Serotonin modulates the electric waveform of the gymnotiform electric fish Brachyhypopomus pinnicaudatus
Department of Biological Sciences, Florida International University, Miami FL 33199, USA
* Author for correspondence (e-mail: stoddard{at}fiu.edu)
Accepted 21 January 2003
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Summary |
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Key words: Gymnotiformes, Hypopomidae, Brachyhypopomus pinnicaudatus, circadian rhythm, communication, electric organ discharge, 5-hydroxytryptamine
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Introduction |
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Our interest in serotonin stems from its possible role in the regulation of
communication behavior in gymnotiform electric fish. Weakly electric fish
produce electric organ discharges (EODs) for electrolocation and
communication. Most species in the genus Brachyhypopomus produce
sexually dimorphic EODs consisting of discrete, biphasic pulses. The female
EOD is a symmetric sinusoid. The male's EOD differs from the female's in two
ways: its amplitude is greater and the repolarization time of the second phase
(P2) is much longer (Hopkins et al.,
1990; Stoddard et al.,
1999
). Extending the repolarization time of P2 boosts the energy
in the sensory range of the ampullary electroreceptors approximately five
times (Stoddard, 2002
), of
little consequence for electrolocation, but of great significance for
communication (Naruse and Kawasaki,
1998
; for a review, see
Stoddard, 2002
).
Males dynamically regulate the shape of their EOD waveforms with a
circadian rhythm that maximizes their masculine signal traits (amplitude and
repolarization time) in the early hours of the night, when social activities
peak (Franchina and Stoddard,
1998; Hagedorn,
1995
). Starting in the late afternoon, EOD amplitude increases in
both phases, reaching a maximum shortly after dark when spawning is most
likely to occur. Repolarization time of P2 increases, but begins its ascent
later in the day than amplitude, but rising faster, to peak about the same
time. Of key importance, males also alter these signal traits in response to
social encounters. Typically the EOD amplitude rises and P2 repolarization
time increases within a few minutes of the initial encounter. If the male
loses the encounter, duration of P2 drops more than that of the victor, as
seen by an increase in peak spectral frequency of the EOD
(Hagedorn and Zelick,
1989
).
We began screening neuroactive substances to find chemical modulators of
the EOD waveform, initially focusing on those known to have peripheral as well
as central effects. A prior study of gymnotiform electric fish demonstrated
the expected central effect of serotonin on behavior
(Maler and Ellis, 1987);
serotonin inhibits the production of aggressive signaling, reducing how often
the fish accelerates the EOD rate (chirp signals) in agonistic encounters.
Based on the typical vertebrate pattern, one might expect serotonin to reduce
the amplitude and repolarization time of the EOD, as both these EOD measures
are associated with big, reproductive males
(Curtis and Stoddard, in press
;
Hopkins et al., 1990
), and
both increase on social challenge
(Franchina et al., 2001
).
However, our preliminary screen showed that serotonin injected peripherally
caused a rapid and transient increase in amplitude and repolarization
time of the EOD waveform. Here we characterize the response of the electric
waveform to exogenous serotonin, making no assumptions or conclusions about
the site of action.
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Materials and methods |
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Data collection: the EOD machine
EODs were recorded in automated measurement tanks, 120 cmx44
cmx44 cm, shielded with grounded copper screen. Eight such tanks resided
within a light- and temperature-controlled room on a 12 h:12 h L:D light
cycle. Each tank was divided into thirds by plastic screening, with screen
funnels directing fish through an unglazed ceramic tube that joined the outer
two compartments (Fig. 1).
Unlike plastic tubes, unglazed ceramic tubes interfere minimally with the
electric fields. The fish rested in the tube during daylight hours and passed
through frequently at night. Graphite electrodes on the ceramic tube
registered the fish's position in a dedicated analog circuit that compared
rectified signal amplitudes against preset thresholds, customized for each
fish. When this fish-in-tube detector registered an EOD from a fish centered
in the tube, a TTL pulse was sent to a ring-buffered, analog-to-digital
converter (ADC) (Tucker-Davis Technologies RP2, Gainesville, FL, USA) that
digitized the entire EOD at approx. 50 kHz across a different pair of
electrodes at either end of the tank. EODs were amplified 200x and
lowpass filtered with an AC-coupled 8-pole Bessel filter set to a corner
frequency of 10·kHz. Up to nine consecutive EODs were digitized, one
series every 60·s if the fish was resting in the tube, or at most every
60 s if the fish was passing through on its own volition. The chamber was
heated by an air pump and water temperature was maintained within half a
degree of 27°C by a dedicated computer that monitored thermocouples and
switched fans to exchange warm air for cool. Once a week the ADC and amplifier
were calibrated to equivalent units of mV cm-1 at 10 cm
(Franchina and Stoddard,
1998). Water conductivity was readjusted to 100 µS
cm-1.
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Online data analysis
EODs were analyzed on the fly, and made available to a custom-written data
visualization program. For each EOD, the analysis program measured peak
amplitudes for phase 1 (P1) and phase 2 (P2), durations at 10% of peak
amplitude for each phase, and -P2, the time constant of the
repolarization of phase 2 (Fig.
2). Measurements of amplitude peaks and durations were improved
with cubic spline interpolation to enhance resolution over that obtainable
with a sampling rate of 50 kHz.
-P2 was calculated by fitting an inverse
exponential curve to the repolarization segment of the second phase using
successive approximation in the MATLAB function `fminsearch' (Mathworks,
Natick MA, USA). Median values were graphed as representative of each set of
nine sequential EODs. We found that duration of the second phase measured 10%
above baseline correlated strongly with the time constant
-P2 of the
repolarization of the second phase (r2=0.64;
N=32). We chose
-P2 as our measure of duration of the second
phase of the EOD for several reasons:
-P2 is more reliably measured, it
applies only to the repolarization part of the waveform and is therefore less
likely to be influenced by partial overlap with the first phase
(Hopkins et al., 1990
), and
finally,
-P2 is more easily related to underlying electrophysiological
parameters such as ion-channel inactivation time
(Ferrari et al., 1995
;
McAnelly and Zakon, 2000
).
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Offline data analysis
EOD waveform responses to pharmacological agents are superimposed on each
fish's circadian EOD rhythm (Franchina and
Stoddard, 1998). While the acute responses to serotonin injections
are clearly visible in the data, accurate measurements are confounded to
various degrees by ongoing circadian oscillation in the baselines (Figs
3,
4). We wrote a graphical data
analysis program in MATLAB to separate pharmacological effects from the
circadian oscillations (Fig.
3). First, we performed a least-squares fit of a low-order (2-6)
polynomial to the data segments prior to and following the pharmacological
effect, omitting the time period from the injection to when the EOD parameter
returned to its normal oscillating baseline. We subtracted this polynomial
curve from the data to yield a set of residuals that included only the
pharmacological effect. The order of polynomial was chosen to match the shape
of the data from the preceding and following days when no pharmacological
agents were given. When the pharmacological effect persisted for more than 3-4
h, a fit polynomial could have too much freedom to wander in the excluded time
segment. In those cases, we superimposed the rhythm from the preceding or
following day, adjusted it with linear regression to match the current day's
data, exclusive of the post-injection period, then fitted the polynomial to a
combination of the best subsets of data excluding the pharmacologically
affected data. The data residuals were fit with a high order (5-40) polynomial
function using least-squares regression. The program analyzed the polynomial
function to identify the time and amplitude of the data peaks. Three males
produced amplitude data that were too noisy to analyze and we excluded these
data from further analysis. One male produced a response in
-P2 that was
6 standard deviations beyond the mean so we excluded these data as well.
Further regression analyses and means tests were done with MATLAB.
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EOD amplitude and duration gradually diminish over 7-10 days when males are
kept in social isolation, as they were in this experiment
(Franchina et al., 2001). Thus,
to identify the daynight swing for a given midday injection time, we
found the day and night extremes both before and after the injection date and
interpolated peak-to-peak and trough-to-trough lines to obtain an
instantaneous measure of potential peak and trough values at the injection
time.
Solutions and injection
Serotonin (5-hydroxytryptophan creatinine sulfate complex, Sigma) was
dissolved in physiological saline: NaCl 114 mmol l-1, KCl 2 mmol
l-1, CaCl2.2H2O 4 mmol l-1,
MgCl2.6H2O 2 mmol l-1, Hepes 2 mmol
l-1, pH adjusted to 7.2 with NaOH (modified from
Ferrari and Zakon, 1993). We
selected 25 nmol g-1 as our highest concentration of 5-HT because
this dose had been shown to be active in other studies of fish
(Khan and Thomas, 1992
). At
this dose, however, the fish emerged from their hiding tubes after injection
and swam about the tanks disoriented and often upside down, very odd behavior
for a gymnotiform fish at midday. We therefore tested fish on a variety of
doses down to 0.025 nmol g-1 to generate a doseresponse
curve that could be used to establish the minimum effective dose. All
solutions were prepared on the day of injection.
We allowed the fish to spend a day in the measurement tank before receiving an injection and an additional day after the injection as well. These extra data allowed us to better characterize the circadian changes so we could subtract these from the data trace to reveal the effect of the injection. We injected fish at midday, when visual inspection of plots of EOD repolarization time and amplitude showed these circadian rhythms to be at or approaching their daily minima. To inject a fish, we slid a plastic screen tube inside the ceramic tube where the fish was resting, pinched off the ends of the screen tube, and removed the fish from the tank. The fish was injected while confined to the screen tube and returned to the water within 30 s. Experimental removal and handling without injection was found to have no measurable effect on the subsequent EODs, but injection of saline had a noticeable effect in about half the fish injected. For this reason, we use saline injections as our primary control treatment.
Experimental and control solutions were injected at 1 µl g-1 intramuscularly (i.m.) or intraperitoneally (i.p.) using a Hamilton syringe fitted with a disposable 31.5 gauge needle. Male fish weighed 5-20 g so injection volumes were 5-20 µl. Since we found no difference in results between fish injected i.m. and i.p., we kept to i.m. injections, safer for this very wiggly animal, which has large epaxial muscles and a small peritoneum. We injected at a shallow angle to maximize needle penetration and reduce leakage.
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Results |
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Compared to saline injections, injections of serotonin at doses of 2.5 nmol
g-1 and higher produced greater increases in EOD amplitude,
duration of the second phase (dur-P2), and repolarization time of the second
phase (-P2, e.g. Fig. 5),
but no significant difference in duration of the first phase
(Fig. 6). The increases in
-P2 were dose-dependent (r2=0.50; F=38;
d.f.=1,41; P=0.000002), reaching an asymptote at doses of 2.5 nmol
g-1 (Fig. 7).
Amplitude also increased, but this response was more variable and the best fit
dose-response curve (not shown) was not statistically significant. Effects of
5-HT on the duration of the first phase of the EOD were small and more
variable yet (Fig. 8). In all
cases, the response to serotonin was transitory
(Fig. 8). Temporal distribution
of peaks in
-P2 were bimodal. Five individuals peaked 15-30 min after
injection and the majority peaked later, 60-115 min after injection (Figs
5,
8). Amplitude response was
unimodal, peaking 30 min after injection. The effective half-lives were 2-3 h
for all parameters (Fig. 8). In
some fish, injection of 5-HT increased both
-P2 and amplitude, whereas in
others only
-P2 was affected (Figs
5,
9). In no fish did serotonin
cause amplitude to increase while
-P2 remained flat
(Fig. 9).
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For saturating doses of serotonin (2.5 nmol g-1 and above), the
rises in -P2 and amplitude associated strongly with the magnitudes of
their respective circadian swings (Fig.
10A), parameters that have previously been shown to be under
social control (Franchina et al.,
2001
). Linear regression showed that the magnitude of the
endogenous circadian rhythm in amplitude accounted for approx. 75% of the
variance in the serotonin-induced amplitude rise (r2=0.77;
F=27; d.f.=1,8; P=0.0009). The magnitude of the endogenous
rhythm in
-P2 accounted for approx. one third of the variance in the
5-HT-induced rise in
-P2 (r2=0.36; F=6.1;
d.f.=1,11; P=0.03). Daily minima for all fish in the study were
tightly associated with nightly maxima
(Fig. 9B), (
-P2:
F=323; d.f.=1,39; P=3.5E-20), (amplitude: F=572;
d.f.=1,41; P=2.6E-25). Thus the diurnal baseline is related to the
circadian swing, and accordingly to the responsiveness to serotonin.
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Discussion |
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The tight relationship between daily minima and nightly maxima (Fig. 10B) suggests that a common mechanism regulates both. For instance, EOD amplitude could be a function of the number of active voltage-gated sodium channels (or the number of contributing electrocytes), and a circadian modulator could alter the unitary conductance of those channels. Alternatively, EOD amplitude rhythms could function by taking electrocytes on and offline in a circadian rhythm, with a socially mediated regulator of the sodium current setting a fixed amplitude for every electrocyte.
Our data suggest -P2 is determined more by channel properties than by
collective activity of electrocytes. If increases in
-P2 were derived
from desynchronization of the electrocytes, one would expect a drop in
amplitude when
-P2 increased and a rise in
-P2 when amplitude
decreased. Such effects were suggested by an early study that compared
individuals rather than daynight changes within individuals
(Hopkins et al., 1990
). No
such relationship is apparent in any of our data within individuals. Indeed
-P2 frequently varies significantly while amplitude remains dead flat,
but in over a thousand natural cycles examined to date, we have never seen an
amplitude decline coupled to a
-P2 increase. Thus we believe that
modulation of
-P2 derives in large part from changes in ion-channel
kinetics at the level of individual electrocyte membranes.
Our general finding that serotonin enhances sexual dimorphism in the male's
EOD waveform might be surprising, in that serotonin is widely considered to be
the neurotransmitter of social subordinates. Some researchers, however, now
characterize serotonin in the broader context of social stress
(Edwards and Kravitz, 1997;
Overli et al., 1999
;
Summers, 2001
). Numerous
studies in other teleosts have shown that serotonin turnover is increased in
the brainstem of socially subordinate individuals
(Hoglund et al., 2000
;
Overli et al., 1999
;
Winberg and Lepage, 1998
;
Winberg et al., 1992
,
1996
,
1997
,
2001
). Yet we see here that
serotonin quickly, but transiently, enhances a social signal typical of
dominants, not subordinates (Hagedorn and
Zelick, 1989
). Our pharmacological characterization of the
serotonin receptors in B. pinnicaudatus (P. K. Stoddard, M. R.
Markham, V. L. Salazar and S. Allee, manuscript in preparation) suggests a
solution to the paradox: we have found two pharmacologically distinct
populations of postsynaptic serotonin receptors, a 5HT2A-like receptor that
drives the EOD characters up, and 5HT1A-like receptor that drives them down.
If the excitatory receptors have a shorter action latency or stronger binding
affinity than the inhibitory receptors, the EOD could be initially enhanced by
a surge in serotonin, then perhaps diminished if serotonin release continued
for a long time. This differential time course would be consistent with
results obtained in rainbow trout Oncorhynchus mykiss, where
immediate serotonin activation in the telencephalon occurs in both members of
a paired territorial encounter, but turnover remains high only in the loser
(Overli et al., 1999
), or in
anole lizards Anolis carolinensis, where telencephalic serotonin
turnover of social dominants increases briefly, but rises later in social
subordinates and remains high longer
(Summers et al., 1998
).
Alternately, if the 1A receptor is central and the 2A receptor peripheral,
then our peripheral injections might be acting preferentially on the
excitatory receptor. The action of serotonin via peripheral injection
might be taken to indicate a peripheral action, because serotonin is thought
not to cross the bloodbrain barrier of adult mammals
(Bouchaud, 1972
;
Deutch and Roth, 1999
). In
teleosts, however, the blood brain barrier is less exclusive and peripheral
serotonin readily enters the brain (Genot
et al., 1981
). More recent studies show that the bloodbrain
barrier of rodents is made more permeable by serotonin, and by this mechanism
serotonin can facilitate its own entry into the brain
(Sharma et al., 1995
;
Winkler et al., 1995
). Pending
further investigation, we consider the CNS to be a plausible target for
serotonin's action, perhaps initiating the release of another substance that
acts as the local modulator of EOD amplitude and duration. Different protein
kinases have been shown to work in the periphery as part of second messenger
systems that rapidly modulate the amplitude of sodium currents in other
gymnotiform EODs (Emerick and Agnew,
1989
; Gotter et al.,
1997
; McAnelly and Zakon,
1996
), but the first messengers have yet to be identified.
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Acknowledgments |
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