Central control of electric signaling behavior in the mormyrid Brienomyrus brachyistius: segregation of behavior-specific inputs and the role of modifiable recurrent inhibition
Department of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853, USA
* Author for correspondence (e-mail: bc6s{at}virginia.edu)
Accepted 23 December 2003
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Summary |
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Key words: mormyrid, electric fish, Brienomyrus brachyistius, electric organ discharge, electromotor, central pattern generator, pacemaker, disinhibition, iontophoresis
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Introduction |
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A recent quantitative analysis of bursts in Brienomyrus brachyistius has revealed three modal display categories based on variation in the temporal patterning of EOD output (Fig. 1B; Carlson and Hopkins, unpublished observations). `Scallops' are stereotyped pulse sequences in which intervals suddenly drop to 1020 ms and then immediately return to baseline intervals of 100300 ms. `Accelerations' are graded decreases in interval, typically to values of 2060 ms. Accelerations are less stereotyped than scallops, and minimum intervals for accelerations may be maintained over several EOD cycles with a high degree of regularity. Subjectively, `rasps' appear to combine an initial scallop-like onset with an acceleration-like termination (Fig. 1B), which is supported by the quantitative characteristics of the three displays (Carlson and Hopkins, unpublished observations). Thus, rasps in this species probably result from a combination of two distinct displays.
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Recent anatomical and physiological studies on the electromotor system of
mormyrids have suggested a `closed-loop' circuit that may function as a
relatively simple central pattern generator (CPG) for regulating electromotor
output (Carlson, 2002b,
2003
;
von der Emde et al., 2000
).
Fig. 1A illustrates the
functional connectivity of this network. Each EOD is initiated in the
medullary command nucleus (CN), which activates spinal electromotor neurons
(EMNs) indirectly through a projection to the medullary relay nucleus (MRN;
Bell et al., 1983
;
Grant et al., 1986
). CN
integrates excitatory input from two distinct nuclei, the precommand nucleus
(PCN) in the mesencephalon, and the dorsal posterior nucleus (DP) in the
thalamus (Bell et al., 1983
;
Carlson, 2002b
,
2003
;
von der Emde et al., 2000
). DP
and PCN both receive inhibitory feedback from the electric organ corollary
discharge pathway (von der Emde et al.,
2000
), apparently via a projection from the dorsal
subdivision of the ventroposterior nucleus (VPd) in the torus semicircularis
(Bell et al., 1983
; Carlson,
2002b
,
2003
; Carlson and Hopkins,
2001). This recurrent inhibition probably provides a rate-limiting factor to
the activity of DP and PCN neurons that may be responsible for producing
rhythmic resting electromotor output
(Carlson, 2003
;
von der Emde et al., 2000
). A
few large neurons at the ventral edge of VP also project to DP, PCN and CN
(Bell et al., 1983
;
Carlson, 2002b
), although the
functional role of these neurons has not yet been explored.
DP and PCN neurons in B. brachyistius show a wide diversity of
firing patterns, and correlations between single unit activity and burst
production suggest that distinct neuronal populations are responsible for
generating scallops and accelerations
(Carlson, 2003). In distantly
related gymnotiform electric fish, the central posterior and prepacemaker
nuclei appear analogous to DP and PCN
(Carlson, 2002b
), and the two
are responsible for generating distinct electrical behaviors
(Metzner, 1999
). Based on
these two lines of evidence, we hypothesized that DP and PCN are likewise
responsible for driving different electrical behaviors in B.
brachyistius. Preliminary experiments using extracellular electrical
stimulation support this hypothesis, suggesting that accelerations are
generated by DP, while scallops are generated by PCN (Carlson and Hopkins,
unpublished observations). We tested this hypothesis using iontophoresis of
the excitatory neurotransmitter L-glutamate (L-Glu) to
stimulate DP and PCN neurons and observe the effects on electromotor output.
It is known that L-Glu iontophoresis in PCN drives decreases in EOD
interval in Gnathonemus petersii
(von der Emde et al., 2000
),
although these effects have not been quantified in relation to natural
signaling behavior, and the effects of stimulating DP have not been
assessed.
During scallop and acceleration production, there is a decrease in the
activity of VPd neurons, suggesting that disinhibition may play a role in
driving these displays by releasing DP and PCN neurons from negative feedback
control (Carlson, 2003).
Conversely, increases in inhibition may be responsible for producing
cessations in the discharge. We tested these hypotheses by several means.
Preliminary immunohistochemical studies indicate that PCN is surrounded by
terminals containing the inhibitory neurotransmitter
-amino-butyric
acid (GABA; Niso et al.,
1989
). Thus, we used iontophoresis of GABA in DP and PCN to test
whether this causes increases in EOD interval to verify that DP and PCN
receive GABAergic inhibitory input. Second, we used iontophoresis of
L-Glu in VP to test whether this also causes increases in EOD
interval. Finally, we used iontophoresis of the GABAA receptor
blocker bicuculline methiodide (BMI) in DP and PCN to block inhibitory input
and determine whether eliminating recurrent inhibition drives decreases in EOD
interval.
Differences in the effects of DP and PCN on the SPI are likely to be caused
by differences in their physiology, which may in turn relate to differences in
the strength of recurrent inhibition from VPd neurons
(Carlson, 2003). To test this
hypothesis, we compared the effects of L-Glu iontophoresis in DP
and PCN before and after BMI iontophoresis. If the observed differences
resulting from stimulating the two nuclei with L-Glu are due to
variation in inhibitory feedback, then blocking this inhibition should
eliminate these differences.
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Materials and methods |
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Surgery
Surgical procedures were identical to those described previously (Carlson,
2002b,
2003
). Animals were
anesthetized in a solution of 500 mg l1 tricaine
methanesulfonate (MS-222; Sigma Chemical Co., St Louis, MO, USA) and then
respirated under a solution of 160 mg l1 MS-222 during the
surgery. Fish were placed on a horizontal platform with lateral supports and
completely immersed in aquarium water except for the dorsal surface of the
head. A flap of skin was removed from the head and the underlying tissue was
scraped away to expose the dorsal surface of the skull. Lidocaine
(100200 µl of a 2% solution; Radix Laboratories, Inc., Eau Claire,
WI, USA) was used as a local anesthetic. A metal post was affixed to the skull
using superglue, and a small rectangular portion of the skull and meninges was
removed to expose the dorsal surface of the midbrain and caudal forebrain. A
reference electrode was then placed in the dorsal musculature at the posterior
end of the skull. The fish were then immobilized and electrically silenced
with an intramuscular injection of flaxedil (gallamine triethiodide;
100300 µl of a 3 mg ml1 solution; Sigma Chemical
Co.), and the respiration was switched to freshwater for recovery.
Experimental procedure
Triple-barrel electrodes were pulled using a Sutter Flaming Brown
Micropipette Puller model P-87 (Sutter Instrument Co., Novato, CA, USA) and
broken to a composite diameter of approximately 10 µm, resulting in
individual barrel diameters of 23 µm. Each barrel was filled
with one of the following solutions: (1) 3 mol l1 NaCl for
recording local field potentials; (2) 2% alcian blue (Sigma Chemical Co.) in
Walpole acetate buffer (pH=4.0) for marking electrode locations; (3) 0.1 mol
l1 L-Glu (pH=8.0, adjusted with NaOH) for
excitatory iontophoresis; (4) 0.5 mol l1 GABA (pH=3.5,
adjusted with HCl) for inhibitory iontophoresis or (5) 20 mmol
l1 BMI in 165 mmol l1 NaCl (pH=3.2) for
blocking GABAA receptors.
Electromotor output was monitored by placing a silver wire against the
caudal peduncle with a reference several centimeters away. Although the
electric organ is silenced by flaxedil, the EOD command can be recorded as a
three-spike potential resulting from the synchronous activation of EMN
(Bennett et al., 1967). The
first negative peak in the EMN volley was defined as the reference time for
EOD output (t0), which in a natural situation precedes the
EOD by 45 ms. At the start of each experiment, either DP, PCN or VP was
localized initially through landmarks on the dorsal surface of the brain and
then more precisely by recording characteristic field potentials that were
phase-locked to the EMN volley (see
Carlson, 2002b
). Field
potentials and EMN output were bandpass filtered from 10 Hz to 5000 Hz,
amplified 10 000x on a differential AC amplifier (A-M Systems, Inc.,
Everett, WA, USA; model 1700) and monitored on a digital oscilloscope
(Tektronix, Inc., Beaverton, OR, USA; model 5223). Iontophoretic currents were
provided by a separate amplifier (A-M Systems, Inc.; Neuroprobe model
1600).
After locating a given nucleus, the horizontal position and depth of the electrode were adjusted using a microelectrode drive (Burleigh Instruments, Inc., Fishers, NY, USA; Inchworm 6000) that was held by a micromanipulator (Newport Co., Fountain Valley, CA, USA; model 462-XY-M). The position of the electrode was adjusted in 50 µm steps in all three dimensions and the location where pulsed iontophoresis of L-Glu (0.5 µA, 500 ms pulses at 0.25 Hz) resulted in the strongest modulation in the SPI was used for all subsequent iontophoretic injection experiments in that nucleus (Fig. 2).
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For all experiments, the EMN signal was sent to a Schmitt Trigger, which
was output to an event timer that recorded the time of t0
using a clock rate of 1 MHz (Tucker-Davis Technologies, Alachua, FL, USA;
model ET1). Data on EOD times of occurrence were saved using custom-made
software. For experiments involving L-Glu or GABA iontophoresis, 20
s of data were recorded before iontophoresis, followed by 20 s of
iontophoresis (1.0 µA for L-Glu, +1.0 µA for GABA) and
an additional 20 s of recording. In most cases, opposite polarity current
(+1.0 µA for L-Glu, 1.0 µA for GABA) was tested as a
control, and this resulted in no observable modulation in the SPI. For
experiments involving BMI iontophoresis, 1 min of data were recorded before
iontophoresis, followed by 4 min of iontophoresis (+100 nA), followed by 1 min
of recovery. The longer duration of BMI iontophoresis compared with
L-Glu and GABA iontophoresis was chosen based on results from
previous studies in other systems in which the effects of BMI iontophoresis
occurred after relatively long latencies and persisted for several minutes
after termination (Fujita and Konishi,
1991; Heiligenberg et al.,
1996
). The physiological basis for this difference is unclear but
is probably related to differences in the pharmacological effects of a
receptor blocker compared with naturally occurring neurotransmitters. In some
experiments, the effects of L-Glu iontophoresis in DP and PCN
before and after BMI iontophoresis were determined. The procedure for
L-Glu iontophoresis in these cases was identical to the normal
L-Glu iontophoresis procedure, and L-Glu iontophoresis
was always performed within 2 min after terminating BMI iontophoresis.
Statistica 6.1 (StatSoft, Inc., Tulsa, OK, USA) was used for all statistical
analyses of data on the SPI.
Histology
At the end of each experiment, we marked the location of the electrode by
iontophoretic injection of alcian blue, using a 500 ms, 150 V pulse (Grass
Medical Instruments, Quincy, MA, USA; model S88 stimulator). After completing
the experiments, fish were placed back under general anesthesia (160 mg
l1 MS-222) and then perfused transcardially with Hickman's
ringer solution (6.48 g l1 NaCl, 0.15 g l1
KCl, 0.29 g l1 CaCl2, 0.12 g l1
MgSO4, 0.084 g l1 NaHCO3, 0.06 g
l1 NaH2PO4) followed by ice-cold 4%
paraformaldehyde/1% glutaraldehyde in 0.1 mol l1 phosphate
buffer (PB; pH=7.2) for fixation. The brains were removed and postfixed
overnight and then transferred to 0.1 mol l1 PB for storage.
Brains were transferred to a solution of 30% sucrose in 0.1 mol
l1 PB on the night prior to sectioning. Transverse sections
were cut on a freezing microtome at 50 µm, mounted on chrom-alum-subbed
slides, counterstained with neutral red, dehydrated in a graded alcohol series
and coverslipped with Permount (Sigma Chemical Co.).
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Results |
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In three different fish, doseresponse curves were constructed by measuring the effects of L-Glu iontophoresis on median EMN intervals with varying levels of current magnitude (from 100 nA to 900 nA in steps of 200 nA) in all three nuclei (Fig. 3A). In both DP and PCN, increasing levels of current led to greater shortening of EMN intervals, with the response beginning to saturate at approximately 500 nA and showing complete saturation at 700 nA to 900 nA (Fig. 3B). Similarly, in VP, increasing levels of current led to a greater elongation of EMN intervals, with the response saturating at 700 nA to 900 nA (Fig. 3B). Thus, for all experiments using L-Glu iontophoresis, we used current magnitudes of 1.0 µA, which was well above the level of saturation for all three nuclei and therefore provided maximal stimulation of each nucleus.
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20 s injections of L-Glu into the three nuclei led to characteristic modulations in the SPI (Fig. 4). In both DP and PCN, there was a marked, maintained decrease in EMN interval that persisted throughout the duration of the stimulus, while in VP there was a complete cessation of activity for the whole period of stimulation and usually for many additional seconds after terminating the current. There was a highly significant decrease in EMN intervals during L-Glu iontophoresis in DP and PCN and a highly significant increase in EMN intervals during L-Glu iontophoresis in VP (Table 1).
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Although stimulation of both DP and PCN led to a shortening of EMN
intervals, the responses of the two nuclei were typically quite different.
Stimulation of DP typically resulted in a smooth decrease in interval to
values of 2050 ms that were maintained throughout the period of
stimulation with a high degree of regularity (Figs
4,5).Stimulation
of PCN also led to a decrease in baseline intervals, but this baseline was
typically not as low or regular as during DP stimulation
(Table 1) and was punctuated by
the repeated production of transient, intense bursts reaching minimum
intervals of 1025 ms (Figs
4,
5). In some cases, these
transient bursts appeared identical to scallops, while in most cases, they
simply appeared as non-stereotyped `scallop-like' bursts
(Fig. 5). Stimulation in PCN
led to a significantly greater coefficient of variation (CV) in EMN interval
(Wilcoxon matched pairs test: z22=3.912,
P<0.0001), smaller minimum EMN interval
(z22=2.354, P<0.02) and greater maximum EMN
interval (z22=3.360, P<0.001) compared with
stimulation in DP (Fig. 6), as
expected from the burst-like responses to PCN stimulation.
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GABA iontophoresis
Iontophoresis of GABA in DP (N=15 fish) and PCN (N=17
fish) typically led to an elongation of EMN intervals that was maintained
throughout the duration of the stimulus
(Fig. 7), resulting in a
significant increase in EMN intervals
(Table 2). By contrast, we
observed no response to GABA iontophoresis in VP (N=14 fish;
Fig. 7) and there was no
significant change in EMN intervals (Table
2).
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BMI iontophoresis
Iontophoresis of BMI into DP (N=7 fish) and PCN (N=7
fish) resulted in repetitive bursting behavior that started after a relatively
long latency following stimulus onset (30150 s) and persisted for
several minutes after stimulus termination
(Fig. 8A). Comparing the last
minute of BMI iontophoresis with the 1 min control period prior to BMI
iontophoresis, there was a significant shortening of median EMN interval in
both DP (Wilcoxon matched pairs test; z7=2.3664;
P<0.02) and PCN (z7=2.2678;
P<0.025). The bursts resulting from BMI iontophoresis were
qualitatively similar to those produced by freely behaving animals, and
included scallops, accelerations and rasps
(Fig. 8B). Thus, rather than
simply quantifying overall activity with general descriptors, it was possible
to count the number of bursts produced. There were no significant differences
in the numbers of scallops (MannWhitney U test:
z7,7=1.086; P>0.27), accelerations
(z7,7=0.192; P>0.84) or rasps
(z7,7=0.639; P>0.52) produced by BMI
iontophoresis in DP compared with PCN (Fig.
8C).
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Comparing the effects of L-Glu iontophoresis before and after BMI iontophoresis in both DP and PCN demonstrated a significant increase in the CV in EMN interval (F1,11=7.848; P<0.02), a significant decrease in the minimum EMN interval (F1,11=34.95; P<0.02) and no significant change in the maximum EMN interval (F1,11=3.809; P>0.07). Before BMI iontophoresis, the CV was significantly greater in PCN than in DP (Fig. 9A; MannWhitney U test: z7,6=2.571; P<0.02), although there was no significant difference after BMI (z7,6=0.571; P>0.56). Similarly, the minimum EMN interval was significantly smaller in PCN than in DP before BMI iontophoresis (Fig. 9B; z7,6=2.000; P<0.05), although there was no significant difference after BMI (z7,6=0.428; P>0.66), and the maximum EMN interval was significantly greater in PCN than in DP before BMI iontophoresis (Fig. 9C; z7,6=2.000; P<0.05), though there was no significant difference after (z7,6=0.428; P>0.66). Thus, following BMI iontophoresis, the effects of L-Glu iontophoresis in DP and PCN were statistically identical.
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Discussion |
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Neurons in PCN appear to be surrounded by GABAergic inhibitory terminals
(Niso et al., 1989), and
single units in both DP and PCN receive recurrent inhibitory feedback
via the corollary discharge pathway
(Carlson, 2003
;
von der Emde et al., 2000
).
Anatomically, DP and PCN receive a dense projection from VPd, which in turn
receives input from the corollary discharge pathway
(Carlson, 2002b
). These three
lines of evidence suggest that VPd provides recurrent, GABAergic inhibition to
DP and PCN. The results of the current study support this hypothesis:
iontophoresis of GABA into DP and PCN induces a significant elongation of EOD
intervals, as does stimulation of VPd using L-Glu iontophoresis. In
most cases, stimulation of VPd led to complete cessations in the discharge,
suggesting that cessations may result from increases in the activity of VPd
neurons and therefore stronger recurrent inhibition.
We hypothesized that this recurrent inhibition is responsible for
regulating DP and PCN activity, and thereby maintaining the irregular,
baseline rhythm of 100300 ms EOD intervals. During burst displays, the
activity of VPd neurons decreases
(Carlson, 2003), so we
hypothesized that disinhibition plays a role in disrupting the baseline rhythm
by releasing DP and PCN from their normal rate-limiting factor, thereby
allowing them to drive burst displays. In support of this hypothesis,
application of the GABAA receptor blocker BMI to DP and PCN caused
the SPI to go from a resting rhythm to repetitive bursting. It is unclear how
the activity of VPd neurons is modulated in a natural situation, although the
tectum mesencephali has a strong projection to VPd
(Carlson, 2002b
;
Wullimann and Northcutt, 1990
)
and retrograde labeling suggests that VPd may also receive inputs from
hypothalamic and preoptic areas (Carlson,
2002b
). Application of GABA to VP did not elicit any changes in
EMN activity, suggesting that a reduction in VPd activity is mediated by a
different neurotransmitter or through neuromodulatory inputs.
One potential source of physiological differences between DP and PCN may be
variation in recurrent inhibition from VPd neurons, which produce a
stereotyped burst of action potentials starting within a few milliseconds of
EOD production (Carlson, 2003;
von der Emde et al., 2000
).
Across neurons, there is wide variation in the duration of these bursts. If
different subsets of VPd neurons project to DP and PCN, this variation could
lead to differences in the baseline activity of DP and PCN neurons and
therefore different effects on electromotor output when stimulated. In support
of this hypothesis, the effects of L-Glu iontophoresis in the two
nuclei were identical following BMI iontophoresis. Furthermore, if recurrent
inhibition to DP and PCN is separated into different pathways, this may
provide a means for differentially activating the two nuclei and generating
distinct behaviors.
Although we suggest that disinhibition plays a role in driving burst
displays in a natural situation, we were able to elicit such displays solely
through the application of L-Glu to DP and PCN, which presumably
did not affect recurrent inhibition. Most likely, the increased excitatory
input caused by L-Glu application counterbalanced the ongoing
recurrent inhibition, resulting in increases in EMN activity. The different
effects of L-Glu stimulation in DP and PCN probably relate to the
different strengths of recurrent inhibition that counteract the stimulatory
effects of L-Glu to varying degrees. Application of BMI to these
nuclei, by contrast, leads to a maintained blockage of recurrent inhibition
but no excitatory input. Not surprisingly, this also leads to increases in EMN
activity. Unlike stimulation with L-Glu, however, there were no
observable differences in the output patterns caused by BMI stimulation in DP
and PCN, which can be explained by the fact that BMI application also removed
the source of physiological differences between the two nuclei, which was not
the case with L-Glu stimulation. In a natural situation,
disinhibition is typified by a modest, temporary reduction in inhibitory input
from the baseline level rather than a complete, maintained removal
(Carlson, 2003). Unlike BMI
application, this would not eliminate differences between DP and PCN but would
provide a transient excitatory effect similar to the effects of
L-Glu stimulation, causing the two nuclei to drive different
behaviors.
Convergence in the central control of electromotor behavior
Gymnotiform electric fish from South America have electromotor and
electrosensory systems that share many striking similarities with those of
mormyrids (Hopkins, 1995),
despite overwhelming evidence that their electrogenic and electrosensory
capabilities have evolved independently
(Bullock et al., 1983
). EOD
production in both groups of fish is controlled by a ventral midline nucleus
in the medulla (CN in mormyrids and the pacemaker nucleus, or PN, in
gymnotiforms), which projects to larger, adjacent relay neurons whose axons
descend the spinal cord to innervate electromotor neurons
(Dye and Meyer, 1986
). A
recent anatomical study has suggested that DP and PCN are analogous to the
central posterior (CP) and prepacemaker nuclei (PPN) that provide input to PN
in gymnotiforms (Carlson,
2002b
). In both groups of fish, there is a rostral group of cells
located within a dorsal thalamic nucleus (DP and CP) and a caudal group of
cells that forms a ventrolateral extension of the dorsal thalamus (PCN and
PPN). While the caudal groups of cells are relatively large with thick,
extrinsic dendrites, the rostral groups of cells are small with thin,
intrinsic dendrites.
Stimulating CP in gymnotiforms leads to `rises' (smooth, graded increases
in frequency), while stimulating PPN leads to `chirps' (transient, intense
bursts; Metzner, 1999). This
is strikingly similar to electromotor output patterns induced by stimulation
in DP and PCN, respectively, with the former driving accelerations (smooth,
graded increases in frequency) and the latter driving scallops (transient,
intense bursts). Thus, convergence in anatomical substrates appears to be
directly linked to convergence in the behaviors they control. In gymnotiforms,
the different electrical behaviors resulting from activation of CP and PPN are
related to differences in the location of synapses in PN and differences in
the glutamate receptor subtypes found at these synapses
(Metzner, 1999
). It is
possible that similar differences play a role in the differential effects of
DP and PCN on electromotor behavior in mormyrids, but the findings of the
current study suggest that these differences may be due solely to the effects
of variation in recurrent inhibition.
Diversity in mormyrid electric signaling behavior
Every species of mormyrid that has been studied produces acceleration-like
displays that appear to play a role in aggression, but there is wide diversity
across species in the other types of displays that may be produced
(Carlson, 2002a). In
Gnathonemus petersii, agonistic encounters are often accompanied by
repetitive `pulse pairs', with EOD intervals alternating between 1516
ms and 89 ms (Bauer,
1972
; Bell et al.,
1974
). Such displays have never been observed in B.
brachyistius or any other species
(Carlson, 2002a
), although the
number of species studied is relatively small. By contrast, scallops have
never been described for G. petersii, although they have been
described for B. niger (Serrier
and Moller, 1989
). This suggests the hypothesis that pulse pairs
may be driven by PCN in species that do not produce scallops.
There is also wide diversity in the characteristics of certain displays
between species. For example, scallops in B. niger and B.
brachyistius are quite similar in their basic structure but differ in
minimum interval (Carlson,
2002a; Carlson and Hopkins, unpublished observations;
Serrier and Moller, 1989
).
Such differences are possibly related to differences in the morphology and
physiology of PCN neurons. Field recordings from various Brienomyrus
species in Gabon reveal the production of rasps that differ dramatically from
those in B. brachyistius and do not appear to result from combining a
scallop and an acceleration (Hopkins,
1983
; Hopkins and Bass,
1981
). Scallops have not been described for these species, so it
is possible that PCN controls rasp production in this group. The rich
diversity of mormyrids and the signals they produce provide a rare opportunity
for studying the evolution of neural circuits that govern communication
behavior.
Motor networks and behavior
Much of our understanding of the mechanisms underlying stereotyped motor
output comes from relatively simple networks involved in rhythmic behaviors
such as locomotion, digestion, respiration and heartbeat
(Marder and Bucher, 2001). The
stereotyped, rhythmic output of these central pattern generators (CPGs)
results from a combination of several cellular and molecular specializations,
many of which are shared across different networks. The findings of the
current study, as well as other recent studies (Carlson,
2002b
,
2003
;
von der Emde et al., 2000
),
reveal several similarities between these networks and the mormyrid
electromotor system. For instance, recurrent inhibition plays an important
role in establishing rhythmic motor output in many different networks
(Friesen and Stent, 1978
) as
well as in regulating electromotor output in mormyrids. Similarly,
disinhibition serves a permissive function in activating stereotyped motor
output in several motor systems (Faumont
et al., 1998
; Noga et al.,
1988
; Wang and Bieger,
1991
), which also seems to be the case for generating burst
displays in mormyrids.
Extracellular stimulation of restricted brain regions can elicit the
production of semi-natural, species-specific communication signals in a
variety of vertebrate species (Apfelbach,
1972; Demski and Gerald,
1972
; Fine and Perini,
1994
; Fu and Brudzynski,
1994
; Goodson and Bass,
2000
; Jürgens and
Richter, 1986
; Phillips and
Youngren, 1973
; Schmidt,
1966
; Schuller and
Radtkeschuller, 1990
; Seller
and Armitage, 1983
; Valentine
et al., 2002
; Williams and
Vicario, 1993
). While it is clear that stereotyped signal
production may be controlled by spatially distinct groups of neurons, there is
often insufficient information about anatomical circuitry and how it relates
to patterns of neuronal activity to gain insight into the network and cellular
mechanisms involved in signal generation. Part of the reason for this is that
many vertebrate communication signals are relatively complex, involving
several features that vary semi-independently over time. As a result, the
neural substrates underlying the generation of these signals are similarly
complex, making it difficult to formulate hypotheses that directly link the
activity patterns of individual neurons to specific signal
characteristics.
By contrast, electric signaling behavior in mormyrids is relatively simple,
consisting of two distinct components: a stereotyped EOD waveform and a
variable pattern of EOD production (the SPI). The characteristics of the
former are controlled by the morphophysiological characteristics of the
electric organ (Bennett, 1971),
while the latter is determined by patterns of activity in CN
(Grant et al., 1986
). Thus,
unraveling the mechanisms involved in regulating the SPI breaks down to a
problem of understanding the generation of spike times in CN. As this and
other recent studies have shown (Carlson,
2002b
,
2003
;
von der Emde et al., 2000
),
this relative simplicity makes the mormyrid electromotor network an excellent
model system for studying the mechanisms of generating stereotyped temporal
patterns in vertebrate communication. The many similarities between this
system and the gymnotiform electromotor network, as well as with CPGs in
general, suggest that insights gained into the functioning of this network are
likely to be instructive towards general issues in the motor control of
behavior.
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Acknowledgments |
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References |
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