A hydrodynamic topographic map in the midbrain of goldfish Carassius auratus
1 Institut für Zoologie, Universität Bonn, Poppelsdorfer Schloss,
Bonn, Germany
2 Department of Biology, University of Maryland, College Park, MO 20748,
USA
* Author for correspondence (e-mail: dennis{at}bio2.rwth-aachen.de)
Accepted 2 July 2003
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Summary |
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Key words: lateral line, goldfish, Carassius auratus, torus semicircularis, hydrodynamic sensory system, topographic map, midbrain
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Introduction |
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Lateral line information reaches the brain via lateral line
nerves, which terminate throughout the medial octavolateral nucleus (MON) of
the medulla (Puzdrowski,
1989). Cells of the MON project bilaterally to the midbrain torus
semicircularis (TS), which relays information to the tectum opticum and to the
diencephalon (Wullimann,
1998
). From the diencephalon lateral line information finally
reaches the telencephalon (e.g. Wullimann,
1998
). To study the physiology of the peripheral and central
lateral line, earlier investigators used stationary vibrating spheres
(dipoles) as a stimulus source (e.g.
Harris and van Bergeijk, 1962
;
Münz, 1985
;
Bleckmann and Bullock, 1989
;
Coombs et al., 1996
,
1998
). Using dipole stimuli
applied in still water to a fish rigidly fixed in a holder, researchers
uncovered many physiological properties of the lateral line, such as vibration
amplitude thresholds, dynamic amplitude ranges, and the phase coupling of
peripheral and central lateral line units to sinusoidal water motions (e.g.
Kroese and van Netten, 1989
;
Münz, 1985
;
Plachta et al., 1999
;
Engelmann et al., 2000
).
Natural sources of lateral line stimuli are usually not stationary, and
they rarely oscillate with constant frequency and amplitude. Instead they move
around and produce low-frequency transient water motions with irregular
amplitude and frequency fluctuations
(Enger et al., 1989;
Bleckmann et al., 1991
) and
pressure waves (e.g. Kalmijn,
1988
; Hassan,
1993
). In addition, swimming aquatic animals like fish leave a
vortex trail in the water (Blickhan et al., 1992), which may persist for more
than 1 min (Hanke et al.,
2000
) and may be used by piscivorous animals to track prey fish
(Pohlmann et al., 2001
;
Dehnhardt et al., 2001
).
To stimulate the lateral line with complex water motions, researchers moved
small objects along the side of the fish (e.g.
Bleckmann and Zelick, 1993;
Müller et al., 1996
;
Montgomery and Coombs, 1998
;
Wojtenek et al., 1998
). Using
such stimuli, peripheral and central lateral line units revealed specific
response properties that would not have been discovered with stationary
vibrating spheres. Examples include central lateral line units responding to a
moving object with a short single peak of excitation
(Mogdans and Goenechea, 1999
),
units respondingu with multi-peaked, long-lasting excitations
(Mogdans and Bleckmann, 1998
),
and units responding with inhibition
(Mogdans and Bleckmann, 1998
).
Moving object stimuli also revealed that certain central lateral line units
are highly sensitive to the direction of object motion
(Bleckmann and Zelick, 1993
;
Müller et al., 1996
;
Wojtenek et al., 1998
).
The lateral line does not respond to a moving object but to the water motions caused by that object. Therefore it is desirable to measure and compare water motions caused by the object with the neural responses caused by these water motions. To do so, we combined particle image velocimetry (PIV) with physiological recordings in the midbrain TS (TS for torus semicircularis). Our experiments revealed three types of toral lateral line units. Type TS1 units responded maximally while water velocities across the surface of the fish's body were increased due to sphere movement. It is most likely that units of this type received their input from SNs. Type TS2 units responded only while the sphere passed a certain location on the fish's head or body, but responses did not positively correlate with the water motions at this location. TS2 units were topographically organized. A third type of units (TS3) discharged only after the sphere had passed the fish. The responses of these units could not be attributed to either sphere-caused water motions or the pressure gradients caused by the moving sphere.
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Material and methods |
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Preparation
For surgery fish were anesthetized in iced water. In addition the skin at
the preparation site on the head was infused with the local anesthetic
Xylocaine® (ASTRA-Chemicals). A small area of skin was then carefully
removed. An opening (about 4 mmx4 mm) was made with a drill in the skull
over the contralateral midbrain. Excess fatty tissue and fluids were aspirated
to reveal the optic tectum contralateral to the stimulation side. Following
surgery, Pancuronium Bromide® (0.1-0.2 mg g-1 i.m.; Organon
Teknika, Oberschleissheim, Germany) was administered to immobilize the animal.
The immobilized fish was then transferred to the experimental tank (40
cmx48 cmx25 cm) filled with standing tapwater at room temperature
(20±2°C). To reduce background vibrations the tank rested
on a vibration-free table (Micro-g, TMC®; Peabody, MA, USA).
For electrophysiological recordings fish were positioned on a styrofoam support. The fish was tipped up at about 20° with the dorsal surface of the head just above the water surface. The exposed brain was kept moist with Ringer's solution. To keep the animal in a fixed position, its head was glued with Histoacryl® (Braun Melsungen, Melsungen, Germany) to the tip of a small Plexiglas rod attached to a micro-drive. Aerated freshwater was pumped at a rate of 70-100 ml min-1 over the gills through polyethylene tubing inserted into the fish's mouth.
Stimulation
Hydrodynamic stimuli were generated with a sphere (diameter 8 mm) moved on
a linear path along the side of the fish from anterior to posterior (AP) or
from posterior to anterior (PA). The path of the sphere was guided by a
ball-bearing rail system, positioned at the level of the trunk lateral line
canal, which enabled us to move the sphere without recoil or vibration. A
total length of 23.8 cm on the rail system was marked by trigger contacts. The
extremes of movement exceeded the length marked by the trigger contacts by
about 5 cm, to allow deceleration of the sphere. During each trial the sphere
velocity was held as constant as possible. We changed the mean sphere speed
from trial to trial gradually from slow to fast (3 to 36 cm s-1,
respectively). In all experiments the mean velocity of the sphere was
calculated from the time the sphere needed to pass the two trigger contacts.
Moves were interrupted by a 5-15 s pause to allow the water in the
experimental tank to calm down after each sphere run. The manual control of
sphere velocity proved to be sufficient for a first classification.
Independent of sphere velocity, all units recorded consistently fell into one
of three classes.
A dipole stimulus (50 Hz, 100 Hz, 160 µm peak-to-peak amplitude) was generated by a vibrator (V 106; Ling Dynamic Systems, Royston, USA) at the holder of the sphere. For each unit the sphere was placed along the side of the fish (from snout to tail) in 10 mm steps to examine the unit's responses to dipole stimuli.
Particle Image Velocimetry (PIV)
To measure the water movements across the surface of the fish's body, the
water in the experimental tank was seeded with white neutrally buoyant
particles (Vestosint 1101, donated by Hüls AG, Marl, Germany; mean
diameter 100 µm). Two laser diode modules (output <10 mW) with
cylindrical lenses were mounted on opposite sides of the tank to generate two
light sheets of about 1 mm thickness. One laser was installed to cast the
light sheet vertically between the moving sphere and the fish, the other laser
produced a horizontal light sheet 1-3 mm below the sphere to avoid shadows
(Fig. 1). The light reflected
by the particles was recorded with two CCD cameras. The pictures were
controlled online on a LCD monitor (Citizen LCDTV; Irvine, CA, USA), stored on
a VCR (Panasonic NVF70 HQ) and digitized off-line with a video capture card
(Miro Video DC 30; Pinnacle Systems, Mountain View, CA, USA). The card was set
to a compression factor of 1:10, which does not affect the quality of the PIV
analysis (Freek et al., 1999).
Off-line analysis of the pictures was performed with a computer (IBM
compatible AMD K6) and MatLab 5.1 (cf.
Hanke et al., 2000
). A custom-made script file correlated
subimages of succeeding frames according to the principles of digital PIV,
first introduced by Willert and Gharib
(1991
). The error of this
calculation depends on various parameters, including particle velocity. For
high particle density, slow water velocities result in smaller errors, e.g. 5%
at 2 cm s-1, whereas larger water velocities result in larger
errors, e.g. 10% at 10 cm s-1. However, suboptimal particle density
and small-scale velocity gradients resulted in a bias of the measured
velocities towards lower values. The calculations were converted into a vector
plot, showing the calculated and interpolated water flow within the camera
view (e.g. Fig. 3D). The audio
channel of the video recorder was fed with the signals from the two trigger
contacts that marked the position of the sphere.
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Data acquisition and analysis
Single unit and few-unit recordings were made in the contralateral TS,
using either indium electrodes (impedance <1 M;
Dowben and Rose, 1953
) or
quartz glass filaments (outer diameter 80 µm), whose 30 µm cores were
filled with platinum tungsten (impedance <4 M
at 1000 Hz) (Thomas
Recordings, Marburg, Germany). The tip of the indium electrode was plated with
gold and then platinum to reach a diameter of 4-10 µm. The six
platinum-tungsten electrodes were arranged in a Reitboeck microdrive (Eckhorn
System®, Thomas Recording, Marburg, Germany), which allowed a computer
controlled recoil-free thrust for each electrode with a precision of ±2
µm. The six electrodes of the system were arranged in a rectangle
consisting of two rows. The distance between two electrodes was fixed by
guiding tubes at 250 µm, resulting in a rectangle size of 250
µmx500 µm.
Action potentials were amplified (DAM 80®, WPI or Eckhorn System®, Thomas Recordings), bandpass filtered (300-3000 Hz), displayed on two oscilloscopes (DL 1300A®; Yokogawa, Atlanta, GA, USA) and stored for off-line analysis on an 8-channel digital tape recorder (DTR 1800®; Biologic, Science Products, Hofheim, Germany). Units were isolated from background noise using window discriminators (WPI, Model 121® or Eckhorn System®, Thomas Recording). These delivered TTL (transient transistor level) pulses for each action potential above a selected level or within a level window. A sweep of action potentials as well as the discriminator level selected was displayed on the oscilloscopes during data aquisition. The spike waveforms were visually inspected to discriminate single unit recordings from few-unit clusters. If not otherwise stated this report presents data from single unit recordings.
For final analysis, TTL pulses of the window discriminators were digitized (Instrunet® and SuperScope II®, GWI®) and stored on a computer (Apple Macintosh, Power PC 7300®). The times of occurence of TTL pulses relative to stimulus onset were calculated with a precision of 100 µs. Ongoing activity was calculated for at least 100 ms prior to stimulation and expressed in spikes s-1. Raster plots and peristimulus-time histograms (PSTHs) were computed across 10 stimulus repetitions. Peak spike rates were determined from the bin (binwidth 50 or 100 ms) in the PSTH with the greatest number of spikes and expressed in spikes s-1.
Characterisation of units
In order to distinguish lateral line units from visual, auditory, and
vestibular units the following stimuli were also applied.
Sound stimuli. Acoustic stimulation was presented by a loudspeaker
(see materials in Plachta et al.,
1999), by human voice and handclapping. Units that responded to
any of these stimuli were considered auditory units.
Vibratory stimuli were applied by slightly tapping the edge of the experimental tank with the tip or rubber ball of a pasteur pipette. Units that responded to this stimulus were assumed to receive vibratory input.
Photic stimuli were applied by switching on and off the light of the binocular used to monitor the position of the recording electrodes. Units that responded to changes in illumination or failed to respond to the moving object in complete darkness were assumed to receive visual input.
Unimodal lateral line units were distinguished from all other units in that they responded even in the dark to a sphere (diameter 8 mm) vibrating close by the fish or to a sphere that was moved along the side of the fish. Unimodal lateral line units were classified without any doubt. However, units responsive to acoustic and/or to vibratory stimuli often also responded to the vibrating or the moving sphere. We did not attempt to learn whether these units were unimodal acoustic or received additional lateral line input.
Histology
In 15 cases the location of the recording site was marked with a small
electrolytic lesion. If indium electrodes were used, lesions were obtained by
passing a current of 1-7 µA d.c. for 2-15 min through the electrode. If
platinum tungsten electrodes were used, a high frequency a.c. current
(frequency >500 kHz, Ieff>7 µA) was applied for
10-15 min. Fish were deeply anesthetized with MS 222® and perfused
intracardially with freshwater teleost Ringer's solution followed by 5%
glutaraldehyde solution in 0.1 mol l-1 phosphate buffer (pH 7.4).
Brains were removed, postfixed and cut at 15 µm in a transverse plane
parallel to the electrode penetrations. Sections were stained with Cresyl
Violet and analyzed microscopically. Digital images of slices with lesions
were stored.
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Results |
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Of the 57 units, 48 (83%) did not respond to a stationary vibrating sphere (stimulus frequencies 50 and 100 Hz, peak-to-peak displacement amplitude 160 µm), while 9 units (17%) responded to both the moving sphere and to the stationary vibrating sphere. 17 of the 57 units, called TS1 units (TS = torus semicircularis), responded with a reproducible single burst (duration 200-800 ms; end of burst defined by a gap of neural activity of at least 500 ms) while the object passed the fish and, in most trials, continued to fire for up to 20 s afterwards. The late spike activity of TS1 units was not predictable across stimulus presentations (e.g. see raster plots in Fig. 3A). 35 of the 57 units, called TS2 units, responded only with a reproducible single spike or with a single short (<500 ms) burst of spikes while the object passed the fish (e.g. Figs 3B,right, 5A). Five out of the 57 units, called TS3 units, barely responded while the object passed the fish. However, 300-500 ms after object stop these units fired strong, long-lasting bursts (e.g. Fig. 3C). PIV measurements acquired while recording the responses of TS3 units showed that at burst onset (after end of sphere movement), peak velocity and the water velocity averaged over the fish's body were far below the maximal values in a given trial (for one example see Fig. 3C,D).
|
Sphere position and unit responses
In TS1, TS2 and TS3 units, sphere positions at response onset were
different for motion in the AP and PA directions. For instance, if the sphere,
moving AP, caused a reproducible burst of a TS1 unit while passing a distinct
point P along the longitudinal axis of the fish, sphere movements in the
opposite direction could cause a response before or after the sphere reached
P. In contrast, the ill-defined late response component of a TS1 unit only
occurred after the sphere had passed a distinct rostro-caudal location of the
fish. It was obvious that at the times of neuronal responses of TS1 units,
water velocities across the surface of the fish were enhanced and that the
flow patterns were not reproducible from trial to trial. In contrast to TS1
units, the first stimulus that evoked responses of TS2 units (N=35)
always occurred before the sphere had crossed a distinct location (P) along
the longitudinal axis of the fish. Although not analyzed quantitatively it was
apparent from the particle movements in the video frames that water velocities
at response onset were never pronounced at this location, i.e. TS2 units did
not respond in proportion to water velocity at location P.
Midbrain lateral line map
A further analysis of TS2 unit responses revealed a midbrain lateral line
map (Figs 4,
5,
6). TS2 units recorded in the
anterior TS responded while the sphere passed the head or the anterior body of
the fish, whereas TS2 units recorded in the caudal TS responded while the
sphere passed the posterior body of the fish. Responses from TS2 units in the
medio-lateral part of the TS occurred while the object passed the medial part
of the body (Figs 4,
5,
6).
Fig. 4 shows the main response
areas for all TS2 and 13 TS1 units. Main response areas of TS2 units map
topographically in the midbrain. In five instances two TS2 units were recorded
simultaneously with electrodes spaced 250 µm apart (for an example see
Fig. 5A,B). Action potentials
were usually recorded first with the electrode placed more rostral if the
direction of object motion was AP. If the direction of object motion was PA,
the opposite was true (Figs 5,
6).
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Location of motion-sensitive units
Units that responded exclusively to the moving sphere were, on average,
more ventrally located in the lateral TS than the units that responded
exclusively to the vibrating sphere. Although the vertical separation was not
absolute (Fig. 7), the
difference in depth distribution was significant (Wilcoxon-Mann-Whitney
U-test, Z=2.326, U=489.0625,
P<0.01).
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Discussion |
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Consequently type I primary lateral line afferents, i.e. velocity-sensitive
afferents receiving input from SNs
(Mogdans and Bleckmann, 1998;
Engelmann et al., 2000
,
2002
), continue to respond
after an object has passed the fish
(Mogdans and Bleckmann, 1998
).
Like type I primary lateral line afferents, TS1 units of Carassius
also responded to the transient water motions generated by the passing sphere
and to the water motions in the wake of the moving sphere. Therefore it is
conceivable that TS1 units received their input mainly, or even exclusively,
from the SN system. The same may be true for type MB units found in the TS of
the catfish Ancistrus, which also responded to the wake of a moving
object (Müller et al.,
1996
).
The responses of TS2 units resemble those of type II primary lateral line
afferents, known to receive CN inputs
(Mogdans and Bleckmann, 1998),
and it is conceivable that TS2 units of goldfish received input from CNs.
If that interpretation is correct, that part of the torus semicircularis
which processes the hydrodynamic information caused by a moving object might
contain at least two subsystems: one for the analysis of SN information (TS1
units), and one for the analysis of CN information (TS2 units). A similar
physiological subdivision is present at the level of the MON
(Kröther et al., 2002).
Separation of SN and CN information at the level of the midbrain does not
exclude the possibility that TS1 unit responses can be modulated by CN input
or vice versa. A TS3 unit was first found in the midbrain of the
catfish Ancistrus sp.
(Müller, 1996
). TS3 units
responded with excitation only after the object had passed the fish, and they
may belong to a third subsystem whose functional properties are not yet
understood.
Fish have a visual topographical map in the optic tectum (for a review, see
Northcutt and Wullimann, 1988)
and a computed topogaphical acoustic map in the nucleus centralis of the torus
semicircularis (e.g. Schellart et al.,
1987
). Computed lateral line maps have been found in the clawed
frog Xenopus laevis (Zittlau et
al., 1986
) and in the Axolotl Ambystoma mexicanum
(Bartels et al., 1990
). In
these animals the direction of water surface waves is represented
systematically in the optic tectum. Using a stationary vibrating sphere as a
stimulus, Knudsen (1977
) and
Bleckmann et al. (1989b
) found
a topographical lateral line map in the midbrain of catfish and rays,
respectively. Whether these units received input from the canal system or from
SNs was not investigated. In the present work, we found in the goldfish that
units which respond to a moving object with a short burst topographically map
in the torus semicircularis. If our interpretation that these units received
inputs from CNs is correct, the canal system preserves the information about
the spatial distribution of CNs. Our physiological data support conclusions
drawn from behavioral studies on the mottled sculpin Cottus bairdii.
The initial orienting and approach behavior of this fish to a dipole source
relies on canal rather than SN input
(Coombs et al., 2001
). It is
most likely that C. bairdii uses the point-to-point spatial
representation of a source location along the sensory surface of the lateral
line system to localize a prey object
(Conley and Coombs, 1998
).
We do not know whether the neuronal units described here were recorded from neuron somata or fibres. The spike width of the 57 midbrain units analyzed in this study showed a unimodal distribution (0.8-2.4 ms), i.e. distinct spike populations were not apparent. Therefore it is unlikely that the classification into TS1, TS2 or TS3 units corresponds to a difference between somata recordings and, for instance, incoming MON fibre recordings. In any case further investigations are necessary to reveal more details about midbrain lateral line subsystems and lateral line maps.
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Acknowledgments |
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