the response, we also tested a group of fish after 24 h in
virtually Ca2+-free water containing 0.1 mmol l1
Co2+ (Karlsen and Sand,
1987
). Cobalt treatment had relatively little effect on the
resting behaviour of the fish. The most noticeable deviation from normal
behaviour, indicating effective blocking of the lateral line, was that
individual fish would occasionally bump into each other. This behaviour was
never observed in fish in normal freshwater. Under cobalt blocking, the fish
still responded selectively to the polarity of the stimulus, but for a few
occasional exceptions. There was still a strong tendency for responses to
occur only in the compression side of the chamber, and the trajectories were
still on average in the same direction as the initial acceleration (Figs
4,
5). However, the shooting
distances were reduced slightly, and this correlated with a slower
between-stimulus cruising speed in Co2+-containing water.
|
All lighting in the test room was arranged to avoid any cues to the fish in the form of moving edges or shadows. In addition, we did a number of tests with no acceleration, but with either a moving light or a series of opaque objects and edges moving against a lit background. In no case did these stimuli evoke flight behaviour, and we conclude that the observed escape responses were not to visual cues.
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Discussion |
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The initial acceleration created rarefaction in the leading half of the
test chamber and compression in the trailing half. Maximum positive and
negative pressure amplitudes were created at the end walls while negligible
pressures appeared at the midline of the chamber. Since the test fish were
moving freely about and responses occurred at different positions in the
chamber, we were unable to relate precise pressure thresholds to the startle
responses. However, the hydrophone measurements that were performed indicated
that they were in the order of a few tens of pascals. Even though numerous
studies have characterized the kinematics and the neural basis of startle
behaviour in fish, few studies have been concerned with response thresholds.
Still, the limited data that exist are in agreement with the thresholds of the
present study. Casagrand et al.
(1999) found the acceleration
thresholds for detection of excitatory postsynaptic potentials (EPSPs) from
M-cells in goldfish to be around 0.01 m s2 at 125 Hz.
Casagrand et al. (1999
) also
recalculated the sound pressure threshold given by Lewis and Rogers
(1998
), for eliciting
directional startle behaviours in goldfish, to an acceleration threshold of
0.03 m s2. Blaxter et al.
(1981
) and Blaxter and Hoss
(1981
) found the threshold for
acoustic startle in the herring to be approximately 70 dB above the absolute
threshold, corresponding to pressures in the range 218 Pa(70200
Hz) and to accelerations within the range 0.010.04 m
s2.
The latency of acoustic or vibratory startle responses in fish are
typically in the range 540 ms depending on the stimulus intensity and
frequency (Eaton et al., 1977;
Blaxter et al., 1981
). This is
significantly shorter than the average response latency of 68 ms we observed
at approximately 15 dB above threshold. Although the time resolution of the
employed video system is inadequate for estimating the short latencies of
startle responses evoked by intense acoustic stimuli at sonic frequencies, the
low time resolution is sufficient for a rough estimate of the relatively long
average response latencies to infrasonic stimuli observed in the present
study. Many factors may influence latency, i.e. temperature, fish species,
size etc. However, the relatively long latency in our study may mainly reflect
the low stimulus frequency, and thus an increased time to reach threshold
levels. In any event, the observed latencies were far shorter than the latency
of visually evoked startles, which are typically in the range 100120
ms. The startle responses to infrasonic vibration were not triggered by the
lateral line organs, because selectively blocking this system by using the
cobalt technique (Karlsen and Sand,
1987
) did not eliminate the responses. Thus we feel confident that
all the observed startle responses were triggered by the inner ear. Lateral
line stimulation may still participate in evoking startle responses under
natural conditions. As noted, the swing system was designed to avoid possible
lateral line stimulation, by moving the fish and surrounding water as a unit.
However, a striking predator in the field may be approximated by an acoustic
dipole source, and will generate potent lateral line stimuli at close
range.
Types of startle responses observed
Fish are known to display different types of fast-start escape behaviours
as defined by the pattern of the initial body bending (Domenici and Blake,
1997; Hale, 2002;
Hale et al., 2002
). In the
present study we found that all variants of initial body shapes (C, S and J)
described for fast-start responses in fish could be triggered by infrasound
and thus by output from the inner ear otolith organs alone. The classical
C-response comprised 68% of the infrasound-induced startles we studied in
detail. In freely moving ostariophysan fish, acoustically triggered C-starts
are generally accepted to always involve the Mauthner cell proper, being the
first spinal-projecting neuron activated in the brain stem
(Zottoli, 1977
;
Eaton and Bombardieri, 1978
;
Eaton et al., 1981
; see review
by Zottoli and Faber, 2000
).
In addition to the M-cell, activation of morphologically homologous
commissural neurons in adjacent hindbrain segments are currently also believed
to be important for the full initial C-bend of the body
(Eaton et al., 1982
;
Kimmel et al., 1982
;
Metcalfe et al., 1986
;
Eaton and Lee, 1991
;
Lee et al., 1993
;
Forman and Eaton, 1993
). The
propulsive phase of the C-response, which essentially involves a counter bend
of the body, is postulated to be controlled by a functional group of more
caudal medullar neurons having ipsilateral spinal projections
(Forman and Eaton, 1993
;
Eaton et al., 2001
;
Hale, 2002
). Direct evidence
for the existence of an extensive and hierarchic brain stem escape network has
recently been obtained using calcium imaging to monitor the activity in
reticulospinal neurons in the transparent larvae of zebrafish Danio
rerio H. (see review by Fetcho and
O'Malley, 1997
; Liu and
Fetcho, 1999
; Ritter et al.,
2001
; Gathan et al.,
2002
).
A typical S-escape response, characterized by significant but opposite
initial anterior and posterior body curvatures, was observed in 12% of the
infrasound startles. The initial body shape strongly suggests that this
response most likely does not involve activation of the Mauthner neuron
proper. Hale (2002) instead
proposed that it may be initiated by a parallel activity of M-cell serial
homologs and ipsilateral reticulospinal neurons, activating nearly
simultaneously the frontal contralateral trunk musculature and the caudal
ipsilateral trunk muscles respectively. In addition to being employed to avoid
predators, the S-start behaviour is also used offensively during prey strikes
(Webb and Skadsen, 1980
;
Harper and Blake, 1991
;
Frith and Blake, 1995
;
Johnston et al., 1995
).
The J-response also comprised 12% of the startle responses. It was
characterized by the largest curvature appearing posterior in the animal, with
the tail moving almost perpendicular to the anterior axis. Like the
S-response, the J-response is also typically used both for escape and attack.
Following the model of Hale
(2002), the J-response may
reflect activation of the same pool of ipsilateral reticulospinal neurons that
participate in the typical S-response, but differs from this by showing no
activation of commissural neurons.
The I-response (8%) was characterized by an apparent lack of initial body bending apart from a very small tail bend, and it was typically observed in fish about to shoot straight forward with no change in trajectory. It was unclear to us if the I-response was a true startle response, or if it involved a direct activation of neural circuits for fast undulatory swimming rather than the escape network.
It has been suggested that different startle responses may be viewed as a
degrading series of escape behaviours initiated by different subsets of the
startle neural circuit. Our data seem to fit this idea. In the present study
we did not correlate response type to initial movement velocity or orientation
of the responding fish. Modulation of the escape response by afferent inputs
is, however, known from other studies
(Eaton and Emberley, 1991) and
away-from-stimulus responses are known to occur significantly more often than
toward-stimulus responses (Domenici and
Blake, 1993
).
Eaton et al. (1977)
suggested that fish startles should be unpredictable in order to prevent
predators from learning any fixed patterns of response and compensating for
it. Escape trajectories have also been found to vary considerably after the
initial turn away from the stimulus (Eaton
et al., 1981
; Eaton and
Emberley, 1991
). In the present study we found the escape
responses of juvenile roach to have both a strong deterministic component
(following the direction of initial acceleration) and a significant stochastic
secondary component (wide scatter of the trajectories). The final escape
angles relative to the stimulus direction, as shown in
Fig. 3, indicate a unimodal
distribution and thus no definite preferred escape trajectories as was found
in angelfish and other animals (Domenici
and Blake, 1993
).
Directionality of the startle responses
All the different types of infrasound-induced startle responses that we
recorded were directional, and thus in concurrence with earlier studies of
acoustic startles in fish (Moulton and
Dixon, 1967; Zottoli,
1977
; Blaxter et al.,
1981
; Blaxter and Fuiman,
1990
; Eaton and Emberley,
1991
; Foreman and Eaton, 1993). Even though the flight
trajectories showed a wide scatter, with an envelope occupying approximately a
hemifield (see Figs 2,
3), the average response
direction coincided with the direction of the initial acceleration experienced
by the fish. Fish are assumed to be able to determine the direction to simple
monopole sound sources by comparing the phase of sound pressure to the phase
of the incident particle acceleration. According to this phase model
(Schuijf, 1981
), the direction
of acceleration during sound compression should be interpreted by the fish as
movement away from the source. Movements experienced during rarefaction, on
the other hand, will be towards the source. In our experiments the startle
movements were generally in the direction of the initial acceleration and
during compression, which we interpret as an adaptive movement away from a
threatening sound source such as an advancing predator.
A prerequisite for the phase model is that the fish is able to separately
encode and compare the phases of sound pressure and incident particle motion.
In the ostariophysan hearing specialists, including the roach, such a task is
clearly feasible. The sacculus in these fish detects extremely low pressure
levels by being connected via the Weberian ossicles to the swim
bladder. The sensory hair cells in the sacculus are arranged in two oppositely
oriented populations; one set that depolarises on the compression phase and
the other on the rarefaction phase
(Furukawa and Ishii, 1967;
Hama, 1969
;
Sento and Furukawa, 1987
).
Goldfish is known to discriminate behaviourally between compressions and
rarefactions (Piddington,
1972
). While the sacculus in the ostariophysi appears to be
dedicated to encoding phases of sound pressure, the direction of initial
acceleration may be encoded by the utricle and the lagena (see review by
Popper and Edds-Walton, 1995
).
In both these otolith organs the hair cells are distributed with sensory axes
at a variety of angles across the sensory epithelium
(Popper and Platt, 1983
;
Platt, 1993
).
Role of compression in initiation of startle responses
Casagrand et al. (1999) have
shown that both sound pressure and acceleration cause excitatory postsynaptic
potentials in Mauthner neurons and homologous cells, but sound pressure was a
much more efficient stimulator than acceleration. The authors therefore
concluded that acceleration alone would not be able to initiate a startle
response. In the present study we were not able to elicit startle responses by
pressure increases alone. In natural conditions, neither pressure nor
acceleration will appear separately, and it is thus not surprising that both
components are necessary to elicit startle in fish. Even though acceleration
conveys the crucial directional information to the fish, several studies have
shown that the startle escape appears to be triggered only when the pressure
reaches a critical value (Blaxter and Hoss,
1981
; Blaxter et al.,
1981
; Blaxter and Fuiman,
1990
; Canfield and Eaton,
1990
).
Eaton et al. (1995) and
Guzik et al. (1999
) have
adopted the original phase model for directional hearing to explain the
directional startle responses. Their model is based on the extensive afferent
input from the ear converging on the Mauthner system, and both phases of
pressure are assumed to be able excite and drive the Mauthner neurons.
Contrary to this assumption, we observed that only fish experiencing
acceleration and compression responded, while those that experienced
acceleration in combination with rarefaction did not. Rather unexpectedly,
this suggests that only a pressure increase may elicit acoustic startles,
while rarefactions somehow cancel or inhibit this response at least at
low frequencies. In their behavioural study, Blaxter et al.
(1981
) found the directionality
of acoustic startle responses in herring to be independent of the initial
stimulus polarity being compression or rarefaction. This has been interpreted
as if the herring were responding equally well to both pressure polarities
(Eaton et al., 1995
). However,
this may not be true since Blaxter et al.
(1981
) found the threshold to
initial rarefaction to be about 3 dB lower than for initial compression. The
stimuli used comprised a single cycle of a 80 Hz sine wave, and due to the
mass load (resonance properties) of their setup the amplitude of the first
half cycle was 36 dB lower than for the second half cycle. The
increased sensitivity to initial rarefaction may therefore reflect the fact
that their fish were responding only to compression irrespective of the
stimulus starting with compression or rarefaction. Further studies are clearly
needed to clarify these questions.
Conclusions
Fish have an acute sensitivity to infrasound, or linear accelerations, and
have been proposed to exploit this ability in a number of behaviours including
predatorprey interactions. In the present study we have demonstrated
for the first time that intense infrasound is efficient in eliciting classical
startle responses in fish. The behaviour is triggered by the synergistic
effects of initial acceleration and compression, corresponding to the stimulus
generated by (for example) an approaching predator. This finding supports the
idea that predator detection may have played a significant role in the
evolution of fish hearing and the Mauthner neural system (see review by
Eaton and Popper, 1995).
Unexpectedly, responses were inhibited by rarefaction, suggesting a need for
more behavioural studies designed to further test the validity of current
models for neuronal computation of startle directionality.
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Acknowledgments |
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References |
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Blaxter, J. H. S. and Fuiman, L. A. (1990). The role of the sensory systems of herring larvae in evading predatory fishes. J. Mar. Biol. Assn UK 70,413 -427.
Blaxter, J. H. S. and Hoss, D. E. (1981). Startle response in herring: the effect of sound stimulus frequency, size of the fish and selective interference with the acoustico-lateralis system. J. Mar. Biol. Assn UK 61,871 -879.
Blaxter, J. H. S, Gray, J. A. B. and Denton, E. J. (1981). Sound and startle responses in herring shoals. J. Mar. Biol. Assn UK 61,851 -869.
Bleckmann, H., Breihaupt, T., Blickman, R. and Tautz, J. (1991). The time course and frequency content of local flow fields caused by moving fish, frog and crayfish. J. Comp. Physiol. A 168,749 -757.[Medline]
Buwalda, R. J. A., Schuijf, A. and Hawkins, A. D. (1983). Discrimination by the cod of sounds from opposing directions. J. Comp. Physiol. 150,175 -184.
Canfield, J. G. and Eaton, R. C. (1990). Swimbladder acoustic pressure transduction initiates Mauthner-mediated escape. Nature 347,760 -762.[CrossRef]
Casagrand, J. L., Guzik, A. L. and Eaton, R. C.
(1999). Mauthner and reticulospinal responses to onset of
acoustic pressure and acceleration stimuli. J.
Neurophysiol. 82,1422
-1437.
Domenici, P. and Blake, R. W. (1993). The kinematics and performance of fish fast-start swimming. J. Exp. Biol. 200,1165 -1178.
Eaton, R. C. and Bombardieri, R. A. (1978). Behavioural functions of the Mauthner neuron. In Neurobiology of the Mauthner Cells (ed. D. A. Faber and H. Korn), pp.221 -244. New York: Raven Press.
Eaton, R. C. and Emberley, D. S. (1991). How stimulus direction determines the trajectory of the Mauthner-initiated escape response in a teleost fish. J. Exp. Biol. 161,469 -487.[Abstract]
Eaton, R. C. and Lee, R. K. K. (1991). Idendifiable reticulospinal neurons of the adult zebrafish, Brachydanio rerio. J. Comp. Neurol. 304,34 -52.[Medline]
Eaton, R. C. and Popper, A. N. (1995). The octavolateralis system and the Mauthner cell: interactions and questions? Brain. Behav. Evol. 46,124 -130.[Medline]
Eaton, R. C., Bombardieri, R. A. and Meyer, D. L. (1977). The Mauthner-inititated startle response in teleost fish. J. Exp. Biol. 66,65 -81.[Abstract]
Eaton, R. C., Lavender, W. A. and Wieland, C. M. (1981). Identification of Mauthner initiated response patterns in goldfish: evidence from simultaneous cinematography and electrophysiology. J. Comp. Physiol. A 144,521 -531.
Eaton, R. C., Lavender, W. A. and Wieland, C. M. (1982). Alternative neural pathways initiate fast-start responses following lesions of the Mauthner neuron in Goldfish. J. Comp. Physiol. 145,485 -496.
Eaton, R. C., Canfield, J. G. and Guzik, A. L. (1995). Left-right discrimination of sound onset by the Mauthner system. Brain Behav. Evol. 46,165 -179.[Medline]
Eaton, R. C., Lee, R. K. K. and Foreman, M. B. (2001). The Mauthner cell and other identified neurons of the brainstem escape network of fish. Prog. Neurobiol. 63,467 -485.[CrossRef][Medline]
Enger, P. S., Kalmijn, A. J. and Sand, O. (1989). Behavioral investigations of the function of the lateral line and inner ear in predation. In The Mechanosensory Lateral Line. Neurobiology and Evolution (ed. S. Coombs, P. Görner and H. Münz), pp. 575-587. New York: Springer Verlag.
Faber, D. S., Fetcho, J. R. and Korn, H. (1989). Neural networks underlying the escape response in goldfish. Ann. NY Acad. Sci. 563, 11-33.[Medline]
Faber, D. S., Korn, H. and Lin, J. W. (1991). Role of medullary networks and postsynaptic membrane properties in regulating Mauthner cell responsiveness to sensory excitation. Brain Behav. Evol. 37,286 -297.[Medline]
Fetcho, J. R. and O'Malley, D. M. (1997). Imaging neuronal networks in nehaving animals. Curr. Opin. Neurosci. 7,832 -838.[CrossRef]
Forman, M. B. and Eaton, R. C. (1993). The direction change concept for reticulospinal control of goldfish escape. J. Neurosci. 13,4101 -4113.[Abstract]
Frith, H. R. and Blake, R. W. (1995). The mechanical power output and hydromechanical efficiency of northen pike (Esox lucius) fast starts. J. Exp. Biol. 198,1863 -1873.[Medline]
Furukawa, T. and Ishii, Y (1967).
Neurophysiological studies on hearing in goldfish. J.
Neurophysiol. 30,1377
-1403.
Gathan, E., Sankrithi, N., Campos, J. B. and O'Malley, D. M.
(2002). Evidence for a widespread brain stem escape network in
larval zebrafish. J. Neurophysiol.
87,608
-614.
Guzik, A. L., Eaton, R. C. and Mathis, D. W. (1999). A connectionist model of left-right sound discrimination by the Mauthner system. J. Comput. Neurosci. 6, 121-144.[CrossRef][Medline]
Hale, M. E. (2002). S- and C-start escape responses of the muskellunge (Esox masquinongy) require alternative neuromotor mechanisms. J. Exp. Biol. 205,2005 -2016.[Medline]
Hale, M. E., Long, J. H., Jr, McHenry, M. J. and Westneat, M. W. (2002). Evolution of behaviour and neural control of the fast-start escape response. Evol. 56,993 -1007.
Hama, K. (1969). A study of the fine structure on the saccular macula of the goldfish. Z. Zellforsch. 94,155 -171.[CrossRef][Medline]
Harper, D. G. and Blake, R. W. (1991). Prey capture and the fast-start performance of northen pike Esox lucius.J. Exp. Biol. 155,175 -192.
Johnston, I. A., Van Leeuwen, J. L., Davies, M. L. F. and Bedow, T. (1995). How fish power predation fast-starts. J. Exp. Biol. 198,1851 -1861.[Medline]
Karlsen, H. E. (1992a). The inner ear is responsible for detection of infrasound in the perch (Perca fluviatilis). J. Exp. Biol. 171,163 -172.
Karlsen, H. E. (1992b). Infrasound sensitivity in the plaice (Pleuronectes platessa). J. Exp. Biol. 171,173 -187.
Karlsen, H. E. and Sand, O. (1987). Selective and reversible blocking of the lateral line in freshwater fish. J. Exp. Biol. 133,249 -262.
Karlsen, H. E. and Sand, O. (1991). Infrasound detection in fish. Biom. Res. 12, Suppl. 2, pp.217 -219.
Kimmel, C. B., Powell, S. L, and Metcalfe, W. K. (1982). Brain neurons which project to the spinal cord in young larvae of the zebrafish. J. Comp. Neurol. 205,112 -127.[Medline]
Korn, H. and Faber, D. S. (1996). Escape behaviour brainstem and spinal cord circuitry and function. Curr. Opin. Neurobiol. 6, 826-832.[CrossRef][Medline]
Lee, R. K. K., Eaton, R. C. and Zottoli, S. J. (1993). Segmental arrangement of reticulospinal neurons in the goldfish hindbrain. J. Comp. Neurol. 327, 1-18.[Medline]
Lewis, T. N. and Rogers, P. H. (1998).Directional acoustic response in the goldfish . (Abstract) 16th International Congress of Acoustic and Acoustical Society of America.
Liu, K. S. and Fetcho, J. R. (1999). Laser ablations reveal functional relationships of segmental hindbrain neurons in zebrafish. Neuron 23,325 -335.[Medline]
Metcalfe, W. K., Mendelson, B. and Kimmel, C. B. (1986). Segmental homologies among reticulospinal neurons in the hindbrain of the zebrafish larva. J. Comp. Neurol. 251,147 -159.[Medline]
Moulton, J. M. and Dixon, R. H. (1967). Directional hearing in fishes. In Marine Bioacuostics, Vol 2 (ed. W. N. Tavolga), pp.187 -203. Oxford: Pergamon Press.
Platt, C. (1993). Zebrafish inner ear sensory surfaces are similar to those in goldfish. Hear. Res. 65,133 -140.[CrossRef][Medline]
Piddington, R. W. (1972). Auditory discrimination between compressions and rarefactions by goldfish. J. Exp. Biol. 56,403 -419.[Medline]
Popper, A. N. and Edds-Walton, P. L. (1995). Structural diversity in the inner ear of teleost fishes: implications for the connections to the Mauthner cell. Brain Behav. Evol. 46,131 -140.[CrossRef][Medline]
Popper, A. N. and Platt, C. (1983). Sensory surfaces of the saccule and the lagena in the ears of ostariophysan fishes. J. Morphol. 176,121 -129.
Popper, A. N., Fay, R. R., Platt, C. and Sand, O. (2003). Sound detection mechanisms and capabilities of teleost fishes. In Sensory Processing in the Aquatic Environment (ed. S. P. Collin and J. N. Marshall), pp.3 -38. New York and Heidelberg: Springer Verlag.
Ritter, D. A., Bhatt, D. H. and Fetcho, J. R.
(2001). In vivo imaging of zebrafish reveals differences in the
spinal networks for escape and swimming movements. J.
Neurosci. 21,8956
-8965.
Sand, O. (2002). Sound and source localization: an historical assessment. Bioacoustics 12,199 -201.
Sand, O. and Karlsen, H. E. (1986). Detection of infrasound by the Atlantic cod. J. Exp. Biol. 125,197 -204.[Abstract]
Sand, O., Enger, P. S., Karlsen, H. E. and Knudsen, F. R. (2001). Detection of infrasound in fish and behavioural responses to intense infrasound in juvenile salmonids and European silver eels: a minireview. Am. Fish. Soc. Symp. 26,183 -193.
Schellart, N. A. M. and de Munk, J. C. (1987). A model for directional and distance hearing in swimbladder-bearing fish based on displacement orbits of hair cells. J. Acoust. Soc. Am. 82,822 -829.[Medline]
Schuijf, A. (1975). Directional hearing of cod under approximate free field conditions. J. Comp. Physiol. 98,307 -332.
Schuijf, A. (1981). Models of acoustic localization. In Hearing and Sound Communication in Fishes (ed. W. N. Tavolga, A. N. Popper and R. R. Fay), pp.267 -310. New York: Springer Verlag.
Sento, S. and Furukawa, T. (1987). Intra-axonal labelling of saccular afferents in the goldfish, Carassius auratus: correlations between morphological and physiological characteristics. J. Comp. Neurol. 258,352 -367.[Medline]
Webb, P. W. and Skadsen, J. M. (1980). Strike attacks of Esox. Can. J. Zool. 58,1462 -1469.[Medline]
Zottoli, S. J. (1977). Correlation of the startle reflex and Mauthner cell auditory response in unstrained goldfish. J. Exp. Biol. 66,243 -254.[Abstract]
Zottoli, S. J. and Faber, D. S. (2000). The Mauthner cell: what has it taught us? Neurosci. 6, 26-38.