Sensitivity of the anterior lateral line to natural stimuli in the oyster toadfish, Opsanus tau (Linnaeus)
1 Biology Department, University of Minnesota Duluth, Duluth, MN 55812,
USA
2 Marine Biological Laboratory, Woods Hole, MA 02543, USA
3 ExxonMobil Upstream Research Company, PO Box 2189, Houston, TX 77252,
USA
* Author for correspondence (e-mail: amensing{at}d.umn.edu)
Accepted 28 June 2005
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Summary |
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Key words: lateral line, telemetry, prey, toadfish, Opsanus tau
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Introduction |
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Behavioral and electrophysiological experiments have illustrated that the
lateral line functions in schooling behavior
(Partridge and Pitcher, 1980),
rheotaxis (Montgomery et al.,
1997
) and localization of underwater objects
(Weissert and von Campenhausen,
1981
). The lateral line has also been shown to receive water
displacements generated by moving prey
(Saunders and Montgomery,
1985
; Montgomery and
Macdonald, 1987
; Montgomery et
al., 1988
; Bleckmann and Topp,
2003
; Pohlmann et al.,
2004
). The great diversity in fish body plan and swimming
strategies can generate extremely complex hydrodynamic trails consisting of
unpredictable distributions of local particle activity, alternating eddies and
slightly deformed vortex rings (Blickhan et
al., 1992
; Muller,
1996
). Information about the direction and temporal scale of fish
movement can be contained in these trails
(Hanke et al., 2000
), which
can persist in the water column for several minutes
(Hanke and Bleckmann, 2004
).
However, since the chain of vortices generated by fish movement is difficult
to recreate and/or present during standard neurophysiological preparations,
the activity of the lateral line in response to free-swimming prey has been
difficult to quantify. Instead, vibrating spheres have been used historically
as stimuli for the lateral line (Wubbels
et al., 1993
; Muller,
1996
; Coombs, 1999
;
Kanter and Coombs, 2003
).
While instrumental in determining neuromast characteristics (frequency and
directional sensitivity), pure stationary dipole-like stimuli are rarely
encountered in nature.
The detection of biologically relevant stimuli must often be accomplished
during self-generated movement (e.g. swimming, ventilation). Recent studies
conducted by Palmer et al.
(2003) indicate that the
primary afferents of the anterior lateral line were stimulated during swimming
and ventilatory movements. Various studies have shown that lateral line
filtering during intense stimuli may be performed in higher brain regions.
Tricas and Highstein (1990
,
1991
) identified efferent
modulation of lateral line activity when toadfish viewed live prey, and
Montgomery and Bodznick (1994
)
indicated that the lateral line medullary nuclei contain an adaptive filter
capability that cancels input consistently associated with an animal's own
movements.
The operating range of the lateral line system has been reported to be one
to two body lengths (Denton and Gray,
1983; Kalmijn,
1988
; Coombs, 1999
;
Braun and Coombs, 2000
).
However, to accurately quantify the range and sensitivity of the lateral line
to natural stimuli, neural activity must be monitored from an unconstrained
teleost in quasi-natural settings. Recording neural activity from
free-swimming fish has been complicated by the need for electrode stability
and/or a suitable telemetry device. Terrestrial telemetry modes such as
infrared light or radio waves are rapidly attenuated in seawater and are
ineffective. The development of an inductive neural telemetry system allows
the recording of neural responses from free-ranging toadfish (Mensinger and
Deffenbaugh, 1998
,
2000
;
Palmer and Mensinger, 2004
).
This study reports the activity of the lateral line in response to
free-swimming prey.
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Materials and methods |
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Microwire electrode
Microwire electrodes consisting of three strands of insulated 20
µm-diameter 10% platinum/iridium wire (Sigmund Cohn Corp., Mt Vernon, NY,
USA) were custom fabricated for each implantation. Each microwire strand was
affixed to hard silver-plated copper multistranded wire (25 µm diameter)
with conductive silver paint (Silver Print Paint, GC Electronics, Rockford,
IL, USA). The multistranded wire was attached to silver wire (320 µm) that
terminated into a multipin underwater connector. The anterior portion of the
microwires was threaded through a 1 mm length of polymide tubing (180 µm
outer diameter; A-M Systems Inc., Carlsborg, WA, USA) to maintain the
recording sites in proximity. Any exposed wire/connections were encased in
medical device adhesive (Loctite 3341; Henkel Loctite Corp., Rocky Hill, CT,
USA) and cured with ultraviolet light (ELC #660; Electro-lite Corp., Danbury,
CT, USA). The impedance of each electrode channel was determined with an
impedance-test unit (FHC; Bowdoinham, ME, USA) using 1 kHz input frequency.
Only electrodes with impedances between 0.5 and 1.2 M were used.
Electrode implant
Fish were anesthetized by immersion in 0.005% tricaine (3-aminobenzoic acid
ethyl ester; Sigma, St Louis, MO, USA) and paralyzed with an intramuscular
injection of a 0.01% solution of pancuronium bromide (600 µg
kg-1; Sigma). An incision was made through the dorsal musculature
overlying the sagittal crest, and the muscle was retracted. A small craniotomy
was performed lateral to the sagittal crest and posterior to the transverse
crest to expose the anterior ramus of the anterior lateral line nerve. The
electrode was inserted into the nerve just prior to its exit from the
braincase. Potentials were differentially amplified (Dagan, Minneapolis, MN,
USA) and monitored on a portable computer using Chart5 for Windows software
(ADInstruments, Colorado Springs, CO, USA). The two channels that provided the
highest fidelity signal were chosen for the experiments. Once a candidate
fiber was located, the fish was left undisturbed for 30 min to ensure fiber
stability.
Cyanoacrylate gel (Pacer Technology, Rancho Cucamonga, CA, USA) was used to affix the electrode to the skull and seal the craniotomy. The muscle was restored to its original position, and the muscle, faschia and epidermis were individually sutured to provide a watertight seal over the craniotomy and around the transdermal electrode lead. The differential amplifier was disconnected from the electrode, and the cylindrical telemetry tag (15 mmx38 mm, diameter x length; 8 g) was inserted into the waterproof electrode connector. The tag was sutured parallel to the dorsal fin on the dorsal surface of the fish.
Neural recordings
Chronic extracellular recordings from lateral line primary afferent fibers
were obtained using an inductive telemetry system (Mensinger and Deffenbaugh,
1998,
2000
;
Palmer and Mensinger, 2004
).
In brief, the inductive telemetry system consists of a transmitter tag and
receiver coils. The tag transmits the neural signal as a frequency-modulated
magnetic field (90 kHz carrier, 20 kHz bandwidth), which is detected by
receiver coils embedded in a recharging habitat and stage (RECHABS). To
recharge the tag, the RECHABS produces an oscillating magnetic field (50
µT, 200 kHz), and the tag stores energy from this field in its capacitors.
The RECHABS consists of a cylindrical habitat (12 cmx30 cm, internal
diameter x length) that opens onto an octagonal stage (16 cm per side;
Fig. 1). The RECHABS can both
receive the telemetry signal from the tag and recharge the tag when the tag is
within the habitat or up to a height of approximately 15 cm above the stage.
The tag can be fully charged in less than 30 s and will provide telemetry for
5 min.
|
Killifish (Fundulus heteroclitus; 6-8 cm SL) were used as prey. To maximize predator-prey encounters, a circular plastic barricade surrounded the stage and restricted the killifish to the RECHABS area. Prey that did not approach the toadfish within 15 min were anesthetized (0.0001% MS-222), and a barbless fish hook (size 6) attached to monofilament (1 kg test) was inserted between the premaxilla and maxilla bone of the killifish. Once the tethered Fundulus recovered normal swimming activity, they were placed in the experimental tank. Sufficient slack was maintained in the tether to allow normal swimming movements; however, the tether allowed the fish to be directed towards the toadfish when necessary.
The telemetry signals were recorded up to four days post electrode
implantation and stored on a portable computer using Chart5 software and
analyzed offline with Spike2 software (Cambridge Electronic Design, Cambridge,
UK). Predator-prey interactions were simultaneously recorded on videotape (30
frames s-1; Sony Digital Handycam, Sony Electronics USA, Oradell,
NJ, USA) that was synchronized with the neural telemetry system and analyzed
frame by frame using DV Shelf video frame capture and Scion Imaging software
(Scion Corp., Frederick, MD, USA). Killifish movement alternated between
caudal-fin-mediated forward swimming and stationary positioning via
2-3 Hz oscillation of the pectoral fins. Because the various fins and swimming
motions of fish produce differing stimuli of varying intensity
(Gibb et al., 1994;
Drucker and Lauder, 2001
),
neural activity was only quantified when the prey hovered in the same location
for greater than 500 ms. Prey distance was defined as the distance between the
neuromast and the intersection point of the nearside killifish pectoral fin
with its body axis.
A trial consisted of placing a free-swimming or tethered Fundulus into the arena and monitoring its swimming movements while concurrently recording toadfish lateral line activity for up to 10 min. An encounter consisted of a Fundulus hovering for >500 ms in the same position that was within 20 cm of the innervated neuromast during a trial. Five to 12 trials were conducted per toadfish, with up to 119 encounters recorded per trial. To compare activity between fibers, firing rates were normalized according to the maximum firing rate elicited by prey movements that was recorded in each trial.
Although the microwires often yielded multiunit activity, fiber discrimination was usually limited to a single unit that yielded the greatest action potential amplitude and was clearly discernible from other units. To verify that the same unit was consistently recorded during an experiment, individual fibers were distinguished using rigorous waveform analysis (Spike2) in addition to spike amplitude. During one implant, two units were discovered to be clearly distinguishable based on amplitude and waveform analysis, and both fibers were individually analyzed during the trial.
The streamlined telemetry tag only added 1% to toadfish body mass and its
attachment did not have noticeable effects on behavior. Normal ventilation
rates and equilibrium returned within 30 min of anesthetic withdrawal, and
swimming activity resumed within two hours post-surgery. Recent work has shown
that the sensitivity of the anterior lateral line to mechanical stimuli is
restored within 90 min of anesthetic withdrawal
(Palmer and Mensinger, 2004),
and therefore experiments were not initiated until a minimum of two hours
following anesthetic removal. During all trials, toadfish were monitored for
abnormal physiological (respiration rate) and behavioral (sudden movement,
tail contraction) changes before, during and after the application of the
magnetic field, and no discernible effects were observed. Previous studies
(Mensinger and Deffenbaugh,
1998
,
2000
;
Palmer and Mensinger, 2004
)
demonstrated that the magnetic field does not affect neural activity or
behavior in the toadfish.
Prey stimulus
Still-water trials were conducted with 8 cm SL Fundulus in a large
rectangular tank (2.5 mx1.2 mx0.5 m) with water depth maintained
at 20 cm. Water velocities generated by hovering Fundulus were
calculated by digital particle tracking velocimetry. Fluid flow around the
fish was illuminated by a horizontal laser sheet, 0.5 mm thick, and imaged
from above with a high-resolution digital video camera (Kodak ES 1.0, 1008
pixelsx1018 pixels). The flow was seeded with 20-40 µm-diameter
neutrally buoyant fluorescent particles. For further details, refer to
Anderson et al. (2001).
Statistical analysis
All statistical analysis was performed using GraphPad Software (San Diego,
CA, USA) or SigmaStat for Windows version 3.10 (Systat Software, Inc.,
Richmond, CA, USA). All data represent mean values ± 1
S.E.M. unless otherwise indicated. Fiber
activity during an encounter was binned into 2 cm intervals (distance of
Fundulus fin origin to innervated neuromast). As the range of
activity for the silent fibers was moderate (0-17 Hz), a one-way analysis of
variance (ANOVA) was used to determine differences in spike activity among the
four fibers during prey encounters. For the spontaneous active fibers, firing
rates were normalized according to the maximum firing rate elicited by prey
movements that was recorded in each fiber during a trial. The resulting
percentages were transformed using the arcsine function
(Zar, 1984), and a one-way
ANOVA was used to determine differences in the transformed data for fiber
activity for the combined five spontaneous active fibers. Samples were tested
for normality using the method of Kolmogorov and Smirnov. Bartlett's test was
used to determine the use of parametric or non-parametric testing.
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Results |
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As the distance between the prey and neuromast diminished, silent fibers were stimulated to fire (Fig. 2A). The greatest range at which prey stimulated a silent fiber was 11 cm. Spontaneous fibers showed similar characteristics, with activity significantly increasing (ANOVA, P<0.05) above resting background levels at prey distances of up to 4 cm from the neuromasts (Fig. 2B). Prey at distances between 4 and 8 cm stimulated firing rates above background levels; however, at distances greater than 8 cm, the presence of prey did not lead to elevated rates.
Small fluctuations in action potential frequency may be more valuable for prey detection for the toadfish than statistically significant changes. For silent fibers, the probability of a silent fiber firing during an encounter was plotted versus prey distance (Fig. 3). Silent fibers fired greater than 60% of the time when prey was located within 4 cm of the neuromast. This probability decreased to approximately 20% between 6 and 12 cm, and prey located further than 12 cm failed to stimulate silent fibers. For spontaneous fibers, determining small fluctuations in action potential frequency was not as clear, as spontaneous discharge rates could drift by 5-10% during a trial. Therefore, Fig. 3 includes the probability of spontaneous fibers firing one and/or two standard deviations above their resting discharge rate during an encounter versus prey distance. Thus, even after including a less rigorous benchmark (1 S.D.), the probability of a spontaneous fiber reacting to the prey during an encounter continues to decline sharply with distance.
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The neural response of a spontaneously active fiber and a silent fiber to hovering prey is illustrated in Fig. 6. Both fibers innervated superficial neuromasts located on the infraorbital line of the anterior lateral line. As prey approached within 8 cm, both fibers experienced an increase in neural activity.
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Both silent and spontaneously active fibers were observed to continually fire in phase with the toadfish's ventilation cycle. The fibers fired regularly with each ventilation cycle and were never observed to become habituated (Fig. 8).
The water velocities generated by pectoral and caudal fin movement of 8 cm SL Fundulus were extremely complex (Fig. 9). Maximum water velocities generated by the pectoral fins during hovering were approximately 5 cm s-1, with water displacement rapidly attenuating with distance from the body axis. Velocities between 2 and 3 cm s-1 were often detectable within 2-3 cm of the fin's insertion; however, at distances greater than 5 cm, water movement remained less than 1 cm s-1.
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Discussion |
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As fish swimming combines the locomotion of several independent fin systems
(Drucker and Lauder, 2001),
the generated hydrodynamics can be complex. A swimming fish leaves a
hydrodynamic trail in the water that can persist several minutes after its
passage (Hanke et al., 2000
;
Hanke and Bleckmann, 2004
).
Experiments conducted by Enger et al.
(1989
) concluded that the
lower-frequency accelerations resulting from the prey's motion are
biologically of utmost importance in lateral line detection. The killifish was
chosen for these experiments as it is natural prey for the toadfish
(Chrobot, 1959
). Its swimming
behavior alternates between forward propulsion mediated by body and caudal fin
movement, and stationary hovering using pectoral fin oscillation. Caudal fin
movement generally creates greater water displacement and may consequently
provide a larger stimulus for the lateral line. However, as toadfish
predominantly strike at approaching prey, bow waves or forward fin (pectoral
and/or pelvic) displacement may be more important than caudal movements or
subsequent wakes. To limit the disparity in Fundulus swimming
characteristics, data analysis was restricted to periods when prey were
hovering in the same location for greater than 500 ms. Consequently, much of
the data analysis characterizes lateral line activity in response to
oscillation (
3 Hz) of the killifish pectoral fin.
Digital particle tracking velocimetry allowed analysis of the water velocities generated by hovering Fundulus. Retraction of the pectoral fins in hovering killifish produced maximum water velocities of approximately 5 cm s-1 within the arc traveled by the fin. These velocities rapidly attenuated with distance from the fin's origin. Velocities between 2 and 3 cm s-1 were often detectable within 3 cm of the fin; however, at distances greater than 5 cm from the fin's origin, water movement declined to less than 1 cm s-1 before fading into the background (0.1 cm s-1). Caudal fin motion disrupted a larger volume of water over greater distances. However, as these deflections were lateral and posterior to the pectoral fin currents, there appeared to be little potential for constructive inference between the two sources. As data analysis was restricted to hovering, during which the caudal fin remained relatively stationary, pectoral fin movements were the primary stimulus source.
Previous studies have indicated the persistence of hydrodynamic trails
several minutes following fish passage
(Hanke et al., 2000;
Hanke and Bleckmann, 2004
).
Slowly decaying wakes could complicate determining if the lateral line is
reacting to current prey motion or residual wakes.
Fig. 4 illustrates a typical
trial during which the prey moved throughout the arena. The silent fiber
ceased to fire when the prey moved greater than 10 cm away from the toadfish.
If the hydrodynamic trails continued to persist at a physiological level, the
fiber should have continued to fire after the prey vacated the area. However,
the previous studies examined wakes generated by rapidly swimming fish which
would create greater and more persistent, water disturbance than
Fundulus. Alternatively, the lateral line fibers could have become
habituated to a persistence stimulus and ceased to respond. However, when
lateral line fibers were stimulated for up to 60 s with continuous water flow,
habituation was not evident (Palmer and
Mensinger, 2004
), indicating that a dispersing stimulus and not
habituation was responsible for the return of lateral line activity to
baseline levels.
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Caution must be applied in two areas of our data interpretation. As the recordings were restricted to individual fibers in a localized region of the anterior lateral line, it is possible that other regions may contain neuromasts more sensitive to prey movements. Alternatively, central integration from multiple neuromasts may function to increase resolution and sensitivity and project the detection distance further than an individual neuromast. Additionally, slight changes in firing frequency may provide important information for the fish but fail to be statistically significant, especially when averaged over different neurons and fish, as in the current study. For example, in the 4-8 cm range for spontaneous fibers, the fibers fired well above background discharges and undoubtedly provided information about the prey. However, using less rigorous statistical analysis (1 S.D. above spontaneous rate) did not greatly extend the maximum detection distance. It remains possible that small, transient fluctuations in lateral line activity that were outside our resolution ability encode for prey distance and extend detection distance. However, the response dynamics of the silent fibers, which did not fire in the absence of stimulus, provide support for the limited range of the lateral line as these fibers failed to fire until the prey approached within 11 cm.
Predator-prey interactions are also consistent with lateral line
sensitivity recorded in toadfish. Although behavioral observations are limited
to discerning when the predator visibly reacts to the prey rather than when
detection occurs, they provide further support for close-range detection. Year
one toadfish (8 cm SL; 10 cm TL) feeding on small guppies (2 cm SL) during
daylight trials did not launch strikes at prey that were greater than 5 cm
from the toadfish (Fig. 10;
Price and Mensinger, 1999).
These attacks were probably mediated by both visual and mechanical cues, and
reaction distances under low light conditions would be predicted to be shorter
and more accurate indicators of lateral line range. Ongoing studies in
juvenile toadfish indicate that both reaction distance and attack range are
less in the dark than the light (L. Lundeen and A. F. Mensinger, unpublished)
and are consistent with studies by Enger et al.
(1989
), New and Kang
(2000
) and Richmond et al.
(2004
) that found that
predatory fish without visual cues reacted to prey at distances of less than
50% of the predator's body length.
Although the lateral line can contribute significant information for prey
localization, due to its short range it is evident that other systems are
important in locating distant prey. The far hydrodynamic fields of moving
objects are hypothesized to be mediated by the inner ear
(Kalmijn, 1988). Additionally,
behavioral and physiological experiments have illustrated that tactile,
chemosensory, hydrodynamic and visual stimuli are capable of guiding prey
capture (Montgomery et al.,
2002
).
The oyster toadfish possesses an anterior lateral line dominated by
superficial neuromasts (Clapp,
1898). Although behavioral experiments in other species have
indicated that prey detection and localization is mediated by canal neuromasts
(Coombs et al., 2001
), it
appears that the afferent fibers innervating the superficial neuromasts of the
toadfish anterior lateral line are responsive to the stimuli produced by prey.
Consequently, although canal neuromasts may provide important prey
localization information, superficial neuromasts are able to detect the
low-frequency water displacements generated by prey and contribute to
near-field prey detection.
Efferent innervation of lateral line hair cells has been hypothesized to
inhibit afferent firing (Russell and
Roberts, 1974) and prevent depletion of transmitter from lateral
line hair cells during locomotion or rapid movements
(Russell, 1971
). Tricas and
Highstein (1990
) illustrated
that the lateral line experienced transient inhibition when toadfish were
allowed to view live Fundulus in an adjacent aquarium and that in a
minority of fibers there was a decrease in neural activity in anterior lateral
line afferent fibers during a predatory strike. However, recent studies have
illustrated the ability of hair cells to release neurotransmitters for
prolonged periods with little exhaustion
(Moser and Beutner, 2000
;
Trussell, 2002
). Evidence of
efferent modulation (reduction or cessation of nerve activity) was not
observed during any trial. The length of our trials and the inclusion of
intermittent mechanosensory stimulation may have occluded our ability to
detect efferent modulation. However, the lack of inhibition of toadfish
neuromasts located near the operculum that were continually stimulated by
opercular displacement (present study) or prolonged water current
(Palmer and Mensinger, 2004
)
appears to indicate that efferent modulation was not common in our sample
population.
Both silent and irregular fibers experienced a dramatic increase in firing
during a predatory strike. It is possible that self-generated noise created
during a predatory strike may be filtered by higher order neurons. Montgomery
and Bodznick (1994) indicate
that the lateral line medullary nuclei contain an adaptive filter capability
that cancels inputs consistently associated with an animal's own movements.
Further experiments are required to determine decisively whether the lateral
line conveys self-regulatory information during a predatory strike.
In summary, the toadfish lateral line can detect transient water displacement generated by natural prey. The distance at which stimulation occurred was less than 40% of toadfish body length. This is the first study that investigates the neural response of the anterior lateral line to prey stimuli in free-ranging fish and highlights the importance of the lateral line in near-field prey detection.
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Acknowledgments |
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