Behavioral evidence for post-pause reduced responsiveness in the electrosensory system of Gymnotus carapo
Institut für Biologie I, Hauptstrasse 1, Albert-Ludwigs-Universität Freiburg, D-79104 Freiburg, Germany
e-mail: schustef{at}uni-freiburg.de
Accepted 10 May 2002
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: active sensory system, pacemaker, novelty response, cessation, electrosensory, mechanosensory, electric organ discharge, weakly electric fish, Gymnotus carapo
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
In some of these fish, it is possible to disrupt experimentally the
otherwise continuous train of electric organ discharges (EODs). This should
enable an assessment of how critical the continuous operation of this sensory
system is for its performance. I attempted here to explore the effects of a
pause in EOD activity on the subsequent performance of the so-called novelty
response shown by many pulse-type weakly electric fish. In this response, a
fish briefly raises its discharge frequency after it has detected a novelty in
its environment. Thereby, it increases its electrosensory sampling rate
whenever something novel transpires. The response can generally be elicited
not only by changes in the EOD feedback but also by a variety of other stimuli
(Lissmann, 1958;
Bennett and Grundfest, 1959
;
Westby, 1975
;
Heiligenberg, 1980
;
Kramer et al., 1981
;
Meyer, 1982
;
Barrio et al., 1991
;
Falconi et al., 1995
;
Ciali et al., 1997
;
Corrêa and Hoffmann,
1998
). Thus, it is possible to compare post-pause novelty
responses driven by different sensory stimuli. This comparison, in turn, may
provide hints as to whether an EOD pause affects stimulus detection or the
execution of the response. The present study demonstrates a dramatic failure
of electrosensory, but not mechanosensory, stimuli to elicit novelty responses
after pausing of EODs in the gymnotid fish Gymnotus carapo. The
findings point to two new mechanisms in which continuous activity is required
to ensure either maintained sensitivity to high-frequency electric stimuli or
a high efficacy of tuberous receptor-driven synaptic input to its target cells
in the pacemaking structures.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Experimental paradigm
The derivation of `post-pause efficiency', (n), of a stimulus
in eliciting normal-sized novelty responses when given n EODs after a
pause is illustrated in Fig. 1.
The stimulus was given twice: first at the nth post-pause EOD and
then a second time 10 000 EODs, or approximately 200 s, later during steady
firing. The second stimulation served to determine the `normal' response size,
with which the first post-pause response was then compared. The interval of
approximately 200 s between the first and second stimulus was selected to
ensure independence of the second response from the occurrence of the
first.
|
Monitoring interpulse interval
To monitor the interpulse interval continuously, the EODs of the
experimental fish were recorded using two silver wires fixed on the front and
the back of the tank. The voltage across these wires was amplified (EG&G
5113) and fed into a computer using a data-processing card (DAP 3200a/415,
Microstar Labs; software written in DAPL and Borland Turbo-Pascal 7.0).
Pausing the EODs
Pausing was usually elicited by electrical signals (1 kHz square waves of
up to 1 s in duration, field strength in the fish's shelter of up to
approximately 300 mV cm-1 peak-to-peak) generated by a pulse
generator (Master-8, AMPI) and delivered by a T-shaped dipole electrode
(Westby, 1974,
1975
), whose distance to and
orientation with respect to the fish was varied. Pauses could also be elicited
by optical and mechanical stimuli. However, these stimuli were less efficient
in eliciting pauses than the electrical stimuli. The efficiency of
non-electrical stimuli in eliciting pausing was therefore increased in three
fish. In these, a pause-eliciting electrical stimulus was preceded by a
mechanical stimulus (tapping the tank's wall). After a few trials, the
mechanical stimulus itself was sufficient to elicit pausing. Approximately
10-20 pauses were elicited each day. At least 10 000 EODs were required
between the second stimulus of a previous experiment and a subsequent attempt
to elicit a pause. In some fish, it was not possible to elicit more than one
pause a day. In experiments that required a large number of post-pause
responses to be evaluated, three fish (gc1gc3) were generally used
since pausing could most readily be elicited in these.
Electrical stimuli
The isolated output of a generator (DS 345, Stanford Research) was
automatically triggered at the rising phase of the nth (and
n+10 000th) post-pause EOD and delivered via carbon
electrodes that straddled the fish. Stimulus intensity was determined at the
fish's usual position using two silver wires (1 cm apart, insulated except at
their tips).
Mechanical stimuli
A standardized strong mechanical stimulus that could be triggered
n EODs after a pause was generated by mounting a large contactor (AEG
Elfa VI4040M5) on the desk on which the experimental tank stood. The pressure
wave produced by the knock that resulted from activation of the contactor was
reproducible both in details of its time course and in peak-to-peak amplitude
and remained approximately constant within the porous shelter of the fish
(deviations less than 1 %). This was verified by monitoring the waveform and
amplitude of the pressure wave using a miniature hydrophone (Bruel &
Kjaer, 8113) and a charge-conditioning amplifier (Bruel & Kjaer, Nexus
2692). The peak-to-peak amplitude corresponded to 167 dB re 1 µPa.
Quantifying the stimulus efficiency
In responses elicited during normal firing, the stimulus-induced maximal
excursions T from the pre-stimulus interpulse interval
T0 will be larger for larger values of
T0 (S. Schuster, unpublished observation). To make
response strengths obtained at different values of T0
comparable, the strength (R) of a novelty response was assayed using
the ratio R=
T/T0. The efficiency,
(n), of the stimulus in eliciting a response n EODs
after a pause was defined as the ratio of the post-pause response strength
R1 to the subsequently determined `normal' response
strength R2, i.e.
=R1/R2.
Unless stated otherwise, Student's t-tests were used to determine,
for each individual, whether the mean efficiencies obtained for that
individual under different stimulus regimes differed significantly.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
To obtain a quantitative measure of the reduction in response after a
pause, I determined the post-pause efficiency, (100), i.e. the efficiency
with which the stimulus elicited a novelty response when given 100 EODs after
a pause (see Fig. 1 for an
illustration of how efficiencies were measured). Several measurements were
made of
(100) in each of 10 fish, yielding a set of
(100) values
obtained after a total of 118 pauses that ranged from 1.1 to 76 s in duration
(17.5±14.1 s, mean ± S.D.). Within this data set, no correlation
existed between the efficiency
(100) and the duration of the prior pause.
The mean efficiencies did not differ between fish that could be induced to
pause several times a day and those in which only a few pauses could be
elicited each day. Hence, all post-pause efficiencies of the data set were
pooled to obtain an average efficiency:
(100)=0.43±0.03.
Post-pause responses to a mechanical stimulus
The failure of electrical stimuli to elicit responses immediately after a
pause could mean that novelty responses simply cannot occur after a prior
pause. However, using a mechanosensory stimulus, responses could readily be
elicited, even immediately after a pause
(Fig. 3). In these experiments,
the mechanical stimulus was chosen so that it elicited, during normal firing,
responses of strength comparable with that of responses elicited by the
electrical stimulus used previously.
|
The mechanosensory stimulus elicited clear novelty responses immediately
after a pause. However, the post-pause responses were smaller than those
obtained during steady firing (i.e. <1). This was analyzed using a set
of 82 experiments in which the mechanical stimulus was given 100 EODs after a
pause. This set involved data from all 10 fish, obtained after pauses ranging
in duration from 1 to 75 s (19.6±18.9 s, mean ± S.D.). No
correlation existed between pause duration and post-pause efficiency, and mean
efficiencies did not differ between fish that could be induced to pause
several times or only a few times per day. The efficiencies were therefore
pooled, and an average efficiency,
(100)=0.71±0.02, was obtained.
The 71 % average efficiency of the mechanical stimulus when given 100 EODs
after a pause was significantly greater than the average efficiency (43 %) of
the electrical stimulus (difference between the two averages
P<0.001; t-test).
The efficiency is independent of how pausing is induced
The most efficient stimulus to make a Gymnotus carapo pause its
ongoing train of EODs is a strong electrical `shock'. Such shocks have also
been used to elicit pausing in the previous datasets. Hence, the reduced
efficiency, or even failure, of electrical stimuli in eliciting a novelty
response immediately after a pause could result from an aftereffect of the
electrical shock. This was tested by training three fish so that they
reproducibly paused their EODs in response to mechanical stimuli. In a series
of subsequent experiments, these trained fish were induced to pause by either
an electrical shock or a mechanical stimulus. For each fish, the mean
efficiency of the electrical stimulus (1 cycle of a 1 kHz sinewave, 235 mV
cm-1 peak-to-peak) 100 EODs after the pause was determined after
these two differently elicited pauses. In all three fish, the mean
efficiencies were independent of whether the prior pause had been elicited by
an electrical or a mechanical shock (Fig.
4). This demonstrates that the reduced responsiveness to
electrical stimuli is not caused by an aftereffect of a pause-inducing
electrical shock.
|
Would other electrical stimuli be more efficient in eliciting
post-pause responses?
Both the mechanical and electrical stimuli elicited strong novelty
responses of comparable size during steady firing. Hence, insufficient
`strength' of the electrical stimuli was not a likely cause for their reduced
efficiency in eliciting post-pause novelty responses. However, this conclusion
would not hold if the efficiency of the electrical stimuli was very sensitive
to stimulus intensity. Therefore, a series of experiments with three fish
explored how the efficiency, (100), of the electrical sine-wave pulses
varied as their intensity was varied over a range of almost three orders of
magnitude so as to elicit smaller (field strength 0.9 mV cm-1) or
slightly stronger (field strength 235 mV cm-1) responses during
steady firing than elicited by the mechanosensory stimulus. Within this range,
the post-pause efficiency was independent of stimulus intensity
(Fig. 5A).
|
The mechanical stimulus had a longer duration than the electrical stimulus and a different time course. Could the low post-pause efficiency of the electrical stimulus be due to its shorter duration? To analyze this possibility, two stimulus patterns of longer duration were tested: (i) a continuous sine burst, 100 ms in duration, and (ii) a series of six sine pulses (period 1 ms) with 20 ms intervals of silence between them (Fig. 5B). Both stimuli had an intensity of 235 mV cm-1 (peak-to-peak). The average post-pause efficiency obtained with these stimuli was not statistically different from the average efficiency of a single pulse of the same intensity. Furthermore, for each fish and for each stimulus condition, the average efficiencies differed significantly from the average 71 % post-pause efficiency obtained from the pooled data set described above using the mechanical stimulus (difference between each of the averages shown in Fig. 5B from the 71 % average P<0.001; t-tests).
The efficiency of low-frequency electrical stimuli
Besides their tuberous high-frequency electroreceptors, which monitor the
ongoing EODs, all weakly electric fish possess ampullary receptors that detect
low-frequency stimuli (direct current to approximately 100 Hz; for a review,
see Zakon, 1986). As these
receptors are not tuned to the EODs, they should be little affected by EOD
pausing. It was therefore interesting to determine the post-pause efficiency
of low-frequency stimuli that recruit ampullary receptors. Unfortunately, in
Gymnotus carapo, there is no skin region where only ampullary or only
tuberous receptors occur, so the two types of receptor cannot be activated
selectively by localized stimulation (unlike in Apteronotus
leptorhynchus; e.g. Zakon et al.,
1998
). Moreover, many of the tuberous receptors of Gymnotus
carapo are very broadly tuned, with their sensitivity extending far into
the low-frequency region (Watson and
Bastian, 1979
), so that separating ampullary and tuberous
receptors by varying the spectral energy of the electrical stimulus will be
only partially successful.
While it is thus not possible to stimulate selectively either tuberous or
ampullary receptors in Gymnotus carapo, it is still possible to
investigate whether a greater involvement of ampullary and lesser involvement
of tuberous receptors caused by a transition from a high-frequency to a
low-frequency electrical stimulus might affect post-pause efficiency. To do
this, a single sine-wave cycle of either 2 or 10 Hz, presented at a smaller
than previously used stimulus intensity of 2.35 mV cm-1, was chosen
as the low-frequency stimulus that activates ampullary receptors. The two
frequencies were chosen to assess the possible effects of the absolute pulse
duration. A low-frequency sinusoid of 2 or 10 Hz might still be above the
threshold of some tuberous receptors at these frequencies and, therefore,
might not be expected to be sensed exclusively by ampullary receptors.
However, from the tuning curves reported by Watson and Bastian
(1979), it is clear that, at
the chosen intensity, the high-frequency stimulus will recruit more tuberous
receptors than the low-frequency stimulus. Thus, the relative contribution of
ampullary receptors to the response will be higher for the low-frequency
stimuli.
In the corresponding experiments, the average efficiency 100 EODs after a
pause, (100), was determined for the low-frequency stimulus and compared
with that obtained with a high-frequency stimulus of the same intensity. The
post-pause efficiency of the low-frequency stimuli was higher than that
obtained for high-frequency stimuli (Fig.
6). Because the average efficiencies of the 2 Hz and 10 Hz stimuli
did not differ significantly, both stimuli were included in
Fig. 6 in a single
low-frequency efficiency for each fish that lay between the high-frequency and
mechanical efficiency. In both fish, the observed average low-frequency
post-pause efficiency differed significantly from the averages obtained with
both the high-frequency and mechanical stimuli (all averages differed by at
least P<0.05, t-tests). While the present experiments
cannot exclude the possibility that a complete elimination of tuberous
receptor activity would have yielded a still higher efficiency, they do show
that an increase in the proportion of ampullary receptors recruited by an
electrical stimulus increases its post-pause efficiency.
|
The course of post-pause efficiency
For both the standard electrical (see
Fig. 2) and mechanical (see
Fig. 3) stimuli, an attempt was
made to determine the time course of efficiency from immediately after the
pause until normal response levels were reached. To this end, a series of
experiments was conducted with two fish, in which 486 pauses were elicited and
average post-pause efficiencies (n) were determined for various
set values of n (Fig.
7).
|
The mechanical stimulus elicited responses of approximately 70 % of the
normal response strength as early as 20 EODs after a pause. Interestingly, its
efficiency was constant at this level until approximately 1000 EODs after the
pause, and only then approached the steady-state efficiency (i.e. =1). In
contrast, the efficiency of the electrical stimulus started at zero for
n=20 and appeared to increase continuously with n, attaining
the same efficiency as the mechanical stimulus approximately 1000 EODs or
approximately 20 s after a pause. At 2000 EODs, or 40 s, after the pause, both
the electrical and the mechanical stimulus elicited `normal-sized'
responses.
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Pacemaker and motor output
In gymnotiform fish, each EOD is commanded by a discharge of the medullary
pacemaker nucleus (PMn) (for reviews, see
Bennett, 1971;
Dye and Meyer, 1986
), which
contains a network of pacemaking (PM) and relay (R) cells. The R cells
transmit the command pulse to the spinal electromotor neurons that innervate
the electric organ. This basic organization seems also to hold in Gymnotus
carapo (Bennett et al.,
1967
; Bennett,
1971
; Trujillo-Cénoz et
al., 1993
). At present, we are ignorant of the processes that
occur within the PM and R cells of Gymnotus carapo during a pause in
the EOD. Likely possibilities would be that the PM cells cease to fire during
a pause or that the R cells are blocked. The latter possibility is realized,
for instance, in the pulse-type fish Hypopomus, in which sudden
interruptions are mediated by N-methyl-D-aspartate
(NMDA)-receptor-activated depolarization of the relay cells (Kawasaki and
Heiligenberg, 1989
,
1990
;
Spiro, 1997
) so that a spike
in the PM cells is unable to elicit an R spike. Such a mechanism seems
unlikely for the interruptions of Gymnotus carapo given the course of
post-pause interval changes (Schuster,
2000
; also see left-hand traces in Figs
2,
3). In its so-called sudden
interruptions, Hypopomus fires at a constant frequency and then
suddenly stops firing. If the fish then resumes its discharges after the
pause, it fires immediately at the pre-pause frequency
(Kawasaki and Heiligenberg,
1989
). The situation is quite different in Gymnotus
carapo. This fish was never observed to restart its firing at the
pre-pause frequency but usually at a greatly reduced frequency. This might
indicate that Gymnotus carapo PM cells stop their spontaneous
activity during a pause. However, a direct demonstration of this is currently
not available. In the present interpretation of the changes in post-pause
responsiveness, it is important to consider potential post-pause changes in
the PM and/or R cells, although their nature is unknown. Such changes could be
important in determining the efficiency of a given stimulus-driven synaptic
input to these cells in eliciting postsynaptic potentials.
Novelty-related input to the pacemaker
Tuberous (high-frequency) and ampullary (low-frequency) electroreceptors
send their afferents to the electrosensory lateral line lobe (ELL), which
projects to the torus semicircularis of the midbrain. Recordings from the
torus semicircularis in Gymnotus carapo and Hypopomus
(Grau and Bastian, 1986)
suggest that this structure is involved in detecting the novelty of
electrosensory stimuli. Unfortunately, we are ignorant of the sites of novelty
detection for non-electrosensory stimuli. However, all such sites would issue
a `novelty command', probably via pre-pacemaker structures to the
PMn, thereby causing a brief increase in its firing rate. It is likely that
the sites of novelty detection and the paths over which a novelty command is
sent to the PMn differ for different sensory modalities. Different paths,
affecting different target cells in the PMn and possibly using different types
of transmitter, seem likely and may explain possible differences in the
courses of novelty responses elicited by stimuli that are sensed by different
modalities (e.g. compare the steady-state responses in Figs
2 and
3). Moreover, a command to the
PMn, elicited by input from one sense, may affect the PMn through more than
one path to either the PM or R cells. Even co-activated multiple input to the
same cell is possible, as has recently been demonstrated in Gymnotus
carapo (Curti et al.,
1999
): in Mauthner-cell-induced pacemaker accelerations
(Falconi et al., 1995
), both
NMDA and metabotropic glutamate receptor subtypes appear to be coactivated on
a single PM cell.
Prior pausing affects the tuberous-driven input to the PMn
The failure of the high-frequency electrical but not of the mechanosensory
stimuli to elicit a novelty response after a discharge cessation could be
explained by two, not necessarily exclusive, mechanisms. (i) Both the tuberous
electroreceptors, which sense the ongoing EODs, and their afferents are
continuously (from EOD to EOD) active and could be less sensitive after an EOD
pause. Also, the pathway from the ELL to the site where the novelty is
detected is probably also continuously active (to account for the rapid
detection of the novelty). Interrupting the ongoing activity of the receptors
and their afferent pathway may well lower their sensitivity in an unknown way.
It is not implausible that such effects could occur: preliminary data indicate
post-pause changes in the alternating-current-resistance of the skin of
Gymnotus carapo (S. Schuster, in preparation). It is not yet clear
whether these changes occur as a result of activity-dependent resistance
changes in the receptors. However, even if the receptors are not directly
affected, such changes in skin impedance would be likely to affect the current
flow sensed by the receptors. (ii) The effect could also be caused by the
interaction between synaptic input and the post-pause state of cells in either
the PMn or perhaps also in pre-pacemaker structures. The efficiency of input
to these cells might change as a result of postsynaptic mechanisms: as these
cells are likely to undergo changes at the onset of firing after a pause, even
presynaptic input of fixed size might lead to postsynaptic potentials of less
than normal size, thus causing smaller rate modulations. Such a mechanism
could also explain the 30 % reduction in efficiency observed for the
mechanical stimulus, but would probably be most relevant for the novelty
command input driven by the tuberous electrosensory input and less for
mechanosensory- and ampullary-driven inputs. Mechanosensory- and
ampullary-driven novelty commands presumably activate other paths, possibly
using different transmitters and receptors, in which the efficacy of synaptic
transmission could be less affected by the state of their target cells.
Relevance for studies on the consequences of post-pause changes in
EOD waveform
The novelty response appears to be a powerful tool for studying how changes
in the waveform and amplitude of its EOD
(Franchina and Stoddard, 1998;
Zakon et al., 1999
;
Schuster, 2000
) might affect
the ability of a weakly electric fish to electrolocate. The fastest EOD
changes occur when a Gymnotus carapo resumes its EODs after a
preceding pause (Schuster,
2000
). To address the implications of such EOD changes, it should
be possible to design experiments in which the fish signals with its novelty
response whether it has detected a novelty in its EOD feedback. Placing such a
novelty at various stages of the post-pause recovery in which the successive
EODs either vary in known ways or remain constant could determine whether EOD
changes are detrimental to the fish's ability to electrolocate. However, in
such experiments, I have never observed novelty responses to changes in EOD
feedback during the post-pause period in which the dramatic EOD changes occur.
The present investigation was started as a result of this failure and has
shown that high-frequency electrical stimuli are simply unable to drive a
novelty response after a preceding pause. This finding might also be important
to bear in mind in comparable research on species that show EOD changes
without prior pausing. If EOD changes occurred in correlation with changes in
discharge rate, then the efficiency of a given change in EOD feedback in
eliciting a novelty response could well be reduced as a result of the rate
changes rather than the EOD changes.
Is there an advantage of a lower post-pause responsiveness?
At present, it is only possible to speculate whether the reduced
responsiveness to high-frequency electrical stimuli might be more than a mere
by-product of disrupting an otherwise continuously active system. In a natural
situation, Gymnotus carapo would switch off its electric organ both
as a strong submissive signal to conspecifics
(Black-Cleworth, 1970;
Westby, 1974
) and during an
encounter with one of its predators, the electric eel
(Westby, 1988
). In both types
of encounter, it is not implausible that increases in discharge frequency,
such as those occurring during a novelty response, could be detrimental.
Increases in discharge frequency can be interpreted as aggressive signals by
conspecifics (Black-Cleworth,
1970
; Westby,
1974
), and electric eels are most attracted by high discharge
rates of approximately 100 Hz (Bullock,
1969
), which is above the resting frequency of a Gymnotus
carapo, so it might be a good strategy to suppress rate increases in
response to the electrical stimuli emitted by a superior conspecific or an
electric eel if one is still around after a pause.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Barrio, L. C., Caputi, A., Crispino, L. and Buno, W. (1991). Electric organ discharge frequency modulation evoked by water vibration in Gymnotus carapo. Comp. Biochem. Physiol. 100A,555 -562.
Bennett, M. V. L. (1971). Electric organs. In Fish Physiology, vol. V (ed. W. S. Hoar and D. J. Randall), pp. 347-491. New York: Academic Press.
Bennett, M. V. L. and Grundfest, H. (1959).
Electrophysiology of the electric organ in Gymnotus carapo. J. Gen.
Physiol. 42,1067
-1104.
Bennett, M. V. L., Pappas, G. D., Gimenez, M. and Nakajima,
Y. (1967). Physiology and ultrastructure of electrotonic
junctions. IV. Medullary electromotor nuclei in gymnotid fish. J.
Neurophysiol. 30,236
-300.
Black-Cleworth, P. (1970). The role of electrical discharges in the non-reproductive social behaviour of Gymnotus carapo (Gymnotidae, Pisces). Anim. Behav. 3, 1-77.
Bullock, T. H. (1969). Species differences in effect of electroreceptor input on electric organ pacemakers and other aspects of behaviour in electric fish. Brain Behav. Evol. 2, 85-118.
Ciali, S., Gordon, J. and Moller, P. (1997). Spectral sensitivity of the weakly discharging electric fish Gnathonemus petersii using its electric organ discharges as the response measure. J. Fish Biol. 50,1074 -1087.
Corrêa, S. A. L. and Hoffmann, A. (1998). Novelty response in the weakly electric fish Gymnotus carapo: Seasonal differences and the participation of the telencephalon in its modulation. Comp. Biochem. Physiol. 119A,255 -262.
Curti, S., Falconi, A., Morales, F. R. and Borde, M.
(1999). Mauthner cell-initiated electromotor behavior is mediated
via NMDA and metabotropic glutamatergic receptors on medullary
pacemaker neurons in a gymnotid fish. J. Neurosci.
19,9133
-9140.
Dye, J. C. and Meyer, J. H. (1986). Central control of the electric organ discharge in weakly electric fish. In Electroreception (ed. T. H. Bullock and W. Heiligenberg), pp. 71-102. New York: Wiley.
Falconi, A., Borde, M., Hernández-Cruz, A. and Morales, F. R. (1995). Mauthner cell-initiated abrupt increase of the electric organ discharge in the weakly electric fish Gymnotus carapo.J. Comp. Physiol. A 176,679 -689.
Franchina, C. R. and Stoddard, P. K. (1998). Plasticity of the electric organ discharge waveform of the electric fish Brachyhypopomus pinnicaudatus. I. Quantification of daynight changes. J. Comp. Physiol. A 183,759 -768.[Medline]
Grau, H. J. and Bastian, J. (1986). Neural correlates of novelty detection in pulse-type weakly electric fish. J. Comp. Physiol. A 159,191 -200.[Medline]
Heiligenberg, W. (1977). Principles of Electrolocation and Jamming Avoidance in Electric Fish. Berlin, Heidelberg, New York: Springer.
Heiligenberg, W. (1980). The evaluation of electroreceptive feedback in a gymnotoid fish with pulse-type electric organ discharges. J. Comp. Physiol. A 138,173 -185.
Heiligenberg, W. (1991). Neural Nets in Electric Fish. Cambridge, MA: MIT Press.
Kawasaki, M. and Heiligenberg, W. (1989). Distinct mechanisms of modulation in a neuronal oscillator generate different social signals in the electric fish Hypopomus. J. Comp. Physiol. A 165,731 -741.[Medline]
Kawasaki, M. and Heiligenberg, W. (1990). Different classes of glutamate receptors and GABA mediate distinct modulations of a neuronal oscillator, the medullary pacemaker of a gymnotiform electric fish. J. Neurosci. 10,3896 -3904.[Abstract]
Kramer, B., Tautz, J. and Markl, H. (1981). The EOD sound response in weakly electric fish. J. Comp. Physiol. A 143,435 -441.
Lissmann, H. W. (1958). On the function and evolution of electric organs in fish. J. Exp. Biol. 35,156 -191.
Meyer, J. H. (1982). Behavioral responses of weakly electric fish to complex impedances. J. Comp. Physiol. A 145,459 -470.
Moller, P. (1995). Electric Fishes. History and Behavior. London: Chapman & Hall.
Schuster, S. (2000). Changes in the electric
organ discharge after pausing the electromotor system of Gymnotus carapo.J. Exp. Biol. 203,1433
-1446.
Spiro, J. E. (1997). Differential activation of
glutamate receptor subtypes on a single class of cells enables a neural
oscillator to produce distinct behaviors. J.
Neurophysiol. 78,835
-847.
Trujillo-Cenóz, O., Lorenzo, D. and Bertolotto, C. (1993). Identification of neuronal types in the medullary electromotor nucleus of Gymnotus carapo. J. Comp. Physiol. A 173,750 .
von der Emde, G. (1999). Active electrolocation
of objects in weakly electric fish. J. Exp. Biol.
202,1205
-1215.
Watson, D. and Bastian, J. (1979). Frequency response characteristics of electroreceptors in the weakly electric fish, Gymnotus carapo. J. Comp. Physiol. A 134,191 -202.
Westby, G. W. M. (1974). Assessment of the signal value of certain discharge patterns in the electric fish, Gymnotus carapo, by means of playback. J. Comp. Physiol. 92,327 -341.
Westby, G. W. M. (1975). Has the latency dependent response of Gymnotus carapo to discharge-triggered stimuli a bearing on electric fish communication? J. Comp. Physiol. 96,307 -341.
Westby, G. W. M. (1988). The ecology, discharge diversity and predatory behaviour of gymnotiform electric fish in the coastal streams of French Guiana. Behav. Ecol. Sociobiol. 22,341 -354.
Zakon, H. (1986). The electroreceptive periphery. In Electroreception (ed. T. H. Bullock and W. Heiligenberg), pp. 103-156. New York: Wiley.
Zakon, H., Lu, Y. and Weisleder, P. (1998).
Sensory cells determine afferent terminal morphology in cross-innervated
electroreceptor organs: implications for hair cells. J.
Neurosci. 18,2581
-2591.
Zakon, H., McAnelly, L., Smith, G. T., Dunlap, K., Lopreato, G.,
Oestreich, J. and Few, W. P. (1999). Plasticity of the
electric organ discharge: implications for the regulation of ionic currents.
J. Exp. Biol. 202,1409
-1416.