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First published online August 9, 2007
Journal of Experimental Biology 210, 2873-2884 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.002949
Multiple modulators act on the cardiac ganglion of the crab, Cancer borealis
Volen Center for Complex Systems and Department of Biology, Brandeis University, MS-013, 415 South Street, Waltham, MA 02454, USA
Author for correspondence (e-mail:
marder{at}brandeis.edu)
Accepted 10 June 2007
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: crustacean, pericardial organ, CabTRP Ia, red pigment concentrating hormone, allatostatin, crustacean cardioactive peptide
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Hurley et al., 2004;
Marder and Thirumalai, 2002;
Matheson, 1997;
Nusbaum et al., 2001).
Neuromodulatory substances can alter the properties of individual neurons and
synapses, and consequently alter the output of neuronal circuits
(Harris-Warrick and Marder,
1991; Marder and Bucher,
2007). Neuromodulators can be delivered locally to specific
neurons or groups of neurons from terminals within ganglionic neuropils
(Nusbaum and Beenhakker, 2002;
Nusbaum et al., 2001) or can
be delivered systemically as hormones that can reach multiple sites within the
animal. In this latter case, it is thought that neuromodulators can globally
alter multiple sites within the animal to coordinate behaviors in response to
the endogenous state of the animal or environmental stimuli
(Dircksen, 1998;
Kravitz, 1988).
The cardiac ganglion (CG) of decapod crustaceans, which drives the
contractions of the heart, has been used to study the cellular mechanisms and
synaptic physiology that underlie the generation and modulation of rhythmic
motor patterns (Tazaki and Cooke,
1979a; Tazaki and Cooke,
1979b; Tazaki and Cooke,
1986). It is known that the CG is modulated by substances released
locally from regulatory nerve fibers and by hormones released from endocrine
sites such as the pericardial organs (POs)
(Alexandrowicz and Carlisle,
1953; Christie et al.,
1995; Cooke, 2002;
Cooke and Hartline, 1975;
Li et al., 2003;
Li et al., 2002;
Pulver and Marder, 2002;
Skiebe, 2001). The isolated CG
is sensitive to biogenic amines (Benson,
1984; Berlind,
2001; Cooke and Hartline,
1975; Fort et al.,
2004; Hashemzadeh-Gargari and
Freschi, 1992b; Miller et al.,
1984; Saver et al.,
1999), GABA (Kerrison and
Freschi, 1992), glutamate
(Hashemzadeh-Gargari and Freschi,
1992a), cholinergic agonists
(Freschi, 1991;
Freschi and Livengood, 1989;
Sullivan and Miller, 1990),
proctolin (Freschi, 1989;
Miller and Sullivan, 1981;
Saver et al., 1999;
Sullivan and Miller, 1984),
crustacean cardioactive peptide (CCAP)
(Saver et al., 1999),
FMRFamide-like peptides (FLPs)
(Cruz-Bermúdez et al.,
2006; Saver et al.,
1999) and nitric oxide
(Mahadevan et al., 2004).
Although the aforementioned studies (and others) have provided insights
into the mechanisms underlying the modulation of the CG, these experiments
were performed with variable experimental conditions such as saline
composition or temperature. Such manipulations make it difficult to compare
the actions of different substances on CG motor output. For example, recent
studies using the isolated heart preparation have shown that cardiac
performance in the lobster, Homarus americanus, is
temperature-dependent (Camacho et al.,
2006; Worden et al.,
2006). Secondly, studies on the isolated CG have been done using
many different species, which poses the question of whether the effect of a
single modulator in one particular species can be generalized to related
species. Indeed, there are suggestions that the actions of some modulators may
be species specific (Saver and Wilkens,
1998). For instance, octopamine has been reported to decrease the
CG burst frequency of the crab, Portunus sanguinolentus
(Benson, 1984). On the other
hand, octopamine was shown to increase the burst frequency and depolarize the
CG neurons of the crab, Limulus polyphemus
(Augustine and Fetterer, 1985).
When attempting to reconcile contrasting findings such as these one needs to
determine whether apparent discrepancies reported from different studies are a
product of different experimental conditions, or reflect true species-specific
actions.
To determine how the CG in one species responds to many of the multiple
modulators that are known to be present in key neurosecretory structures like
the POs (DeKeyser et al.,
2007), we decided to measure their physiological actions on the CG
of a single species (the crab, Cancer borealis) under constant
experimental conditions.
In this study we have characterized for the first time in any species the
actions of three peptides on the cardiac ganglion. The peptide RPCH
(pQLNFSPGW-NH2) is present in three distinctive neuroendocrine
sites in crustaceans (including C. borealis): the pericardial organs,
sinus gland and eyestalks (Christie et
al., 1995; Fu et al.,
2005a; Li et al.,
2003; Pulver and Marder,
2002; Stemmler et al.,
2006). RPCH is also found within the terminals of neurons
projecting from anterior ganglia to the stomatogastric ganglion (STG)
(Christie et al., 1997a;
Nusbaum and Marder, 1988;
Thirumalai and Marder, 2002)
and it is considered an endogenous modulator of the stomatogastric nervous
system (STNS) (Dickinson et al.,
1993; Dickinson et al.,
2001; Dickinson and Marder,
1989; Dickinson et al.,
1990; Nusbaum and Marder,
1988).
The neuropeptide CabTRP Ia (APSGFLGMR-NH2) was originally
isolated from the crab, C. borealis, and it is considered to be a
member of the invertebrate tachykinin-related peptide family
(Christie et al., 1997b).
CabTRP Ia has also been identified immunocytochemically in the POs of the
embryonic lobster, H. americanus
(Pulver and Marder, 2002), and
with mass spectrometry in the shrimp, Penaeus vannamei
(Nieto et al., 1998), the
crayfish Procambarus clarkii and lobster, Panulirus
interruptus (Yasuda-Kamatani and
Yasuda, 2004) and in the anterior commissural organ (ACO) of the
crab, Cancer productus (Messinger
et al., 2005). Physiological studies have shown that CabTRP Ia is
a potent modulator of the STG motor output. CabTRP Ia is synaptically released
from a pair of modulatory projection neurons into the neuropil of the STG,
where it increases the pyloric rhythm frequency and activates the gastric mill
motor pattern (Christie et al.,
1997b; Thirumalai and Marder,
2002; Wood et al.,
2000).
The allatostatins (ASTs) consist of a family of peptides present in various
insects including cockroaches (Ding et
al., 1995; Vilaplana et al.,
1999), moths (Audsley and
Weaver, 2003; Kramer et al.,
1991), locusts (Skiebe et al.,
2006; Veelaert et al.,
1996a; Veelaert et al.,
1996b), mosquitoes
(Hernandez-Martinez et al.,
2005) and flies (Duve et al.,
1993; Lenz et al.,
2001; Williamson et al.,
2001). In crustaceans, including C. borealis, AST-like
immunoreactivity has been detected in the POs and other structures
(Christie et al., 1995;
Kilman et al., 1999;
Pulver and Marder, 2002;
Skiebe, 1999;
Skiebe, 2001;
Skiebe and Schneider, 1994;
Yasuda-Kamatani and Yasuda,
2006). AST-3 (GGSLYSFGL-NH2) is an effective inhibitor
of the STG pyloric rhythm (Skiebe and
Schneider, 1994). AST-3 also decreases the amplitude of foregut
muscle contractions (Jorge-Rivera and
Marder, 1997) and modulates sensory information in the STNS
(Billimoria et al., 2006;
Birmingham et al., 2003).
In addition to RPCH, CabTRP Ia, and AST-3, we studied the action of other
neuropeptides and small molecule transmitters and their agonists, whose
actions have been described before in cardiac ganglia of other species. This
study provides the most comprehensive examination to date of the effects of
many of the neuromodulators present in crustaceans directly on the cardiac
ganglion. Preliminary results have been previously presented in abstract
format (Cruz-Bermúdez and Marder,
2006).
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). Briefly, after removing the stomach and the hepatopancreas,
a small piece of carapace with heart attached was separated from the animal.
The muscles around the heart were excised and the heart was subsequently
removed and pinned ventral side up in a SylgardTM-coated (Dow Corning,
Midland, MI, USA) dish. A V-shaped cut was made from the sternal artery on the
ventral wall of the heart towards each of the ventral ostia to expose the CG,
which sits directly on the dorsal inner wall of the heart. The ganglion was
isolated from the muscle by transecting each of the nerve roots at the most
distal point at which the root penetrates the muscle. In some preparations, a
small non-contracting piece of muscle was left attached to the posterior end
of the main trunk. The isolated ganglion was then pinned dorsal side up in a
SylgardTM-coated 25 ml dish (60x15 mm) containing chilled
(10–12°C) saline.
Solutions
The modulators used in this study were: allatostatin III type A (AST-3),
crustacean cardioactive peptide (CCAP) (Bachem, Torrance, CA, USA); Cancer
borealis tachykinin-related peptide Ia (CabTRP Ia; courtesy of Dr M. P.
Nusbaum, University of Pennsylvania School of Medicine, Philadelphia, PA,
USA); dopamine, 
-aminobutyric acid (GABA), histamine, nicotine,
octopamine, pilocarpine, proctolin, serotonin (Sigma, St Louis, MO, USA); red
pigment concentrating hormone (RPCH), SDRNFLRFamide, TNRNFLRFamide (American
Peptide Company, Sunnyvale, CA, USA); Cancer borealis allatostatin
type B (CbAST-B1), orcomyotropin-related peptide (OMTR) and NRNFLRFamide
(courtesy of Dr Lingjun Li, University of Wisconsin School of Pharmacy,
Madison, WI, USA). Peptides were dissolved in distilled water at
10–2 or 10–3 mol l–1,
stored at –20°C, and diluted in C. borealis saline at the
desired concentrations immediately before each application.
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glass microelectrodes filled with 0.6 mol
l–1 K2SO4 and 20 mmol
l–1 KCl and an Axoclamp 2A (Axon Instruments, Foster City,
CA, USA). Signals were amplified and filtered using an A-M Systems 1700
Differential AC amplifier (Carlsborg, WA, USA). Data were recorded to a
computer hard drive using a Digidata 1322A data acquisition board and pClamp 8
software (Axon Instruments). Data files were analyzed in Spike 2 (version 5;
Cambridge Electronic Design, Cambridge, UK). Statistical tests and graphs were
performed in SigmaPlot (version 8), SigmaStat (version 3.5; Systat Software
Inc., Richmond, CA, USA) and StatView (version 5; SAS Institute, Cary, NC,
USA). Figures were made in Canvas (version 10; ACD Systems of America, Inc.,
Miami, FL, USA). Time stretches of several minutes in which the range of
values did not change visibly were assumed to represent the steady state and
used to determine the means. We performed paired Student's t-tests
for statistical significance, indicated in bar plots by asterisks
(*P<0.05; **P<0.01), one-way
ANOVA or, alternatively Kruskal–Wallis one-way ANOVA when normality
tests failed and multiple pairwise comparisons of means (Dunn's Method). All
histograms represent the mean ± s.e.m. unless stated otherwise.
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). The heart muscle fibers are innervated by five motor
neurons (Alexandrowicz, 1932)
that make reciprocal chemical and electrical excitatory synapses with four
pacemaker neurons that initiate the bursting activity of the whole network
(Hartline, 1967;
Hartline, 1979;
Mayeri, 1973;
Tazaki and Cooke, 1979a;
Tazaki and Cooke, 1979b;
Tazaki and Cooke, 1979c). The
CG also receives excitatory and inhibitory inputs from the central nervous
system and the CG is a direct target for neuromodulators released from the POs
(Alexandrowicz, 1932;
Cooke, 2002). In C.
borealis, three of the motor neurons are located in the antero-lateral
nerves (A-l.n.), 2–4 mm away from the anterior bifurcation
(Fig. 1A). The remaining two
motor neurons and the pacemaker cells are located in the posterior bifurcation
near the junction of the two postero-lateral nerves (P-l.n.). The ganglionic
trunk is 
1 cm in length. The CG generates bursts of motor neuron action potentials that synaptically depolarize the heart muscle fibers. Fig. 1B shows simultaneous extracellular and intracellular recordings of the CG motor pattern. The motor neuron (large units; top trace) and pacemaker neuron (small units; top trace) action potentials were recorded extracellularly from the ganglionic trunk. The intracellular recording from the motor neuron axon (Fig. 1B, bottom trace) was done by removing the connective tissue that wraps the neurons' processes at the anterior junction (Fig. 1A), and shows subthreshold information such as the EPSPs from the pacemaker neurons and the slow wave depolarization that generates the burst. Because the motor neuron spikes are the only impulses that directly elicit contractions, all measurements reported here are from the bursts of impulses generated by the motor neurons (large units in traces; Fig. 1B).
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3
to 5. On average (N=12), RPCH significantly changed all the CG output
parameters (Fig. 2B;
Table 1) including burst
frequency (0.17±0.02 Hz in control and 0.20±0.02 Hz in RPCH;
P<0.05); duty cycle (the burst duration divided by the cycle
period) (0.10±0.02 in control and 0.15±0.01 in RPCH;
P<0.01); number of spikes per burst (4±0.76 in control and
6±0.81 in RPCH; P<0.01); and spike frequency in the burst
(5.31±0.96 Hz in control and 7.97±1.43 Hz in RPCH;
P<0.01).
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Fig. 3 shows the physiological actions of CabTRP Ia on the CG. The top trace of Fig. 3A shows a recording from a motor neuron. In control saline the frequency of the CG burst was 0.16 Hz with 4–5 spikes/burst (Fig. 3A; top trace). In this preparation, CabTRP Ia increased the burst frequency and number of spikes per burst (Fig. 3A; bottom trace) and depolarized the CG motor neurons (Fig. 3B). Fig. 3C shows plots of the burst frequency (left) and number of spikes per burst (right) against time for another CG in control, CabTRP Ia perfusion (gray bar) and wash. On average (N=12), 10–6 mol l–1 CabTRP Ia significantly increased the CG burst frequency and duty cycle (Fig. 3D; Table 1). Although CabTRP Ia increased the number of spikes/burst and spike frequency in some preparations, the pooled data across all preparations failed to reach significance (Fig. 3D; Table 1).
Fig. 4A shows intra-axonal representative recordings of the inhibitory effect of 10–6 mol l–1AST-3 on the CG motor pattern. In this preparation, AST-3 completely abolished the bursting pattern without changing the baseline membrane potential. Note the few dispersed EPSPs coming from the pacemaker cells during AST-3 bath-application (Fig. 4A, middle trace). In three out of six preparations all motor neuron activity was reversibly inhibited in AST-3, while in the remaining preparations the motor neuron activity was very substantially reduced. Fig. 4B and Table 1 show pooled data documenting the inhibitory actions of AST-3 on the isolated CG (N=6): burst frequency (0.21±0.02 Hz in control and 0.05±0.02 Hz in AST-3; P<0.05); duty cycle (0.14±0.01 in control and 0.03±0.01 in AST-3; P<0.01); number of spikes per bursts (4±0.58 in control and 2±0.72 in AST-3; P<0.05); and spike frequency in the burst (6.92±1.28 Hz in control and 2.71±1.30; P<0.05).
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Effects of the proctolin, CCAP and FMRF-like peptides (FLPs)
Proctolin, CCAP, and a variety of FLPs have been studied on the CGs and
hearts of a variety of species, where they are generally excitatory
(Fort et al., 2007;
Saver and Wilkens, 1998).
Fig. 5 shows intra-axonal recordings from a motor neuron of a single CG to which we applied proctolin and CCAP. Fig. 5A shows the recording in control (top trace) and in the presence of 10–6 mol l–1 proctolin (bottom trace). In data pooled from multiple preparations (Fig. 5B; Table 1), proctolin significantly increased the burst frequency, duty cycle, number of motor neuron spikes and spike frequency in the burst. After proctolin washout from the preparation shown in Fig. 5A, CCAP (10–6 mol l–1) was applied (Fig. 5C). Like proctolin, CCAP caused increases in the burst frequency, duty cycle, number of motor neuron spikes and spike frequency in the burst (Fig. 5D; Table 1). Both proctolin and CCAP increased the slow wave depolarization of the motor neurons in the C. borealis CG.
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The FLP family members SDRNFLRFamide, TNRNFLRFamide and NRNFLRFamide are
all found in the C. borealis POs
(Christie et al., 1995;
Li et al., 2003). We recently
compared the effects of SDRNFLRFa, TNRNFLRFa and a new family member,
GAHKNYLRFa, on the burst frequency of the C. borealis CG
(Cruz-Bermúdez et al.,
2006). In the present study, we have combined data from those
experiments with other preparations (new data) to which we have applied FLPs
and analyzed additional burst parameters. As expected, SDRNFLRFa, TNRNFLRFa
and NRNFLRFa elicited excitatory effects on the isolated C. borealis
CG (Table 1). On average,
SDRNFLRFa and TNRNFLRFa increased the burst frequency to the same value, 0.30
Hz. The three related peptides elicited almost identical changes in other
parameters such as duty cycle and number of spikes.
Effects of other newly identified peptides on the cardiac ganglion
We applied two peptides that have been recently identified in C.
borealis to the CG: orcomyotopin-related peptide (OMTR)
(Billimoria et al., 2005) and
Cancer borealis allatostatin type B (CbAST-B1)
(Fu et al., 2007). At
10–6 mol l–1, neither OMTR nor CbAST-B1
significantly changed any parameter of the CG bursting pattern
(Table 1).
Effects of amines on the cardiac ganglion
There are numerous early and recent studies of the effects of biogenic
amines on the CG (Benson, 1984;
Berlind, 1998;
Fort et al., 2004). In
Fig. 6, we show the effects of
serotonin and dopamine on the CG motor pattern.
Fig. 6A shows extracellular
recordings in control (top trace) and during 10–6 mol
l–1 serotonin perfusion (bottom trace). In data pooled from
seven experiments, serotonin significantly increased burst frequency, duty
cycle, number of spikes per burst and spike frequency in the burst
(Fig. 6B;
Table 1).
Fig. 6C shows recordings from
another CG in control (top trace) and in the presence of 10–5
mol l–1 dopamine (bottom trace). Like serotonin, dopamine
significantly increased the burst frequency, duty cycle, number of spikes per
burst and spike frequency in the burst
(Fig. 6D,
Table 1). Similar results have
been found in many other CG of different species
(Berlind, 1998;
Berlind, 2001;
Cooke and Hartline, 1975;
Fort et al., 2004;
Miller et al., 1984;
Saver et al., 1999).
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In contrast to serotonin and dopamine, neither octopamine nor histamine (Table 1) induced statistically significant changes in any burst parameter measured.
Actions of cholinergic agonists and GABA on the cardiac ganglion
Acetylcholine (ACh) is thought to be the neurotransmitter that is released
from one of the acceleratory fibers projecting from the CNS to the CG to
increase cardiac activity (Cooke,
2002), and the sensitivity of the CG to ACh and muscarinic
cholinergic agonists has been described in other species
(Freschi, 1991;
Freschi and Livengood, 1989;
Sullivan and Miller, 1990).
Fig. 7A shows extracellular
recordings in control (top trace) and in the presence of 10–5
mol l–1 pilocarpine, the muscarinic ACh receptor agonist
(bottom trace). Fig. 7C shows
recordings from the same CG during wash (top trace) and during
10–5 mol l–1 nicotine perfusion (bottom
trace). Both pilocarpine and nicotine increased the burst frequency and the
number of motor neuron spikes in this preparation. On average, both
cholinergic agonists elicited excitatory effects on all burst parameters
measured (Fig. 7B,D;
Table 1).
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;
Cooke, 2002;
Delgado et al., 2000). |
Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Marder and Bucher, 2007).
Although it is likely that many other neuronal networks are equally richly
modulated, there are relatively few systems in which the effects of multiple
neuromodulators have been studied on the same neuronal circuit. Previous work
on the intact heart has shown that each of five different substances alters
the heartbeat in different ways (Saver and
Wilkens, 1998). Given the fact that some of these effects are
caused by actions of neuromodulators on heart muscle and neuromuscular
junctions (Saver and Wilkens,
1998), and given the pivotal location and function of the
crustacean CG, we thought it would be interesting to determine the extent to
which it, like the stomatogastric ganglion, is also modulated by a large
number of different substances. Fig.
8 summarizes the results of this study, and illustrates that the
cardiac ganglion is a direct target of an array of neuromodulatory agents.
This must be viewed as an incomplete list, because new mass spectrometry
methods are rapidly leading to the identification of additional neuropeptides
in neurosecretory structures (Fu et al.,
2005a; Fu et al.,
2005b; Fu and Li,
2005; Li et al.,
2003; Stemmler et al.,
2005), and many of these newly identified substances have yet to
be studied physiologically.
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The actions of RPCH, CabTRP Ia and AST-3 on the CG are described here for
the first time in any species. AST-3 joins GABA as a substance with potent
inhibitory actions. These results, together with the inhibitory actions of
AST-3 described previously in the STG and stomach muscles
(Jorge-Rivera and Marder,
1997; Skiebe and Schneider,
1994), make AST-3 a common inhibitory peptide for both the heart
and stomach in crustaceans. Similarly, RPCH and CabTRP Ia are generally
excitatory on both the CG and the stomatogastric nervous system.
The effects reported here for modulators that have been previously
described in other species were, in many cases, consistent with previous
studies. For example, in C. sapidus CCAP and dopamine increased duty
cycle and the number of spikes/burst much as we found
(Fort et al., 2004;
Fort et al., 2007). In H.
americanus histamine activates a chloride conductance in the motor
neurons, but the burst frequency is unaffected
(Hashemzadeh-Gargari and Freschi,
1992a). Therefore, it is possible that the apparent lack of
histamine action on overall burst parameters in C. borealis may
nonetheless be associated with the presence of receptors that can be revealed
with more detailed biophysical analyses.
Comparisons with previous work on other species are complicated by the fact
that modulators affect different features of the heart output at different
concentrations. For example, in C. sapidus low concentrations of CCAP
can influence contraction amplitude, while higher concentrations increase
burst duration and the number of spikes/burst
(Fort et al., 2007). This also
makes it difficult to quantitatively compare the effects of multiple
modulators on any of the burst parameters we measured in a meaningful manner.
Although we used modulator concentrations that were suggested by previous work
on crustacean systems to be saturating, or close to saturation, in the absence
of complete dose–response curves for each substance it is difficult to
determine unambiguously the extent to which modulators may differentially act
to alter specific parameters of the cardiac ganglion output. Initially we had
hoped to determine if some neuromodulators affected frequency more than burst
duration or duty cycle, and vice versa
(Table 1). Thus far,
statistical comparisons across the modulators showed no significant
differences on these parameters among those substances that excited the
cardiac ganglion. Because many, if not all, of the modulators that act on the
cardiac ganglion may also act on the cardiac muscle or neuromuscular
junctions, it is very possible that modulators that have qualitatively similar
actions when studied on the cardiac ganglion alone may influence cardiac
output, and other aspects of heart performance differentially
(Fort et al., 2004;
Fort et al., 2007;
Saver and Wilkens, 1998).
Unfortunately, the `simple' cardiac ganglion has a complex anatomical structure that makes it difficult to determine easily whether neuromodulators act on the pacemaker neurons, the motor neurons, or both. Because the pacemaker cell axons run in the trunk of the ganglion in which the motor neurons are found, and because the motor neuron axons run through the region containing the somata of the pacemaker cells (Fig. 1), it is not possible to simply cut the two regions apart, nor to apply neuromodulators only to one class of neurons. Moreover, the extensive electrical coupling further complicates the isolation of neurons. These problems are acute in C. borealis because the pacemaker cells are closer to the most posterior motor neurons than is the case in other species. Consequently, we were unable to determine whether any or all of the modulators studied have receptors that are restricted to either the pacemaker or motor neurons.
Do neurohormones act alone?
In this study we assayed the action of multiple modulators by applying each
one at a time followed by long washes to return to baseline. However, it is
very likely that in vivo structures like the POs might release two,
three or more of these modulators simultaneously. Such hormonal corelease
suggests a few possible pharmacological scenarios. Some modulators might
occlude each other's actions (Swensen and
Marder, 2000), or synergistically enhance physiological responses
elicited by their joint actions.
In the lobster H. americanus, CG, proctolin and cholinergic
agonists activate a voltage-dependent Na+ current
(Freschi, 1989;
Freschi and Livengood, 1989)
that is probably the same voltage-dependent inward conductance activated by
proctolin (Golowasch and Marder,
1992), pilocarpine, RPCH, CabTRP Ia, CCAP and TNRNFLRFamide
(Swensen and Marder, 2000;
Swensen and Marder, 2001) in
STG neurons. Because of the structural dissimilarity of these agonists, it is
unlikely that any of them except for the FLP family members activate the same
receptor (Cruz-Bermúdez et al.,
2006). Thus, convergence of their actions on the same membrane
channel likely occurs at some point in the signal transduction pathway between
receptor and channel. Consequently, in a network as `simple' as the cardiac
ganglion, it may not be surprising that many of the excitatory neuropeptides
have similar actions on the output of the network. Of course, if the receptors
for some neuromodulators are preferentially found on the motor neurons, and
others on the pacemaker neurons, this would influence the extent to which the
neuromodulator affected frequency or duty cycle, etc. of the motor neuron
burst. If several neuromodulators are coreleased or are circulating at the
same time, their responses will depend on their concentrations as well as on
the state of the signal transduction pathways in their target neurons.
Do hormonal modulators coordinate the activity of multiple systems in the animal?
Most of the modulators studied here have strong physiological actions on
the CG. Excitatory modulators could be hormonally released to increase
activity not only of the heart, but also of other organs when the overall
internal activity of the animal is low. For instance, substances released from
the POs including dopamine and octopamine are involved in ionic regulation and
branchial exchange in crabs (Morris,
2001). In the digestive system, peptides such as proctolin, CCAP,
FLPs and RPCH have excitatory effects on the STG motor patterns, on identified
synapses within the circuit and on many stomach muscles
(Hooper and Marder, 1984;
Jorge-Rivera and Marder, 1996;
Jorge-Rivera et al., 1998;
Nusbaum and Marder, 1988;
Nusbaum and Marder, 1989a;
Nusbaum and Marder, 1989b;
Weimann et al., 1997). At the
behavioral level, increased amounts of serotonin in the lobster, H.
americanus' circulatory system are correlated with aggressive behaviors
(Huber et al., 1997a;
Huber et al., 1997b;
Kravitz, 1988;
Kravitz, 2000;
Kravitz and Huber, 2003).
Differences in circulating levels of serotonin, dopamine and octopamine
between winners and losers after confrontation have been also reported in the
crab, C. maenas (Sneddon et al.,
2000).
The sensitivity of the CG to multiple substances may be a reliable mechanism to increase its cardiac activity and deliver neurohormones released from the POs and other structures in a particular physiological context. One might imagine that if it is important that a hormonally released substance quickly reach distant tissues, it would be advantageous for that substance to act directly on the heart to enhance cardiac performance, and the delivery of the substance. This could explain why it is important for the heart to respond to so many of the neuromodulatory substances found in the animal.
List of abbreviations
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Acknowledgments |
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Footnotes |
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References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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